sex and evolution (1975) by george christopher williams

8/15/2019 Sex and Evolution (1975) by George Christopher Williams

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MNGRPHS IN PPUTIN BGY

EE BY RBER M MAY

The They f Isand Bgegraphy, by Rbert H Marthurd Edwad . Wsn

Evutn n Changng Envrnments Sme Thereta Epratns, by Rhard evns

daptve emety f Trees, by Heny S H

4 Thereta spets f Ppuatn Genets, by Mt Kmuraand Tmk hta

5 Ppuatns n a Seasna Envnment, by Stephen D. Fetwe

Stabty and Cmpety n Mde Esystems, by Rbet MMay

Cmpettn and the Strutue f Brd Cmmuntes, by MartnCdy

Se and Evutn, by Gege C Wams

Sex and

Evolution

GG WLLM

PRINEON NE JERSEY

PRINETON UNIERSITY PRESS15



o rt © 15 reto erst resss e r eto erst ress r eto o o

ALL RH REERELibr o o gress t ogig i Pbictio t wi be od

o te st pri ted p ge o t is book

is book s bee composed i Mootype Bskervi ePrited i te U ited St tes o Americ

Prfa

Thi oo i written from a conviction that the revaenceof eua rerouction in hiher ant an anima i inconi-tent with current evoutionary theory My uroe i to ro

oe minima moication of the theory in orer to accountfor th eritence of o eeminy maaative a characterMany we informe reaer may iaree with much of myreaonin ut I hoe at eat to convince them that therei a in of crii at han in evoutionary iooy an thatmy uetion are auie enouh to warrant eriouconieration

Th concetua comeitie and diverity of reevant information on eua rerouction oth in reation to arwiniantne an to onterm hyogenetic eect ar o grt that

a uefu conenu may e ome me in comin. Hefu contriution can e cte fm reat variety o ioogicaiciine I hoe that thi oo timuate ome ae theoritto attac the concetua roem and encourae eciaitin ivere onomic rou to document thoe detai o ifecyce an rerouctive natura hitorie that can rovie etimate to reace uee on crucia qantitative roem

I di mot of the rain and writin uring ummer of1970 1971 an 1972 when I had acce to the uerirarie o the Univerity of Tronto an Roya Ontrio

ueum I wih to than th ta o thee intitution orany hefu courtie hot o inividua contriutd none way or another o the iea eree. Joeh FeenteinJohn Maynard Smith, an Ror L river wore throughthe whoe manucrit corrected many error an mae vauae ugetion F Jame Roh an John R G Turnerhed with concetua and oranization rom o hater Othr aitance i acnoweed i the tet

v



PREFACE

am gateu t te aemi ess em t e-t igues 4 t Dag Mlle a te seiiet-atets asigsistitutt igue t te Siet the Stu Euti gue 1 t James . CwMt Kmua a the Uiesit Cag ess ig-ue 14 Oigal igues 3 1 a ats 13 wee aw Sigu Guass Reai ela a te est

Kae is f St B New Y

V

Cntnts

ND CHR

AN MORTANT QUESTON TS ESYANSWER AND TE CONSEQUENT

PARADOXoss of genes in miotic oogenesis gives sexual poduction a 50% disadvantage in lation to asexual.exal epoduction ought to disappa in diploidoganisms aadoxically it coexists in volutionayequilibim with asxual in many life cycles in whicits ocence is elated to ecological ange and ncetainty

2 E APDROTER MODEL

When clones compete in conned spaces, the ttest

one may exclde all othes. exally epoducecolonists to suc a abitat will be moe dives tantos asexally poduced, and moe likely to incldete winning gnotyp his advantage balancs the"ost of meiosis so as to establish an equilibium inthe elative fquency of sexual and asexalepoduction

3 TE STRABRRYCORAL MODEL

Envionmental gadints st limits to the vegetativespead of sessile oganisms and act somewt likehabitat boundaies in the idRotif Modl tevoltionay eqilibium some esouces will be devoted to poducing genetically divese popagulessom of whic may be able to suvive elsewhee in theenvionmental gadients

4 TE ELMOYSTER MODL

Wen lage numbes of yong of a sessile fomcompete fo space fully tiliable by one adlt it islikely that one of te vey few ttest will win all o

3

1 ®

26

3



N E N S

most of the space Genetally dvese ae ore likelthan unfom pogenies to incude te ttest few. Iths advantage moe tan bances the ost of meoisasexua epoduton will disappea

OTHER MODES

Reasons ae gven fo belevng that sexual epoducton wil augment numbes at the top end of te t

ness dstbution when adult movements ae limited,feundty s hgh and young a widey dspesed aomon patte n ane oganss Wth sently ntense seleton ts advantage may baaneecobinatona oad and the ost of meioss Evolutonay equlbum ous wth exsivey sexualepoducton

6. NATURAL SECT ON N_HGH

FCUDITY POPULATIONS : THEOR

Models n Capters 4 an 5 dema n tat selecton n

high-fecu ndty opatons s more ntense tan sgeneraly reaized. Arguents n suport of t ro

poston a nd mpcatons for ts accetance are

dsussed

7 NTR SECTO N HHCDTY POPTONS EVDCEON VLTY

Pubshed nfoaton on adaptve pefomane onompettve eatons aong developing young andon gene-feqeny gadents n eaton to dspesa

suppot te popostion of enomos vaty vaatonamong genotypes n high-feundty popuations

8 TR SECTO HGHECDTY POPLTONS : EVDECEO ERTLTY

Data on ge pants and on ses ndate enomos vaaton n fetty Ts vaaton must epaty genet and ontbutes to vaaton n tness.

v

44

77

9 1

N N S

9 DRVED OWECDTYPOPLTONS

Poesses envsone n Captes 4 and 5 esut inexcusvely sexual popuatons Te phyogenetdesendants may ak peadaptatons fo seondayausiton o asexua epoducton, even wee itwould be adaptve Pathengeness, wee physoogay feasibe, apidy eplaes sexua epodutonin lowfeundty ogansms

10 PTTRS OF SEXTY

Explanatons ae suggested fo some of te phenoena of opaatve sexuaty: ansogay emapodts seng pathenogeness Soe of teelatons wit pevously poposed models aedisussed

1 1 WHY R MES MSCLE DMLS FEMNE D, OCCSON

LLY V VERS

Deenes between ae and femae epodutvebeavo and pysology folow fom egg-spe ontast n sze. Othe fatos su as ntea fetiaton and teitoalty pedspose a spees towadsetan evolutonay anges in te oes of te sexesMuh of outshp and famy fe s intepetabe asesutng fom aty onitng male and femalestateges

1 SEX S FCTOR ORC

EVOLTOReent lteatue on ths top ontains a dvesty ofopnon but o st of the wo s based on te assmton tat ality to nopoate favoabe mutatons ommony mits the ate f evoluton and tatebnaton must aet ts abty It s popoed nstead tat potental ates of gene substtutonae aways geate than atual, and tat eomnaton s signcant manly fo mantanng genotypvesatty n unpedtae envonents

102

1 1

14

140



CONT EN TS

3. SEX AS A FACTOR IN BIOTIC

EVOLUTION

Group selection in relation to sexual rproducion isdiscussed It is sugesed hat exincion ccurs, nofrom lack of adapaion bu from adapaion o niches that become untenable Field sudies how ha

asexual or hihly inbred species often have a compeiive advanae over sxual forms, and are especially successful in novel environments Yet the phylo-eneic distribuion of loss of recmbinaion suessha this condition increases daner of extincion Thecontradiction remains larely unresolved.

BIBLIOGRAPHY

INDE

x

55

70

195

Sex and

Evolution



C H P T E R O E

An Iprtant Qustn,

It's Easy Answr,

and th Cnsqunt Parad

Orgnsms dt to stresses by ysolocl or bvorl rsonss, s n mns rcton to cold by ererl vsoconstrcton, ncresed mtbolsm, nd wrmthseekng bhvorTt tese r noml resonss, sown only by lvng ndvduls, s vdnc tt they re dttons to cold Logcllyts vdnc s ndendnt of ny understndn of nsul

ton or mtbolc t roducton smlr roc cnb mde to t uston Wt us s sx?" rcntly osdby Mynrd Smt ( 19 f t cn be sown, for vrtyof orgnsms tt cn reroduc bot sxully nd sexully,tt ty usully rroduc sexully, but us sexul rructon n scl stuton s t nswer rses from nsctonSx s n dtton to secl stuton s Ts s vld concluson regrdlss of ossbl nornce s to wy t souldbe dtv n rlton to s

So t nswer to t quston Wht us s sx?" s tt

roosd by onner ( 1958 sex s rntl dtton tot lkelood of t osrng vng to fc cngd or uncrtn condtons For nstnc, f t lfe cycl zygot tozygot ncluds svrl sxul d on sxul generton,t sxul rroducton wll occur wer cologcl drncswll b gretst btwen two sccessv gnrtons Wrbot sxul nd sxul rroducton cn occur smultnously, t sxul osrng wll devlo mmdtly ndnr t rent, but dormnt, wdly dsersed rogules wllb roducd sxully



Q S A D P A R A D X

Bal ( 196 and Harpr ( 1965 and B eviw the ph-nomna and a thoretical tatmnt o adaptiv dormancyi povidd by Cohn ( 1968 Hi raoning aum popula-tionwid optimization bliv it t b qually applicabland mo biologically rlvant to progny optimiation

ieenc in mortality ate mut follow from dincin i dipal and domancy Larg oganim gnallyhav low mortality at than mall and larg i indicategar ouce Lngditanc dipral mut be pciallyhazardou whn favoabl habitat ae mall and iolatdLong dormancy inca the ime during which dath rmaccidnt dia or pdation can occur

Th accuracy with which oping nvionmnt can b p-dicd fom parental nvionmn i obviouly rlatd to dipal though tim and pac inpt h dict dlop-

mnt of axual opring and th indirct dvlopmnt of thxual a pat of th am pattn An adult oganim dvlop-ing in a crtain plac i living proof that th habitat i favo-abl phap xtaordinarily o for an adut of th gnotypand hat in th pat it wa favorabl fo arli tag of dvl-opmnt t i not pcially iky that thi habiat i now agood n fo an mbyo o lava dling which will havequimnt and chalnge dint from ho of th adultAxual poduction of oping in th immdiat vicinity fh arnt m to b adaptiv only whn an oring quicky

bcom adult in it cological rquirmnt f it will b co-lgicaly din a a eult of bing ontogntically dirntgnotypic divicatin i th nomal atgy

Th comparion of intniti of ction of axual andxua poduction rqui om laboatin f on com-pa lcion within pgni th anwr i tautologicallyvidnt Th can b no natua lction in th genticalyunifom pogny o a comparion of ction btwn twoaxua pgni wih ha bwn two xual on hinc i h v hat claimd Th intndd com

Q S A P A R A D X

paion i th hypothtical on of intenity of nvionmentalcrutiny of genotype Naural election of widly diperded and eedling of trawbrry would mor inten thanthat of a ampl of runnerppagatd individual of th amgenetic diverity

THE PARADOX OF SEXUALITY

knw of no obvation clarly count to tho umma-izd abov Hncforth aum that th aociation btwnxua reproduction and changd condiion a lationhiecognizd by many and dicued in dtail by onn i adquatly upported vn though th natu h lationhipand of what i implid b changd conditin i not yt clarlypcied So aum tha th anwr to h qutin Whatu i x?" i ttld but in a way dirent fom MaynardSmith concluion H found littl upport for th ida ofx a an immdiatly adaptive fatu of production andargud for a form o traditiona view (laborad by H JMul threfo ullerian, Chat 1 tha mpha-iz longtrm ct on gn ubtitution My reaoning imuch l rigorou than Maynad Smih horough mahma

tical teatmen but think hat hav th mor liabl cn-cluion Fo anwing quetion on function in biology com-parativ vidnc i mo liabl than mathematicalaoning

Exact raoning from plauibl aumption on h naturallction of vaiation in proc of xual eproduction iobviouly ncary Th concluion that x i an adaptationto changed condition i not vr atfying until w undrtand to om dge why it i adaptive to changd cnditinotunaly i i ai to aon fom a of prmi toa valid concluion if you know th concluion in advancHaing larnd from comparativ vidnc wha x i



QU E S T I O N A N D P A R A D O X

adaptive to, houd make it eaier to how, by deductive anay

i, why it is adaptiveThi book will be largely devoted to nswering thi econ-

dary quetion. The tak would eem immensely difcult, a

Maynard Smith (1971A, 1 9 7 1 B ) has clearly recognized, be-

cause we can immediatey ee an enormou diadvantage inexual reproduction. Jut how enormous i a complicated que-

tion I aume for the moment that an evaluation can be made

by coparing two kinds of individual One i parthenogenetic

nd produces diploid egg of parental genotype The otherproduces genetically diverse haploi eggs that require fertiiza-

tion The reative ucces of these two inividuals wil specify

the relative tness of aexua an exua reproduction. On th

bai the arguments belw ow that the parthenogenetic in-ividua has twice the tne of t sex ual. Tis imediate

advantage of aexual reprouction is generally concede bythose who have eriouy conerne themeves with the prb-lem. If the reaer ha any doubts on this matter a discssed in the paragraphs below, he can fnd a more ext treatment in Maynar Smith' ( 1971B ) discussion.

Consider a population with two female genotype At a cer

tai tage in the ife hitory, genotype AA produce unre

duce eggs that develop into genetic replicas o the mother.

Genotype A3A4 produce reduced egg that mut be fertiized

An Aallee from a sperm can be caled A Thus ·an opring

o the exual parent i either A3A or AA It has one, notbth of the materna gene All the opring of the partheno-

genetic parent have the ful materna genotype AA. Unle

omething caue a dierence in the number of opring, the

asexua parent has double the genetic repreentation of theexua in the pring generation It i the same tory in thenext generation. Both genes of the aexual prgenitor will be

preent in each of the grandchildren, but only half of the de

scenant of the sexual individual wil have either A or A,which are therefore own to a quarter of their original fre

8

Q U ES T I O N A N D P A R A D O X

quency. Each ex gene" uer a 50% hazard per generation,

relative to aexual aternative Purit who object to the impi-

cation that an aexua cone i a part of a Mendeian popula-

tion can edow the gene for parthenogenei with le than

perfect penetrance.

A gene that caue exua reproduction ony in certaingenetic and environmenta circumtances wi uer the 5

o only infrequenty The character till ha the 50% diad

vantage, even though the eect may be infrequent or diused

over many loci. Alo, any advantage we might attribute to

the character will likewise be infrequent when penetrance i

low The argument o far appies only to female. The imposi

bility f parthenogenetic development of perm make it inap-

picabe to maes, unles a mae can reprduce vegetativey,

as dicused below The reasoning asumes the poibility of

producing iploid eggs, o it does not appy to hapoidorganism

An important aumption is that diploid an haploid eggs

are equally expenive. Thi can only be apprximatey true,

but the inaccuracy wud uualy be minor There i only haf

a much DNA in a haploid nuceu, but there is no reasn

to beieve that DNA i epecially icult to prduce, com

pared to RNA or proteins Even if DNA ynthesi made extra-

ordinary nutritioa demand, meiois would not achieve any

aving where polar bodie are hed with the egg In pece

that resorb polar bodie the DNA aving woud til be light,becaue nuclear DNA i only a sall fraction of that in the

egg Even the minute egg of the ea urchin has much more

DNA in yok and mitochondria than in the nucleu (B rachet

and Malpoi, 1 97 1 ) Reduced and unreuced egg may be

nearly identical phyicaly and 'hemicly The important

dierence lie in genetic information content

The concept of cost of meiois i clearest when the compari-

on i between exua and parthenogenetic egg production,

but i equaly valid in relation to sexual egg roduction versu

9



Q U E S T I O N A N D P A R A D O X

ve analysis, must as surely be true by comparative evidence ,

and vie versa y approach to this paradox is to accept the

comparatve evdence and ty to revise the analyss so as to

make the two compatible, although my revsion requires what

some might consider rather drastic modications of current

evolutonary thought

PREVIOUS SUGGESTIONS ON SEX AS A

REPRODUCTIVE ADAPTATION

A belief that sex may be adaptive by diversifying ospringpotentiality in relation to uncertain conditions dates at least

rom Weismann 1 88 9 , but critical discussons are fewClausen ( 1 954) proposed a model of evolutionary equilibrium between asexual and sexual reprodutio, bu oly in refer-ence to rare sexuality in normally apomictic hybri plants.

His reasoning was not quantitatve and did not recognze thecost of meosis. In a critique of group selection I prposed (Williams, 1966A) that all longterm dvantags that hadbeen proposed for sexuality were alid as immedate adapta-tions fo maximizing progeny success I pointed out hat theassociation of sex and changed conditions in heterogonic (al-ternatng asexual and sexual) life cycles implied adaptationto uncertanty. Ghiselin ( 1969 ) also suggested progeny successas the important consideration and criticized te Mulleriantheory for " . . ailing to accoun

t for the increase of genes for sexualty wthin the population." Maynard Smith ( 971A)analyzed the possibility of progeny diversty as a reproductivadaptation and found it unlikely to produce any advantageThis was with both a general model, without ny special lifehstory features, and a form of the AphdRotfer Mdel(Chapter 2 . Williams and Mitton 1 9 73 ) reexamined theAphdRotifer Model and concluded that the special life-history eatures of the model organisms would result in a fre-quencydependent advantage in sexual rep oduction such that

2

Q U E S T I O N A N D P A R A D O X

evolutionary equilibrium would occur with several to many

asexual generations per lfe cycle They also introduced the

ElmOyster Model (Chapter 4) .

Elen 973 : 5456 presented a graphic model of the

favorabe selecton of sexualty requency dstrbuton f o-

spring on a scale of tness dosage is shown as having the samemean for both an asexual and a sexual progeny, but the sexual

has the broader distribution If selection is so ntense that only

those at the upper end of the scale have an apprecable chance

of survival and reproducton, there may be more successes n

the sexual progeny, whch would therefore have the higher

mean tness This would depend on a nonlnear relation be-

tween position on the dosage scale and tness Emlen uses a

threshold relation, wth only those above a high dosage beng

t," and all those below being unt"

This is justed in a brief ntroducton such as Emlens ,but sharp tness thresholds are unlikely n nature I prefer

a more complex representation ( igure ) where a tness

gradient ( shown as density of stppling replaces Emlen's

threshold I have also lowered mean dosage n the sexual pro

geny to ndicate recombinational load

A qualication is necessary It is not enough tha a sexual

progeny be more variable than the asexual What is required

is that a sexually produced ndividual have a wider probablty

distributon of tness, and this need not always be true or

instance, f the parental generaton is consttuted from extremetypes, whch would produce a intermediate F1) the ospring

group would be less varable if produced sexually The rela

tionshps among population and progeny tness frequencies

and individual tness probablities are discussed further in

Chapter 5.

The models roposed here ( Chapters 2 to 5) all assure a

greater variance in tness dosage among sexually produced

individuals, and are therefore all examples of Emlen's more

general model as moded here These assurances come from

1 3



Q S A D P A R A D X

specal fehstory features such as ntesnse comp titIOn

wthn progenes and speca breedng structures. I belevethat adtonal moels may be vad but that all wl requrespecal lfehstory eatures aynard Smths 9 7 1 analss

FTNSS DOSAGFIGURE 1. Gene mo el o vo ble se lect on o sex l ty s est o nc e se tness vton e sex l ogeny s te loe ve ge os ge o tness bec se o ecombn-t on l lo bt exten s to ge vles bec se o ts getev blty Dens ty o stng nctes tness

convnces me of the unlkelhood of ayone ever ndng asucently powerul advantage n seua repructon wthbroadly applcable models that use only such general proper-tes as mutaton rates populaton ses seecton coecentsetc

1 4

C H A P T E R T W O

Th Aphd-Rtfr Md

Suppose you were oere ths choce n a lottery ether oucould have several derent tckets or you could have thesame number of copes of the same tcket Obvously youwould elect to have several derent tckets The theory presented n ths chapter cams that seually prouce osprngmay be anaogous to ottery tckets and those aseualy prouce analogous to redundant copes of the same tcket fand when the anaogy s val seual reproducton s morelkey to prouce wnners

Ths chapter wll atempt to show for heterogonc cycles that genetc dverscaton of progeny may carry atleast twoold advantage and thereby justfy the cost ofmeoss It enlarges on the AphdRotfer oel propose byWllams and tton 197 ) but neeless to say leaves manynterestng questons untouched y purpose s merey toargue the lkehood of n avantage n seual reprouctonthat s freuecy dependent n a way that may eplan therelatve frequences of seual and aseua reproducton n lfecycles such as those of aphds rotfers and many parastes

Subsequent chpters wll deal wth other knds of lfe cyces

TE MODE

Consder populaton wth the followng lfe hstory It vesn smll dscontnuous habtats uch as a host organsm ora woodland pool It s dpod and produces a number of generatons a year aseualy so that a sngle ndvdual on reach-ng a sutble habtat can form a clone that saturates themted envronment Once a year a generaton of wdey ds

1



A P H D R F R M D

prd diploid propagul i roducd Th Mod rlat oth rativ advantag of axual and xua rproduction forth production of th widly diprd propagul

Aphid that form clon on hrbacou hot in aonalclimat would b an obviou xmp Rotifr, turbllarian,

an othr mall invrtbrat of tmporary watr would bothr Som protit av th appropriat coogica lif hitory and o gntic matria in th formation of macrogamt, g th iatom ritch, 95; Prcott, 968 andprhap om porozoan Kudo, 966) Th mod may bapplicabl to thm, but it i irrlvant to th many haploidiogamtic protit

n th prouction of widy diprd propagu lt gno-typ produc thm axualy, o that a hav th parntalgnotyp Gnotyp produc tm xualy, o tt thy

hav gnotyp c d e tc An avrag of proagul fromach parntal gnotyp talih thmv in accb nwhabitat, and ach thn proifrat conally until th abitati aturat Thraftr th con wth h ocy bt gnotyp wil continu to incra unti it i th xcluiv or domi-nant con

Linag tablihd in a habitat may b m of gnotyp from th axua parnt, and on ach of gnotyp i j k

a tota of n ) from th xua parnt Thr i only onchanc in + n that th bt adaptd clon il b t i

initially th mot numrou, it tarting numbr bing x-pctd to qua a th othr combin, but aftr a longprio of comptition in a aturatd nvironmnt, th gnotypic proportion may b dcidd mor by minor drncin phyiology than by maor inqualiti of initial abundancBing n tim a ikly to produc th on ttt gnotypmay ultimaty mor than compnat for th twofold cotof mioi

h nviion advantag of xua rprouction i that itgiv on' gn rprntation in a varity of clon, thrby

