2004 - wesolowski, t. - the origin of parental care in birds; a reassessment.pdf

7/22/2019 2004 - Wesolowski, T. - The origin of parental care in birds; a reassessment.pdf

1/4

The origin of parental care in birds:a reassessment

Tomasz WesoowskiDepartment of Avian Ecology, Wrocaw University, 50 335 Wrocaw, Sienkiewicza 21, Poland

Birds reproductive biology is unique in several respects,including patterns of parental care. Biparental care is thenorm in birds; it occurs in more than 90% of living species(Kendeigh, 1952), whereas in all other animal groups, ifbiparental care occurs at all, it is much less common than isuniparental paternal or maternal care (Clutton-Brock, 1991).The reasons for this peculiar pattern are still not fullyunderstood. The studies on avian parental care usuallyassumed that biparental care was primitive in birds, andtheoretical effort was concentrated on finding ways to explainhow unaided male or female care could have evolved from it

(references in Wesoowski, 1994). The problem of how thisavian biparental care system has evolved in the first place wasusually completely ignored. Fortunately this situation hasbeen changing lately. Several studies pursued problems of theevolutionary origins of parental care by attempting toreconstruct the earliest stages of parental care in birds. Thefirst serious attempt to derive parental care origins from thereptilian state was made by Kavanau (1987). He proposed thatthe appearance of parental care and further changes in itsmode in stem reptiles constituted the first major event inavian evolution. In other words, the first step on the wayleading to birds was the achievement of advanced biparentalcare (consisting of egg guarding, as well as grooming, pro-tecting, and escorting of young) by stem reptiles. All otherchanges, such as attaining homeothermy and the ability to fly,

came later. So the first birds would have been biparental withprecocial young. Kavanau also proposed that the main forcebehind the evolution of flight was the need in arborealreptiles to gain rapid access to ground nests.

Van Rhijn (1984, 1990), El_zzanowski (1985), and Handfordand Mares (1985) were the first to suggest that the earliestform of parental care in birds was unaided male care derivedfrom lack of care in the reptilian ancestors. Following theirarguments and other sources of information, I proposeda multistage model of the origin of parental care and theevolution of parental roles in birds (Wesoowski, 1994) as analternative to Kavanaus scenario. It assumed that poweredflight evolved for reasons independent of reproduction, andthat parental care evolved as a response to it, withina framework of limitations set by adaptations to aerial loco-motion. The unique system of care was then explained interms of evolutionary responses to the design constraintscreated by, and ecological opportunities associated with, theorigin of flight. It was proposed that evolution proceededinitially through stages without parental care (main adapta-tions to flight appeared then) but with increasing investmentin eggs, resulting in the appearance of sequential ovulationand of very large eggs, thus producing young able to flyshortly after hatching. It was suggested that parental careappeared only at that stage, and that it was unaided paternalcare (preserved in some groups). Biparental care then evolvedfrom unaided male care. This model was corroborated andextended by Ligon (1999). Moreover, results of an analysis ofincubation patterns in extant birds by Vehrencamp (2000)also suggested that the ancestral state for birds was sole male

incubation, from which several forms of shared incubationand female only care have arisen.

However, several investigators (Burley and Johnson, 2002;Prum, 2002; Tullberg et al., 2002; Varricchio et al., 1999) haverecently challenged the no care to male care first hypothesisand proposed that parental care is primitive in Archosuaria.They proposeanalogously to Kavanaus (1987) modelthatchanges in the mode of parental care in some ordinaryreptiles constituted the first major event in avian evolution;that is, the first step along the way leading to birds was theachievement of advanced biparental care (consisting of egg

guarding, incubation, as well as protecting and escorting ofyoung) by reptiles. The ability to fly came later, without a tightrelationship to the parental care mode. Tullberg et al. (2002)and Burley and Johnson (2002) claim to reject the male carefirst scenarios, and the latter investigators write, Argumentsfor the male care first hypothesis have not been presented inany detail. . ., and thus they cannot be inspected closely. . .Proponents of the male care first hypothesis need to articulatescenarios that would obviate these problems. Being one ofthem, I feel called to the blackboard.

