evolution in the genus homo

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Evolution in the GenusHomoBernard Wood1 and Jennifer Baker1,2

1Center for the Advanced Study of Hominid Paleobiology and 2 Hominid PaleobiologyGraduate Program, Department of Anthropology, George Washington University,

Washington, DC 20052; email: [email protected]

Annu. Rev. Ecol. Evol. Syst. 2011. 42:4769

First published online as a Review in Advance onAugust 11, 2011

TheAnnual Review of Ecology, Evolution, andSystematicsis online at ecolsys.annualreviews.org

This articles doi:10.1146/annurev-ecolsys-102209-144653

Copyright c2011 by Annual Reviews.All rights reserved

1543-592X/11/1201-0047$20.00

Keywords

clade, grade,Homo habilis, modern human genome

Abstract

We review the fossil and genetic evidence that relate to evolution genusHomo. We focus on the origin ofHomoand on the evidence f

onomic diversity at the beginning of the evolutionary history ofHom

in the last 200,000 years. We set out the arguments for recognizingond earlyHomotaxon,Homo rudolfensis,and the arguments for and a

including Homo habilis sensu stricto and Homo rudolfensiswithin Homend by reviewing recent genomic evolution withinHomo. The challe

the upcoming decades is to meld innovations in molecular genetic mand technology with evidence from the fossil record to generate hypo

about the developmental bases of the phenotypic and behavioral dements we see within the genusHomo.

47

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INTRODUCTION

Carl Linnaeus introduced the genus Homo to zoological nomenclature in 1758, including it his Order Primates along with monkeys and lemurs. As originally conceived by Linnaeus,Hom

included two species,Homo sapiens(i.e., modern humans) andHomo troglodytes,a taxon based a melding of de Bondts (1658) Homo sylvestrisOrang Outang that may have been based on

real orangutan or an unusually hirsute modern human and contemporary Swedish descriptioof albino people living in caves in the Moluccas. This review focuses on the interpretation of th

genusHomoimplied by the inclusion of onlyH. sapiensof these two; consideration ofH. troglodyis best left to historians of science.

The history of the various ways the genusHomohas been interpreted since its introduction

the tenth edition of Linnaeuss Systema Naturaehas been reviewed elsewhere (Wood 2009). Tquick and dirty version of that review is that there have been episodic relaxations, some expli

and some implicit, of the criteria used to decide which taxa should be included within the genHomo. Each episode has resulted in the addition of one or more extinct taxa to the list of spec

recognized withinHomo(Table 1).

Table 1 Significant specific additions to the genus Homo

Reference Taxon name Type specimen Phenotypic implications

Linnaeus 1758 Homo sapiens None designated The genusHomowas erected on the basis of the

phenotype of modern Europeans.

King 1864 Homo neanderthalensis Neanderthal 1 Crania with rounded supraorbital margins, faces

that project in the midline, distinctive parietal

and occipital morphology; robust limb bones

with relatively large joint surfaces.

Schoetensack 1908 Homo heidelbergensis Mauer mandible Mandible that lacks a true chin and has a more

robust corpus than that seen in modern human

and Neanderthals.

Smith Woodward

1921

Homo rhodesiensis Kabwe 1 (aka E 686) Crania and long bones are substantially more

robust than those of modern humans and

Neanderthals.Oppenoorth 1932 Homo(Javanthropus)soloensis Ngandong 1

(by implication)

Crania with lower and longer brain cases that ar

widest across the base.

Mayr 1944 Homo erectus Trinil 1 Crania with a smaller brain case than any of the

taxa above, plus a continuous supraorbital toru

angular, occipital, and sagittal tori; and

compressed femoral and tibial shafts.

Leakey et al. 1964 Homo habilis OH 7 Crania with an even smaller brain case

(approximately 600 cm3). The authors

interpretedH. habilisas being dexterous, uprigh

and bipedal as well as capable of spoken

language, but fresh evidence and fresh

interpretations of existing evidence have ledothers to offer rather different functional

assessments of the same material.

Groves 1989 Homo rudolfensis KNM-ER 1470 Contra all of the above, the middle of the face is

broader than the upper part, the cheek bones a

more anteriorly situated, and the premolars and

molars are larger and have more complex cusps

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4

3

2

1

0

Ardipithecus ramidus

Australopithecusafarensis

Paranthropusrobustus

6

5

7

8

Orrorin tugene

Homoneanderthalensis

Homo sapiens

Sahelanthropustchadensis

Mya

Homo oresiensis

Transitional hominins

Premodern Homo

Megadont archaic hominins

Archaic hominins

Possible early hominins

Anatomically modern Homo

Australopithecussediba

Homoheidelbergensis

Homoantecessor

Homoergaster

Homorudolfensis

Homohabilis

Australopithecusbahrelghazali

Kenyanthropusplatyops

Australopithecusafricanus

Australopithecusanamensis

Paranthaethiop

Australopithecusgarhi

Paranthbois

Ardipithecuskadabba

Homoerectus

Figure 1

The taxa recognized in a typical speciose hominin taxonomy; the species conventionally included withinHomoare emphasized iThe taxa are sorted into grades (see Wood 2010a for details); the three grades that containHomotaxa are in bold. The height ofcolumns reflects either uncertainties about the temporal age of a taxon, or in cases in which there are well-dated horizons at sevesites, it reflects current evidence about the earliest, called the first appearance datum (FAD), and the most recent, called the lastappearance datum (LAD), fossil evidence of any particular hominin taxon. However, the time between the FAD and the LAD isto be represent the minimum time span of a taxon, for it is highly unlikely that the fossil record of a taxon, and particularly the relsparse fossil records of early hominin taxa, include the earliest and most recent fossil evidence of a taxon.