1

A P H D R F R M D

incraing th hanc of tranmitting thm to winning clonThr i a co formal analogy with th lottry tickt Animportant aumption i that th propagul from on parntor parnal clon may hav acc to only a fw nw habi-tat, but that mor than on, prhap many, may rach a habi-

tat that i accibl rom th habitat tandpoint, coonitar a imitd and vry nonrandom ampl of th ntir parnta population Anothr important aumption i that clonaldcndant of multipl proagu compt with ach othrfor a lv of ucc that on propagul coud achiv by it-lf ncraing th nubr of gnotyp zygot raching thwatr in a bromiad may hav no mor inunc on th naliz of clon than xroxing on lottry tickt would havon on winning

Th nviion proc impy normou dirnc in

gnotyic lction cocint in on zygottozygot cyclhraftr life cycle a oppod to generation which may bithr axual or xual Th mor or compt rplacmnt of on con by anothr in a vralmonth growing a-on i coogicaly raitic, but it corrpon to a manifolddirnc in ction cocint pr lif cycl Th 50% diadvantag of mioi ma b mry on of a larg numbrof trong lctiv ct an n not b dciiv

t might b obctd that axua propagu, in rtaininga gnotyp that provd it tn in a prviou clona compti

tion, ha a bttr than avrag chanc of winning th nxtcomptition Any uch btwnhabitat hritability of tnwoul rduc th propod advantag of xuaity Gi' 197 ) xprimnt how that minor irnc in conition,comparab prhap to irnc btwn ucciv habitat,can inunc outcom of comption btwn train of Paramcium Btwnhabitat hritabiity f tn would apparnty b ow in th organim

Rativ tn of gnotyp mut alo chang uring apriod of cona comptition, a a rut of incra rowding



A P H D R R M D

nd perhps ssonl chnges The tnsses ssumed n themode must b verges ovr the prod of competton nd ts ssumed tht verge derences re gret enough to cuseconsderble chnge n retve bunnce n few gener-tons There s form possblty of clones coestng n

numercl eulbrum but he condtns r strngent Bevn Stwrt nd Levn If the prncple fcompette ecluson s vr vld t shoud be vld forclones of the sme populton competng wthn crcumscrd hbtt

The vrous pusbl wys n whch the dvntg of gentcy ds progen cn be reduced do not etrct frmthe geerl logc of the mdel They cn be compnstdere y proongng th prod of clonl competton or byncrsng the number of propgues recng ech new hb

tt s ndcted n the net secton

FREQUENY OF SEXAL REPRDUO INEVOLUTIONARY EQUILIRIUM

The longer the perods of clonl competton the more wllderencs n gnotpe result n derences n bundnce Sothe more genertons per fe cycle th greter the dvntgen the med strtegy of seulty If ths dvtge s more

thn twofold se hs nt selctve dvntge nd shouldncrese n fruency Ths ncrse wl ruce the ngth ofthe lfe cycle nd therey reduce the dvntge of seultyEvolutonr ulbrum occurs when the medstrtgy d-vntge just brely pys for meoss

ms nd tton 73 smulted ths rtonshp on computer Th clculted rlt numers o seuldscndnts o two sets o propgues n crcumscred htt On st rom one prnt or prent clon ws suproducd nd l hd the sme tnss eZo Th othr set ws

8

A P H D R R M D

sully roducd y pr o prnts or prntl clons nhd rous tnsss eX Colonz htts wer ully ccssbl to oth sts o propguls so tht rg numro stlsd su propguls uld vrg numro stlshd seul propguls Both nd wr chosn

romth sm osson dstrbuton mn

AFtnsss

wr obtnd rom tbl o rndom norml numbrs wth nd x Th stndr dvton o ws consdr rlstc whn su rproducton s y nry ssonut hghr vlus wr consdr mor lly wth prolcprthnognss

After t genertons the colonzd hbtt th escndntsof th sul propgules would mke p

2 etX

i=l2 etX eXi=l

of th tot* Averges for number of vus of t nd Tle2 showed tht ths rto rechs the crtcl vlue of 2 fterfrom 2 to more thn 00 genertons wth shortr tmes for

* Proessor Rober M M y h s rov e he oow ng commen ryon hs ro

x be chosen r n omy ro norm sr b on wh m n nd v rnce he ver ge v e o h e ness nc on etl s

(2 q )-� f ex [x ( x xo)/2q ] d x zo u

hs rcry we re e ng w h re vey rge me nnmber o roges (rge so h s s c c ons resmoohed o he n v seec ve v n ge o sex over n sex roge s g ven by he or ex q. hereore hesex orm w hve ne seec ve vn ge once h s cor e ee s , e on e q> n or > 118)q be dervesrom he secc ssmon q 01, whence we exec he sexorm o re om n e on e > 1, wh ch cords w h he n mer s mons



A P H D - R T F R M D

2. s nd nts o s x ro gs s o ort on o tot n-b r o o ttors vy n s s r t tos o b n tons o ro g n b r (;) nd n b r o s x g n r tons t) nw s x bov t n) nd sx b ow t n ) s n ts t v dvnt g ro Ws nd tton 1973)

t

247

12

20

3050

100

0

3 4

. 51 49 50 . 52 53 54

52 59

65 59

ji

6962

7064

73

. 69 76

n ro g nb r (;)6 9 12 16 2 5

5 1 50 50 51 51

52 52 . 53 5 1 51

55 54 . 56 .55 . 53

. 59 .61 63 58 .62

64 70 73 71 . 74

72 .77 75 . 79 .8074 82 87 84 86.81 81 90 88 . 93

83 89 9 1 . 93 95

50 100

51 .50 51 .5 3

. 54 .55

66 67

74 73

81 8596 9293 99

97 .98

larger values of A. Equilibrium times also decrese in inverse

proportionality with (, If ( 1 only onetenth as much time

is required he model is merely illustrative, and cnnt predict

durations of clonal multiplication, because ony guesses are pos

sible on values of and A, and because other factors that woud

aect the se lection of seua reroduction in nature are left ut

of account hese other factors coud make the critical value

rather dierent from 2/ Use of a singe of eX for each geno-

type does not mean that each clone continues to increase at

the same eponential rate It merely means tat ratios of such

eponential functions continue to represent ratios of clonalabundance Each eX represents a mean relative rate of increase

up to time t.

he importat properties of the model are not dependen

on the form of the distribution of x or on tness being distrib

uted as eX, or n aseual and seual propagules havig eacty

the same tness distribution All that is required is that the

distributions be roughly the same, and that withinhabitat

heritability of tness is much greater than betweenhabitat

heritability

2 0

\

A P I D R I I R M D

PARAMETERS OF HETEROGONIC IFE CYCLES

If stability is achieved after t generations, and if fecundity

per generaton is F, the potential increase per life cyce is pt.

If selection is more intense with higher fecundity, as will be

argued in later chapters, F and t should be inversey reated,with equilibrium being reached with fewer generations in more

individually proic organisms he natural history of hetero

gonic nimals may give some support to the proposition that

Ft potentia ygotetoygote increase, henceforth ZZI is

rather invariant over a diverse taonomic array of organisms

For eample, parthenogenetic females of Daphnia pulex can

roduce about 40 young per lifetime, with generation ength

about three weeks at room temperatures Frank, et a, 1954 .

Under average eld conditions in a simonth growing season,

generation length would probably average more like si weeksA singe ygote at the start of the season could thereby gve

rise to about ten million by the end ZZI = 0 ) A atworm

that divided by ssion oce a week for the same period would

have about the same ZZI A protist with ssion every day or

two would have to have several seual phases per year to kee

its ZZI down to ten million A careful study of fecundities

and numbers of generations pe life cycle of a variety of het-

erogonic animals would be of great interest

Either the physiological feasibiity or seective value f

seua reproduction, or both, may be contingent on environ-mental cyces Seuality for Dahnia may have greatest value

at a certain time of yar, and day ength or other cues may

be utilied for synchroniing the developmenta processes lead

ing to mictic individuas An annua cycle woud be feasibe,

but not a slightly shorter or longr cycle Seasonality of life

cycles may be rather resistant to evolutionary change

In reation to the model, there could still be slight adjust

ments in the verage frequency of seual reproduction his

would reult from change in proportions of mictic individuas

2 1



A P H D R R M D

In a Daphna culure, some ndvduals may form wner eggswhe ohers connue to reproduce parhenogenetcally, aleas for a whle, and s possble for wner eggs o be produced parhenogenecally Bacc, 965 So f some genoypesoccasonally skp he seual phase whle ohers ndulge, the

ZZI wll readus tself afer a longterm envronmenal orevoluonary aleraon n s value

The same readjustment could be made by al erng the

fecundity er generaion. Suppose a population were a equi-

librium wth an average of 4 parhenogenetic generatons per

annual cycle and 56 eggs per generaion (ZZI = 1 0) . An

envronmenal or genec change ha allowed tme for an

average of only 3 9 genera ins would make annual sexuali y

of above optimal frequency. Clones with greaer han average

ndividual egg producton woul ha near the op ium ZZI

and wold e avorably selected In he absence of oherchanges, equilibrum could be resored b ncreasing fecundiy

to about 60 eggsIn ZZI = Ft, neither F nor t has an upper lmit . The lowr

lmt for s wo bnary sson and or t s one no clonalmultplcaton a all If evolutonary equlbrum occurs aa certan ZZI, follows algebracally that there s a valueof F at whch the requste ZZI would be obaned wh onegeneraton per lfe cycle Above a certan level of lfetmefemale fecundty and wh compeon whn habats of he

sort envsoned n hs chapter, we mgh epec o nd eclusvely seual organsms They would logcally form a specalcase of he AphdRotfer odel, bu t s convenent o treatthem wh a model that s at least supercally deren

Chaper 4

OPTIMA TIMING OF SEXUA REPRODUTION

Supose there are several perods of mulplcaton n a lfecycle, as n some remaodes The queston arses whch of

2 2

A P H D R R M D

hese reproucve phases should be seual An answer canbe found n he argumens presened Seualy should occurwhere there s mnmal ness herably and mamum lkelhood of nw genoypes beng of greates ness In otherwords, where condons on he rgh of Table 1 age 4are mamally developed

Some eamples of assocaon between seual reproduconand changed condns were gven n Chapter 1 A long lstof anmal parases that conform to the patern ould be gvenReproducton whn hoss s aseual; producton of propagules o colone new hosts s seual Where there s more

than one oblgae host, he nal host where seual reroducton akes place wll be the mos moble and dserse heparase mos wdely Thus he frequen rematode patternof a snal for nermedate ost, and vertebrae or squd

for nal Raher han belabor these nstances of conformyo epectaton, I wll here menton some doubul or seemnglyeceptonal cases They are taken from general works onparastology Baer, 1952 Cable, 197 1 ; Cheng, 964

There s a sporooan n whch a urle s te secondary and

a leech he nal host Nether would obvously dserse theparase more wdely nor be harder to nd than the otherFor he maaral parase t s no at all clear whether mosqutoor vertebrae s more wdely dspersed, or whch transfer be-tween hoss hould be subect to greatest selecton Of course

hs paraste conforms o epectatons to the een ha reproducton wthn hoss s aseual Oly n the roducon of prop-agules for transfer rom mosquto o verebrate s reproductonseual

Round worms often lack aseual reproducton an areseldom relevant to the dscusson here are a few n whchseual

reproducon alernates wh a sngle parhenogenec

generaton I cannot cnceve of ths a an evoluoary equlbrum I suggest that an ancesor had many arthenogenetcgeneratons per lfe cycle The clonal perod may then have



A H D RT F R M D

b rsricd by iroml chg d h oul-io my h lckd rdios for rsblishig hquiibrium I o roudworm wih sigl rogicgrio h rroduci rs r oosi of hosrdicd T ifci sg is frilizd fm wich rlss giclly dirs youg wihi sig mggo Tsyoug roduc rogiclly idiiduls h will lh mggo d coul i soil

T ssociio of sul rroducio wih chgd codiios is lso udrsdbl s dio for frliigorgisms d my mls could b gi from grlworks o lowr ls d imls will r o som rl- fcs i rlio o som br kow mls

Wir ggs of i r o cssrily roducd iiciio of wir roug h mrur ufor-

bl fd my ll simul ir roducio Wr huforb codiio h giclly dirs wir ggs lidorm uil forbl circumscs rur Thy my r-u i fll or rs o uil th followig srig lio mog mrur rifl d lig my b rhrdir i succssi srigs Floodig d or fcors mydisrs dorm ggs o dir ociis Thr c b odoub i is dorm ggs h wil roduc h gr-io wi codiios ls rdicbl d s r h ggsusully roducd sully

T sul hss of hi d ohr smll irbrsof lrg lks my b ifrqu or bs This is udrsd-bl o h bsis of h grr sbiliy d rdicbiliy ofcodiios i lrg rm bodis of wr foruyfor is li of rsoig i is h clol hss h rmissig mog mri rrsis I c oly scu i sbl mri irom y smll moil irbr c rroduc suly ll will h rocsscomly rlc h sul Eclusily sul pouliosy h high robbiiy of icio ( Chr 1 3 )

2 4

A P H D R T F R M D

Some recent work on the popultion genetics of rotifers sup-ports the model King ( 1 972 ) showed tht there are greatseasonal changes in clonl composition in wild popultions. One of hi proposed expations ( called "compete genetic discontinuity" ) conforms to the model proposed here. Theohr dos o

This chr d h hr o follow cocr o d-ig mjor dg of s of h sor idicd i Figur1 ( 4 o blc h mjor cos of miosis dmidlyhis is oo limid iw d or fcors will wrr co-sidrio Brdmor ( 963 ) Ghisli ( 969) d MyrdSmih ( 9 7 1 9 7 ) h discussd som of h ddiiolslciv forcs h mus iuc h rli dgs ofsul d sul rroducio Probbly h mos morddiiol disdg of s is h i grs rcombi

iol lod Oblig oucrossig would lso hdic fugii scis i wich coloizio of morry hbis mydd o sigl roguls Mior dgs o sul rroducio c b s i ossibl sc from gilyrsmid hogs rducd suscibiliy o cogiod rducd comiio (s show by Brdmor) i giclly divrs rogis

;

5



S T R A W B E R R Y - C O R A L M O D E L

Are o occupny n biom re etermine y the equ-

librium between cpture of resources by feeing ( coral) or

photoynthesi (strwberry an ome orl) an their use n

mintenance n repcement o loe to grzers n pr-

ites An itionl emn or intnce ee prouction

woul require reuction in reource for maintenance anvegettive growth n ultimately mller biom an re

of ccupancy. If k i the maximum number or bioms tat

coul conceivaby be mintine the ue of a certain ropor-

tion of vilable resource for exual reprouction woul re

duce the clone ize to pk ( 0 < p < 1 ) . Sexual reprouction

woul therefore men lower ie expectancy, becaue the

maller the territory the more likely it woul be for all of

it to become uninhabitable or_lot to a competing cone

On the other hn it is clear tha any gee will ipper

in a geologically hort time i it can not untie its fortunes fromthoe of an inevitably morta clone Evoutionary ucces will

require vagile propgule caabe o establihing themselve

beyon clonal bounries Since these bounries dene the

region o equacy o the cone genotype it is necessary that

thee propgue be sexully produce. A genetically ivere

progeny woul hve a nite probbility o including invi-

ul capble of etablihing themelve elsewhere in the envir

onment graient an my be worth the 50% cot of meioi

The Moel may be applicable to lrge prt of the Earth'

vegettion n to much o the marine fun. Many spongesessile polychete bryozon protochorte, n other

mrine animal strt life a wiely ispered planktonic young

tt coonize uitable urces Once estblihe an iniviul

prouce a colony tht preas in all irection as long it

cn When two uch coonie meet one will grow at the ex

pense of te other even if te physical limits of the olonie

become obcured in the process The great mjority o niti-

ate cone will be crowed out or overgrown or perish rom

other cues Mture colonies will oten live in conition

2 8

S T R A W B E R R Y C O R A L M O D E L

of maxim crowing with each able to perit or long time

in it limite ream, but unble to spre urther long the

environmenta grient in which it i foun.

SELECTION IN A POPULATION OFLOCALIZED CLONES

A more etie look t known or probabe pocese in the

ecoogy an genetic of uch orgnim as strawberries an

cor as pluibility to the moel he ituation epicted

in Figure 2, in ny persistent community my be the outcome

of mny years of eection or locally ttet genotype hoe

actuly preent cn ony be minute raction of those tht

hve prticipate in the contet The competitive excluion

principe houl appy in extreme orm Even a minute

vantage for one clone can asure at let the prtial eimin-

tion of a competitor. Every yer enormous number of new

genotypes ente the el aginst the establishe clone, ech

o which hs already emontrte extrorinrily high tness

or its region of occupncy A newcomer only h minute

chance of etabishing itef where fte locate it in the envi

ronmental graients Occsionall one uccees an cow ut

one or more oler clones wholy or prtly Therefter the pre-

vaiing clones repreent n even more select array.

he trtegic vue of ex in population o ocaized clone

becomes cer if tnes i nlyze into a genera an a locl

component A given genotype tete in repreentative smple

o natur conitions would be foun to have a certin averge

tnes but its tness would vry with position in the hbitt

Hbitat space could be repreente a an ptive lanscpe

of hill an valeys tht woul iicate the tness of every

poition for the genotype in question Variation in this local

tnes, or at least that part of it that i unrelate to general

tne, woul be n indepenent itional contribution to

vriation in tnes The tnes of given genotype in given

2 9



S R A W B R R Y C R A M D

poitio would be ei+, wher e x i the geeral an y he local

compoent

Wit electio o te intenity enviioed, ucce een

o avig bot x a y abor mally large To be in te top

milliot o te ditr ibutio of general te may be of no

avail to a r oagule at la at a point w ere it local tne

i elow te media value._ It may not e a t a an iniviual

tat i mer ely i te top touant o te gener al tne di

tr ibutio ad alo i te to touadt o local te Ay

er itet clone ow ot oly tat it a an etr emely t

geotype i geeral, ut alo tat it wa etr emely or tuate

i ettlg i a part o te abitat tat i uuually well uited

to it genotype. Figur e 3 how the eviioned r elatiohip be-

tween te a oitio i a cro ection o uc a com

muity a tat rereeted i Fig 2 Clone � B, ad C

curretly occuy tat par t o te graiet r epr eeted All

oter geotye ave diaeared or ailed to get etalied,

eier ecae o low geeral tne (or examle, E) low

/

A

"B

_ _ v

, �

-

, /

-

/ *

- . , i - ,

FIGURE 3 Fitne clne nctin envirnmentg ient in ectin tg rt bit t ce Si ine in ic te egin ct ccncy Brken ine wegin t t te g entye w ccy i cm eting cnewee bent m rk itin initi etting f cne

3

S R A W B R R Y C R A M D

local tne at oition o ettlig ( ) , or ot () i aumed to ave ettled an prea to te let eore B arrive

an uurped te regio o iitial etalimet nature,te overwelmig majority o geotype would ave generaland local tne like tat of ; a few woul ave ig geeral,ut mediocre local te, or vice vera, like or an only

a minute ractio would e o ig i ot a to actually wipart o te aitat

Coider ow te logterm callege aced y clone B

t a te ttet genotype, for it limited regio, tat a everad acce to tat region, ut i large umer o ew geotype are eig introuced, one may omeday rove to e eventter Tat evet or an evironmental cage may cauecloal etiction To acieve genetic urvival eyod it itecloal urvival, B mut get it gee rereeted i oter

cloe t mut dipere genetically variale rpagule toregio eyod it curret oldig A imortat aumtioollow rom te cloe circumcried ditriutio Te inaility o B to read into regio occuied y ad emontrate te iadequacy o it geotye in aacet regioomewere, pera, i aoter locality were B woul ettet, ut witi te reaily acceile regio it i likely tatcodition grow wore i all directio Oly y geetically

diveriyig te wideread propagule i tere ay oe oproducig any wit uciently ig local te

VEGEAIVE AND SEXUAL REPRODUTION INEVOLUIONARY EQUILIRIUM

All orgaim are eecte to aportio reource acordigto a optimum compromie etwee te cometig eed ogrowt, maiteace, ad reructio Strawerrie adcoral mut alo acieve an otimum i aortioig reourceetwee two mode o reproductio To alace te cot omeioi, a give ivetmet i eual reroductio would aveto ave twice te prot i oprig o te ame ivetmet

in aeual rerouctio3



S T R A W B R R Y R A M D

Asexual rer oduction clear ly shows a r o over cost as long

as the clone is sr eading When the sread has stoed invet-

ment in asexual rer oduction is still necessar y to maintain the

size of te clone but te only r ot" is yield to grazer s and

ar asites Maximizing clonal size is imortant to sexua r er o-

duction ; te ar ger the clone the more zygotes it can r oduce

At te ame time, investment in exual pr ocesses dier ts re-

sour ce fr om clonal maintenance and must caue a smaler

clona size. The balance between rates of aexual and sexual

r eproduction is assur ed by bot processes r eaching a point of

diminishing r eturn wit incr easing investment

An individual wel within the r egion eld by the clone

woud ave an esecially low rot on investment in asexual

reroduction. Incr easing te denity of genetically identical

individual in its immediate viciit old itnify compti

tion witin te clone Investment in widely disper sed (and

therefore sexua) propagules woud avoid t waste� So cen

trally located individuals would be expected to invet more

in sexual r epr oduction tan would periper a ones. Of course

the twofold tax on sexuality must always be a major deter mi-

nant in optimizing the program of investments. Investment

in sexual r er oduction must not ony be wor th the los of re-

sources from other possible uses it must be wort the cost

of meiosi

THEORETIA EXTENSIONS AND EMPIRIAL TESTS

hoe that te reasoning above will be considered lausibleeven toug it is baed soley on an intuitive visualization ofte genetics and ecology of a oulation of eristent localizedcone tat give o genetically diverse disersal stages. number of imicit assumtions have not been justied. aveassumed that environmental gradient behave in such a waythat a successful genotye's loca tness has a negligible canceof being higer at any sot likey to be reached by the diersal

3 2

S T R A W B R Y R A M D

stage ndoubtedly modes of environmenta variation couldbe roosed in wic nearly identical conditions wit simiar

otimum genotyes coud recur rather frequently Te modelwoud not be valid for suc an environment t would notbe vaid witout considerable genotyeenvironment interaction in detemining tness This second oint is documentedto ome extent below and in aters and 8

Given these two condition te model seems to rooefavorable election of exuaity as a result of negative eritability of local tness. A value in one ocaity i likely tobe a eak value and indicative of lower vaue elsewere. am not clear on weter thi feature is esentia to te modelnoter ossible instance of negative tne eritabiity is examined in hater 5

Te moe is certainly reated to ta roosed in ater2 n its envisioned roe of ex in genotye diversication aa way of adating to new environmental conditions it i obviouy related to models of ongterm evolutionary advantages

Rigoru demonstration of esential dierence in tee ro

osals or of te extent to wich they a all merey secialalications of a genera theory would certainly require mucainstaking work by abe theorists

Te theoretica work is not likey to be done witout reiminary indications as to the kind of theory tat is ikely tohave exlanatory vaue. o desite ogica uncertainies feel

tat te model is cear enoug to warrant examination of theextent to wich theoretial exectation is realized in observation Tis chater wil cose with oe available evidence onte validity of te Strawberryora Model (and to some ex-tent of the idRotir Model ) and wit uggestions ongatering additional evience

Many cro ants so considerable genotyeenvironmentinteraction in the detemination of measurabe characters(discussion and referencs in Baker and Freeman anderkins nviromentvariety interaction often ac

3 3



R A W B R R R A M D

counts for 20% to 30% o te variance. is is not directevidence of enotyeenvironment interction to tis extentin eterminin tness A vrible cracter my in act aveitte inuence on tness and i it does tness may be comlex unction of tat carcter. Tese uncertainties do notinvalidate te assumtion tat mor source of variabilityin a caracter wl often be a major source of variabiity intat caracters contributon to tness. Te freuently investiated caracter yield" must be closely related to tness inte envronments in wic it is measured

ny ed ul of veetatvey reroducin lants tat asosexualy roduce seeds at n areciabe rte cn rovide criti-ca tests of te moe. Clones sould rove to be loclizedwit but imite over between clonal territories Well estabised clones sould ersist or a on tie but wit terrtoeso uctuatin size Ony rarey soud a new clone from asexualy roduced seeln ersist more tan briey.