I begin these comments by addressing the strength andvalidity of the main paleontological, phylogenetic, and cost/benefit arguments put forward in favor of the maternal carefirst scenarios. I conclude by proposing a set of minimumrequirements that any comprehensive theory of the origin of

parental care should fulfill.As not all investigators using terms such as parental care,incubation, or (in a paleontological context) even birdor avian mean the same, it is necessary to define these termsto avoid ambiguities. In the present discussion, parentalcare will be limited to behavioral aspects of the enhancementof egg and/or young survival by parents, taking place in thepostoviposition period (Wesoowski, 1994); bird or avian,to the first organisms capable of powered flight and all oftheir ancestors; and incubation to direct transfer of heatfrom parents body to eggs.

Have dinosaurs incubated?

In a recent review, Prum (2002) writes, It is little appreciatedthat fundamental aspects of avian reproductive biologyevolved during early archosaurian and theropod ancestry. Itis easy to see, however, that extensive parental care is primitiveto archosaurs. What is the justification for these statements?

Norell et al. (1995) described from Upper Cretaceousdeposits of Mongolia an Oviraptorspecimen fossilized on topof a nest with eggs. They suggest that this individualsproximity to the nest was related to parental care andconclude that this finding provides the strongest evidenceyet that modern avian brooding behavior evolved long beforethe origin of modern birds and among non-avian manirap-toran theropods. Varricchio et al. (1997) describe two nestsofTroodon formosusfrom Late Cretaceous deposits in Montanacontaining partially buried eggs. One of them contained 22eggs, bottom parts of which formed a paired arrangement.

Behavioral Ecology Vol. 15 No. 3: 520523DOI: 10.1093/beheco/arh039

Behavioral Ecology vol. 15 no. 3 International Society for Behavioral Ecology 2004; all rights reserved.


2/4

This pattern, though, was not visible in the second clutchcomposed of 24 eggs, in which the eggs were tightly packed(their bottom parts were not visible). They use theseobservations and that of a nest structure, to conjecture that(1) eggs were laid two at a time at one- to several-day intervals,so a lengthy laying period was necessary to complete a clutch;(2) eggs were incubated by direct body contact; and (3) thesame was true for

Oviraptor. In the second article, describing

the same two nests (Varricchio et al., 1999) these suggestionsturn to facts: The nest protected the eggs by creating asuitable micro-environment during the lengthy egg-laying andincubation periods. . . Some reproductive features typicallyassociated with living birds first evolved within non-aviancoelurosaurian theropods like Troodon. These conclusionsare cited without any caveats in review articles by Padian andChiappe (1998) and Prum (2002); so by repetition, they arebecoming an orthodoxy.

Deeming (2002), after examination of published data onpositioning of eggs in theOviraptors nests and on the egg size,shape, and shell structure concludes that the Oviraptors eggswere almost certainly completely covered by substrate, mostlikely sand, and the animal was laying on top of nest mound,rather than sitting directly on top of the eggs. Contact

incubation was not possible. The possibility of Troodonincubating eggs has not been critically scrutinized so far.The conjectures of Varricchio et al. (1997) on ovulation pat-terns and lengthy egg-laying periods are based exclusively onthe egg arrangement in one of the nests. However, thepositioning of eggs need not be in any way dependent on thetemporal pattern of laying-even mass-laying organisms layconsecutively, only one egg at a time. Thus, laying femaleshave behavioral control of placement of their consecutiveeggs. For example, although all birds lay eggs singly at longintervals, they either put all eggs into a single nest or depositeggs in several nests (brood parasites).

Summing up, the paleontological data demonstrate theexistence of early forms of parental care (nest guarding) insome theropod dinosaurs, but contrary to the claims, they do

not provide solid evidence for the existence of contactincubation or presence of lengthy egg-laying periods in anytheropod species. Therefore, for the time being, the two latterfeatures should be treated, as before, as unique avian traits.

Parental care in crocodiles, dinosaurs, and birds:homologous or analogous?

Varricchio et. al. (1999) and Prum (2002) propose that par-ental care is primitive in Archosuaria. Tullberg et al. (2002)and Burley and Johnson (2002) share this view and indicatefemales as the caring sex. They propose that the commonancestor of crocodilians dinosaurs and birds was an animal inwhich females provided parental care. Thus, the presenceof parental care in the extant crocodilians and birds isa homologous trait, derived from the common ancestor. Thisis the most parsimonious explanation. However, the mostparsimonious answer is not automatically true (for review, seeHarvey and Pagel, 1991). Parsimony is only a useful analyticaltool, and not an intransgressible law of nature; it cannot beused to dismiss other possibilities without even consideringthem. What other arguments, besides parsimony, speak infavor of homologous origin and/or against independentorigin of parental care in birds and crocodiles?