Some paleoanthropologists support a much more inclusive interpretation of the genusHomothantheonesetoutin Figure 1. For example, John Robinson (1972) proposed thatAustralopithecus

be sunk intoHomo. Curnoe & Thorne (2003) went even further, suggesting that only three speciesshould be recognized in the hominin clade and including all three in Homo(i.e.,Homo ramidus,

Homo africanus,andH. sapiens). This review will focus on the more mainstream interpretation ofthe genusHomoset out inFigure 1.

DEFINING HOMO

Genus definitions applicable to the fossil record use two different categories of inference (Wood

2010b). The first employs phenotypic evidence to generate hypotheses about the closeness, orotherwise, of the relationships among the species in question. Are the taxa in the same clade? The

second also employs phenotypic evidence, but uses it to generate hypotheses about the adaptive

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grade of the taxa. Are the taxa in the same grade? Wood (2009) includes thumbnail reviews

contemporary genus definitions, but most researchers who focus on the hominin fossil reco

implicitly, if not explicitly, subscribe to a genus definition that combines information about cladand grades. This is certainly the case for the way most researchers interpret the genusHomo.

It is widely assumed, but rarely articulated, that the species included inHomo should comprismonophyletic group or a clade; in other words, they should share a most recent common ancest

that is not shared with taxa belonging to a different monophyletic group. But although all geneshould be clades, not all clades are necessarily genera. This is because most paleoanthropologi

assume (but also rarely articulate) that the taxa within a genus should share the same functioncharacteristics or competencies. In the case ofHomo, suggested shared competencies include t

ability to use complex language; to make the only type of tools, stone tools, that can be reliabdetected in the early archeological record (as in Man the toolmaker); and to hunt (as in M

the hunter). Therefore, the search for the origin of the genusHomo is a search for the origin of

entity that is both a clade (sensuHennig 1966) and a grade (sensuHuxley 1958) (Wood & Colla1999).

There are two options for applying the two main criteria for genus identification (i.e., monphyly and adaptive coherence). One can start in the present and work back in time, or one c

start in the past and work toward the present. The former top-down approach focuses on thtype species of the genusHomo(i.e.,H. sapiens). It involves taking stock of hypotheses about t

nature of its derived morphology and behavior, deciding on the cardinal features and behaviothat define the adaptive zone ofH. sapiens,and deciding on the characters that will be used to ge

erate hypotheses about the relationships among the extinct taxa that are candidates for inclusioinHomo. Then one works backward into the tree of life, applying the same tests to each homin

taxon encountered. Is there reliable evidence (i.e., the same cladogram is generated even if o

changes details of the operational taxonomic units and/or uses different outgroups, different combinations of characters, etc.) that the taxon is in the same subclade as H. sapiens? Is there reliab

evidence (i.e., reliable quantitative proxies of behaviors) that the taxon is in the same adaptizone asH. sapiens? The bottom-up approach involves making a subjective judgment about wh

in the past one starts to pick up the trail leading to Homo. One then works toward the presenapplying the tests set out above to all the hominin taxa encountered. The difference between th

approach and the top-down option is that, in general, the deeper into the past the sparser tfossil evidence, thus making it more difficult to generate reliable evidence about monophyly a

adaptive similarity.Most researchers apparently consider the hypothesis that laterHomotaxa (i.e.,H. sapiens,Hom

neanderthalensis,Homo heidelbergensis,Homo erectus; we discussHomo floresiensisseparately) formmonophyletic group to be so obviously correct that it does not require formal testing, for the

have been few attempts to assess the relationships of those taxa. For example, although Eldred

& Tattersall (1975, figure 4) includedH. neanderthalensis,H. heidelbergensis, andH. erectusin thpioneering application of cladistic methods to hominin relationships, they did not carry out a

formal analysis of the relationships among these taxa.

WHEN DOES HOMO BEGIN?

Some researchers (e.g.,Kimbelet al. 2004, Strait & Grine 2004) have presented what they interprto be compelling cladistic evidence thatHomo habilis sensu strictoand Homo rudolfensisshould

included along with H. sapiens, H. neanderthalensis, H. heidelbergensis, and H. erectuswithin tgenus Homo, and many researchers concur with this judgment. However, we suspect that t

authors who support the inclusion ofH. habilis sensu strictoand H. rudolfensiswithin Homo al

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1

2

Ardipithecus ramidus

Australopithecus anamensis

Australopithecus afarensis

Australopithecus africanus

Kenyanthropus platyops

Paranthropus robustus

Paranthropus boisei

Paranthropus aethiopicus

Homo habilis sensustricto

Homo rudolfensis

Homo erectus sensu lato

Homo sapiens

Australopithecus garhi

Sahelanthropus tchadensis

Figure 2

A cladogram presenting one hypothesis regarding the relationships among early hominins. The nodes 1 and2 represent two hypotheses for the lower boundary of theHomoclade. IfHomowere to include node 1, itwould embrace the species presently included in earlyHomo(i.e.,H. habilis sensu stricto andH. rudolfensis). IfHomowas defined so as to exclude node 1, and to include just node 2, then it would be confined to earlyAfricanH. erectusand temporally later, more derived Homospecies (adapted from Wood 2009).

accept that the evidence for including them is not as strong as the evidence for including, say,H. neanderthalensis,H. heidelbergensis, andH. erectus. Thus, as far as relationships are concerned,

there seem to be two options for the lower, older, boundary of the genus Homo: to draw theboundary so that it includes H. habilis sensu stricto and H. rudolfensis(Figure 2, node 1), or to

draw it beneath early AfricanH. erectusso that it excludesH. habilis sensu strictoandH. rudolfensis(Figure 2, node 2).