Undoubtedy te arorite scales o measurement wilvry reatly. Clones o lare ants soud ocuy larger ter-ritories and ave reater ie exectancies tan tose of smalllants. Uniform environments sould resut in arer territories tan eterogeneous ones Mode and reuency o botasexual and sexua reroduction soul inuence clona szeesstence and distribution. or instance tere is ltte orno sexua seed rouction cones may be few �nd widesreaTis in fct as been veried Grant nd Grant 1 9 7 1

Harberd 1967 Secies tat rouce an abundance o seedssoud consist o more numerous and localized cones. Teimited inormation indicates tat tis is true in some areasbut tat averae size of cona terrtory can vary reatly overte rne of suc seces (Harberd and Owen 1969 Harbers tecniues of cona identiction and anlysis ofdistribuions strike me as extremely romisn

3

CHA T R O UR

Th Em-Oystr Md

arlier ruments relate to oranisms for wic tere is noteoretial limit to conl roliferation o a sinle enotye will now consider oranisms tt ve no con roliertion at al. very ysioloicly distinct individual is eneti-ly uniue and cn not be dulicted. t can row but terere rel i exibe limits on attainable size. Tere is also a

time mttion. Senescence reduces ife exectancies for oderindividuas

Desite te dierences in relation to revious radimesI believe tat te essence of te earlier models is still ai-abe. Ems and oysters ve no veettive rerodution butdults are enormously variable in size nd fertiity. More imortant a tyica adult size covers not one but many distinctbitats tt coud be occued by are numbers o comettorsdurin early rowt. Cometition beteen undreds or tousns of seedins or sat in an rea tat can suort onlyone adult is muc te sme as tat between djacent conesof strawberry or coral. Wie teoreticaly elms nd oyster

my die o old ae adult survivorsi is reatly variable andsenescence in ntural oulations is seldom more tan a minormodyn inuence on ae structure Hamiton 1966

Tis cater arues tat te otimum comromise betweenasexua and sexua reroduction n te mode oranisms is zero reuency of te asexual t assumes tat readatationsor rtenoenetic e or aomictic see roduction are ade-ute or teir rai acuisition soud tey become adative.Tis assumtion my often be untrue esecialy n animls.

3



M Y S R M D

NATURAL SLETON AND OMPETTON NUVEILE ELMS AND OYSTERS

Seletin in inpent eul reprutin i reiyiulie fr the lm Mny peple lie ner em n nee them heing ee an ter bere te eeing they

prin up n fe minute ne n ee ine tree tn re with eed mny time mre enely thn ult emul eer eit Te eeing n lly frm lmt lwnf reenery with enity mny rer f mgnitue greterthn tht ttinbl by dut

wu regr te pae nrmlly upie by n utem frmlly nlgu t the nne hbitt in the

Aphitifer el One eelin re el etbliheeletin wil lrgey perte n by the ue e f nen epe f nther but by ne being ighty etter blet pprprite reure n minimie le t prite nrer thn it neighbr niiul re gruly eliinteby prlne debiittin y the pig te eletin be-me mt eterminiti with ne f the few bet gentypelmt ertin t reil hpter 7 reiew ertn htjutify thi iew f eletin in immture elm

The eneti utme f thi intene eletin wul be litteltere by hn n pring gentype repreentd mrethn ne t wl be wteful reuny t t nult ie hbitt with mre than ne welletbihe yunf the me gentype When tree he hunre r a thu-n ee int n re tt n upprt ne ult the wyt mimie the lelih tht the winning ee wil be nef it wn nd t me ther tree i t ierify themgenetilly

Three eent eement in the elm life hitry meeul ee reprutiey intgeu n unt frit eluiely eul reprutin The rt i it gret p-

3

M Y S R M D

utiity f ee, ftr tht permit are munt f

eetin t te ple in ingle enertin nte n pe

22 thi i imiting e f the Aphi tifer MeThe en ftr i the prpe eneti eetiity f the

mpetitin between jent mpeitr Slight ierenein ibility mng eelin n plin me gret ier-

ene in their reltie prpet fr uril n iniiuwin ut er e t ril it ireing ie me it utgrme prblem n grw int ther inluing mpetitinwith mre remte iniiul tht re the itr ferlier mpetitin efre it n reh mturity n em mutpre itelf in enthy uein f elil nihe withierent et f nitin n hlene wu prpetht n enrmu munt f eetin te ple in ne gen-ertin f elm hpter 68) The t f meii i mereyne f lrge number f mjr eetie ftr

The thir eentil feture i the rible but rel eiingn winning ttinble by een the ttet gentype A pef 10 0 meter n be fully upie by inle elm e-rie frm inle ee f the winning gentype f tht gen-type h been repreente in tht pe by hunre eeit wul nt he inree the prie t ll Multiple pief the me gentype wu be wteful multiple pur-he f the me lttery tiet f ine f thi wtegie mre thn twfl nte eu reprutini lwy wrth the t f meii n pmiti ee prdu-tin wul be niteny elete int

Oyter my be mll mpre t elm but their lrere mirpi n thund my ette in pe uientfr ny ne ult Amn enrmu number f mpetitrfr ingle pe me will be lightly mre tlernt f lnitin n mre eetie t pprpriting reure Theywill grw mre rpiy n rw ut their neighbr Muhmrtlty reult frm eeminly rnm pretin but the

3 7



E M O Y S T E R M O D E

FIGUE 4 Simatd compettn between asexay and sex-ay prodced conists on a habitat srace Unshaded areasare occpied by aexa coonists, stipped areas by sexascrosshatched by nether

uter rgram wud nrmay quantify the twdimensinamde by inear scnning and adjacent transects wud nearly redundant. her wud be n advanage ver an rig-inaly linear de.

Fr cmer smulatin Wiiams and Mittn (1973)

randmy scaered ragules n a habitat units ng.Each rague the:n aemted t grw 1 units in each directin Fitnese wer asigned as in the grahic mde abveand cneted rgin awarded t the tt est cntetant. Prgue numbe wee given y Pin distriutin wit te

4

E L M O Y S T E R M O D E L

mbdas indicated Figure 5 ) . t wud aear that underthe cnditins f cmetitin and tness variatin asumedby the mdel the seual rgeny has mre than twice thesuccess f · the aseua when rague numbers in the ttahaitat ae are mre than abut 7 r abut 14 er mi

• •

O7

r

exuals win

Asexuals wnc •uu •g

06'J: ••••

O

5

.

I

00 00 600 800Propague number

FIGUE 5 Proportion o habitat space won by sexa propages( Ps ) as a nction o propage nmber ( in compter sim-ation o the EmOyster Mode Each P is the mean o 40trias (rom Wiiams and Mitton 17 3

mum adut sace. In any uatin fr which the mde isdescritive and this quantitative requirement is met seualrerductin wud have a net seective advantage Parthengenesis wud fai t becme estabished r if aready resentwd be st and an ecuivey seua uatin wdremain.

The mde deas with aseua and eua arent whenevertheir rgenies are in cmetitin. t vaidity is unaectedby whether aseual r eua rerductin is mre cmmn.

4



CHAP R I VE

Othr Mds

hr rmn mny sully rprucn rnsms h n cnfrm ny mels rps s fr hs cher wllel wh nmls h r s mbl hruhu lfe h rmnn cls sscn f sbs, an ssenl fur f llrlr mls, s unlkely wll b my ls mp eplanse as n nvual aan r ll her ccurrences, neclusvly sul lwfcuny rnsms fr nsnc, wllpal hsrcl cnsrns h rsrve sul rprucn when hs cs b p (Chpr 9

Sessl rnsms n h ms freely mble rresn w

ns f a cnnuum Mels vele n rln ssslfrms r hs f sl hs shul be rly cble smwh lss senry frms, r hs f smewhlrr r mprfecly sl hbs In hs chaer I wllfrmlly rr such anmls s srsh a rns s w

rnn n ensv hbas, vn huh mny uls mymv bu ll fr ln prs f me On pln, e myfen n n steas r saste pr le my hve benhere ms f s lf n b h sl survvr n bs nypfr h lcn vn fr such nmls s he c, frs such

s rrrly, hmn hbual swnn rns, nspclz hb rqurmns my mke brhrs an ssrsmr cmpv hn nvuls n rnm frm hpuln, n hrfr an lemn f runncy rucn f enclly ncl srn

Mr relvan, rhs, r lmns n mbly urnvlpmn A c lrv r nwly sl bnhc nvrbrcn b rr s ccuyn he cnr f a lcl nghbr-h (lm war mss r bnhc r) Dnsypnn

O T H E R M O E L S

mrly my pr smwh nepnnly n rnnehbrhs n subjec hr nhbns cmpeve rlns smwh lke hs nvsne n erlr mels nrwn n such nhbrh n nvul rws n lrr n nhb by cmprs h hve prv hrnss n rlr cmns

hs her my be sm plcbly f rler mels such nmls s c n srh, bu hn h h pplc-bly s me, n n sucn epln h clusvelysul rprucn f hs rnsms Sm l fcrs mus prs

FTNESS VARALTY AND SSYPHEAN GENOTYPES

h mls b cnsr r plusbl nly wh hssumpn h selecn n ulns f hhfcuny n-mls, ven frly mle ns, s r nens, n nss muchmr vrbl, hn mny ele wll n nuvly ccep-bl s ncssary h sm juscn f hs ssumnb prv bfre he lc f he mels s presne

wll b scussn rnsms h, l hs lry s-cuss, hv hh ZZ n nly nnssml survvl frmzyg mury he nrmus fecuny erms n rar ms f he lrvl sh r nvrbrs f wr msss nvbl n reln h squnc f eclcl mnsh mus b m bfre mury s reche h ppulancul prss ven f nly sll frcn f hse lrve hnys h wul erm survvl hs selc fw wulcnsu genet ete n Dbzhnsky's (9 rmnl-gy I ws n reln sus f lw fcuny Dsphlh Dbzhnsky sule ec le s mr crl cncp fr rnsms wh a hh ZZ.

enetc ete my b an unfrun rm rfrs vl scnc cnce h s v f mrl r scl sncnc hs my n reven sme lymn frm nn s m

5



O T H E R M O D E L S

ornce o iooiss nd usin his oservion s if i werescienic suor for rcil eiis hiosoh. Before i ecomes eer esishe I would lie o sues susiuinhe erm yphean genotype

Sisyphus r epeedly pushes bouer up seep sope unl

on he vere of rechin he pek i oes ou of conro n

rols o he oom in. Anoousl n inividu in he

op end of he ness disr iuion hs chieved is ner mxi-

mum of ness b n onl momenril eecive cominion

of eneics nd individu hisor. The necessr il ow heri

biity of such tness would pr obay rop that same genotype

down into the range of mediocr ity in the next generation.

Extr emely high tness would have to e r egener ated y some

new combination. A denition of sisyphean in my dictionary

( Webster's New International, 1 923 ) is "requiring coninuous

redoin."Sisyphean tness is a relationship between a limited set o

genotypes and a par ticular succession of environments en-

counter ed during deveopment. Dobzhansky proposed that any

indiviual more than two standard deviations above average

be recognized as elite. I will use the term sisyphean in the

mor e extr eme sense of individuals of many times the average

tness The existence of such iniviuals follows from three

common assumptions on ftness deter minatio: ( 1 ) many

ier et genes contr iute to variation in tness dosage, which

can be regarded as continuous and normaly distriuted ; ( 2 )tness dierences per locus ar e in the range of one to ten

per cent; ( 3 ) dosage contr iutions are functionaly indepen-

dent and multipicative. Uner these conditions tness would

be a highly skewed lognor mal distriution, and an individual's

ness would e roorion o

= +:·

where is reroducive vue he zoe se nd is is ness dose. he erm a woud deermine soue


ness nd reroducive vues n he re of increse or e-crese of he oulion while b ou mesure vere erures from muiicive cominion. I would e ess hnuni nd reuce he vrince of he isriuion if here erecomensor relions mon ness conribuions hresholdsof dequc nd similr inercions row's (1968) discus

sion suors he commonness o snerisic inercions hwoul rise he vue of b he snheic lehls" of Kosudnd oriwi ( 1 9 7 1 woud be ood exmles

This discussion rises he issues of eneic od cos ofnurl selecion nd reled mers h re currenl einwrml debed nd would e imossile o re equelin few rrhs. Reers unfmilir wih hese ssues mconsul such references s Kimur nd Oh ( 1 9 7 1 ) n Wllce ( 1970) he osiio en here is h a cn e s res is necessr o ccoun for he ersisence of he oulion

(he densideenden form of sof selecion". he fcorb m liewise be less hn uni (s in hreshold models ofsof selecion bu I will ssume h funcion indeendenceof ness conribuions nd consequen hih vrince in ness is enerl rue

he conce of hreshold selecion (Kin 1967; MnrSmih 1968; Sve 968 m nd some convincin exm-es in sensor mechnisms I is lusile h n lms erfecl nsimic ens coul be roduce wih rher lowminimum numer of fvorl sleced enes h ec lenssmmer A somewh smller dose m rouce severesimism wih serious reucion in ness. Wih his ndof cnlizion of nerl oiml chrcers mos of he un-fvore enes h re eimined woul e los lon wihoher unfvore enes. Selecio of iven inensi wourequire lower morli hn if ness were mulilicive.

or ohe chrcers esecill for hose wih oim inni or zero nd for relions beween funcinll dieren

chrcers muilicive relionshi is es s lusible.

4 7



O T H E R M O D E S

In prmtve ma, visual acuity, malara resistace, intelli

gence, eetness, and fertility must have varied largely inepen-

dently and aected tness in a multiplicative way, and each

of these chaactes may be regare as a complex of several.

For instance, resistence to malaria must be detemied by

several lagely indepedent physiological ad behavioral char-

acters When the data are adequate to distinguish the two

ossibilities, quantitative chaactes are often foud to have

lonomal rathe than omal istributios as would follow

from multiplicative inteaction (Bliss and Reiner, 1 964 ; Ker-

foot, 1 969 ) . Bliss ad Reinker proposed ecological factors and

Jackso ( 1 970 ) developmental mechanisms that would make

lonormal dstrbutons the eneral ruleThe assumton that comlex adate characters n nature

are wdely arable n the conbts t tess s abudantly usted by efomance data hee s no edencethat adate eformance mechanca strength dsease resstance etc. ) ee show commoly acheed but eer eeededmaxma as would be mled b threshold slecton Such data fact may show oste skew few ndduals may suea stress fo seeal tmes the modal duraton Hgh aranceand oste sew on oe mortant eformance statstc fetlty wll be documented Chater 8 genotyc selectoncoecet must be a summary of erformance scores an fndual scores are hghly arable the mea

or other eneral summary should be ee more so

Curent norance obously ermts a wde ane of onon o the nature and extent of tness arato n aturebut there can hardly be ay suort for the dea that thereare no genetcally and fuctonally neenent contrbutosto tness Een f oly a small oorton of the combedeects are multlcate they could stll generate an aroxmaton to a logormal dstrbuton wth cosderable osteskew an ales (1965 statement that tness sknown to be neately sewed wth a secondary mode at

8

O T H E R M O D E S

lethalty ad sterlty must relate to the hysolocally otmzed and edator free eronments of laboratory stocsn the wl wth atual mortalty sucent to ee the oulato n hec assume that most of the ndduals VaValens rmary mode would be shfte to the cty of thesecondary

I geotc tess n ma or rosohla s detemnedartl b multlcate teractons

_the same must be tue to

a greater extet orgass such as starsh that deelothrough a successo o ecologcal ches Ftess baralarae ad mm mm ad mm ueles admm adult stash eures derent ds o adatatosad ther geetc bases should be atl deenet thcolete deedece ad as the obablt o sugoe stage the robablt o surg stages would be Ths roduct would be lonorma dstrbuted ee

the seaate s were notFgure 6 s an ntentoall extreme ew of how zyoteto

adult ablty erhas the maor comonent of tness)mght be dstrbuted n a hhfecundty oulaton at eastmllons of zyotes e adult) To regard an nddual wtha sural obablty of less than one n a hunded thousaas lethal would be consstent wth conentoal usage and wththeshold selecton models that hae been roosed On thatbass we can egard the whole sble dstrbuton Fure 6

as showg only lethal geotyes ables whch wll account

for nearly all of the next roud of reoducton all le othe grah beyond 10• Chance largely determnes whch oneou of hudreds or thousands of these ssyhean enotyes

acutally sues a eroduces.The aldty of ucomn argments does not deed on

the logormal ben closely descte of tness dstrbutonWhat s eured s that tness hae hh aance and osteskew and that reoducte success deends on hang someosrng of many tmes the mean tness The subseuen




10 - 1 0 9 0 8 0 7 10 6

PROBABLITY OF ZGOTE O� DT SU RVIVA

FIGURE 6. Possible distribution of viability in a hig-fecundity population A dierence of one standard deviation in genetic

tness dosage causes a tenfold dierence in viability. Such

viability variation would result from approximatel the follow-

ing conditions: 2,0 loci contribute to variation in tness ;

optimal and suboptimal genotypes at each locus dier by .0 5

in viability; probability o suboptimal genotype at eac h locus

is 0 1 0 adjustment for density dependence of mortality (the

term a defned on pages 46--47 ) is 95.

apes on seetion in igeundty populaions wil provide arguments and evidene in suppor o ese assumpions

For te moment will leave is disussion and proeed wtmodels o seletion o sexuaiy in motile marine anmals

THE TRITON ODE

s generally agreed a sexual popuatons are more ikelyto survive anged onditions tan asexual ones suspet ats is true bu or reasons dierent rom tose ommonlyassumed ( Capters 1 2 and 1 3 ) Regardess o te nature o

5 0


te advantage o seuality i its strengt s suient to pro-due a major eet n one or a very ew generatons it abe regarded as a maor ator n seeton among indvduaso a popuaton suggest ere tat tere may be popuationsin w seleton is so strong tat a sexua indvidua beauseo te evolutionary potentia o its neage may ave more

tan twe as many immedate desendants as an asexualSu popuations may b ommon in salow tropial andwar temperate seas and a triton (ymatum may be agd exampe

A triton is a arge gastropod tat sares e olowing araterists wit many oter moie enti nvertebrates smovements as an adut may be onsiderabe on a loa salebut on a art o a maor par o te oean an adut abitaan be represened by a pont y onrast its enormous num-bers o young are plankton or many monts and oean

urrents being wa ey are is implies dispersa or undreds or tousands o klomeers is dispersa an bestrongy direional beause maor urrent systems run in on-sisten diretons Larvae originating n one loalt are arriedaway and may seldom partiipate in restoking at oaity

emograpi impliations o tese longdistane dispersastages are disussed b Seltema ( 9 1 ) Observations onrates o deveopmen and on te distribution o developmentalstages in te Nort Atanti ompe te onusion tat dispersal on a maor geograp sale reguarly takes plae Adulttritons o Florida may ave oiginated as zygotes ar to tesouteast in te West ndies Zygotes produed in Flrida mayrea adutood mu urter downstream" in e arolnasperaps Sexual reprodution in Carolina may onribute ote stoking o urope and te Mditerranean Te likeoodo transoeani dispersal is one o te man pons o Sel-temas dsusson He reasons tat te Gu Sream is an agento westeast and te tradewind driven euaoral urrent anagent o eastwes ispersa

5



O T E R M O D E L S O H E O D E L S



O T E R M O D E L S

rents o oastal embayments e neigorood olonized inwi an individual develops to adultod an be large andis olonized by te young o a large number parentsroters and sisters onstitute a negligible ration o a givenindividual's ompetitors

e extensive movements o an adult od do not inalidate

e neigbord onept Migrations are yli and residentso a given neigborood move togeter and usually returnto te same spawning ground year ater year (Harden Jones1 968 ) A spawning stok may be ysially reognizable bysermen wo speak o spring raes" summer raes in-sore and osore stoks et Wynnedwards ( 1962 )amassed a great und o evidene in upport o te lolizedbreedinggroup onept or a variety o animals would dis-agree wit i s assumption tat ese egborood gups onstitute populations in te geneti sense

Coloists settling in dierent neigbroods must alreaybe onsiderably dierent ey are a emnant ew at avesurvived te speial pysial onditions patgens and pretor pressures o te water masses at ave brougt tem todierent neigboroods Ater establisment in a neigbor-ood only a tiny ration will survive te speial allengeso tat loality and rea maturity. Penotypially and genei-ally te adults o a given neigborood are uniuely distin-tive not beause tey are reprodutively ioated rom oterneigboroods but beause seletion is suiently intense o

generate te distributions anew or ea generation videein support o tis interpretation is presented in Capter

Mating between neigbors tereore means tat an individ-uals mate will usually be more similar to itsel tan it wouldbe i seleted at random rom e population Su assortatvemating produes progeny more variable an teir parensbeause similar parental penoypes may ave been based ona variety o genotypes is latent variation is ten expressedin ospring reombinations otatie atng may not be

5 4


an entirely appropriate term beause it normally implies ative mate seletion bu e result o te penotypi similarityis e same weter it arises by ative disrimination or teenvisioned imits on mate availability e ospring are morevariable tan eir parents and more variable tan wouldbe produed by asexual reprodution Pollen vetor beavior

may result in penotypi assortative mating in plants (Levinand erster 193 )

A simple and exreme example o assortative mating ayelp lariy te idea r tose not well versed in uantitativegenetis Suppose a population as a arater tat varies disontinuously rm 2 o +2 wit only integral values beinssible as in arge an enzyme moleule ariatio isompletely determined by variaion at two loi o two allelesea and all gene reuenies are 05 Genotype reueniesare in HardyWeinberg and linkage euilibria elations be

tween genotypes and penypes and relative numbers ogenotypes are as ollows

notyi zygot g noty ndv s r tiv nbrs

AABB ) AaBB (2), AABb ) AAbb ) aaBB )AaBb (4)