Generally, any homology assumption would be wellsupported if (1) the trait considered was unique and/orcomplicated (its origin would be very improbable or difficult),(2) the compared groups were close relatives, and (3) dif-ferences were of only quantitative character. None of theseconditions seem to hold in the crocodile-bird case.

The initial steps of parental care evolution (egg/youngguarding) have been independently reached by manyorganisms in many major invertebrate and vertebrate groups(for review, see Clutton-Brock, 1991; Reynolds et al., 2002), sosuch behavior evolves easily and the presence of egg guardingin crocodiles is not anything unique, anything that could notindependently evolve in different lineages of Archosauria.

Though crocodiles are closest living relatives of birds, theyare nevertheless only distantly related, the last commonancestor of birds and crocodiles lived more than 200 (possiblyas long as 260) million years ago (Broom, 1913; Walker, 1972).We do not know anything about the presence of parental careand its form in this ancestor or in its descendants leading tobirds and crocodiles, respectively. In proposing homology, wehave to assume that in all of these forms females guardedeggs, that no cases of care loss and regaining could haveoccurred. It is unclear how this assumption could hold true,when only within Chardriformes, a single order of birds,several independent instances of maternal care gain and losstook place (Szekely and Reynolds, 1995).

Thorough knowledge of phylogenetic relationships amongdifferent groups of fossil reptiles/early birds and theirbreeding habits would be critical in resolving the homology

issue and in reconstructing consecutive evolutionary transi-tions of parental care patterns. Recent surge of discoveries ofnew fossils of early birds (for review, see Padian and Chiappe,1998; Prum, 2002) brings some hope for the future, butcurrently we are rather far from this goal; relationshipsamong different lineages are still hotly debated (for review,see Prum, 2002).

In a situation in which most taxa are missing from thereconstructed phylogenies, the usage of formal cladisticanalysis cannot be of much help in resolving the problem(Burley and Johnson, 2002; Grant, 2001; Harvey and Pagel,1991; Schluter et al., 1997). The results of such analysis ofpatterns of parental care in birds and other terrestrialvertebrates by Tullberg et al. (2002) clearly demonstrate thelimitations of the cladistic techniques in such circumstances.

Their cladograms suggest several quite unrealistic evolution-ary scenarios; that is, maternal care would be primitive notonly in Archosuaria, but in all reptiles (parental care inmammals and crocodiles would be homologous), andmaternal care would be lost in Chelonia and Squamata.

Taken together, the above arguments indicate that in thecrocodile-bird case the homology hypothesis seems veryweakly substantiated, so the possibility of independent originsof parental care has to be seriously considered in any attemptsto reconstruct the evolution of parental care in differentArchosaurian lineages (Ligon, 1999; Wesoowski, 1994).

Could paternal care in birds evolve first?

Burley and Johnson (2002) think not. They maintain that thearguments for the male care first hypothesis have not beenpresented in sufficient detail, and they raise several issues(nest building, anisogamy, paternity certainty, and incuba-tion) purported to prevent the evolution of paternal care butapparently not adequately covered. However, to large extent,Burley and Johnson (2002) criticize arguments never putforward in the original models. They impute that a male carefirst scenario would require that birds evolved from anancestor in which females showed no preparation of nestsite. . . after evolving surface nesting, whereas Wesoowski(1994) proposed that initially there was no post-ovipositionalegg care and that the ancestors of birds probably buried eggsin reptilian fashion. Similarly, nowhere in Wesoowski (1994)is there a slightest hint, suggesting that the continuousincubation of eggs could have occurred in the first stages of

Wesoowski Origin of parental care in birds 521


3/4

evolution, yet Burley and Johnson (2002) claim that paternalcare could not evolve because continuous incubation wouldcompromise a males ability to defend his territory an locateadditional mates. Several paragraphs in Wesoowski (1994)are devoted to discussion of the certainty of paternityproblem. In line with arguments put forward by numerousinvestigators (for review, see Clutton-Brock, 1991), conditionsin which parental males could combine female attraction,paternity assurance, and egg guarding were specified. Briefly,males controlling access to the laying grounds could tradecopulations for egg-laying; females would not be permitted tolay eggs within a territory without having first copulating andstaying for some time with the territory owner. Moreover,recent molecular studies onJacana jacana(Emlen et al., 1998)and Struthio camelus (Kimwele and Graves, 2003), showinghigh frequency of mixed brood paternity, demonstrate thatthe extensive paternal care can co-occur with low paternitycertainty. Burley and Johnson (2002) do not question thesearguments, yet they raise the lack of paternity certainty todismiss the possibility of sole male care evolution. The last ofarguments against the paternal care first put forward by themis anisogamy. It is true that there is a built-in asymmetry in theno care situation, because females have to choose nest sites,