GRADE CRITERIA FOR INCLUDING TAXA WITHINHOMO

As far as the grade criterion is concerned, Wood & Collard (1999) suggested that adaptive sim-

ilarity should be judged on the basis of data (preferably quantitative) taken directly from thehard tissue evidence rather than on secondary inferences generated from the hard tissue evi-

dence. The adaptive criteria they suggested included body size and shape (as reflected in longbone lengths, limb proportions, etc.), posture and locomotion (as reflected in the morphology of

the limbs and the bony labyrinth), circumstantial evidence of cognitive ability (as reflected inabsolute and relative brain size, etc.), evidence of dexterity (as reflected in digit proportions,

carpal bone morphology, etc.), diet (as reflected in mandibular corpus area, postcanine crown

area, enamel thickness, enamel microwear, etc.) and life history (as reflected in the only availableproxies for life history, the developmental tempo of teeth and bones).



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With respect to body size and shape, Richmond et al. (2002) demonstrated that the lim

proportions of OH (Olduvai Hominid) 62, the only associated skeleton securely assigned

H. habilis sensu stricto, are not statistically significantly different from the limb proportions A.L. (Afar Locality) 288-1 (also known as Lucy), the best-preserved associated skeleton belongi

toAustralopithecus afarensis. However, Reno et al. (2005) have suggested that any estimate of tlength of the OH 62 femur (and thus the estimated value of the humerofemoral index of O

62) must be treated with caution. Haeusler & McHenry (2004, 2007) also investigated the limproportions of earlyHomo by looking at OH 62 and a second probable H. habilis sensu striassociated skeleton, KNM-ER (Kenyan National Museums-East Rudolf) 3735, from Koobi Foin Kenya. They concluded that the limb proportions of both of these skeletons are more mode

humanlike than chimpanzee-like. However, their use of OH 34 to derive the limb proportionsOH 62 is controversial, as are their conclusions with respect to KNM-ER 3735. Thus, althoug

there is still doubt about the precise limb proportions of the individuals represented by OH

and KNM-ER 3735, it is fair to say that most informed observers subscribe to the view that tlimb proportions of OH 62 are more similar to those of archaic hominins (i.e., Australopithec

than to the limb proportions of modern humans and extinct laterHomotaxa such asH. erectus.No limb bones are assigned to H. rudolfensis, but what can be concluded about the postu

and locomotion ofH. habilis sensu stricto? The only postcranial material from Olduvai Gorthat can be securely attributed to H. habilis sensu stricto is the OH 62 associated skeleton. As w

have seen above, what can be inferred about its limb proportions would argue against a lat

Homo-like posture and locomotion. Ruff (2009) compared cross-sectional bone strength measur

ments at two locations in the femur and humerus of OH 62 with those taken at what were judgeto be equivalent locations in modern humans and chimpanzees as well as in two earlyH. erecspecimens: KNM-WT (Kenyan National Museums-West Turkana) 15000 and KNM-ER 180

For each combination of section locations, the femoral to humeral strength proportions of O62 fall below the 95% confidence interval of modern humans, but for most comparisons th

are within the 95% confidence interval of chimpanzees. In contrast, the two H. erectusspecimeboth fell within or above the modern human distributions. This indicates that load distributi

between the limbs and by implication, locomotor behavior, was significantly different inH. hab

sensu stricto from that seen inH. erectusand modern humans. When considered along with oth

postcranial evidence, Ruff (2009) suggests that the most likely interpretation is that H. habialthough bipedal when terrestrial, still engaged in frequent arboreal behavior, whileH. erectusw

a completely committed terrestrial biped (Ruff 2009, p. 90). Larson (2007) reached comparabconclusions about the shoulder.

Evidence from thesize andshape of thebony labyrinth, which houses thereceptorsthat monitmovement and posture, of early hominins has also been used to make inferences about postu

and locomotor mode (Spoor et al. 1994); this method has the obvious advantage that it uses da

obtained from crania, which are usually more confidently assigned to a taxon than are isolatlimb bones. Among the early hominin specimens considered in that study were Stw (Sterkfonte

Witwatersrand) 53, assigned by some toH. habilis, and SK (Swartkrans) 847, which some assito H. habilisand others to H. erectus. The semicircular canal morphology of the former was

different from that of modern humans that Spoor et al. (1994) suggested that Stw 53 relied leon bipedal behavior than the australopithecines (p. 648). They also suggested that the extrem

differences in labyrinthine morphology between SK 847 and Stw 53 make attribution of bospecimens to the same species, on this evidence alone, highly unlikely (p. 648). In an analysis

the labyrinthine morphology of Sangiran 2 and 4, OH 9 (i.e.,H. erectus) and SK 847, Spoor (199suggested that the dimensions of the semicircular canals (of these taxa) are similar to those

modern humans (p. 254). Thus, whatever taxon Stw 53 belongs to, be itH. habilisor a differe

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earlyHomotaxon (e.g., Grine et al. 1996, Curnoe & Tobias 2006), these results suggest that the

locomotor repertoire of Stw 53 was very different from that ofH. erectusand modern humans.