A bb ) Bb ) bb )

ese zygotes are disributed at random among many neig-

boroods ea o wi permis only one unpreditable penotype o survive Table 3 analyzes ree possibilities or repro-dtion among te survivors asexual reprodution randommatin in a pool o individuals rom two neigboroods andmating entirely witin neigboroods All maematiallynonredundan possibiliies are swn Ospring variabilityrom witinneigborood main is always a leas as greatas rom eiter o te oter orms o reprodution and is usually greater Wat appens is tat asexual reprodution merelyepeats watever variabiliy ere is in e parents Sexual re

5 5

O T H E R M O D E S O H E R M O D E S



O T H E R M O D E S

produion repes prenl penoypes plus oers exep

or ompeely mozygous neigboroods e ming n

be beween neigoroods inermedies end o be produed

is endeny oes no our wi wiinneigborood

ming

n nure nong pprong is exreme exmple ould

be expeed Evey neigborood would onin onsiderble

TABLE 3 R esu lts o three modes of reproduction aft er n eghborhoods peci c s elect on

Parental ph enotype d emaned spring phenotypc v ari anc e

by by from fro m fro m atng�e anoh er as exu al rando m w thin

locality loc alty reproduction mating loc alites

2 2 0 0 0

2 1 . 25 38 5

2 0 1 84 1 33

2 1 2 2 5 1 3 2 50

2 - 2 4 2 4

1 1 0 5 5

1 0 25 71 84

1 1 1 1 1 . 5

2 2 .25 1 3 8 2 5

0 0 0 . 67 .67

vribiliy nd nly pr o i woud be geneily deer

mined Crow nd Kimur ( 1 90 1 55 ) lule n inresein sndrd deviion o bou 3% i bo eribiiy nd

beweenme orreion eul 0 e 05 my be oo ig

or ypi wiinneigborood orreion Perps 1 %

would be more resonbe esime o verge inrese in

vribiiy per rer wi populions su s ose posu

ed in e model Perps is is enoug wi lrge numberso su rers onribuing o ness Ming wiin

neigboroods wuld provide e nex generion wi greer

5 6

O H E R M O D E S

vribiiy nd ereore greer numbers in e sisypen

rnge o ness

e rgumen gins pusibiiy on niderion o proper

ies o igy skewed disribuions su s igvrine

ognorm m indebed o J S rris or pien insruion

in properies o e ognorml disribuion Noing

ve proposed woud er e genei ness dosge or ge-meri men o ness bu even wi onsn geomeri

men e rimei men o ognorm disribuion is

doubled by inresing e vrine by e onsn 2 n2 or

bou 4 is e rimei men is sruinied by sele

ion is or ws operive in simulions o e Em

Oyser Model Assignmen o ness dosge ws unbised nd

e geomeri men o ness ws e sme or sexu nd

sexu progenies Ye e greer vribiliy o e sexuls

gve em greer rimei men o ness s indied

by greer oupny o bi speFigure sows ypoeil lognorml disribuions -

ness or sexully nd sexuly produed progenies A ve

e sme men o genoypi ness dosge bu dierenes in

vrine use dierenes in men ness Noe wi in

resed vrine in ness (inresed inensiy o seeion)

disribuions diering by or o wo ome resembe

e oer more losey e greer e vrine o ness

e esier i is or ssorive ming o double e rmei

men by inresing genei diversiy

e onusion olows seleion my suppress prenogenesis in erin kinds o igeundiy popuions be-

use e vrine o sexuly produed ospring woud be

indeue or genering e sisypen genoyps on wi

gene surviv depends e rguen pplies o popul-

ions in i ming is so ssorive nd seeion so inense

prenogenesis would produe progeny wi ness

vrine mre n 4 unis below o sex progeny

ness is redy igy vrible 4 my be sml pr

5 7

T H E R M D E L S T H E R M O D E S



4

"

,

,

T H E R M D E L S

Vi

=

1 .2

5

= 2.50 - - - - -

W

= 2

5

' = 5.00 - - -

W 5 0 V

= I O.O O - - -

I 2 3 4 5 6 7

MULTPLES OF GEOMTRC MEAN OF FITNSS

FIGURE 7. Doubling of mean tness by increased varianceof tness dosage ( Cod-Starsh Model) All distributions havethe same geometric mean (same arithmetic ean of tnessdosage) . Paired distributions dier by a factor of 2 i n arthmeticmean and by 2 In2 in variance

of the otal varince, and mathematically ony minor dier-

ence eween the two modes of reproduction

The argumen has det with characterisics o the popula

tion s whole, but does not depend on he success of one

populaion in reation to another t is not a groupseection

argument Al of he frequency distribuions for groups are

formly valid nd have their entire bioogical signicance as

proiity distribuions for individuals

5 8

T H E R M O D E S

COMPARISON WITH OTHR MODELS

te modes proposed earier in is book an asexualy

produced iividua was uikey o be of sisyphean ess

because eve if i had a wini genoype ere woud prob-

ay e other individuas of he same genoype with which

it would have o share the winnings No such special within

progeny compeition is operaive in the CodStarsh Moe

Here an asexuay produced individua is less ikey to have

a winning genotype The modes are no mutuay excusive.

f sperm or poen ranspor is much shorer han larv or

seed transpor such organisms as oysters and srawberries

coud conform to te Triton or CodStarsh Mode

The modes al operae y sexual reproducion generating

a variety of ew genoypes afer seecion has produced a gen-

eraion of specialists for a paricuar sequence of environ-

mentl conditios tha hs a negigible proabiity of recuring

for the ospring Tus all show forma simiariies to those

in which sex is proposed as a ongrange groupreaed adapa

tion They mere poin out how certain kinds of ife istories

may give the proposed benets a hithero unsuspeced impor-

ance in a singe ife cyce This is especiay true of Maynard

Smih's ( 1968 ) sugestion hat recombinaion is of vaue

mainy when organisms from dierent populaions of he same

species invade a new territor Colonists may be al AAbb from

one population and aaBB from another It may be tha ong

term survival is then possie ol if mos individuals have

at eas one A and one B The requisite genoypes would be

produced immediatey y sexual reproduction They woud

probay not have time to be produced at al b asexua My

suggestion is that this sor of advange, given cerain lifehis

tory feaures can assume grea imporace in singe ife

cyce

Maynard Smiths ( 19 71 ) reasoning on sex as n individual

adptation is menioned briey in Chapter 1 . He found no

5 9



H O R Y



C H A P T E R S I

Natural Selection In

High-fecundity Populations : Theory

Ths chapter oes a pror reasons for beleving that te

ntensty of seleco n a opulaton as a postive relaton

to ts fecudity Chapters 7 and 8 oer emprcal evdence

for the same conclusion. Both arguments and evdece relate

mainly to organsms that have a hgh ZZI as a result of adults

beng hghly prolc. So the �a relevance s to Chapters

4 ad 5 The proposton that n tese organsms a tremedou

amount of genetc cage ca occur in a single generation requres specal substataion I assume that o secial sup

port s needed fo the dea tat consderable genetc change

can occur n a single lfe cycle that cludes a long perod

of competiton among clones

For purposes of dscusson I wll dvde the spectrum of

fecudty nto three ranges Lowfecudty organsms re tose

wth fewer tan 1 03 zygotes per average adult female lfetme.

Those wth between 1 03 and 10 lifetm output are of

medum fecundity Hgh-fecundty organsms have more tan

1 06 zygotes per adult female Fertility wll refer to indvida variato i producto of young at the stage of tal de

pendece from parents ( Capter 8 ) .

� It is far to say that current nformation and tinkng on

ecologcal genetcs are based towards low-fecundty orgasms :

mammals brds frut ies and other nsects, crop plants and

weedy auals. Until recently tere was litle informatio on

te opulaton genets of ig-feudty organsms : lage

trees with small seeds, large shes and invertebrates wit small

2

eggs marosop lower plants wt mrosop spores Ibeleve tat t s only i tese organsms ad n tose n wloal proleraton o genotypes an take plae tat sexualreprodutio a be adaptve and urrently i evolutionaryeulbrum wt asexual I beleve tat evolutonary teorsts ad ot bee so preouped wit loweudty orga

sms wit simple lie yles tey would ave long ago seete sigae o sexualty

FEUNDITY TE STRUGGLE FOR EXISTENE ANDTE INTENSITY OF SELETION

Seleto relaton to eundty an be approaed stru-tively by orgetting or a momet te abstrat genet meaningo tess and osiderng t as an immaet pysologal

proerty o a orgasm in relato to immedate problemsI we take a large smle o a populaton and subet t toa severe stress we may rea a ot at w al te sampleas suumbed Almost ertinly tere wll be some geetderee betwee te dead ad te lvg Ts s te sorto tg most biologists wo are not teoretial eetiiststink o as dieretial tness

I te stress did ave ts geneti bas t a be desrbedas a seletive evet Ultimately te rate o seleto s determned ot by absolute tme or by generatons or by idvdual

deats but by te ux o seletive evets Were tere are myseletve evets per geerato seleto wll ve markedeets one geerato As a example supose te erapsunlkely propostio tat uvele dets Plestoee maand od were eually seletve geetlly In ma perapsal o omal brts survved to puberty Te mortality anbe attributed to a seuee o stresses ea o w removes10 o a ge oort It ould take su stresses to produete reuisite killg ow supose tere is a geotype tat as

3



N A T U A L S E L E C I O N

PROBABILITY OF

H E O R Y



PROBABILITY OF

ESCAING GETIC DEAH

10- 10 9 107 105 103I i

AR

n

YEAR

n +

103 10 109 107 105

ZYT- MAURT Y SURVIVAL

FIGURE 8. Interaction of genetic and enironmental vaatnin producing dierences in yearclass strength in a highfecun-dity population. Values on the upper scale are a hundredtimes greater than those on the lower to reect a high fre-quency of random mortality Genetic variation is shown bythe spread of the cure and is assumed to be similar eachyear Variations in habitat suitability are indicated by shiftsof the entire cure along the surival axis

7 0

s normally distributed, survivorship would have a lognorma

distribution. Examination of published data, which unfortu

nately seldom provide large samples of year-class values, gives

some support to the proposal that these vaues have lognormal

distributions (Figure 9 ) . Southwood ( 1 967 considered tho-

4

= .

,

) 1 0

YEAR - CLASS S IZ OGARTHM OF YAR CASS SE

FIGURE 9 Frequency distrbutions f yearclass strength nmarine shes The normalizing eect of logarithmic transformation supports the inferences of (1) functionally independent(multiplicative) eects of environmental factors in determining survival (2) a lognormal distribution of environmental suitabil-ity, and ( 3 ) lack of canalization of the character tness

Top cuves a rom measurements on a grah publied by Graham( 956) Midde curves are from data tabulated by Clark and Marr (1 96) .

Bottom curves are rom measurements o catches o 8 to -yearoldsgraphed by no ( 1957 ) Two o te data oints are omitted rom telogarithmic ot or the sardine hey are or year cass olowing t e"colase o the opulation and is repace ent by an anchovy eseyea casses would lie a to the let o the distribution shown e transormation ehizes the extraordinar ature o this coap

retical aspects of regulation in widely uctuating populatons,

and found that permisible uctuatons are related to fecun

dity, although gret numerical variation is possible with ZZI

as low as 50.

7 1



T U R S E E T I O T H E O R Y



remnan od poplaion is apable, vry w yars, oproding normos year lasses

Oldr vnils o yllown na ar also larg enog oener e sry, and ven avragsize yar lasses may balmos omplly rmovd beore y av ime o mare(avido, 1965 ) r is no sggsion a railmen

o zyo prodion as any advers on nmbrs oyllown na

Csin ( 19 1 ) rnly prodd a ogprvokinganalysis o e sokrerimn problm Maniold variaionin rrimn rom a givn sok siz is nivrsal in all spis, b Csing ond a by ombining daa rom manysdis o a given speis old g averag rlaionsipso som signian Rrimn is posiivly orrlaed wiparn sok siz in spis a rod mr osands orns o osands o egg per male pr yar For sis a

ommonly lay eggs in e ndrds o osands, sok andrrimn sm ompleely indpeden For spis wiendiy in millions, s a od and · na, a ngaivorrlaion boms apparn vidly r is so ovrompnsaing densiydepndn in s igndiypoplaions. n my view disapparan o posiiv orrlaion bwn ndiis o 0 and 0 ( rogly 0 o0 pr mal liim) domns ransiion rom sliglyarkovian o nonMarkovian poplaions

wold b o gra val o arry o s sdis as

Csings wi or ses and or grops o oranisms alewi is only a mdimndiy s, b rown ( 19 2 )ond slig ngaiv orrlaions bwen is sok siz andrrimn ovr a riod o svral yars Harpr ( 1966 )ond a s prion and rrimn in mdimndiy poppi wre largly indpndn, b a ras som ndny or inrmdia lvls o sed prodiono prod rar nmbrs o reris

n old adag among mirobiologiss olds a all possible

7 4

miobes are laen vrywer, and all one nd do is spplya rain envionmn and appropriae mirobial spis willappear in appropriae nmbrs Van der Pi l ( 969 sggessa is idea may be appliable, wi obvios limiaions, oproli igr plans wold also sgges appliabiliy, noonly o speies omposion o a ommniy, b also o

genoypi omposiion o a speies A given nvironmen willsele is sisypan ew rom e vas pool o availabl gnoypes Gne renies o ese sle w may prove iediren rom os in original pool ivrsiaion ognoype among widesprad propaguls produes agmndnmbrs o sisypans and is spially adapive in nonMarkovian poplaions

THE SEARCH FOR EVIDENCE

e proposiion a igndiy organisms ommonlyexperiene grea gnei ange in a singl generaion is obvi-osly i no always asily, sabl by daa rom ld and laboraory Masres o adapive perorman in lm seedlings,oysr larvae, , sold sow onsiderabl individal varia-ion e eviden sold sppor e assmpion a diern gnoyps av markdly diern liklioods o srvivinga given pisod o srss or o xploiing opporniies Pysiologially masred inbreding deprssion sold b onsiderabl Rsponseosleion xprimns sold gnra gra

angs in a singl gnraion No only sold slion ora given arar b abl o aomplis signian progressin one gnraion, b indir sleion rgims sold alsoas signian ang For insan, progny o pairo oysrs raisd in nvironmns a dir in mprare,saliniy, ood organisms, kind o prdaors, sold sowmarkdly dirn gene and gnoype rnis a som loiar ig moraliy sags ar passed

ndividals rom wild poplaions sold b ond o dier

7

N A T U R A L S E L E T I N

C H A P T E R S E V E N



greatly in measurable kinds o adaptive prormane For instane tere sould b great ertility variaton Field studieso igeundity speies sould sow marked sits in genreueny between loalties even wn gene ow is so greatas to approa panmixa Environmental utuatio in timesould b losely traked by gnet anges among nabi

tants o te anging evironment Tis should be espeiallyobservable among annual speies at ig latitudes erentyear lasses at te same loality sould sow dieret geneand genotype reuenis Te amplitude o geneti utuaton sould parallel tat o environmetal utuation Wtina year lass at a singl loalty markd departures romHardyWeinberg euilibria sould araterz som loi Tenext two aptrs summarze evidene on some o tese points

7 6

C H A P T E R S E V E N

Natura Stn n Hh-Fundty

Ppuats: Evdn n Vabty

Tis apter presents two kinds o evidene on te generaliyo large tness dierenes in igeundity populations Terst douments individual variation in pysiologial measureso vability in stags wit eavy mortality Survival must beinuened by te genotypi omponent of tis varability andtis inuene ould be elt many times during te developmeno oort troug igmortality stages

T more important kind o evidene relates to genetigradents in relation o dispersal nearby loalities sow

marked dernes in gene reueny in a widely dispersedspeies it mst mean tat powerul seletion is operatng Tesam onlusion ollows ro geneti variation among ageoorts at a single loality

VARIATION IN ADATIVE ERFORMANCE

Tere s a large mass o poorly doumented senti olklore tat bears on variation in pysiologial measurs o viabil-

ity n gmortalty stags Tose wo grow seedlings or sry ommonly nd great dierenes n siz and ter super-ial signs o vigor any onsidrable raton o su variation as a genet basis great genotypi variabilty in tnssmust be reunt ndiations o te geneti origin o muo te variation in vigor are dsussd in Capter 8.

Rently te progress o siz variation and mortality asbeen observed in dtal r experimental platings and on-rmng evidene gatered or wld populations Te data re

7 7

N A T U R A L S E L E C T I O N

l i f l f ll h f

E V I D E N C E O N .V I A B I L I T Y

li Ch i l i i f h h i b



late to a variety of plants, from small hers to forest trees

The account below is a smmary of the work of Koyama and

ira ( 1956 ) , Bliss and Reinker ( 1964) , Stern ( 1965) , Risser

( 1970) , Hett ( 197 1 ) , Hett and Loucks ( 197 ) , and especiallyWhite and Harper ( 19 70) and Ross and Harper (1 972 )

Seeds and seedlings commonly show an approximately nr-

mal size distribution and modest variability. In nature, andin crowded experimental plantings, variaility increases with

age, and the distributin grows more askew. The asymmetry

gets so great that Koyama and Kira speak of an L-shaped

size distriution. The high variability and skewness result from

amplication of what are originally slight dierences in indi-

vidual vigor and in the local level of crowding. An individual

that has a slight initial advantage, in the occupation of what

Ross and Harper call "biological pace, can use that dvan-

tage to win additinal advantage

During growth of an age cohort there is steady mortality,with the rate per unit time decreasing as time passes onsis-

tently it is the smaller individuals that suer heaiest loss This

conclusion is supported by direct obsevation, and White and

Harper calculated that a steady culling of the smaller individ

uals must e assumed to account for the observed changes

in size and number through time The cometitive relations

during development and the size bias in mortality are pre

cisely those postulated for the ElmOyster Model The nal

survivors must e those at the top o the dstributions of both

general individual tness and of haitat tness for the individual The size dierences also have implications for fertility

•

variation, which is discussed i the next chapter

I am sure that the intuitions o oystermen and sh culturists

would support the generalization that similar develpments

in size and mortality are characteristic of crowded groups ofjuvenile nimals, but I know of only one careful study Rose

( 195 9) showed that size variation rapidly increases durig

tadpole development and that smaller individuals suer

7 8

greater mortality Chemical contamination of the haitat by

the larger individuals was the responsible factor Populaton

densities in natural tadpole habiats are great enough for the

eect to be important in nature. Comparale phenomena

among shes of open waters must have some other immediate

cause

Besides the steady attrition often seen in a develpingcohort, there are sometimes mass mortalities, such as "damp-

ing in a tray o seedlings, or comarale calamities among

sh fry The mortalities may result from fungal or acterial

inestations or physical stresses that kill the great majority ut

leave others apparently unaected If even a small fraction

of such deaths are inuenced by gnotype, such an event could

greatly change gene frequencies in an age cohort Yet there

culd still e thousands o individuals left from a single pair,

and this group could be subject to many more selective events

before maturity

GENETIC LOAD IN HIGH-FECUNDITY POPULATIONS

Absence of a relationshp between fecundity and selection,

as implied by those who claim that heavy juvenile mortalities

are nonselective, implies that selectivity f death at a given

ealy developmental stage must be quite low in a highecun

dity populatin It would be expected tat demonstrably low

viability genotypes, or any indication of inbreeding depression,

would e harder to demonstrte at an early stage of development in a highecundity species On the other hand, if

deaths are as selective in highmortality stages as in others,they should show n great uniformity in measures of viability

Crumpacker ( 196 7 ) reviewed vidence of genetic lad and

inbreeding depression in a great variety o plants and animals

of widely variable ecundity There is no indication tht low-

viaility genotypes are inrequent in the higher range o

ecundity Most of the evidence relates to cultivated foms

7 9



N T U R S E E C T I O N

one or anoter or bot o a pair o simlar substanes maybe present in a single individual in parallel wit expeted

E V I D E N C E O N V I B I I T Y

are transported by oean urrents rom one to several montsdepending on temperature and transport or undreds okil t i ( M t 1965 E i t l t



omo and eterozygotes Penotypi proportions in a sampleusually approximate a HardyWeinberg distribution Similarenzyme variants an be sown to beave as Mendelian unitaraters n rosopila and oter organisms t s reasonableto assume tat ea substane is te produt o a partiularallele at a unue lous Given adeuate samples it is a smple

matter to estmate a gene reueny o say od at a givenstation on te Norwegan oast and to ompare it wit smlarestmates rom arter nort or sout or rom oter timesat te same loality

A onsderable mass o normaton s reviewed by Ligny( 1969 ) Te best studied spees is te European od orw Mller's ( 196 9) map o emoglobin rueny nortern Norway is sown as Fgure 10 od egs and larvae

7

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7 °

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2684

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• 8

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91

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r; , 269• 84° 8° ° 26 " · °

.•

F 1 0 Freqencies o cod blood type E o northernNorway (rom Mer 1

8 2

kilometers is ommon ( Marty 1965 Even i te later ve-nile and ault stages were ompletely sedentary we mgt wellexpet gene reuenies to ange but little over undredsperaps tousands o kilometers n at tey an be strikinglyderent n mu less tan 100 kilometers e steepness ote gradients an only be eplained by postulatng large ( 10%

or more) onelous dierenes in seletion oeients betweenloaltes Maniold wolegenotype dierenes must be ommon Many similar examples are reviewed by Ligny and oasionally tere is evidene as to wat environmental atoris responsible or te seletion Jonson ( 1 9 1 ) or eamplesowed a temperature dependene or an enzyme poly-morpsm o a blenny

t is usual or sery biologists to attribute genereuenydierenes to spatal solation o stoks and t is stok denton tat motivates te studies at te dierenes are main

tained by adults o dierent loalties sows tat neigboroodgroups do remain separate as reured by te odStarsModel Tis is all a sery bologst needs to know or stokdenition A populaton genetist needs to know more Geneti dierenes between lalities reet te ont ation oseletion and isolation Any deieny o isolaton at any stageo development an be ompensated by greater seleton pressures in mantaning a gradient Wt adeuate seleton anyderene n gene reueny ould be mantained even iadults were only partly isolated and te young not at all

Lak o appreiaton o te power o seletion in a geundity population led Mller to wat regard as an untenable onlsion He noted tt nearsore and osoresamples dered onsistently in gene reeny despite teoten sort ditanes involved Tese dstanes seemed so minor n relaton to te dspersal potential tat e reaoned tatonly an intrinsi solating meanism ould aont or te