prepare laying sites, and lay eggs before leaving the place. Theappearance of paternal care in such conditions constitutesreally a challenge, as birds are the most anisogamous ofanimals. However, anisogamy itself does not constitute aninsurmountable hurdle. Sole paternal care has evolved manytimes in different organisms (invertebrates, fishes, or am-phibians; for review, seen Clutton-Brock, 1991; Reynolds et al.,2002). The problem of why avian males engage so frequentlyin parental care, despite extreme anisogamy, is fully recog-nized by Wesoowski (1994); large sections of this article aredevoted to addressing this puzzle.

Problems with the paternal care first scenarios seem to becaused to a large extent by misunderstanding of theirarguments by Burley and Johnson (2002) and not by seriousbiological flaws inherent in these scenarios. Refutation of the

no to sole paternal care avenue of the parental care originsin birds would demand providing arguments stronger thanthose currently available. Therefore, for the time being, thisscenario should remain a working hypothesis, worth furthertesting.

Requirements of a comprehensive theory ofthe parental care origin in birds

As follows from the previous discussion, the issue of parentalcare origins in birds is still controversial and will (hopefully)stimulate further theoretical and empirical work in the yearsto come. However, it seems that suggesting some guidelinesand some minimum methodical requirements that the futureproposals should abide would be helpful in making theseefforts more efficient.

First of all, the models should simultaneously account forall the existing patterns: origins of surface nesting, sequentialovulation, incubation, enormous increase in egg size, changeof copulatory mode combined with loss of phallus (Frey, 1995;Wesoowski, 1999), and participation of each sex in parentalduties. They should relate these traits to the appearance offeatures connected with powered flight (high metabolic rate,endothermy, determinate growth, very fast growth rates,stiffening of trunk, and shortening of abdomen). They shouldalso propose a relative timing for all of these events, as well asrelationships among them-which factors were causal, whichpermissive, and which necessary but insufficient themselves(e.g., whether sequential ovulation evolved before or afteronset of incubation, what selective agents lay behind the

development of the former or the latter). They also have toaccount for the known taxonomic distribution of differentcare modes; that is, they should propose why uniparentalfemale care in extant birds occurs in several separate lineagessituated near the tips of phylogenetic branches, whereasgroups with uniparental male care or with sole maleincubation are situated close to the base of the tree (Szekelyand Reynolds, 1995; Vehrencamp, 2000). They have toexplain, as well, the existence of superprecociality in at leastsome Upper Cretaceous Enatiornithes, (young of Gobipteryxwere able to fly shortly after hatching; El_zzanowski, 1985).

All these explanations must be internally coherent. Aquestion of monophyletic versus parallel origin of parentalcare in birds should be addressed as well. All cost/benefitanalyses of parental options must not use good for theopposite sex arguments (it would be good for females ifmales). This is important because fitness can be compared onlywithin a sex. Whether one sex evolves care is not dependentupon advantages or disadvantages to theothersex buton fitnessdifferences of same-sex individuals showing versus nonshowinga given type of behavior (Fisher, 1958; Maynard Smith, 1977).Finally, a more critical evaluation of evidence, both alreadyknown and forthcoming in future work (especially of fossil

data) should be made before drawing any inferences. Specif-ically, using the physical association of a fossil animal with eggs,without examining all the available evidence, as a sole argumentforthe existence of incubation, shouldbe avoided, as it canleadto the wrong conclusions (Deeming, 2002).

I do hope that if future models are prepared according tothese specifications, it would bring us closer to the final goal-reconstruction of the actual history of the of parental careorigin in birds.

I am grateful to all the people who have recently published articles onthe origins of parental care in birds. Although sometimes I disagree

with their arguments, their work has inspired me to rethink my ideason this subject and stimulated me to write these comments. I alsohighly appreciate comments of Sandra Vehrencamp and anonymous

refrees on an earlier draft of this manuscript.

Address correspondence to T. Wesoowski. E-mail: [email protected].

Received 14 February 2003; revised 5 July 2003; accepted 17 August2003.

REFERENCES

Broom R, 1913. On the South African pseudosuchian Euparkeriaandallied genera. Proc Zool Soc Lond 1913:619633.