Brain size as reflected in the volume of the endocranial cavity is an obvious but imperfectproxy for cognition. The difference between the endocranial volumes of chimpanzees and mod-

ern humans apparently match the markedly different cognitive capacities of the two taxa, butat a finer level we are at a loss to explain what the difference between a hominin taxon with

a mean endocranial volume of 600 cm3 and one with a mean of 900 cm3 means in terms ofcognitive capacity. Also, the data usually used to show temporal trends in hominin endocranial

volume, including an apparent increase in endocranial volume around the time of the appearance of

H. habilis sensu stricto andH. rudolfensis, contain a lot more noise owing to measurement and dating

error than most plots of hominin brain size through time suggest.With respect to hard tissue proxies for dexterity, Tocheri and colleagues (Tocheri 2007,

Tocheri et al. 2007) have pioneered the use of 3D analytical methods to study carpal bone shape

in the extant great apes and in fossil hominins. Tocheri et al. (2007) make a convincing case thatthe morphology of the type specimen ofH. habilis sensu stricto(OH 7) resembles the carpal mor-

phology seen in archaic hominins such as A. afarensis. Although they make the point that thisprimitive wrist morphology did not necessarily preclude its owners from using and making stone

tools, the retention of such a primitive carpal morphology in the type specimen ofH. habilis sensu

strictocertainly does not strengthen the claim that the latter taxon should be in the same adaptive

zone as modern humans, at least in terms of dexterity.Hard tissue proxies for diet include the size and shape of the mandibular corpus and the surface

area of the postcanine tooth crowns. Wood & Aiello (1998) used extant taxa to generate twocomparative regressions (a simian one based on 23 taxa and a hominoid one based on 6 taxa) for

the relationship between the means of actual body mass and the height of the mandibular corpus

at the first molar (M1). The authors used the height of the mandibular corpus at M1and the two

comparative regressions to predict body mass for H. habilis sensu stricto (N = 5), H. rudolfensis

(N = 6) and early African H. erectus(N = 7), and then they compared these mandible-basedbody mass predictions with the body masses predicted using either postcranial or nonmandibular

(e.g., orbital height) cranial evidence. The hominoid mandible-based body mass predictions for

H. habilis sensu stricto and for H. rudolfensiswere, respectively, 75% and 100% larger than the

estimates of body mass based on the nonmandibular evidence. Similar discrepancies were seen for

A. afarensisand Australopithecus africanus(Wood & Aiello 1998, figures 3 and 5). In contrast, the

hominoid mandible-based body mass predictions for early African H. erectusmatched those basedon the nonmandibular evidence. Thus, H. habilis sensu stricto and H. rudolfensishave relatively

larger mandibles than early African H. erectus. As for postcanine tooth area, McHenry (1988)developed the megadontia quotient (MQ) as a way to compare the size of the postcanine teeth

of hominins with different overall body sizes. McHenry & Coffing (2000) showed that the endsof the range of the MQ for hominin taxa are 0.9 for H. sapiensand 2.7 for Paranthropus boisei.The body mass estimates they use forH. rudolfensisare almost certainly too large, but the MQ

estimate forH. habilis sensu strictoof 1.9 is likely to be closer to the mark. When compared withthe MQs of 1.7 and 2.0 forA. afarensisand A. africanus, respectively,H. habilis sensu strictoshows

no evidence of any reduction in relative postcanine tooth crown area compared with the twoarchaic hominins with the largest hypodigms. Indeed, its MQ is only a little smaller than the

MQ (2.2) ofParanthropus robustus, whereas the MQ of early African H. erectus(0.9) is the sameas that forH. sapiens. Thus, both sets of results (i.e., mandibular corpus cross-sectional area and

the surface area of the postcanine dentition) suggest that significant reduction in the size of themasticatory apparatus within the hominin clade did not occur until the emergence of early African

H. erectus.



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Researchers interested in using microwear to reconstruct paleodiet are becoming much mo

discriminating about the specimens they judge to contain evidence about microwear. This

because trampling or rolling in the beds of streams and rivers produces microscopic damagethe tooth enamel that could be confused with the microscopic damage produced when tee

make contact with food during chewing. When Ungar et al. (2006) and Ungar & Scott (200applied these more stringent criteria to their initial sample of 83 earlyHomospecimens from thr

southern African and seven east African sites, the sample size decreased to just 18 specimenUngar et al. (2006) concluded that H. erectusand individuals from Swartkrans Member 1 ate,

least occasionally, more tough or brittle foods than didH. habilisand individuals from SterkfonteMember 5C (p. 91). This is more, albeit tenuous, evidence that the diet of early AfricanHomdiffered from that ofH. habilis sensu stricto(see also Ungar et al. 2011).

The life history of a taxon is a reflection of the way the individual members of a taxon ada

to their ecological context by dividing their energy among the tasks of maintenance of the

milieu interieur, production of offspring, and maintenance of offspring prior to them becomiindependent. As far as fossil taxa are concerned, the rate of development of the hard tissues i

proxy for the tempo of ontogeny. Several recent studies have examined the rate of dental deveopment (as judged from dental microstructure) in later hominins (Bermudez de Castro & Ros

2001, Bermudez de Castro et al. 2003, Macchiarelli et al. 2006, Ramirez Rozzi & Bermudez Castro 2004). These studies suggested that the enamel formation rates of the anterior teeth

Neanderthalswere faster than those inH. sapiens, butsubsequent investigations of the developmeof Neanderthal postcanine teeth suggested that the developmental tempo ofH. neanderthalenwas modern human-like (Dean et al. 2001, Guatelli-Sternberg et al. 2005, but see Smith et 2010). Clearly, larger samples are needed, andresearchers should cross-validate their methods, b

Smith et al. (2007) recently demonstrated that the distinctively slow dental development seen

living modern humans can be traced back to at least 160 ka. Even if the developmental scheduleH. heidelbergensis(see above) was not like that of modern humans, it was almost certainly mo

similar to the developmental schedule ofH. sapiensthan to those of chimpanzees and gorillas. contrast, preliminary results suggest that the developmental schedules ofH. erectus sensu stric

earlyAfricanH. erectus,H. habilis sensu stricto,andH. rudolfensiswere more like those of chimpanzeand gorillas than that of living modern humans (Dean & Smith 2009, Robson & Wood 2008

Dean et al. (2001) used long-period cross striations and an empirically derived modal periodicity9 days to estimate enamel formation times, and then they plotted the latter against enamel thic

ness. These analyses show that archaic hominins take, on average, 100 fewer days than modehumans to reach an enamel thickness of 1,000 m. The authors conclude that none of t

trajectories of enamel growth in apes, australopiths or fossils attributed to Homo habilis, Hom

rudolfensis. . . falls within that of the sample from modern humans (Dean et al. 2001, p. 629

Similarly, in his analysis of root formation time in OH 16 (a specimen assigned to H. habili

Dean (1995) identified a nonmodern humanlike pattern.