8 3




wide dispersal ere may be some acors operaing o preservee geneic ideniy o local socks Unorunaely or is in-erpreaion ere i new evidence agains any geneically con


viewed by Ligny ( 969 ) and are inerreed as evidence omixing o dieren sock ierences in elecion pressureson dieren age coor is an alenaive explnaion year



erpreaion ere i new evidence agains any geneically con-sisen local ock Williams Koen and Mion ( 1973 swed a newly arrived elver a some o e localiiesdered signicanly rom older residens Unpublied addi-ional nding ow a elvers arriving in dieren year oreven a ew week aar in e same year may sow dierences

comparable o ose beeen localiies undreds o kilomeersapar Clearly e recrui o a given coasal localiy are genei-cally eerogeneous ariaion among successive groups o re-crui mus reul rom dierences in elecion presures indieren waer masse a deliver em o e coas

eides e abundan evidence on ic Scmid ( 9 25 )based is onepopulaion eo re are oer supporingobservaions ladykov ( 964) repored a norou gradi-en in sex raio; norern pecimens are mainly emale ou-ern ones male ere is no geograpic variaion in umbers

o verebrae or n rays (Wenner 1 97 ) i almo alaysound in widespread es ( Jenen 944) i means noonly a ere i no srong localiypecic selecion ormeriic caracers bu also a residens a widely separaedlocaliies mus ave ad eir earl developmen in e amecondiions i well known a dieren emperaures andsaliniies during early devlopmen produce dieren merisiccaracers in geneically imilar socks e onepopulaioneory can be considered more rongly suppored now anever beore

Tere are no oer genereuency comparion among agegroups o es bu ere are comparions beween izegroup Fujino and ang ( 1 96 ) ound slig genereuencycanges ad marked decrease in eerozygoe exces beeenuvenile and adul ize o skipack una Onelocus nesdierence o pera 20% or a racion o e lie cycle arendicaed Several les exreme izegroup dierences are re

8 6

on dieren age coor is an alenaive explnaion yearclases are ound o dier rom eac oer bu o be conienroug ime i would uppor my inrpreaion o igmoraliy sages being e one in wic mo o e selecion akesplace

Sudie o singlelocu polymorp im in loecundiy

organisms oen indicae eerozygoe advanage Selecion oriypean genoype would mainain polymorpisms by re-uency dependence and environmenal eerogeneiy Heerozygoe deciency raer an exce i expeced rom isind o eleion i ere i ever any mixing o dierenlyseleced groups even o dieren age coor A expecedere are many convincng example o eerozygoe deciencyin marine se and very ew o eerozygoe exce (Ligny1 969; Mler 969 )

LOCAL VARIATION IN REATION TO DISPERSALIN OTHER ORGANISMS

Scop and ooc ( 97 1 ) oed a cline in gene reuencyin an ecoproc along e souern New England coa wimarked dierences wiin 10 kilomeers ey aribuee dierences o an isolaiobdiance a is mde poible by e young ecoproc' being plankonic only a eour i explanaion i inadeuae A ew our i enoug

or idal curren in i region o ranso a larva 0 kilomeer or more inerpre e genereuency dierence a enirely aribuable o localiyecic and waermaspecicselecion on a geneically well mixed pool o lavae e common mussel o i region as a larva a i plankonic orany days oen and Mion ( 9 72 ) and on uranoand Mion ( 1 97 3 ) ound geneic dierence beween amle

8 7


rom ineridal levels mere meers apar is sould onvineanyone a genei dierenes an arise in e oal abseneo isolaion in ig eundiy animals


saw, 1 968; Cook, Leebvre and MNeilly, 92 ) Heavyeal onenraions an ane rom negligible o severe ina ew meers and degree o resisane o e onainan



o isolaion in igeundiy animalsBeni marine inverebraes wi ig ZZ are exellen

maerial or esing e ideas presned ere, and a leas onesuden o ese animals seems o sare my belie a eyare sube o inense seleion, grea variaion in ness, ande need or a sraegy a an lead o geneially diverse

ospring (Grassle, 19 1 ) Tere is onsiderable inormaion on e populaion gene

is o ig and mediueundiy owering plans, bu i ioen iul o inerpre beause even order o magniudeesimaes on e key aor o dispersal may be unavailablerli and Raven ( 1 969 ) inline owards onsevaive esimaes or pollen dispersal, wi e regard s norally ona sale o meers and only rarely kilomeers Faegri and vander Pil ( 196 6) believe in iger values, espeially or windpollinaion Tey give as an average axim" a isane

o 50 kilomeers or wind pollinaed rees, bu sae a pinepollen an be abundan undreds o kiloeers rom esore Levin, erser, and Niedzlek ( 1 9 1 ) noe a insepollinaors end o oninue in onsisen direons and ais inreases ranspor disanes over ose a would prevailwi random movemens beween owers

eed dispersal is also diul o uaniy Larger windblown seeds o rees an omonly be seen o ravel ensor undreds o meers Many weeds mus ave similar rangeso dispersal an der Pil's ( 1969 ) review suggess a seed

dispersal or several kilomeers may be ommon in soe speies, bu a a ew meers is probably e rule or any

Te mos onvining evidene o seleion overoing massive gene ow is in e reenly sudied exaples o seepgenei lines were ere are seep gradiens in eavymealonainaion o so ils (Anonovis and Bradsaw, 1 90 ;Anonovis, Bradsaw and Trner, 1 9 1 ; MNeilly and Brad

a ew meers, and degree o resisane o e onainanby adul plans, sows a parallel seepness o gradien A igerabiliy o resisane is experimenally demonsraed Aonsiderable gene ow by pollen and seed ranspor is ap-paren ro oparing age groups Plans on eavily onmi-naed soils bear large numbers o nonresisan or less resisan

seeds ikewise seedlings any eers ro e onainaedarea may be resisan, and adul plans on unonaminaedsoil may produe a ig proporion o resisan seeds Pollenranspor o 00 meers or more, in e direion o revailingwinds, is indiaed by seed ess in windpollinaed grassesNonresisan genoypes ay be leal wi onainaionlevels a permi grow and suessul reproduion by resisan ypes, and e resisan genoypes ay be a a 50 ompeiive disadvanage on unonminaed soil eep gradiensin geneially deermined emial deense meanisms in

oer plans are ainained by seleive predaion on seedlings(Crowordideboam, 1 92 )

e araers and genei variaion reviewed above areose a we would expe o be srongly seleed, and mayno b ypial o ness variaion rom oer araers andgene loi Also e soil onaminaion rom ining wases maybe abnormally severe and e gradiens unusually see Oerevidene, owever, less exreme bu more naural, as sggesed o boaniss rom a leas e ie o Turesson ( 19 22 )a seep lines are ainained by seleion despie rapid gene

ow uresson believed a os o e seleion ook plaein igmoraliy seedling sages Te evidene was reenlyreviewe by ebbins ( 90 ) wo nludes a

e srong seleive pressures exered by e pysial environmen upon early developmenal sages eble planpopulaions, even wen normally ourossed, o resis gene

8 9



A T U R A L S E L E C T I O

vewed teren) Most arcltral varetes are more nortan natral poplatons bt ew are clonal Comparson be-tween varetes may overestmate and wtn strans nder

E V I D E C E O F E R T I I T Y

tat abot 65 o scalecont varance n a snake mst begenetc o watever extent tness s correlated to scaleconts a consderable part o ts varaton mst be enetc



tween varetes may overestmate and wtn strans nderestmate varaton n natral poplatons ere s normallya lare genetc component ( 50 % or more ) o varablty nsc anttes as yeld n ran wc wold be closely related to ertlty n natre Varaton n sze wc s closelyrelated to ertlty n ost plants s known to ave a large

enetc component (rpp and Caten 1 97 1 ) ere s also evdence or wld poplatons Classc works

on plant systematcs ( e resson 192 2 Clasen andesey 1958) were ntended to estmate enetc derencesbetween ecotypes bt ncdentally provde normaton onvaraton wtn poplatons or nstance Clasen andesey (pp 1928) sowed anold enetc dereneswtn eotypes n sze vgor and oter caracters related toertlty.

O varos measrable caracters only vablty an ertl

ty measred natre can be related lnerly t tess Mea-sres o adaptve perormance sc as eetness or stress ress-tance mst be monotoncally related to tness bt a smplelnear relaton between tness and te nvestgators measre-ments s nlkely Many easly measred metrcal caractersmst ave opta near te mean o te dstrbton and tness wold declne wt ncreasn steeness n bot drectonsrom te optmm Oonald ( 19 7 1 ) and oters advocate ageneral rle tat tness sold decrease as te sared devaton rom te optmm Regardless o te exact relatonsp

t seems sae to assme tat a caracter s more arablet wll case more varaton n tness tan t were less varable It can lso be assmed tat a large racton o teobserved varablty o a caracter s enetc a large ractono te varablty n tness cased by tat caracter mst begenetc

eroot ( 169 ) sowed rom maternaloetal comparsons

9 2

p Keroot's tecne really measres ertablty wc mstbe less tan te total entypc determnaton o a caracterad mst tereore ve mnmm estmates Maternaloetalcomparsons natral poplatons o eelpot (Scmdt1917 Ee 1 942 ) and artcal stocks o gppes ( Scmdt

1919) also sow ertabltes n te range o 50% or varosmerstc caracters

e evdence s ardly as satsactory as mgt be wsedAll tat ca be sad s tat ( 1 ) tere s consderable genetcvarablty n ertlty o cltvated plants and no reason toasse tat tey are markedly derent n ts respect romter wld proentors ( 2 ) tere s no reason to assme tatertlty varaton s arkedly derent rom oter anttatvecaracters n natral poplatons wc generally prove tobe largely geetc n orgn and (3) many caracters closely

corelated wt ertlty sc as sze n many orgasms areknown to ave great varaton

eoretcal consderatos ake t dclt to see ow anycaracter related to tness cold al to be sbect to botenetc and envronmental nences Sppose a caracteroptmm s X and an ndvdal as te sboptmal valeX +�X t makes no derence to selecton weter te departre rom te deal reslts rom avng a enotype tatspeces X + �x or one tat seced X bt permtted envronmental nences to alter te speced vale by �x Selec

ton s eally concerned to elmnate wrongvale eotypesad redcedcaalzaton geotyps So as long selectos a domnant orce n determn geotypes tat preval tseems nevtable tat departres rom optma wll ave bota maor genetc ad a aor envronmental component

we knew tat redced tness rom wrongvale geotypestends to arse by mtaton ad recombnaton to te sae ex

9 3

N A T U R A L S E L E C T I O N

tent as from reducedcanazaton genotypes w could nferth t h d d l b l

E I D E N C E O N E R T I L I T

per year that are at least manly monocarpc to assure that



that the genetc and epgeetc oads must always be equalEqual roductn of the two knds of mutaton woud folowfrom shftng th argument from mutatons that aect pheno-types to mutatons that aect mutatons A gene that permtsncreased podcto of ether knd of reducedtness mta

on would be eqay selected aganst The reatonshps ofgenetc to egenetc load ougt to get some attenton boththoetc ad expermetal

The remade of the chapter s based on the ssumptontha a consdeabe fracton perhaps about half of the fertltyrance natra popatons s of enetc orgn It shouldbe borne n mnd that te bsered araton s reduced toe degee that ftlty and ablty are correated We onlymeasure fertty n gansms tat a n act sd tosexua mauty Fo any obsred felty dstrbuton we can

assume that many abnormay low aues that theoretcayought to be there hae been culled out because ofertltygenotypes are often lowablty genoyps

FETIITY VARIATION IN HIGHER PANTS

s noted n the precedng capter sze araton n an agecohort of hgher plants s often enormousy arabe The closdepenence of fertty on sze must ma that fertlty senormously arae Te ny major source of quanttate

data on pnt ertlty s Salsbury's ( 1 942 compaton ofcounts of frts er pant and seeds per frt of mostly herbaceus pants of Brtan They are mly of medum fecundty 0 0 as sugested n Capte 6 Sed cunts of largewoody ats would he been more germane and the dtaare unsatsacry n othe espects Those fo a sngle secesmay lp ndduas o derent ages and derent ocatesFrom Salsburys many examples I hae chsen ony thosetat ca ha seed otpt n a leas the tens of thousands

4

the data reate to a snge cohort that come from a snglelocalty and that nclude counts on at east a hundred specmens The data support the oncluso that fertty aratons enormous n the popuatons studed Fgure 1 2 The top0% usually has seera tmes the fertlty of the bottom 0%

d o d

Hy scyamus - Coho of 1936

C oh o of 938

Coho of 1939

hoss o s

15

F Seed ertlity distribtons o monoarpi plantpoplatons, rom Sasbry ( 4

9 5

0N T U R S E E C T I O N E V I D E N C E O N E R T I I T Y

A postve skew s apparent for every dstruon Salsury

admtted to under representng te smaller and more easly



10

10 20

200

100

12 24

0

0 20

ymnademia conopsea

30 40 0 60 0Thousands of Seeds

Paver dbim

36 48 60 72 84 96Tosds o Seeds

roeas

30 0 50 0 70osads o eeds

FIGE 2 Continud

9 6

80 90

120 32 144

80 90

admtted to underrepresentng te smaller and more easlyoverlooked memers of a populaton If even e smalles specmens d een represented equally wt te larges te dstruons would be even more skewed

A recen study of apaver by Harper 966 ndcaes aneven more varale and skewed dstruton tan ose foundy Salsury I s to be oped ta oter suc work wll bedone preferal on trees and wt counts for deren agecoorts n sngle stands an of sngle coorts over several years

FRTILITY VARIATION IN FISS

Sze varably n ses mples grea erlty varabltybecause female ferlty s closely relaed to sze Bagenal 66 concluded from volumnous data on place and oerprolc speces tat age as no mportant nuence on fertl-ty apart from s eect on sze Snce te fertlty varaltyof females s n addon to and partly correlated wvablty varaon te assumpton of grea varaton n tnesss tereby supported Capter ndcates tat fertlty vara-ton n males s greater tan n females n mos speces

Acual data on fertlty n relaton o age are less commontan on ferlty and sze but suc nformaton s gateredfrom tme to tme Fgure 3 Tere are undoutedly oerrelevant studes u tose presened sould e sucien Teywere cosen solely on te bass of avalablty of pulcaonsand te adequacy and relevance of nformaon I requreda least tweny ferlty values per coor wc were eermeasured on scaer dagrams or taken drecty from abes

nfortunately ere s no assu!ance ta e samples represent sngle populatons n e endelan and coogcal senseTey are merely ses caug n a ed ara wt standardcommercal gea wc may be based n favor of larger specmens Te lamprey daa came from several rvers ut al ad

N U R L S E L E C T I O N E V I D E N C E O N E R T I L I T Y

-Year - Od Plaice



5

5

/

I

5

Gad Bak Haddoc

Hodd 6

M o of Egg

9 - Year - Old Cod

IO:arid Cod

Nwfoundnd Labrdor Cod

(M ay , 9

�M l ons o Eggs

on Rogh D d Poputon

3 s n 1958

B nl 1 95 )

Thosnds of ggs

FGURE 3. Sineseason e prodction in shes

15

1

5

5

4-Yea O Pac,

Clye Popuaton

(Bagea,

5Thosands of Egs

2Yr- d P a c,

2

a Rochll Popuon

B n l , 9 6 3 )

Thosnds of s

3

4yod ac

8a-od c

Sotr igh of NorSa

(Simo

Touad o, Egg

FIGRE 3. Contined

N T U R L S L C T O N

Sea Lam e s (Te ial S a ig ) Mi chga (A legate )

V N C O N R T L T Y

giing adequate representtion to both the largest and smaesspemens



Sea Lampreys (Terial Spawnig ) Mi chga n (Applegate, )

24

Sea ampeTemna Spawnngake Supea n ( 2

� r ousads of Eggs

Tua gg

IGUE 3 Contined

spent ost of their lies in a single lake and al are descendedfro a few founders that entered the upper reat Lakes

through canalsThe distributions all show considerable ariability andconform to the lognormal distribution as well as can be expected of small samples This is especially true of the specieswith the higher fecundites Only with the lamprey wouldthere seem to be any doubt This species matures at a certainsze spawns, and dies Spawning groups may therefore be ofariable age but not of ery ariable size and fecundity Thebimodality of Applegate's data must reect his stated am of

0 0

spemensThere seems to be a tendency for ariabiity to increase with

age An extreme example is the trout studied by Wydoski andCooper ( 1 966 in which dierences between upper and lowerends of the distribution increased from about twofold toeightfod in three years The gadid and atsh popuationsin Figre 3 are all heaily shed except possibly the longroug dab The greater life expectancies in unexploited popuations would increase tness ariability measured oer wholelifetimes t follows from principles operatie in the eolutionof senescence (Hamilton 966 Emlen, 973 that fertlitydierences and other aspects of tness ariation should in-crease with age The eectieness of selection should declinewith increasing age to exactly the same extent for genetic andepigenetic load.

ata summarized aboe indcate that egg or seed fertiityin nature is widey ariable The distributions generally showbetter conformity to lognormal than to symmetrical or truncate models and support the assumption of multiplicatie interactions among genetic and enironmenta contributions tothis important component of tness n conjunction with theo-retical considerations (Chapters 5 and 6 and data on iability(Chapter 7 they support the inference that tness in hgh-fecundity populations can be approximated by highariancelognormal distributions and that only a few sisyphean geno

types make an eectie contriution to the next generationThe cost of meiosis is thereby a minor part of a commonlymanifold dierence in tness amog genotypes t partheno-genetic aoidance would not be worth the sacrice of benetsfro genetically dierse progenies as indicated in the earliechapters

0



D E R I V E D O W F E C U N D I T Y P O P U A T I O N S

of a heterogonic life cycle with asexal and sexal reprodction in eoltionary eqilibrim No rodent wold hae a high

D E R I V E D O W F E C U N D I Y P O P U L A I O N S

selectie adantages This is not tre of any compromise between the two Selffertilization, endomeiosis, restoration of



tion in eoltionary eqilibrim No rodent wold hae a highenogh fecndity to achiee the reqisite ZZI in a ingle yearThe fact that parthenogenesis or its eqialent if fond ina ertebrate poplation, has always replaced sexal reprodction entirely is decisie eidence of the maladaptie natre

of sexaity in these organisms.Een among inertebrates it wold appear that the initiation of parthenogenesis normaly rests in the loss of sexalitySeconarily heterogonic life cycles are characteristic o somemajor grops sch as aphids and rotifers bt the taxonomicditribtion of sch life cycle sggest that they hae onlyeoed a few times mong weeis and ies parthenogenesishas eoled independently seeral times and in each casesexal reprodction disappeared Wie 7

The facltatie apomictic seed prodction of many plant

mst be in eqilibrim with sexal seed prodction as eni-ioned in the phidRotifer Model. Obligate apomictic eproction is less common and saly associated wi sexallysterile hybrids and polyploids sker 70 , and earlierpapers in this eries It reslt from the inability of pantswith abnormal chromosome complement to proceed with anoma meiosi Similar conditions arie in the frns and gierise to ameiotic sporogenesis and parthenogenetic egg deelop-ment Eans 6 I wold attribte the scarcity of aexaspore prodction b ern to their enormo pore fecndiy

and conformity to the ElmOyster Moel

UNIPARENTAL SEXUAL REPRODUCTION

ario modes of reprodction that might eem inermediate between asexal and sexal are discsse in Chapter 0For the present discssion two highly adaptie reprodctiemodes can be recognied the perfectly aexal and the otcrossed exal With each we can asociate a complete et of

1 0

diploidy with a polar body, etc, may oer no adantages oeasexal reprodction, and may oer serios disadantagesfrm loss of genetic material or inbreeding depression I inter-pret the prealence of these niparental sexal processes asindications that perfectly asexal egg or seed prodction

wold hae been eoled, gien the reqisite preadaptationsThe learest case is the gynogenetic shs Their reprodctionis genetically asexal bt they retain the need for the stimlsof insemination to initiate deelopment. If deelopment withot this stims cold be eoled, these allfemale sheswol be free of the necessity of liing only in areas inhabitedby elated species that the can begile int a genetically nprodctie contribtion of gamees

Somewhat aalogos are those plants tat hae achieeda eneticaly asexal eed prodction bt are still brdenedwith the necessit of endosperm fertiliation Haskell, 66;Nygren 66 In some ies meiosis takes place bt diploidyis restored by resorbing the second polar body considerableroportion of ethal homozygotes are thereb prodced Salker 56 , bt their los is apparently worth the partialaoidance of the cost of meiosis

Selffertilization aoids the cost of eiosis a a genomewieaerage. For eery gene that is abandoned another is dobledThe rarity of habital selffertiization indicate that the reslting ibeeding depression is so seere as to oset te 0 adantage of aoiding the cost of meiosis, at leat in te majorityof plants and aimals. Mot plants otcross if they can andselffertilie as a second choice In poplaions that mst oftenresort to the seco choice genmes toerant to high leelsof homozygoity will eole Inbreeding depression may bemitigated to the point at which the cos of meiosis will bea greater los Thereafter the plant will preferentially seffer-tilie and otcrossing will be a rare abnormality.