Burley NT, Johnson K, 2002. The evolution of avian parental care. PhilTrans R Soc Lond B 357:241250.

Clutton-Brock TH, 1991. The evolution of parental care. Princeton,

New Jersey: Princeton University Press.Deeming DC, 2002. Importance and evolution of incubation in avian

reproduction. In: Avian incubation (Deeming DC, ed). Oxford:Oxford University Press; 17.

El_zzanowski A, 1985. The evolution of parental care in birds withreference to fossil embryos. In: Acta XVIII Congressus Internation-alis Ornithologici, Moscow, 1982, vol. 1 (Ilyichev VD, Gavrilov VM,eds). Moscow: Nauka; 178183.

Emlen ST, Wrege PH, Webster MS, 1998. Cuckoldry as a cost ofpolyandry in the sex-role reversed wattled jacana, Jacana jacana.Proc R Soc Lond B 265:23592364.

Fisher RA, 1958. The genetical theory of natural selection. New York:Dover.

Frey R, 1995. Copulatory organ, mating posture and locomotion: theirinterrelationship in non-mammalian vertebrates. J Zool Syst EvolRes 33:1731.

522 Behavioral Ecology Vol. 15 No. 3


4/4

Grant PR, 2001. Reconstructing the evolution of birds on islands: 100years of research. Oikos 92:385403.

Handford P, Mares MA, 1985. The mating systems of ratites andtinamous: an evolutionary perspective. Biol J Linn Soc 25:77104.

Harvey PH, Pagel MD, 1991. The comparative method in evolutionarybiology. Oxford: Oxford University Press.

Kavanau JL, 1987. Lovebirds, cockatiels, budgerigars: behavior andevolution. Los Angeles: Science Software Systems.

Kendeigh SC, 1952. Parental care and its evolution in birds. IllinoisBiol Mon 22:1358.Kimwele CN, Graves JA, 2003. A molecular genetic analysis of the

communal nesting of the ostrich (Struthio camelus). Mol Ecol 12:229236.

Ligon JD, 1999. The evolution of avian breeding systems. Oxford:Oxford University Press.

Maynard Smith J, 1977. Parental investment: a prospective analysis.Anim Behav 25:19.

Norell MA, Clark JM, Chiappe LM, Dashzeveg D, 1995. A nestingdinosaur. Nature 378:774776.

Padian K, Chiappe LM, 1998. Skad sie wziey ptaki. SSwiat Nauki 4:2635.

Prum RO, 2002. Why ornithologists should care about the theropodorigin of birds. Auk 119:117.

Reynolds JD, Goodwin NB, Freckleton RP, 2002. Evolutionarytransitions in parental care and live bearing in vertebrates. Phil

Trans R Soc Lond B 357:269281.

Schluter D, Price T, Mooers AO, Ludwig D, 1997. Likelihood ofancestor states in adaptive radiation. Evolution 51:16991711.

Szekely T, Reynolds JD, 1995. Evolutionary transitions in parental carein shorebirds. Proc R Soc Lond B 262:5764.

Tullberg BS, Ah-King M, Temrin H, 2002. Phylogenetic reconstructionof parental-care systems in the ancestors of birds. Phil Trans R SocLond B 357:251257.

van Rhijn J, 1984. Phylogenetical constraints in the evolution of

parental care strategies in birds. Neth J Zool 34:103122.van Rhijn JG, 1990. Unidirectionality in the phylogeny of socialorganization, with special reference to birds. Behaviour 115:53174.

Varricchio DJ, Jackson F, Borkowski JJ, Horner JR, 1997. Nest and eggclutches of the dinosaurTroodon formosusand the evolution of avianreproductive traits. Nature 385:247250.

Varricchio DJ, Jackson F, Treuman CN, 1999. A nesting trace with eggsfor the Cretaceous theropod dinosaur Troodon formosus. J VertPaleont 19:91100.

Vehrencamp SL, 2000. Evolutionary routes to joint-female nesting inbirds. Behav Ecol 11:334344.

Walker A.D, 1972. New light on the origin of birds and crocodiles.Nature 237:257263.

Wesoowski T, 1994. On the origin of parental care and the earlyevolution of male and female parental roles in birds. Am Nat 143:3958.

Wesoowski T, 1999. Reduction of phallus in birds: an avian way to safe

sex? J Avian Biol 30:483485.

Wesoowski Origin of parental care in birds 523

2004 - wesolowski, t. - the origin of parental care in birds; a reassessment.pdf

Documents