THE LOWER BOUNDARY OFHOMO

How well does this evidence about adaptive coherence match the cladistic evidence? On the baof adaptation, is it possible to distinguishH. habilis sensu strictoand H. rudolfensisfrom potent

precursor archaic hominins such as A. afarensis? We suggest that, taken overall, the evidenreviewed above suggests that the adaptive regimes of bothH. habilis sensu strictoandH. rudolfenhave as much, if not more, in common with those of archaic hominin taxa (e.g., A. afarensisa

A. africanus) as they do with premodern Homo taxa such as H. erectus. This is why we pref

to include these taxa in a separate grade of transitional hominins rather than including the

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withH. erectus in premodernHomo (Wood 2010a) (Figure 1). Moreover, if the combination

of a modern human-sized brain and the skeletal correlates of obligate long-range bipedalism are

chosen as the adaptive criteria forHomo, then the boundary ofHomowould be set so that it includesH. heidelbergensisbut notH. erectus. But if a modern human body shape and obligate bipedalism

are deemed to be the adaptive criteria for Homo, then the boundary would be set so thatHomoincludes early African H. erectusbut notH. habilis sensu stricto and H. rudolfensis, i.e., node 2 in

Figure 2(for a different interpretation, see Haeusler & McHenry 2004, 2007).

EVOLUTION WITHIN THE GENUS HOMO

If we assume, for the sake of argument, thatH. habilis sensu strictoandH. rudolfensisare included in

Homo (i.e., node 1 in Figure 2), what can be concludedabout evolutionwithin the genusHomo? Do

new species arise primarily through anagenesis, or is there evidence of cladogenesis within Homo?

Are species withinHomoalways time successive, or do the temporal ranges ofHomotaxa overlap?Obviously, answers to these questions are determined partly by the taxonomic philosophy of

the researcher. If species are recognized only sparingly, then anagenesis is a more likely, if not aninevitable, description of evolution within the genus Homo. However, if species are interpreted

as more exclusive entities (Figure 1), then researchers are more likely to recognize a patternthat is consistent with cladogenesis. To what extent are the proposed taxa synchronic? Are they

sympatric? And within long-lasting taxa, is the dominant signal one of stasis or gradual change?Our examination of these issues focuses on just two periods during the evolutionary history of the

Homoclade, one at the beginning of the clade and one in the most recent 200 ka of its history.

EVIDENCE FOR TAXONOMIC DIVERSITY IN EARLYHOMO

In 1964 a new hominin species, H. habilis, was announced with OH 7 from FLKNN (Frida

Leakey Korongo North North) at Olduvai Gorge as its type specimen (Leakey et al. 1964). Theannouncement of a small-brained species attributed to Homo caused considerable controversy,

largely because the date of 1.75 Ma for H. habilisextended the age for the earliest evidence of

Homoby a million years and because the cranial capacity was estimated to be approximately 670

680 cm3, below the generally accepted cerebral rubicon for Homo, which at the time was set (forno particularly compelling reason) between 700 and 800 cm3.

Although Tobias (1991) made a persuasive case that all of the nonmegadont archaic homininsfrom Bed I and Lower Bed II at Olduvai Gorge could be subsumed in a single taxon, H. habilis

sensu stricto,during the first half of the 1970s, it became clear that the earlyHomocranial (e.g.,KNM-ER 1470, 1478, 1590, 1805, 1813, 3732, 3735, 3891) and mandibular (e.g., KNM-ER

1501, 1502, 1802, 1802, 3734, 3891) discoveries from Koobi Fora (East Turkana) were less easyto accommodate within a single taxon. Thus, whereas some researchers supported the retention

of a single taxon for what they interpreted to be the expanded sample ofH. habilis sensu lato (e.g.,

Miller 1991, Suwa et al. 1996), others supported a two-taxon solution (Grine et al. 1996, Krameret al. 1995, Lieberman et al. 1988, Prat 1997, Stringer 1986, Wood 1985). For example, Wood

(1991, 1993) showed that variation within the hypodigm ofH. habilis sensu lato exceeded the degreeof variation in comparative samples ofGorillaandH. sapiensand within other generally accepted

early hominin species (e.g.,A. africanusandH. erectus). He also suggested that the pattern of thevariation within the hypodigm ofH. habilis sensu latowas unlike that seen in other taxa in the African

ape clade. Finally, he showed that the hypodigm ofH. habilis sensu latosubsumes more variabilityin some nonmetrical features (e.g., mandibular premolar root morphology) than is seen in the

comparative samples. Various two-taxon schemes for earlyHomohave been proposed, but the one



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that has received most support sorts the material into H. habilis sensu strictoandH. rudolfensis(s

below andFigures 1and2).