1 0 7



E R I V E D L O W - F E C U N D I T Y P O P U L A T I O N S

They woud be replaced by oshoots from near relatves that

have not yet made the dscovery Ths knd of bas n taxo-

C H A T E R T E N

f S



nomc extncton whch should not be confused wth group

selecton as usually understood (Chapter 3 could keep ex-

clusvey asexua speces n low frequency n the bota, despte

a frequent oss of sexualty

0

Patterns of Sexuality

The presence of meotc oogeness n hgher anmals and plants

s the major challenge n sexua reproducton but clearly tereare many others Ths chapter sketchly consders some other

probems especaly those related to the man one of the cost

of meoss Related ssues on the roles of the sexes n doecous

anmals are reserved for Chapter

PRIMIIVE SEXUALIY

Asexul reproducton s any process that produces osprng

n such a way that they precsely nhert the parental genotype

It requres the pror evoluton of eact mechansms for preserv-

ng ndvdualty and genotypc ntegrty Bacteral tranduc-

ton and transformaton are symptoms of the mperfecton of

these mechansms n organsms that lack wellorganzed nucle

and mtotc machnery Ths sort of recobnaton must have

bee frequent n early, realy prmtve organsms Although

ot eotcaly dversed" ( Table p. 4 ther repro

ducton must have been, n eect sexual and muc evoluton

ay advance had to occur before genetcally unform clonng

became possble These dea have been expressed before

(Boydan 954 Ehrensvrd, 96 ; arker Baker and Smth

9 , but hstorcal prorty s often assumed for asexual

reproducto

As long as a bacterum or potst cell s lvng unde cond-

tons that provde the necesstes for ncrease n nuber, t

s lkely that the same genotype one cellgeneraton later, wll

enjoy the same promsng condtons but f there s dculty

n mere mantenance prospects are unfavorable A gene that



P T T E R N S O F S E X U I T Y

gametes and reject sperm The theory s the same whetherthe two knds of gametemakng strategy are employed by ah h d d O b

P T T E R N S O S E X U I T Y

whether t relates to growth processes egetate reprducton or utlzes stuctures more prmtely used n sexual

d h d ll



hermaphrodte or two doecous organsms One sex may beregarded as parastzng the parental nestment of the otherIn hermaphrodtes the parastsm s mutual

Once ansogamy s eoled the only way to escape genetcparastsm by sperm s to abandon syngamy and become parthenogenetc Any female that can accomplsh ths n anotherwse exclusely sexual populaton thereby doubles hertness One mnor problem that remans s the orgn of polar-body formaton The result would be the same whether n eggswth polar bodes were formed from n oogona or wthoutpolar bodes from n oogona I suggest that t prodes bettercontrol oer eents n the egg for t to reman dplod as longas ossble untl after the egg s ockd wth olk seresOnce the cytoplasm s really bulky symmetrcal sson be-comes mechancally dcult but the buddng o of mnutepolar bodes ery easy

CLASSIICATION O MODES OF REPRODUCTION

ahendra and Sharma (1955) proposed that reproductonbe dded nto eotc and aeotc� whch would be equalent to sexual and asexual as used here There s a problemn the possblty that meoss could occur and reproductonstll be n eect asexual as wh fertlzaton by the rspolar body Also the presence or absence of a cytologcallyrecognzable meoss s less mportant than the genetc dstncton of whether recombnaton s present or absent ecob-

natonal and nonecobnatonal would express exactly themportant dstncton The more facle terms sexual andasexual can do the same and hae been used n ths senseby recent wrters on the eolutonary sgncance ofrecombnaton

In asexual reproducton a major dstncton would be

1

producton parthenogenetc eggs apomctc seeds motcallyproduced spores It s also mportant to dstngush prmtefrom dered asexualty The dered would nclude al nstances of asexual reproducton n organsms that had an ex-clusely sexual ancestor Ameotc parthenogeness s always

dered Some nstances of egetate reproducton n aousplants and worms may also be dered as s certany tepolyembryony of the armadllo

ost sexual reproducton can aptly be termed euphac

It requres producton of haplod gametes that must unte npars to form an at least momentarly dplod zygote Thegametes that unte must come from derent ndduals sothat the zygote generaton s genetcally derse Whether theres sogamy or ansogamy and whether the parents are monoe-cous or doecous are secondary consderatons The most m-portant of the subordnate dstnctons would whethermacrogametc haplody results from a selfosed genetccost or rom nutrtonal consderatons

nally there s what may be called degenerate sexualtyof whch selffertlzaton by hermaphrodtes would be thecommonest form Another possblty would the restoratonof dplody n a haplod egg by any of the methods dscussedby Crew ( 1965) Asher ( 197) and asln 1968) haeanalyzed the theoretcal consequences of arous modcatonsof the meotc process pror to parthenogeness It s charac-erstc of all forms of degenerate sexualty that the populatontends towards complete nddual homozygosty but oftenwh hgh leel of polymorphsm n the populaton Ashershowed that the tendency towars homozygosty can be op-posed by selecton so as to ge a farly hgh equlbrum leelof heterozygosty sadantages of degenerate sexualty weredscussed on pages 1618

Bexual s sometmes used to descrbe poulatons of male!1 1

A T T E R N S O F S E X U A L T Y

nd emle individuals, nd sometimes the opposite, o echindividual being o both sexes For this reason Tomliso 968 urged that the term be avoided altogether He also

A T T E R N S O F S E X U A I T Y

natSn by apdits Exaps Mndls as s ss

atnnsis wnv t pcss ails t psv t atna



968 urged that the term be avoided altogether He alsopointed out that gonochotc and doecou seem to men thesame thing Reproduction my also be divided into unpaen

tal and bpaental ayr, 963 This avoids the diculproblem o careully distinguishing such things as partheno

genesis and selertilization, but unortunately, these dicultdistinctions are the theoretically important ones The geneticonsequences and evolutionary signicance o selertilizationand ameiotic parthenogenesis are entirely dierent, and igoring the distinction will obscure some important issues

In discussing the AphidRotier odel I made the custom-ary assumption tha parthenogenetic reproduction in themodel organisms is in act clonal hs has onl recel beenclarly estblished or rotiers Birky and ilbert 9 andor aphnia Herbert and Ward, 9 2 Aphid oogenesis re

sembles that o aphnia in the ormation o a single oarbody which remains outside the egg, ad a n sage is theegg visibly haploid Unortunately there are no genetic datato support the clonl nature o aphid parthenogenesis, and thepoint remains inconclusive Bacci, 96

The suggested classication o modes o reproduction outlined below is designed or discussions o the adaptive signi-cance o sexuality For other purposes, o course, other classications o reproductive processes may be more appropriate

Sxal pdctin

idial sin ntyps atd bcas caniss ntypic maintnanc a py dvpd dn anais bactialtansdctin and tansatin

EasicCnsvativ isay aplid ptists wit n a bdisd) Exas sxal dctin in st tzans andsip ala

Cstly (50% ntic ss in nsis) Exas sxal pdctin in diats?) ls an

'

o

, I

I

I

p pnty Exaps aticiay indcd dvpnt aplids

ts

Asxal dctin

iitiv always ssi vtativ) Exaps ittic ssin inptsts vtativ dctin spns

ivdVtativ Exapls: pybyny i anias pbabys wtatd spad i plants pbably ssin ins w ps

ictatic Exapls any dvpnt va sps tctat psv t atna nty

COMPARAIVE SEXUAIY O HIGHER ORGANISMS

Evolutionary biology is devoted to explaining diversity, and

lie cycles are as diverse as the structures seen by the comparaive antomist Consider that a single class o animals can include the lie cycles o aphid, honey bee, year cicad, andmosquito erhaps the rst century o arwinism can e ex-cused or not oten giving explicit recognition to the idea thatthe organization o a lie cycle is a product o natural selectionToday I sense an increased awareness o the great wealth ochalenges in the evolution o lie cycles, and some importantpioneer work hs been accomplished adgil and Bossert,9 0 Hamilton 966, 96 Lloyd and ybas, 966, 966 rker, Baker, and Smith, 9 2

For organisms that practice euphrasic sexual reproduction,we hve only made a bare beginning at explaining the diversity to be seen ather 940 as the rst to theorize, in manner cceptable by modern standards, on the phylgenetic distribution o hermaphroditism in the animal kingdom He arued that dioecy is primarily a mechanism o outbreeding, and hermaphroditism a compensation or locomotor de

1 1

A T T E R N S O S E X A L T Y

ciencies of parents The most important recent contribtionon animal hermaphroditism is hiselin' s 96 9 reiew, whichproposes seeral eoluonary explanaions for the obsered

A T T E R N S O S E X U A L I Y

lshed, is irreersible, but that these dioecious plnts hae agreater rate of extinction than the other tw On the forcesof selecion operating on thes characters ewis generally fol



proposes seeral eoluonary explanaions for the obsereddistribtions This work and Maynard Smith's 9 analysis of hermaphroditism in relation to cost of meiosis are discussed blow

Bacci 96 reiewed parthenogenesis in relation to sexual

reproducion ad the cytological cycles of heterogonic animalsarthenoenesis and gynogenesis in the ertebrates are reiewd by Batty 9 6 and zzell 9 , and insect par-thenoesis by Somalainen 969 Whit 9 dscussespatheoenesis in both ertebrates and insects, and Olier 9 in aachnids Mcilray 92 eported lifecycleariation within a secies of aphid In some areas i showsthe usual hetergoic lif cycle ohers it is entirely parthenogeetic, ad in still others fertile males are produed,bu no mictic females

Hawes 963 discussed the distribution of asexal andsexual repodction in protozoa and cncluded that absenceof sexuality is a deried condition eoled seeral times idependently The protozoa er many compx problems incomparatie repoduction One need ot go beyond the genusaramecum for a wealth of unexlained cytosexual phe-nomena Incopatibilit systems of certain fungi oer chal-lengin eotionary puzzles Rape, 966 ll te worksised are ainly escriptie reiws, but proide mines of in-foration for anyoe interested in eneralizing on ways i

whic sexual reproduction is adaptiely mdied in relationto other aspects of a life cycle

ewis 942 classic work on comparaie sexuality ofhiger plants masalled eidence that a frequent trend isfrom haing both sexes in each ower to 2 haing maleowes and female owers on the same pan to 3 haingseparat male and feale plants he taxonomic distributionof these characer sugests that the nal stage, if well estab

of selecion operating on thes characters, ewis generally follows Mather 94 and partly anticipates hisein' s 99 ene ispersal Model discssed below wis work is ful otheoretical suggestions and ideas for testig them with coaratie data

Higher lants may be especially faorable material for tesing teories on the eolution of sexal processes egetatiemtiplication, mictic and apomictic seed, arios forms ofhermaphroditism and selfincopatabiity systems may ormay not presen, and may or may not be related to aria-tion in ploiy sker, 9 Orndu, 9 hat great ariation can occur ithin a genus sows that plants are ofte pradated fo changes in these caracters and may respdrapidly to selection for modicatio of rprodutie straegCytological mechaisms of higher plants are usualy moreeasily stdied than tose of animals and show great diersiyans, 969 Wet, 6

This section does little more than indicate that on canrecognize a eld of comparai anatomy of life cycles, hatarious modications of sexual reproduction form a key element in te organization of any lif cycle, that a fai massof releant data has been accumulated, and that some rdimet of concetual systematization hae bee accolisheh mai work of proiding a workabl theoretcal stcturefor understanding the enrmous diersity of life cycles remainsto be do

CONTROVERSIL SPECTS OF HERMPHRODITSM

important princple that emered forty years ago wthR Fisher is that there can be no aerage adata oone sx oer the other i ioecios organisms arius implicatos, such as rates of parental inestmnt in sons and daugh

P A T T R N S F S X U A I T Y

ers and he sage a which males and emales should beequally numerous hae been worked ou by more recenworkers n imlicaion ha has no goen much aenion

I

P A T T R N S F S X U A I T Y

Wih selng here is no comeiion beween indiiduals orerilizable eggs Selecion should maximize uncional eciency in erilizaion and no aor waseul mechanisms o



gis ha male and emale uncions mus be equally expensieHermahrodiic lans or example mus be sending re-sources equally on ollen producion and disribuion and onoule and seed roducion i were oherwise i or in

sance i were less o a sacrice o pollenae oher lans hano be ollenaed and nourish erilized embryos ino maureseeds and associaed srucures a plan ha increased isollen roducion and reduced ha o seds would hae aselecie adanage The oulaion would eole higherollen and lower seed roducion unil i was spendingequally on boh

The expense o pollen roucion shoud make hermahro-diic plans less producie o sees han emale ones o hesame secies This execaion is well conrmed (Lewis and

Crowe 96 The amoun o deression in seed erliy execed in hermaphrodies depends on ossible correlaions beween hermaphrodiism and size or igor on he poulaionsex raio and on requency o selng ( Ross and Shaw 9 aldeyron ommee and aldeyron 9 3

In a compleely hermaprhodiic oulaion no eery indiidual need send equally on male and emale uncions buhe opulaion as a whole mus This conclusion should alyo all oucrossed simulaneous hermaphrodies regardless ophysiological deails In his I ollow arker Baker and Smih

( 9 and disagre wih aynard Smih's ( 9 reasoningha hermaphrodiic animals wih ecien (inernal eriliza-ion will spend lile on male uncions and hereby largelyaoid he cos o meiosis I he male uncions were reallycheaer he indiidual ha erilized more and was erilizedless would be a an adanage and he oulaion wouldeole a greaer emhasis on male uncions Onl whenselng is he rule would he cos o meiosis be largely aoided

0

:

1

comeiion I assume ha a normally selerilizing lan oranimal spends more on emale han on male uncions

This conclusion ha male and emale uncions are quallyexpensie in oucrossed hermaphrodies een when eriliza

ion is inernal can be supored or reued by sudies on reproducie behaior and physiology in animals ha mee hespecicaions such as oligochaes and pulmonaes eneralworks on he anaomy o hese organisms illusrae male reroducie organs as complex sysems o comarable bulk ohe emae Sexual conac in oligochaes is a mechanicallycomplex rocess ha akes rom many minues o seeralhours wih larer species requiring longer ime (Sephenson930 There is nohing o sugges ha male uncions areesecially chea The eriod o conac mus include boh

courshi and copulaion wih courshi sering mainly oenable each aricipan o gaher inormaion on boh hemale and emale suiabiliy o he parner

The expense o maleness is esecially conincing in hpulmonaes ale reproducie sysems are bulky arrays ospecialized organs and courshi is an elaborae aair lasingas much as hree hours The selerilizaion ha may occurin isolaed indiiduals akes place in he gonad and makesno use o he accessory male organs which are designed orcourshi and copulaion These would aear o be as wase

ully compeiie in hese hermahrodies as in dioecious animals In many aquaic pulmonaes coulaion is polarizedwih one indiidual acing as male and he oher as emale is esecially clear here h i being he mal resuled nmore osring per uni cos maleness would be aored b y

selecion unil he diminishing suly o erilizable oa orcedhe more persisenly male indiiduals o greaer and morecosly eor There seems be no acual usicaion or



H P T E V

\;hy .e �1ales asculine nd Femles

Feme and Ocasioaly,

M A L E A N D E M A L E B E H A V I O R

m r r ro h ge sze deren uc c crctr r uuay optimal for mae� and fm

i cctr for emaes. e n urn wth hree po sexu reproducon gamee producton achevement oertaton care of osprng



Feme and, Ocasioaly,

Vice-Versa?

The essenta derence between the sexes s that femaesproduce arge mmoble gametes and males produce smalmobe ones In nonreproductve aspects of lfe a mae anda female of the same popuaton usually have smar ecolog-cal reatons roughy the same habtats dets dseases andso on The ultmate goa for both mxal gnetc represen-taton n th same poplaton Yet ther mmedate goals neprducton may seem strkngy derent ales of morefamlar hgher anmas tke less of an nterest n the oungn courtshp they take a more actve roe are les dscrnat-ng n choce of mates more ncned toward promscuty andpolygamy and more contentous among themselves

Of al these aspects of masculnty only the last tem hasgotten serous attenton and even the best works on sexuarvalry from arwn ( 18 1 ) to Oonad ( 19 2 manly takethe general roes of the sexes as somethng gven and drectattenton to tactca detals of sexual rvalry The one compre-hensve attempt to provde a general explanaton for the formsand dstrbuton of masculnty and femnnty WynneEd-wards 1 92 ) I regard as totally erroneous Wlams 1 9) .

The masculnefemnne contrast s a prma face dcutyfor evolutonary theory Why f each ndvdual s maxmzngts own genetc survval should a female be ess anxous tohave her eggs fertlzed than a ma s to fertlze them andwhy should the young be of greater nterest to one than tothe other? Ths chapter attempts to sho that derent opt

1 2

ertaton care of osprng

AMETE PROCTO

Over part of the possble range of fecundty t must be true

that the more gametes are produced the more descendants resut but the reatonshp must sooner or later break downIf no other factor ntervenes depeton of parental resourcesw There must be an optmum level of expendture on repro-ductve functons dependent on the relatve vaues of mmed-ate and ongrnge reproductve nterests and on an optmumapportonmen of ths expendture among derent aspects ofreproducton Optmzaton of total eort for derent specesbut not for derent sexes was dscussed b adgl and Bssert( 19 0) and by Wlams ( 19)

eproducton of sesse marne nmas often requres ttlebeyond producton and reease of gametes and here we expecta mnmum of ontrastng mascunty and femnnty Fertlzaton s aceved by nearly synchronous release of eggs adsperm or by release of sper and ter transport to exposedbut attached eggs There s no reason to dobt that 10% moreggs woud mean 10% more zygotes Smlarly the productoof 10% more sperm wl rase b 10% th probabty thata gven egg wl be fertlzed by ones own sperm and not bysomeone elses or not at all Ths s true except the probably

nfrequent stuaton of most of the nearby eggs beng areadyfertlzed by one's own sperm ess ther s broodng orvvparty maes and females of a sessl marne nvertebrateshoud spend equally on gamete producto I kno of no dataon ths pont but Kamus and Smth ( 1 90 ) state that sessmarne nvertebrates have smar sze ovares and testes ad

2

M A L E AN D F E M A L E B E H A V I O R

is is erai e ipresio oe ges ro gross dissecios

aa a sea Daa seaa sz ae

i oser goads are ora ge io spei e

sex o e individuals sudied (Galtso, 1964; Sasry ad

Bl k 1971

M A L E A N D FE M A L E B E H A V I O R

lusios ae bee bo alleged ne-Edards� 1 962

ad sped ckes 196 \ b ma oers eale

ed i a aials i cos al ollos eriliza

o ill be adapive i reaio o e res o te reproducive

program ad ma be ell below tat wic is p siologicall



Blake, 1971

oile nimls chieve erilizio y lose coupling nd

cosequent reducion of sperm wstge A smll mou o

mteril devoted o sperm producio my e deque o s

sure ertilizion of ll e eggs o s mny femles s re likelyto be available. For the female i may remain rue tha ouput

o osprig is linerly relted o egg numer So i moile

nils te mss o eggs sould gretly excee o sperm,

except s is relion is complicted y suc cors s vivi-

priy Comprison o gond sizes i n oviprous shes conrms

his expecion, wit teses generlly etween hl nd

en the size of ovries in specimens o comprle size

(Gunson, 1 968 ; Helly, 197 1 ; Hoyt, 1 9 1 ; Ky nd Hsler,

1972 ; Krumholtz, 1958, 1 959 ; Mhur, 1 62 ; Norden, 196 ;

Osu d Hnsen, 1 962 ) . Te urter reucion in testis size in shes wi inernl ferilizion conrms ecienc o sper

use s te essentil fctor Moser ( 1967 ) recorded 0- o

20-fold dierence in gond size in mles nd femle o the

inernlly ferilized Sebastes. The ides proposed here indicte

no reson wy lrge mle should hve lrger testis thn

smll mle Gunston ( 1968 found tht reltive testis size

decresed wit incresing ody size o slmon

In mammas he cost o the femae comes almost entirely

after fertilizaion, and this may be true to a lesser exent in

birds. Reproductive eciecy demands tat fecudity be appropriae o resources likely o be avaiable later to te young.

In bird populations sudied by Lack ( 1954, 1 968) he was able

to show at increased egg fecundity beyond an optima level

results in a lower, not a higer number of edglings produced,

or at leas in edglings of reduced weigt and survivorship.

Comparable indicaions were found or mammals. These con

1 2 6

program ad may be ell below tat wic is pysiologically

acievable. In thes orgaiss we d, as expeced, small

teses and in ammals an essentially estis-size ovary

ACHIEVEMENT OF FERTILIZATION/'"

ierences in expeced male and female strategies would

again be minimal or a sessile arine invertebrate Both sexes

can reproduce merely by releasing gametes at te same time

as one or more individuals of opposite sex. Syncronizaion

can be achieved by iming by readily perceived physical factors

such as lght or temperaure, whenever these are predictive

of ptimum timig of reproduction. More precise syncrony

is possible if one individual can signal the start of its spawning

to ohers of the opposite sex. Te male would be more eective in giving such a signal. Sperm are readily transported

by currents, along with possible cheical stimuli present in

he semen A perceiving female can ten release her eggs wih

a high probability o fertilizaion. I she spawned rst, the

eggs could sink or oat and not be readily detected by males.

A chemial stimulus released with suc eggs would diuse in

a way dierent from the scattering of eggs and be poorly pre

dictive o teir presence. It is uderstandable that a general

synchronizaion by physical cues, wit prior spawning by maes

as an immediate stimulus to females, is the geneal rule amongsessile marine invertebrates ( Thorson, 950 . Taking the initi

ative in spawning is the sole expresson of masculiniy in these

animals.

Mobie aimals, with copulaion and ecient use o sperm,

show more pronounced masculine-feminine dierentiation

Fertilization of nearly all eggs produced by one or even severa

1 2 7



M A L E A K D E M A L E B E H A Y O dna n n oo aos pon n eodcti\-e prgram may be sia lly ad aagos for

oe member o ce n ca way adly d and a a pa dadanao oha ons at indug n such ac Trrs inrprts

M A L E A N E A L E B E H A V O mou a o col pod oa ma

be ml h o ab ombiao amog seaJ ale

sa. E" bo pa obud qualy o ano o don a a faonoud a a o ad c on h motrs nrsts



much o coursip and ratd haor in rds as aptsto prsr ons own optons and rstrict thos o th matCourtship o cours has othr uncions Is ro in prntingintrspcic matings is wl documntd

Anothr dirnc in sxual stratgy is sn in th canaiza-ion o rproducti unctions Fmal unctions must prcsly coordinatd caus on malunction may produc agrat was o rsourcs In mals n gross abnormaitssuch as homosxuaity or courtship haior at inappropriatsasons will rsult in triia losss ad no stongly stdagainst Noraly th only srios loss would b a missd opportnity or a producti mating A riw o idnc thatmal rproducti unctios ar poorly canalizd s prddby Williams 66 Additiona data on su onts as th

gratr frquncy o ma homosxuality nounctional juni sx bhaior and substandard parntal bhaior ar proidd by Andrw 66 Bach 64 Bourlir 64 and Hard 2

I onc conurrd Willias 66 in th common iwrnty docatd by Orians 6 that mal discrimination faors th gntically ttst mal as this tnss is x-prssd hrough his phnotyp Supposdly sh an thrbyoptimiz th gnotyps of hr yong I now fl that thiswould rqui an unalisticaly high hritability of tnss

h important fma adaptation in rlation to ourtship isan ability to prdict utr rsourcs or hr ospring froh apparanc and circumstancs of a ourting mal

n in monogamous spcis in which oportunity or frtiizng ggs of mor tha on al is usually abst thpctd masculinfminin contrasts shoud appar onog

3 0

han s on H an qicky pac astd gats and brady or anohr at Sh can not so radily rplac a masso yoky ggs or nd a subst ar or an xpctd littrHr optm hao prior to copuation should show a

much ratr dgr o caton an th masTh contrast sould mor strongly dlopd in polygy

nos spcs in whch as usuay contrit no support orth ospring T gratr masculinty should consist mainyo gratr dopmnt of charactrs usd in comptition withothr mals iscrimination y th mal should mordircty rlatd o haitat rsourcs al succss would mainly dpndnt on ho many mals h can kp inaccssil to othr mals his wil largly dpnd on th siz ohis trritory and its attractinss to mals

Th importanc o trritory suitaility or attracting malsis ndicatd by thos birds that show gratr fmal dlityto a trritory thn to a mat arnr 64 Trirs 2 riws othr instancs of mal choic that rlat mor toth loca thn to th attndant mal Fma dragonisoos th bst oiposition sits and mat with whatr malhappns to aailal at th sit al rialry shos minlyin comptition for trritoris that includ god oipositionsits and courtship conssts o adrizing th sit

h litratur is ful of dscriptions of malfmal dir

ncs in rpructi bhaior n acordanc with th idasxprssd inlding th xpectd irncs twn moogamous and polygynous spcis mas ar rst on th brdinggrounds; poygyny is commn poyandry rar ; nonnctinalcourtship and mating such as homosxuality is mor commonin mals it is th mas that ha aborat courtship displys

3

M A E A N D F E M A L E B E H AV I O R

etc tepetatios ay o thooghy eeos to the e-

ghte teatet b Dohoe a itag 7

Oas 6 Seae 6 L a Tie 7

owhower ad itage proie a weaayze sty

of cotastig maefeae stategies They fo that a fe

M A E A N D F E M A L E B E H A O R

gget that ch o the oihet o th ebyo IS po-

e b th othe O a tae t o epoct

hioog a sette the atte o eate ot to a a

eae

Mot o the extat ioatio coes fro casa obsea



mae goun squirel wo be most sccessfu as a mother

when she had a male an his teritoy al to herself Membes

of haems were ess sccessful an mea success i haems

of two was greater tha that i thee the lagest obseve

size As expecte females show a sexal stategy designed to

minimize harem size They istract males couting other fe

males ad behave aggressively towads rivas For the mae

as expected the more wives he has the moe osprig he po-

dces up to a point Calcatios idicated that a harem size

of abot 25 wod be optimal for a mae The outcome was

a moda harem size of two a somewhat malefavoed

compromise

REVERSED SRATEGIES IN RELAION TOFERIIZAION

An obvious test of this explanation of masculinefeminine

contrast is provided by those animals in whic the male advan-

tage in mutipe copuation and female dvantage i optimum

timing and mate seection would be partly reversed In the

seahorsepipesh fami Syngnathidae copation resuts in

transfer of ova to the male who becomes pegnant with

embryos partly dependent on a pacental attachment Copula

tion commits a mae to a proonged burden and there mst

be a limitation on the number of females whose eggs can be

accommodated by one mae The limit may often be one In

a seahorse ( Strawn 958 and a pipesh ( Takai and Mizo-

kami 9 59 the ovaries of a femae have on the average about

the same number of eggs as the number of embryos normay

found in a male brood poch The small size of the young

and the fact that some yok remains in the yolk sac at birth

3

ti ote by amateu aqaist bt it appears that the theo

etical expectatios are ealize There are umeos reports

of femaes being more bightly coloe an aggessive ha the

maes This picte emege ceay fo the thee species cae-

fuy stuied by Fiele ( 955 . Genea eviews of what is

kow of repodctio i this family ( Beer a Rose

966 ; Hea 61 ) sppot the expectatio that at least

partial evesal of sex stategy shod be fod Udobtey

a etaied study of reprouctio i these shes wold sho

that both physioogical bures ad behavio patterns ae

highly vaied I predict that the behaviora mascuiity an

femininity wil cosely parale variation i paeta burdens

of mae ad femae

Other forms of egg holing by males ae foun in Pycno

gonids ( Hedgpeth 963 , some anuras an a few insects

The brden for the male midwife toad is merey mechaical

bt there must be some imit to the mber he can cary

We would expect a reduction in courtship activity as the

burden increases and pehaps an icreased coutship by the

female but apparenty little is known about reproductive be

havior in this species ahne ( 9 4 reported that the female

had a mating call and that it W;S louder than the mae's his

was accepted by Noble ( 93 but ignored b ater writers

Nothing is known of sexal behavio or seriousness of the male

bue in those wate bgs in which the maes carry eggs

This phenomenon in dendrobatiQ frogs is a brief ransport

of hatching eggs or tadpoes from the est to water and prob-

aby costs very litte ( Stebbins and Hendrickso 959 ; Sav

age 968 .