In 1972 the KNM-ER 1470 cranium was found in Area 131 at Koobi Fora in strata below tKBS (Kay Behrensmeyer Site) Tuff. Its flat, tall, and wide midface and relatively large brain a

peared to distinguish it from specimens from Olduvai named as paratypes ofH. habilis sensu stri(e.g., OH 13). In 1986 the Russian anthropologist Valery Alexeev named a new species Pithecathropus rudolfensis(Pithecanthropusis a genus that was sunk intoHomoin 1940) for KNM-ER 147he suggested this was justified because of the morphological differences between the Koobi Fo

cranium and the fossils from Olduvai Gorge allocated to H. habilis sensu stricto (Alexeev 198Groves (1989) later suggested thatP. rudolfensisshould be transferred to the genus Homo su

that its formal name would be Homo rudolfensis. Some claimed that when Alexeev establish

P. rudolfensis, he violated the rules of The International Code of Zoological Nomenclatu

(Kennedy 1999), but although Alexeevs proposal was idiosyncratic and did not follow all of t

recommendations of the Code, it did comply with its rules (Wood 1999). Thus, ifH. habilis senlato does subsume more variability than is consistent with it being a single species, and if KNM-E

1470 is judged to belong to a different species than the type specimen ofH. habilis sensu stricto(i.OH 7), thenH. rudolfensisis available as the name of a second earlyHomotaxon.

Those who subscribe to a two-taxon solution with H. rudolfensis as the second taxon haclaimed thatH. rudolfensisandH. habilis sensu strictoshow a different mix of primitive and deriv

features (e.g., Wood 1991). For example, the face of KNM-ER 1470 is widest at its mid-pawhereas the faces of OH 13 and KNM-ER 1813 are widest superiorly. The absolute size of t

brain case of KNM-ER 1470 (approximately 750800 cm3) suggests that the cranial capacity ofleast oneH. rudolfensisindividual is greater than that estimated for OH 7 (approximately 670 c

but when the absolute size of the brain of KNM-ER 1470 is related to estimates of body mass, itnot significantly larger than the estimated sizes of the brains of OH 13 or KNM-ER 1813. It h

been suggested that the more primitive face ofH. rudolfensisis combined with a robust mandibu

corpus and postcanine teeth with larger crowns and more complex premolar root systems (e.KNM-ER 1802) than those seen in most specimens ofH. habilis sensu stricto(Wood 1991).

In his comparative analysis of the variation subsumed in the separate and combined Tanzaniand Kenyan/Ethiopian samples of earlyHomo, Wood (1991) made it plain that the hypodig

from Koobi Fora most probably samples more than one, and probably two, taxa of earlyHomthe same data suggest that these two taxa are marginally more likely to be synchronic than tim

successive (p. 250). He was also careful to suggest that the hypothesis of distinct early and la

Homotaxa cannot be confidently falsified, nor can these data categorically exclude a single taxo

solution (Wood 1991, p. 250). Clearly, additional specimens are needed to test the two-taxohypothesis and existing proposals for allocating individual specimens to the hypodigms of the tw

hypothetical taxa. New material recently discovered at Koobi Fora and currently under study mhelp resolve some of these issues.

Most of the fossil evidence forH. erectuslike fossils comes from sites in the Turkana Basi

Fossils recovered from Koobi Fora have provided well-preserved crania (e.g., KNM-ER 3733883, 24700)andmandibles (e.g., KNM-ER730, 820, 992); there is alsoa fragmentary butdiseas

associated skeleton, KNM-ER 1808, and a second less complete associated skeleton, KNM-E803. A morphologically distinctive occipital fragment, KNM-ER 2598, from 4 m below the KB

Tuff has also provided the current approximately 1.87-Ma first appearance datum forH. erectThere is debate about whetherH. habilisand H. erectusare time successive (i.e., allochronic)

synchronic taxa. In 2001, KNM-ER 42700, a 1.55-Ma cranium lacking the face, was recoverfrom the Koobi Fora Formation at Ileret. Its size overlaps some of the earlier nonmegado

crania included inH. habilis sensu lato, but it displays morphology typical of AsianH. erectus. Ea

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AfricanH. erectushad been given the name Homo ergasterafter Groves & Mazak (1975) named

this species and designated mandible, KNM-ER 992, as the type specimen. However, KNM-ER

42700 demonstrates the extent of the variation seen inH. erectus(as does the magnificent collectionof hominins from Dmanisi), and when compared with otherH. erectusskulls such as OH 9, Spoor

et al. (2007) suggest it is consistent with a high degree of sexual dimorphism and with Africanand Asian Homo erectusbelonging to the same species. The Koobi Fora material also provided

evidence pertinent to the origins ofH. erectus, for the discovery of a maxilla, KNM-ER 42703,dated at 1.44 Ma, which represents the youngestH. habilisknown, indicates these two hominin

taxa coexisted for close to half a million years. This makes it less likely (but not impossible) thatthe latter evolved into the former and is evidence in favor of cladogenesis within earlyHomo.

EVIDENCE FOR TAXONOMIC DIVERSITY IN LATERHOMO

There is also evidence of taxonomic diversity, but not necessarily sympatry, much more recentlywithin theHomoclade. It has long been accepted thatH. sapiensandH. neanderthalensisoverlapped

in time if not in space, but more recently Grun et al. (1997) suggestedthatH. erectuspersisted muchlater than most researchers had conceded (but see Indriati et al. 2011), and even more recently

has come the proposal that at least one additional species should be recognized during this time,

H. floresiensis, a novel dwarfedH. erectus-like species (Morwood & Jungers 2009).

The speciesH. floresiensiswas erected by Brown et al. (2004) to accommodate LB (Liang Bua)1, a partial adult hominin skeleton, and LB2, an isolated premolar tooth, recovered in 2003 from

the Liang Bua cave on the Indonesian island of Flores. More material belonging to LB1 andevidence allocated to more individuals (LB 49), including a second partial skeleton, LB6, was

recovered in 2004 (Morwood et al. 2005). The hypodigm now includes close to 100 specimens thatare estimated to represent fewer than 10 individuals. The taxon was immediately controversial

for at least two reasons. First, its estimated geological age of between approximately 74 and

approximately 17 ka substantially overlapped evidence of the presence of modern humans inSoutheast Asia. Second, although its discoverers and describers acknowledge its small overall

size (the stature of LB1 is approximately 105 cm and its body mass is between 25 and 30 kg), itsespecially small brain (approximately 417 cm3) for an adult hominin, andits primitive morphology,

they have suggested that the collection of fossils is most parsimoniously interpreted as evidenceof a novel endemically dwarfed premodernHomo. A vociferous minority claims that no new taxon

needs to be erected because it considersH. floresiensisto sample a population ofH. sapiensmostlikely related to the small-statured Rampasasa people who live on Flores todayafflicted by either

an endocrine disorder or one, or more, of a range of syndromes that include microcephaly (i.e., apathologically small brain) as part of its phenotype. Both explanations are exotic, but those who

espouse a pathological explanation for the individuals represented by LB115 need to explain whatpathology results in an earlyHomo-like cranial vault; primitive mandibular, dental, carpal andpedal

morphology; and a brain that, although small, apparently has none of the morphological features

associated with the majority of syndromes that include microcephaly. Initially Brown et al. (2004)suggested thatH. floresiensiswas a dwarfedH. erectus, but the burden of subsequent analyses (Argue

et al. 2009, Brown & Maeda 2009, Morwood & Jungers 2009, Tocheri et al. 2007) suggests thatit may be more closely related to a transitional hominin such asH. habilis sensu stricto.

EMERGENCE OF MODERN HUMANS

By approximately 200 ka, hominins with a more vertical forehead, reduced supraorbital tori,

rounded occipitals, a less projecting midface, a true chin, and a more gracile skeleton are found



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unknown hominin was published (Krause et al. 2010). Later in the same year, an enlarged group

of researchers published the nuclear genome sequence of the same fossilized phalanx, along with

an analysis of the mtDNA and the morphological affinities of a left upper second (M2) or third(M3) molar that had been recovered from layer 11.1 in the south gallery of the Denisova Cave

in 2000 (Reich et al. 2010). Comparisons with the nuclear genomes of modern humans and

H. neanderthalensis indicate that although the Denisova hominin sequence is more similar to

Neanderthal DNA, it is nonetheless distinct enough to be considered a separate population,which the researchers sensibly referred to only informally as Denisovans (Reich et al. 2010, but

see Caldararo & Guthrie 2011). Apparently, at least some Melanesian populations ofH. sapiensshare approximately 46% of their DNA with the Denisovans. These landmark papers suggest

there is evidence of gene flow from premodern Homo species to modern H. sapiensat two dif-ferent time periods. The initial episode of admixture occurred soon after anatomically modern

humans left Africa, and the second episode involved the ancestors of Melanesian modern human

populations living in present day Papua New Guinea.

EVIDENCE OF GENETIC EVOLUTION WITHIN THE GENUS HOMO

The publication of the draft Pan troglodytes verus genome sequence opened up the possibil-ity of generating hypotheses about the genetic changes that have taken place between the

most recent common ancestor (or MRCA) of modern humans and chimpanzees/bonobos(Chimpanzee Seq. Anal. Consort. 2005). Bradley (2008) reviewed what was then known about

evidence for positive selection in the hominin clade. In this last part of our review, we supple-ment this information with more recent data (Figure 3) and exploit the publication of the draft

sequence of the Neanderthal genome to explore the genetic changes that are hypothesized tohave taken place since the divergence of the separate lineages leading to modern humans and

Neanderthals.

Possible genetic modifications range from single-nucleotide substitutions to extensive chro-mosomal transformations. Three mechanisms have been put forward to explain the phenotypic

differences between modern humans and chimpanzees/bonobos. The first stresses modificationsto protein-coding genes, andthus many genomic studies have focusedon detecting protein-coding

sequences that have undergone accelerated evolution, i.e., a greater rate of nonsynonymous aminoacid substitutions as compared with the rate of synonymous amino acid substitutions (Arbiza et al.

2006, Bakewell et al. 2007, Kosiol et al. 2008, Nielsen et al. 2005). The second hypothesis fo-cuses on gene loss (hence it is called the less-is-more hypothesis) to explain the development of

the modern human phenotype (Olson 1999). The third hypothesis stems from an observationby King & Wilson (1975), who suggested that the reason chimpanzees and modern humans are

so similar genetically and yet so dissimilar phenotypically is because small changes in the reg-ulatory regions of the genes result in significant changes in gene expression. There has been

considerable debate about the relative contributions made by these three mechanisms, but evi-

dence increasingly indicates that regulatory differences have played a major role in the evolutionof the modern human phenotype (Caceres et al. 2003, Enard et al. 2002, Marques-Bonet et al.