In some shes the fertilized eggs are carried in the mouth

of the mother ad in others that of the father Oral incubation

3 3

M A L E A N D F E M A L E B E H A V I O R

as ahouh a d o o pgnac han ha o

h sgahds, oud pced o poduce soe vsa

o se saegs. I s suggsv ha n spcs wh a

oodng, as show gh nupa coors and aes an

dull. Wh �ale oodng o coopave nestng, h ss are

M A L E A N D F E M A L E B E H A V I O R

eoa and na aon padap a spcs o

h vouon o paena ca h a. Inna za-

on hou roa preaaps th spcs o paena

care y th a. Connous assocaon of h parns ar

fertzaon prs th evouton o parena care y oth



slary coored ( Baends and Bands, 1 90 ; Myrg,

196

A rare but taxonomcally wdespread phenomenon among

brds s he ale's assumpon of he entire buden of ncuba-

ton. These revese-ro brds ae convniently reviewed by

Kendegh ( 1 952 ) and, along with some doubully compar

able custacean developmnts, by Wynne-Edwards ( 1962 ) In

a few xamps here s a thorough reversal of the sex roles

in reproducion : emaes polyandrous, moe brghtly colored,

more acve n courtship. In oher the eversls are rial

For nsance, brushland tinamou males and females have smi

lar plumag, polyandry is rae, and males are, at least initially,

more actv n courtshp (Lancaster, 1 964 ) .

Evn partial rversals of masculinty and femniniy occur

ony where als assume urdens usualy taken y females.

This is strong evdence for the view that n most species mas-

culine characters are individually opimum for males and

feminine ones for females No enettothespecies interpre-

tation o reproductive ehavior need be invoked This is also

a choice illustration of the logic of he comparative method

If there were no such anmas as seahorses or tinamous, the

explanation oered would e copatile with the evidence

ut not forcefully supported It is the exceptions to the rule

of masculine males and feminine females that prove the theory

that explains oth rule and exceptions

CARE OF THE YOUNG

Kin slection may promote the evolution of parental care

o the young, if the necessary preadaptatons are present ale

1 3 4

sees

Most ony shs hav eternal frtilizaion, and male terr-

orialty is common. The funcon of erritoalty is a currenty

deated ssue, u a leas it is clear that large teritores in

preerred hatas favo repoductive success over those hatare smaler or n margnal haiats. Tyicaly in terrtoria

shes the eggs are lad and reman in he terrtory. The female

s driven away, ut the male remans associated with his o-

spring, and defense of terrtory ecomes incidentally a defense

of young Tendencies o defend against predators other than

rival maes, to avoid harmful disturances to eggs already laid,

to rerain from eating eggs or young, to kp them free rom

parasites, etc, are readly evolved y kn selection This ex

plais the hgh frequency of paternal tending of externally

fertilzed eggs in shes, and the rarity of such ehavior yfemales

Emlen ( 1 973 : 148 ) suggested another eplanation He rea

soned that indeerminate growth and depedence o female

fertility on sze will plac a special premium on the female's

use of resources for further growth She can presumaly grow

more rapidly without the urden of nest guarding and is

selected o leave the eggs entiely in the care of the male

Unfortunately for this argument, there may e an even greater

advantage for the male in growing large Size can e impor

tant in competition or territories and n courtship The fact

that males re oten larger than feales in nest tending species

indicaes that large size is more important for the male

A male sh guarding a nest of eggs has a task largely unre-

lated to their numer It must e nearly as demanding to de-

end a hundred as a million This is true wherever eggs re

3 5



M A A F M A A

sonsbtes found n other grous must be stbe evouton-r equbrum t fertton the mes hve nvested ttemore thn gmetes so tht the ctor of cumutve nvest-ment to be rotected s envsone�n Trvers modes seemsnot to y The contnued vbty of swnng femes

M A A F M A A

7 reeed edence tht me nsects re ess we cn-ed hsoogc nd ess toernt of envronment stress

reter rnce n me tness not on ets otmton of rerodutve behvor but trbutry sects ofdtve orgnton mes deveoment rogrm must

b dd h f



s hghy robbe n these troc shes wth extended breedng sesons It my be tht the exnton w emerge fromconsderton of not just one but sequence f broods Theseshs hve roonged r ndng n ctvty t my betht sutbe terrtory hed jonty wth cooertve femes ongterm resource so hrd to wn tht once secured tshoud not b jeordzed for ossbe mmedte gn fromcourtng nother feme

SEX AND MORTALIY

beeve tht Trvers 972 gves the correct exntonfor why mes hve greter mortty rtes thn femes eesy dscredts the myth tht whchever ex hetrogmetcha hgher mortty rtes from vunerbty to deeterous re-cessves on the snge Xchromosome, nd rgues tht the sxwt greter vrnce n tness shoud hve greter morttyn mny seces tyc dut fme w enjoy somethngke the men reroducte success me, esecy noygynous seces, my not reroduce t erhs onythe ttst 25 of the mes w reroduce, and the to my enjoy mny tmes the men reroductve success t evrymoment n ts gme of fe the mscune sex s yng forhgher stkes ts ossbe wnnngs, ether n mmedte rero-ducton or n n utmte emre of wves nd kn, re greterSo re ts ossbtes for mmdt bkrtcy det h orermnent nsovency from nvountry but unvodbe ce-bcy Trver dscusses number of obsertons of the gretervunerbty of mes reter me suscetbty to sychosomtc dmge s documented by urdoch 966 ese

3 8

gmbe gnst odds n n eort to ttn the uer t ofthe tness dstrbuton femes eed merey cne gnstmfunctons Feme mortt w be found to exceed menot n seces wth feme heterogmety but n those wthfeme mscunt

3

C A T E R T W E E

Sex as a actor in Organic Evolution

S EX N O G AN C EV O U T O N

a ork tat has been done, and mura and Ohta arue that suh vews as ars and Dobzhansks are ontrar to a mortant thought sne sher and uer.

n ths manstream of theor the concuson usua suorted and the on one serous onsdered s that recomb-naton ncreases the rate at whch favorabe mutatons can



If genetic recombination can be an immediate reproductive

adaptation (Chapters 25 ) appeals to long-term benets of

evolutonary potental are inappropriate in an explanation for

the orgn and persistence of sex in a population. On the otherhand, it is unlikely that sex could be irrelevant to the evolu

onary process. Its role n evoluton is a problem of basic im

portance, formay separabe rom that o sex as a character

shaped by seletion. It is dicult, on the bass of brief state-

ments in textbooks, to decide exacty what is the generay

accepted vew. Benets of sexua reproduction are oftn said

to e in the production of a diverse array of genotypes or

seection to act upon. An exampe is Mar's ( 1963 )

statement:

Through recombnaton a ouaton an generate amegenotc vaabt or man generatons wthout angenetc nut (b mutaton of gene ow whatever.

A cose smar statement s made b Dobzhansk (Ta andCaender, 960 5

In m onon ths ouar vew s the one most ke tobe correctame genotc varet ma be a safeguardaganst etnctonbut m reason s the ooste of thatusua assumed. The reason usua gven s that recombna-on ncreases resonsveness to seecton and the rate of adatve change. Ths chater rooses that seua reroductonusua ooses the eect o seecton, and the na chaterrooses that ths retardaton of adatve evoluton ma ro-duce a ongterm grou advantage. Nether vew o the roleo se n evouton s suorted b an o the serous theoret

4 0

naton ncreases the rate at whch favorabe mutatons canbe ncororated n an evovn ouaton. The benets ofsea reroducton are sad to reate to ongterm advancesthat arse from stead reaement of an orgna germ asm

b new mutatons that are favorabe hen the arse and re-man so as other favorabe mutatons arse at other oc. AsKmura and Ohta eressed t Seua reroducton hasled ver mortant roe n seedng evouton n theast hen to roduce man beore the sun n our soarsstem burns out.

TH MULLRIA THORY

Recent thought on the evoutonar eects of recombnaon

s n a bzarre state of contenton after fort ears of uncrtcacomacenc. The comacent erod began wth R. A. Fsher( 930 and eseca H J. Muer ( 93 whose cassc essabens otmstca wth the cam

. . . that genetcs has na soved the ageod roblem othe reason for the estence (.e., the functon of seuatand se, and that on enetcsts can roer answer thequeston s se necessar."

nd then goes on to deveo the vew now genera acceted

b ouaton genetcsts. It assumes that se can scarce beadvantageous to the reroducng ndvdua nd must be roduced and mantaned b grou seecton. Even f there wereno genera objectons to the concet of dataton throughgrou seecton, there woud be n adequate one here. Theestence o ouatons n whch seual and seu reo

4

S E X I N O G A N I C E V O I O N

duct ion occur in evoutonary stabi ity demontrates that se

gives some advantage that baane reombinationa oad and

the ost of meiosis

Muer and ihers theory rooses that sex is favored by

grou seection because it shoud increase the seed wth

which a ouation can incororate favorabe mutations With

S E X I N O G A N I C V O L U T I O N



which a ouation can incororate favorabe mutations With

exua reroduction, a mutation that arises in one individua

can never be resent in members of another cone. With sexua

reroduction two individuas can have descendants in com

mon, and genes from dieret sources can come together incommon descendants Recombination roduces genotyes that

woud not otherwise arise and utting two avorabe muta

tions together suosedy increases the seection o both

This theory was modernized by Crow and Kimura ( 19 65 )

wo summarized the uerian iew in a ahic mode

(Figure 1 4 Their ubcation sarked te beginning of a

renewed interest in sex as an evoutionary factor. At about

this time the WynneEdwards theory of grou seecton was

being warmy debated and Manard Smit 1964 was

among tose who rejected te teory in its aication to reroductive ysiology and socia beavior It was his thinkn

on grou seection in reation to reroduction and ouation

reguation that ed him to consider it as a ossibe factor in te

orig o sexua reroduction (aynard Smith, 1971)

Crow and Kimura found that sex is of no imortance in

acceerating evoution in uations of ess than a thousand,

but that it can enormousy acceerate adative change in realy

arge ouations They conrmed Muer's reasoning tat a

favorabe mutation coud ony rarely be estabised in a sma

ouation By contrast, even rare mutations can occur atnite frequency in enormous ouations Sexua reroduction

coud bring favorable mutations togeter · so that they coud

enhance, rather tan comete wit eac oter

Atough tey seemed to conrm the Muerian view, Crow

and imura realy made tat view a bit susect. heories of

grou seection rey heaviy on ouations being numerous

4 2

L A R G E P O P U L A T I O N

I

S

E

XU

L

�

SMALL P O P U A O N

SE

XU A

�

FIGURE 14 Model of incorporation of favorable mutations

in asexual and sexual populations, from Crow and Kimura( 1 965 A, B, and C are favrable mutations and all threeindependently replace ancestral allees in the large sexual population In the large asexual population, clones with mutatonsB and C prevail over the ancestral genotype for a whlebut die out in competition with clone A Only when B andC arise again in a member of clone A can they be incorporated.In the small populations favorable mutations are so rare thateach completely replaes competing allees beore the nextis likely to arise, and this is true regardess of whether reproduc�tion is asexual or sexal.

4 3

S E X I N O R G A N C E V O L U T I O N

an mall rather than large. The requirement that populatio

size e well over a thousan removes the theory's applicaility

to some interesting organisms. This requirement has been ras-

tically revise upwars by later ork an is iscusse further

elow The theory also implies assumptions on gene interac

tion in the determination of tness that would not be univer-

S E X N O R G A N I C E V O L U T O N

reache this last conclusion without recoring his calculations

ut id not appreciate its inapplicaility to nite populations

Kimura an Ohta ( 1 97 1 ) also introuce a more stochasti

moel as a renement of the one by Crow nd Kimura. I

concurre in the conclusion that populations would have to

e in the millions for recomination to be important in in



tion in the determination of tness that would not be univer

slly ccepted s the norm for favorale muttions.

These are serious prolems an so is tht pointed out in

criticism by Maynar Smith ( 1 968 ; see also reply Crow

and Kimura 1 969 He argued that Crow an Kimur arecorrect only if the fvorble mutations are unique events Wth

nite rate of origin for ech mutation nd with the ssump-

tion tht mutuations t dierent loci occur ndependently it is

simple matter to clculate frequency for ech genotyp

The frequencies will be ectly the se hether rproductio

is sexl, seul or miture of the two Sex would have

an eect only in popultion in which genotype frequencies

did not conform to the "independence reltion ( inkage equi

librim) epected to rise by mutation ressre his could

happen from the mixing of separte opulations. So aynardSmith conclued tht se is importnt in facilitting adapa-

tion to new habitats invded by colonists from divergent

sources.More recently Mynrd Smith ( 9 7 ) reinvestigte the

problem in greter detil. He conrmed his erlier view of

the importance of seual reproduction among colonizers, ut

lso found support for modied form of t he Mullerian theory.

He conclude that se would be of negligile longrange im-

po�tnce with population sizes less thn bout ten times the

reciprocl of rates of favorable mutation. Thus if typiclfavorable muttion arises in one in million gmetes the

population would hve to be lrger than ten million for se

to accelerate evolution. In an innite popultion sex would

accelerate evolution by a fctor equl to the number of loci

t which fvorble muttions cn occur. R A Fisher hd

4 4

p

creasing the sprea of favorale muttions. Kimur nd

Oht lso point out tht recombination s disadvntageous

when tness epens on heterosis or epistasi

Bdmer ( 9 70, 972 considered early staes of incorporation of favorale mutations and calculated that seual repro-

duction may acclerate the formation of recombinants by a fac

tor of two or more at each locus This advantage would be

aditive among loci an greater for small populations thn

for large Bodmer proposed this as the reason for seual rero-

uction eing more common in eukryote thn in prokaryot

populations. It is only in the eukaryotes that popultions

ould ordinrily be so smll that there wold be a signican

benet from recombination. Bodmers conclusion on the eect

of population size is the eact opposite of everyone elses. Itis my unerstnding tht Joseph F elsenstein i s prepring

tretment of this mtter which oints out n error in Bod

mers resoning.

Bodmer ls recognized the advntges of aseual reroduc-

tion as way of preserving nd muliplying highly t combin

tions. He suggested tht the optimum evolutionry potential

my consist of some combination of aseul and sexual repro

duction. The same suggestion is made from time to time by

otanists nd theoreticl reasons why the combination should

e dvntageous were iscussed by Wright ( 956 )Eshel nd eldmn ( 9 70 ) alon mong recent contriu-

tors hve proposed tht evolution my normally be retrded

in eclusively sexul s opposed to eclusively sexual popul-

tions. They nd the production of new gene combinations y

meiosis nd fertiliztion to be in some circumstnces a less

4



S E X N O R G A N C E V O U T O Nf v C f v C

'

S X N O R G A N C E V O U T O Nte oosed advantages and dsavantges of te two modesof reducton Aseua eodcton emts the ttest coneto arorate a nnce of adataton and ocay wn outover a Mendean opuaton Te Mendean ouaton,after an envronmenta change can rady shft to t eastte genera neghborhood of the new nnaces If t hs both

d d b h



C 000 0o �ft<o% 00 04 0 0o o+Qc 00o 0 o 0 0

o 0 • 0 08 0o 00'o 0 0

o 0.0 • 0 0 I

000 • •o 0

'

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+

o 0 �

000 o�Oo 0 0 o<8 co 0 0 0 0 %o < 0 0o

000o o

o

o 0 0 0 0 0 °�a

#�

•

•

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5. et o aexal and exal reprodtion on hortterm evoltionary hane nitial tate are hown to the let,thoe ollowin an environmental hane to the riht Membero lone hown a , exlively exal individa a o Ordinate and abia are mltilo enotype ntion hoen

to maximize lter reoltion by twodimenional projetionAA' how evel o tne, initially a enera daptive peakwith three pinnale well within the variability o a inlepopation BB how genotype ditribtion o one inap-able o reproding exally CC how ditribtion or aMendelian popation, perhap anetral to the lone DD'how lone and Mendelian poplation in ompetition opa-tion o the adaptive pinnale by the lone reatly depree

1 5

aseua and seua reroducton ouaton can enoy bothadvantages Te concet of a gener adatve eak bengmade u of a come of nnaces and deressons has some

fctu suort fom studes of Drosoha ( Band, 97 Theustrated numera eatons mong cones and seua ou-atons has some suot from data evewed n the netchter

The mode (Fgure 1 ncudes estatement of MaynadSmth's (1968 1971 ) suggeston that seua reoductonhas ts most ostve eect when oagues from eensources coonze new abtat I woud urge that the coon-ton ocess not be gven too naowy geograhc an ntere-taton In a heteogeneous and uctuatng envronment, ec

new geneaton y be egaded as consts enterng new n-vonments If these coonsts wee seuay oduced, they aemoe key to ncude genotyes favored under the new condtons If seecton s ntense tese temoary fvoed ndvduas woud have the ssyhen genotyes dscussed n Cha-ter Aguments on cometton between seua nd seuandvdus n a ouaton can be etaoated to comettonbetween seua and seua outons Contnued suvvamay deend on oducng a dvesty of genotyes t east

abndane o exa EE how the ame ompetition, btwith the oriinal lone amed apable o oaional exalreprodtion, whih permit opation o the new adaptivepinnale The oriinal lone are everely depreed in nmberby the environmental hane and oneqent redtion intheir tne, and by omptition rom other genotype o hihertne, epeially the new lone in EE

1 5 3

S X N O R G A N C E V O O N

s often s envroment chnge ters the retve tness ofgenotes

COCLSIOS

The suggeston mde here s tht genotc vret rovdes mrgn of sfet gnst envronment uncertnt nd tht

C A T E R T I R T E E N

Sex as a Factor Botc Evoluto

Th k d f f b (W



mrgn of sfet gnst envronment uncertnt nd thtths m be more mortnt to outon survv thn srecse dtton to current condtons Seu reroducton

cttes evouton ndrect b mkng etncton ess kenot b mkng hlogenetc chnge more rd A survvngouton m utmte gve rse to gret rr of newt An etnct one obvous cnnot As onted out t thestrt of the chter the de tht genotc vret s of ongterm benet s revent n gener works on evuton butI beeve th the resonng behnd t s often fut. It mbe bsed on sound nference tht recombnton cn occ-son roduce genote of hgh tness It gnoes theequ vd ont tht seu reroduton ust s red

destros such genotesBoth onts of vew re n conct wth most of the creful

theoretc work from Fsher ( 930 ) to nrd Smth( 9 7 ) nd Kmu nd Oht ( 9 1 Ths work roosestht recombnton fcttes gene substtuton nd therebseeds hogenetc chnge Ths s esec ect n thework of Kmur nd Oht

nfortunte the fcts of boog s revewed n the netchter oer tte encourgement on n of hese three theores I woud erhs cm tht the normton s somewht

ess embrssng or m own theor thn or ether of theothers It m be noted here tht three theores ssume thtse s n some w of longrnge benet As the net chterw ttemt to show even ths ssumton m be regrdedwth suscon

4

There re two knds of evouton of nterest to boogsts (W ms 966) Orgnc evouton s chnge n the genetc consttuton of outon Botc evouton s chnge n the

comoston o bot If uton evoves b orgnc eouton the bot to whch t beongs so evoves but bocevouton need not m orgnc evouton A successon ofseces n n bndoned ed n etrton or successfuvso n chnge n retve bundnce of seces woud be botc evouton The cn occur wthout genetcchne n the consttuent outons

The knd of botc evouton o rmr concern n thschter s the orgn nd etcton o t on the Erth s whoe over consderbe engths of geoogc tme The mn

queston to be consdered s : Does the resence or bsence ofseu reroduco derent t nuence botc evoutonb terng rtes of etncton nd f so how?

Before consderng the secc roe of seut more gener dscusson o etncton nd botc evouton s necessrEtcton esec o hgher t s obvous o gret mortnce both s cuse nd eect n botc evouton Orgncevouton durng the esozoc roduced rr o dttons tht consttuted the dnosurwofe Becuse of etncton these mn dttons re now mssng from the

bot Ther bsence ws udoubted mjor contrbutonto the rolferton of mmmln dttos

Geer ccetnce of the mortnce of etncton stl ermts wde rnge of onon on the nture o tht mortnceThere re those wh roose tht etncton o ocl outos s so requent nd strongl bsed n reton to derent



S X N B C V Ngushed boogsts hod otherwse Smson ( 63 8 sasthat btween envronmenta demand and evoutonar re-sonse there ma be a . . . ag (etreme common theusua or unversa cause f etcton " and on age 5 hesas To ean an artcuar case of etncton t s thennecessar to secf two thngs what ertnent change oc-

d h d h f h

S X N B C V Nb becomng better adated to t A that s requred s thatncrasng adataton have a rogressve advese eect ontota resources. The etraton of a host b a deendent ara-ste s mere one eame of eoters adverse aectn aresource.

Andewartha nd Bch ( 1 54 summarze a are amountf d h b



cured n the envronment and what factors n the oua-ton revented sucent adatve change.

Ths ustrates the f�ac of regardng adataton not as

that b whch an ndvdua mamzes ts genetc nuenceon the ouaton to whch t beongs but as that whch normay acts to revent etncton The word sucent" cearndcates Smson beef that adatve change s awas a drecton arorate to foresta etncton but s not a-was fast enough I woud contend that whe evoton alwas fast enough t ma be narorate n reaton toouaton suvva

The most obvous eame woud be a ouaton thatadats more and more erfect to a saarng habtat.

Pehas the assenger geon had a new acqured obgatearaste that was efectng ts arastc secazaton at annusual rad ate Consde aso the green turte ouatonthat nests on Ascencon Isand It sends most of ts fe neaAmercan shores but ever two ear the aduts undertakea remakabe feat of navgaton and ocate the tny breedngaea n the mdde of the Atantc. I assume that ths oua-ton s cose adated to ts ecoogca nche whch ncudesths geograhca restcted breedng ground If eoson re-vas ove constructve forces and the sand dsaeas the

ast turte to a her eggs there ma st be etreme weadated to he nche but t s a nche that n the net genea-ton w emt a tota of zero occuants.

The saearance of an ecoogca nche must be a farmore genera henomenon than the destructon of a bt ofgeograh. A ouaton may even obterate ts own nche

1 8

of crcumstanta evdence that oca etratons ma be com-monace eseca n nsects and Skeam ( 1 55 cacuatedthat een wth consderabe denstdeendent contro ran-

dom uctuatons that woud seem mnor on a scae of earsma make a random wak to zero amost nevtabe on a scaeof mena. A hgh frequenc of oca etratons and tao-nomc etnctons s necessa to a theor of grou seectonbut t s not sucent The etnctons must occur n grousthat ae consstent derent from those that survve.

arous consstent reasons fo etncton have been ro-osed arous grous became etnct because the were ove-secazed. Ths s undoubted true n the tautoogca sensethat the more strngent the requrements for survva the ess

ke the are to be met The dsaeaance of gmnosermtaa s attrbuted ether to a suosed nferort of ther vascua sstem o to the eosed seeds. The suosed nferowng suort of terodacts (comared to bats s mcatedn ther etncton. Ths sort of secuaton s emt of scentc meanng because there s sedom an ea evdence forthe nfeot of the adatatons n queston and never anfor ts roe n etncton. ven f such evdence were roducedt ma be nadequate suort for genea concusons on basn etncton. Sngenger wng suort ma have been an

unfortunate commttment for the terodacts but coud benear dea fo some other gou. avng severa nges feefo some othe functons coud readat a grou to motantevolutonary deveoments.

On m vew etncton overtakes organsms that have aboutas cose an aomaton to evoutonar equbum n ther

1



S EX I N B I O T I C E V O U T I O N

numerous It is unreasonale to attrute ths entrel to the

alt of a parthenogen to estalsh itself from a single colon-

st Both the asexual and sexual forms ma occur n the mdst

of a continuous land mass here each seems to have spread

out to the lmts of ts envronmental tolerance The partheno

f h d d l

S EX I N B I O T I C E V O L U T I O N



genetc forms havng spread more del must e more versa

tile in their requrements than the seuals That the can sur

vive in broder range f conditions no means that the

could etter wthstand an envronmental change ithn ther

present ranges.

Other examples of the seemngl greater evolutionar po

tential of asexual forms as judged from current ecologcal

an ogeographc observatons are found in psocd nsects

( Mockford 197 and hakweds ( Stens 950 . Parthe

nogenetc (o ften polploid) forms re re despread and

aundant than closel related seuals. In the psocis t is the

sexual forms that are found manl n unusual hatats eco

logicall and geographicall The onl possle example that

I hve found of sexual forms beng more widespead ad nu-

merous than related aseuals s i the lzar genus Cnemido-

phous ( Zwefel, 196 Wrght and Lowe, 968

EVIDENCE FROM TAXONOMIC DISTRIBUTION

An ndrect but potentll decsive wa of evaluatng sex

as an evolutionar factor is to look at ts taonomc distribu-

ton The alternatve chracter sttes presence and absence

of seual reproducton ill e distributed dierentl among

comnent of a iota accordng to varous evolutonary cn-

sdertons : rate of evolution from presene to asence the

reverse rte and the rates of extnction and cladogeness wth

and ithout sexual reproduction As hpothetcal illustra

tion consder the charcter states black nd white in Figure

16 If it could e shon that the phlogenetic distruton

1 6 2

FIGURE 1 6. Evolution of hypothetical character states blackand white. At the eft, black occasionally changes to white,but the reverse happens even more readily In the center,black occasionally changes irreversibly to white, and this in-creases the danger of extinction. At he right, black changesto white only once, but here it makes extinction less likelyThe data of systematics would not ordinarily distinguish theleft from the center phylogeny

of absence of sexualt ere dstruted much the same as

white in the center dendrogram there would e clear evdence

of a positve eect of sex on opulaton suval

The clam that sex is of longterm advntage in evolution

is often supported an argument from taxonomc dstriu-

ton (Mar 963 Rollins 1967 ; Stens 957 197 0 ; Weis-

mann 1 889 Mar for eample states that exclusvel asex-

ual reproduct on gans onl a shortterm advantage,

and ith the apparent excepon of the delloids virtuall

ever case of parthenogeness in the animal kngdom has all

the earmarks of recenc." As should e clear from the gure

low taxonomc rank of groups with a certan character state

could e used instead as an argument for he read reversbil

t of that stte Onl if it could e shon that loss of sexualt

is rreversile would the low txonomc rank of aected groups

(M ar's earmarks of recenc) be evdence of a longterm

disadvantage n the loss of sexualit It ould also e desirable

1 6 3

S X I N B I O T I C V O L T I O N

to get some rea data on the tendenc of strt aseua taato be of ow rank

I t does seem ausbe hat comete oss of the machnerof seua reroducton woud be rreversbe but t ma bethat a return to seuat s atent n man current aseua

1-

S X I N B I O T I C V O L T I O N



ouatons In a number of ants the absence of seuathas a sme genetc bass that coud be eas reversed b

mutato or ntroresson and favorabe seecton for euat( ews 42 Seua stere trods can be cured batere od Gnogenetc shes ma become seua f maesof ther own seces are avaabe

It s aso often true that the ack of seuat n a secesn margna habtats has no genetc bass at a. It arses fromenvronmenta condtons that make t mosse to carr outsome rocess essenta to seua rroucon. Remane andScheer ( 1 1 descrbe man eames among ants andanmas from the sea or fresh waters that have nvaded brack-

sh waters There are seaweeds that form nonfunctona soranga and hgher ants that ower but st no ed. Fo someanma forms the abnorma sant revents fertaton andn others the arvae are unabe to survve Adut stages of athese organsms reroduce vegetatve and thereb mantanthemseves bracksh water Stress of abnorma sant sundoubted on one of man factors that ma nterfere wththe come rocess of seua reroducton n margnahabtats

To be convncng, the argument from taonomc rank w

requre a more thorough documentaton than t has recevedThe attern of branchng and etcton n the two eft den-drograms (Fgure 16 was seected as of sutabe gentra com-et from some ure random hogenes ( Fgure 1 7 These were generated as foows. A hghrank taon wth tensubordnate taa s reresented b ten nes rsng from thebottom of the grah An taonomc eve can be assumedbut for araesm wth tetbook eames of etncton and

1 6 4

IGUR 7 nd phln, ntd xpind in

h x, nd pnd in d incn cc f thp hl.

adatve raaton I w seak of a cass wth ten orders E-tncton an branchng are randomed On the average oeancestra order s reresente b one descendant order afterone unt of tme but wth chance etncton baanced on the

6 5

X C

avrag han aogn aum ha gn nm-r o urvving orr rom a oon iruon wh = a rai mo Th gur how m r n ranomhogni n orr o inrang a u

nruv o arh h ranom hogn or un hi h

I

X B C

Soka ( 3 ma urnh om n mhooog Branh-ng hor hou a aa o urvva an inono aa a o h urvva an non o muaion(Shar 0

Whhr aqua hogn aa ar avaa for i i h



non o on omnan grou or whih om aaroh mgh oua or mor a aron whhmigh b aru o om roo inror or aavraaon rom anor ha u ovou hav ha gravoonar ona rogniza rha n om aavnnovaon or gnra aaaon an or uh anomaia iving o ao inruv o omar om oh ranom hogni wh ha u Wrigh ( 1 6 avn or h ivn o non of vrra aa

A rai mo o ranom aogn nonwou rou mor vara hogn han ho iura bau on o h onan ough ra o vara

aon o ing or non hou oh hag inm an var among orr o r aran in a onvironmna hang hav no ugon on wha woub a rai arn o varaon in ra of nvironmahang

Th unform im a ak gur a onrvatvmo o ranom variaon n hogni u an fai-ur u u iura om ia o nuvargumn on au an n vouionar hior Suoh on a wa aua an h ninh ua On now

rrn b a ng ivng o an h ohr 0orr rom 3 irn anor On migh m oaru h grar u of h ninh o i ua rro-uion u hi onuon wou no gnian a h00 v Dmonraon o onn au n hognman ha ming a b in raion o nu hoh a on ra mo of ranom hogn Mho o numria hogn a vo Snah an

1 6 6

ng or onn a n non an raaion i anohrrom o a n raon o rn or an o

ua rrouon wou rain on o h mor moran hogn rom o aak ao in monion aou h on on or whh hr i om kihooo ov nng onva ha a omwhamar ro in h m an h ah ha on i Suhuniona mar m unik or grnn or an ohra aur ha h ma hav n ommon

CONCLSONS

ma om m or a ra maur of nonranomn in h hogni iruion o h o o uaiw aar Manwh am nn o a rovonah nuiion o aing anma an an mai romWmann o Mar an Sn an aum ha o o u-a ra o ru ro or ongrm urviva naav raaon h onuon i orr how o wron i wh vn rvw abov ha aua anrz m o vra n aang o novnvronmn

A o rouon ma oun in h mo o orgno aua . Sbn ( 50 : 1 01 0 ugg ha thavanag of h aua orm ma rv, no rom hirown vouionar r bu from mma anraua form Som ua i ma oaona rounvua ab rrou aua u no ua rrar uh a v nivua ma hav a han gno- n raon o oa onon w om oa

6



B I B L I O G R A P H Y

Ctteborou R G and R Tomas 969 ava ecoogy o e wesen Austraan marne crays wt notesuon oter anurd arvae rom te eastern Indan Oceantraan J arne and rehw. e.� 0 993

Ca Fances and Jon C a 9 ouaton dynamcs o te acc sardne a oop ceanc h


: adane and odrn Boogy 6 R Donamraju edor Batoe Jons Hokns xv + 333

and Motoo mura 96 vouton n sea anaseua uatons mer. ara� 99 43940

and 969. Evouton n seua and aseaoaons bd 03 99



namcs o te acc sardne a oop ceanc h.

nvet� et� 93 4Care C A C G C Dckson and M Sead 963.

ava coor atten n apo demodoc voton�

303 Casen J ens 94 arta aoms as an eqbrm sysem

n evoluton aryooga� 6 (S 46949 and W M Hesey 9 ermenta sdes on te

na o seces Genetc strcte o ecoogca racesarnege nt. Wahngon b.� 6 3

Cegg T R W Aad A ae 9 I s te enee unt o seecton? vdence om wo eementa ant

olaons roc at. cad c 69444oe Wesey R 93 Resgen oaons o ltora manenvetebates and te deendence on ocean cents andtda crents coogy 34 9

Coen Dan 96 A genea mode o otma erodctonn a randomy varyng envonment J coogy� 6 9

Cook M 9 oecn o nara eecton. ondonHtcnson Unv b 0

ook Sea C A Cade eeve Tomas celly 9Cometton between meta toeant and norma an

oaons on noma so voon� 6 3663awodSdebotam T J 9 T ole o sgs and snas mantenance te cyanogeness oymosms oot corncat and rom repen eredy� 404

Crew F A 96 ex deermnaon ondon euenv +

Crow James F 96 T cost o evoon and genetc loads

4

oaons bd� 03 99 and 0 n nrocon to popaton g

nec heory. New York Harer and Rowe xv + 9 Crumace D W 96 Genetc oads n mase (ea may

and oter crossetzed ants and anmas voon

ary Bo� 30644.Cusn D H 9 Te deendence o recrutment on

aent stock n deent rous o ses J d one

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o meoss von� 33Downowe Jey F and ennet B Amtage 9 Te

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Bacc, G, 22, 1 18aker, R R., 1 1, 120Baeson, G, 169bdelod roifers, 163Beardmore, J A, 25

beauty, in reation to age, 128boc evouon, 155bipinnara, 49birds, as owfecundiy organisms,

1 02 ; eggs of, 103 ; reproducvecoss, 126; wih reversed sexuaroles, 134

bisexual, 11 5blennies ( shes , 83Bodmer, W F, 91, 145, 146Bonner, J. T, 3, 4, 7Boorman, S. A., 156

budding vs parthenogenesis, 10

canalzaton, of character optima,91, 93 94; of tness, 68, 70,7 1 ; and genetc domnance,1 09 ; of reproductive functons,1 30 ; of visual mechansms, 47

care of young, mae vs femalestrategies, 134

Carson, H 105Chra 95cicada, 1 17cchld shes, 136cladogenesis, random, 165166Clausen, ], 92clones, competiton between, 1 7,

1 8, 29, 34, 62 ; sze of errory, 28, 34

Cnemidphru 161 , 162cod, adult movements, 54 ; bood

ypes, 82, 83 ; fertiity vs. age,98 ; fertilty excess, 67, 68 ; nensy of selection, 65 ; avaecology, 44, 45, 54, 66, 83 ;local dereniation, 82, 83,84 ; selectivty of death, 63,64 ; sockrecruitmen relaton,72, 73

CodStarsh Model, 52, 83 ;compared to other modes, 59

coelenteraes, 5, 1 1, 52Cohen, J , 6cohor halflife 64, 67colonzing speces, frequency of

selfers and asexuals, 160comparatve evidence, 3, 78, 1 34competiton between clones, 1 7,

18, 29, 34, 62competon n juvene stages,

36compettive exclusion, 18, 29, 30

1 9 5



X

nkage 108vng fo 47 166looly pne 80ote 52ognomal tne dtuton 48

49 57 58 6972ognomal fetlty dtuton

94 0 0ong ough da 98l 15 1 7 37 53

motaty nuence of ex 1 3813 9 ; nuence of e 667879

moqutoe 23Mule H. ]., 7 141Mulean heoy 7 14muel 87 88mutaton (ate adaptve adjut-

ment of 47; n eaton tolf h f 148 1 49

X

pant (oweng comp titIOn

dung gowth 77 78 ; dpe-a and gene ow 88; dvety of epoductve mode106 07 19 ; fetty vaaton 9 92 94; ocal de-entaton 88; etance toheavy metal 8889 ; evaaton 92 See a eedand epaate pece

eveeole he 132Rcklef R 127Roe S M 78Ro M A, 78otfe 5 6 06oundwom 23 24

Sage G R 43Sauy ]., 65 69 94amon 126



lottey anaogy 15 1 7 37 53Louck . L. 78 90Lowenty Mode 22low fecundty dened 62 ; popu-

aton 62 12

Mcelly . 88 89mammal 62 12 26 137 See

a epaate peceman (pmtve natual elec-

ton 48 6366 ; fetty exce6768 ; mate electon 2 8

Makovan v nonMakovanpopulaton 7275

male pegnancy 32

mate electon male v femaletatege 128 3Mathe K 1 17, 18May R M 19nMaynad Smth ]. cot of meo-

8 1 ; dplody and dom-nance 13 48; genetc load25 47 ; goup electon 14 2 ;eouce allocaton n hemaphodte 1 20 ; pmtve exualty 1 12 ; ole of ecom-naton n evouton 7 59 14453 154; ex a hottemadaptaton 3 12 14 25 59

60 144 53May . 64 140 163 167mce 81mdwfe toad 133Mtton ] B, advantage of exu-

alty 2 1 8 2 38 4 41 ;oyme vaaton 84 87 88

Mole 82 83 87m�lluk 102. See a epaate

pecemonogamy 3 131 138

lfe htoy featue 148 1 49 ;oe n Muean heoy 65

142 143

neghohood eedng gop53 56 61

ocean cuent 553 83 87onald P 92 124 128hta 47 141 145 54ogochaete 2 123oa ncuaton 3 3 1 34 36an G, 130 3 2ovepecaaton 15 8 1 59oyte ecology of ealy tage

37 38 75 ; gonad and fcun-dty 38 3 12; electon expement 75 ; genetc load80 8

Papaver 96Paramecum 7paate extpaton o hot

159paentopng conct 03Pake G A 1 1 120pathenoene v exual egg

poucton 8; v vegetatveepoducton 10; otace to

evouton of 1 31 04 ; expe-ment 4 ; facutatve 1 046; n veteate 15 ntukey 05 ; n fen 1 06 ; nDrpha 105 ; n weevl16 1 1 62 ; clacaton 17

paenge pgeon 157158phyogene andom 65 1 66ppeh 32Paer 44place 8 97 99

9 8

p ppanulae 5

poecd he 129poa ode evouton of 1 14polen expene of 120polyandy 131polyemyony ee twnnngpoygyny 131 132 138polymophm and envonmental

gan 60polypody 104populaton e oe n Mullean

heoy 142pmtve man ee manpmtve exuaty 1 1 2 1 16pott 43potooan 6 7 23 73 1 8

pocd nect 162Perdum 80pteodacty 1 59pulmonate 121122pycnogond 133

ecomnaton adequacy of lowate 168 69; electon ochanged ate 109

epoductve eot optmatonof 125

epoductve functon canala-ton of 130

epoductve olaton 13

epoductve mode clacatonof 11 4epoductve value 46 7 1 28eptle egg 13eptle 103 15 155156

158159 16162eouce depleton y nceaed

adaptaton 159eponeto electon expemen t

75 47 16eveeole d 13 4

Samplng o Model 2 2 1 23

Scheltema R. S 51 52Schopf J M. 87Scott pne 80ea uchn 126eahoe 13 2Sebae 26eed dpeal and domancy 5Selande R. K 81 132 147electon had and oft 47 48 ;

of ate of development 66 ;thehold 13 47 48

electve event 63eectvty of juvene death 65elf fetla ton 1 7 08. See

a needng genetc oadelf ncompatalty mechanm18

enecence 35 11ex deence n tne vaal

ty 97 3 813 9 ; n epoductve tategy 124; n motal-ty 138139

ex ato 1 19 1 20exual epoducton advantage

of 3 7 12 39 7601 1 1 1 2 1 40 14 1 52 15 355; compaed to aexual epoducton 4; dened

1 141 1 7 ; dvety and cla-caton 106108 1 1 11 17 15 equlum wth aexual 1 1 8 31 32 63 141 42 ; evolu-tonay o 02103 105662; a maladaptve chaac-e 02103 06 191 10 ;optmum tmng 45 22

exual v aexual popuaton acoone 144 1521536062 164; evolutonay

9 9

I X

procee 14, 146, 12 3 ; extinction rate 4,6; genotypic compoition3, 14, 14, 2, 6, 6

exua eection 24 28, 13Simbero . S. 16Simpon G G 4, 8iyphean genotye 2, 3, 37,

40, 760, 7, 01, 3, 167SizeAdvantage Model 22S i h V G F 1 2

dierence in reroductivetrategy 1232, 338

trout 1tuna 74, 86turbearian 6, 2 turkey 10urner J R G. 10turtle 23, 8twinning 13, 1 1

i l d i 6

ibray of Congre Cataloging in ubliction Data

Wlams, Gor Chrstophr 1926Sx and oluton

Monoaphs n populaton oloy 8

Bloaphy p



Smith V G F, 1 , 2nai 23, 08, 1222Solbrig . . 6piny lobter 2porozoan 6, 23quid 23quirrel 8, 32tarh 44, Stebbin G , on eection in

pant population 6, 8, 0 ;on aexual reproduction inplant 04, 1, 62, 167,68 ; on taxonomic ditributiono lo o exuality 63, 167

teriemale method o pouationcontrol 72, 73

tockrecruitment relation 68,72, 7

trawberrie 7StrawberryCoral Model 26;

compared to other mode 33,3, 38, 42, 44

trugge or exitence 63Suomalainen . 160 61yngnathid he 13 2, 13 6ynthetic lethal 47

tadole 78, 7tapeworm 18territoriality 3, 3, 3, 37

tree 6, 8, 80, See alsoelmtrematode 22, 23, 8riton Model river R. on ex dierence

in mortaity 38, 13; on ex

uniparental reproduction 6, 6

Van Val en , 8vertebrate arthenogenei in

0 ; a trematode or porozoan hot 23

viability variation in highecundity population 4, 0,

vole 81

Wadingtn C. 6Warburton F . 60, 2, 1 3wa 3 6Waton . M. S. 64, 6weevi 6, 61

Weimann A. 2, 63, 67White J, 8White M. J 006, 18Wiliam G C AphidRotie

and myter Mode 123, 820, 384 ; eel varia-tion 84; mutation rate481; organic v. bioticevolution ; ex dierence24, 30

Wilon . 6Wright S. 66Wynnedward V C. 64, 8

124, 127, 134, 12, 6

yearcla uctuation 6872

ZZ (zygotetozygote increae 22, 43, 4, 62, 7 , 88, ,12, 06

2 0 0

p y p1 Eoluton x Boloy I Ttl

II rs [DNLM 1 Eouton 2 Rproducton3 x W1 M0568L 8/Q471 W723s]Q371W54 7 74298

IBN 0691081476IBN 0691081522 pk

sex and evolution (1975) by george christopher williams

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