2009, Sholtis & Noonan 2010, Uddin et al. 2004). There is a caveat to the discussion above.Comparing the genomes of two different species necessitates high-quality sequences if a bal-

anced view of the variation between the two genomes is to be obtained. The modern human andchimpanzee genomes were sequenced using different methods, and therefore direct comparison

of the coverage of the two is difficult. Because the chimpanzee sequence is not sequenced tothe same standard as the modern human genomethe chimpanzee draft sequence has only 6coverage, compared with the 30 coverage of the modern human sequencedifficulties have



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Pathogen resistance CMAH (Chou et al. 2002), CASP12(Wang et al. 2006)

Hair protein KRTHAP1(Winter et al. 2001)

Geneloss

Proteinevolution

Generegulationevolution

Chimpanzee Human

Hearing(Clark et al. 2003)

Y genes(Hughes

et al. 2005)

Jaw musculature MYH16(Stedman et al. 2004)Olfactory organsMOXD2(Hahn Y. et al. 2007)Skin physiologyS100A15A(Hahn Y. et al. 2007)

Brain sizeASPM (Evans et al. 2004b), MCPH1(Evans et al. 2004a)Aerobic energy metabolismAEMgenes (Uddin et al. 2008)

Skeletaldevelopment(Clark et al. 2003)

Brain development PDYN(Rockman et al. 2005), HAR1(Pollard et al. 2006a,b),THBS2and THBS4(Ccares et al. 2007)

Limb development HACNS1(Prabhakar et al. 2008)

Skin physiology RPTN(Green et al. 2010)Sperm motilitySPAG17(Green et al. 2010)Wound healingPCD16(Green et al. 2010)rRNA regulationTTF1(Green et al. 2010)Hair and skin colorMC1R(Lalueza-Fox et al. 2007)

Neanderthal

Hair andskin color

MC1R (Lalueza-Fox et al. 2007)

Nervous system(Dorus et al. 2004)SpeechFOXP2 (Enard et al. 2002)

Figure 3

Examples of potentially functionally important genetic changes along the human and chimpanzee lineages. Genetic changes of all typ(protein evolution, gene regulation evolution, gene loss) have been identified. As current research largely focuses on modern human-rather than ape-, specific changes, fewer changes along the chimpanzee lineage are known. The placement does not indicate anychronological order. Adapted with permission from Bradley (2008); updated information is in red.

arisen in determining true differences between the two as opposed to artifacts of the techniquused.

PROTEIN EVOLUTION

Sequence comparisons between modern human and chimpanzee genomes provide evidence f

genes that have been positivelyselected in modernhumans since thedivergence of thetwolineagNow, with thepublication of theNeanderthal genome, it is possible to compare themodern hum

and the Neanderthal genomes to hunt for genetic changes that have occurred recently. Thus fa78 substitutions in protein-coding genes have been noted between the two, and in each case t

Neanderthals possessed the ancestral state and modern humans the derived condition (Green et2010). The modifications in the modern human lineage include changes toRPTN, which encod

for the protein repetin involved in skin physiology; SPAG17, which encodes for a protein involv

in sperm motility; TTF1, which is involved in ribosomal gene transcription control; PCD16cell-cell adhesion molecule that has a likely role in wound healing; and CAN15, which encod

for a protein whose function is currently unknown.

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Aerobic Energy Metabolism Genes

A bigger brain is metabolically expensive, so it makes sense that over time modern humans andtheir immediate ancestors would have evolved mechanisms that allowed for the evolution of these

larger brains. Mitochondria are fundamental to efficient production of aerobic energy, and anygenetic changes that would have allowed for their more efficient functioning most likely would

have been positively selected for with time. Studies have shown that the genes that code forthe proteins of the oxidative phosphorylation pathway were positively selected in the ape stem

line between 25 and 6 Ma, potentially helping to fuel the development of a larger brain in apeevolution. Furthermore, since the time of divergence, aerobic energy metabolism (AEM) genes in

the chimpanzee and modern human genomes have each separately continued to undergo adaptive

evolution (Goodman & Sterner 2010, Goodman et al. 2009, Uddin et al. 2008). Notably, AEMgenes are among those whose expression is highly upregulated in the neocortex of modern humans

as compared with great apes (Uddin et al. 2004).

Microcephaly Genes

Although no link has been demonstrated between normal haplotype variation ofabnormal spindle-like microcephaly associated(ASPM) andMicrocephalin (MCPH1) and either brain size or intelligence,

individuals possessing loss-of-function mutations in these genes have pathologically small (i.e., mi-crocephalic) brains owing to effects on the dynamics of mitotic division in neuroprogenitor cells ofthe cerebral cortex (Evans et al. 2004a,b; Mekel-Bobrov et al. 2007; Timpson et al. 2007). There is

evidence of positive selection onMCPH1prior to the MRCA of chimpanzees/bonobos and mod-ern humans and onASPMin the modern human lineage since the MRCA (Goodman & Sterner

2010, Goodman et al. 2009). Onestudy suggested that haplogroup D, the derivedform ofMCPH1,

developed in an earlier hominin lineage that subsequently separated from modern humans at ap-proximately 1.1 Ma, introgressed into the lineage leading to modern humans at approximately

37 ka, and spread everywhere except in sub-Saharan Africa to a frequency of 70% (Evans et al.2006). Neanderthals were identified as a possible source of the movement of haplogroup D back

intoH. sapiens(Evans et al. 2006), but recent studies of Neanderthal nuclear DNA from Monti

Lessini, Italy, do not lend support to this hypothesis (Lari et al. 2010). Ongoing research into theseand other known microcephaly genes (CENPJ, CDK5RAP2) suggests a sex-specific association ineach microcephaly gene exceptCENPJduring neurogenesis (Rimol et al. 2010).

Melanocortin 1 Receptor

The evolution of skin color has generated great interest in the scientific community, and one ofthe outcomes of the publication of the draft chimpanzee genome sequence was the finding that

a rapid divergence in the genes coding for skin differentiation has occurred in the two lineages

(Chimpanzee Seq. Anal. Consort. 2005, Jablonski & Chaplin 2010). Changes in skin physiologyare believed to have occurred after the emergence of the genus Homo, and it is hypothesized that

these were associated with the loss of body hair ( Jablonski & Chaplin 2010, Rogers et al. 2004).One of the many genes involved in the phenotypic variation seen in modern human pigmentation

is the melanocortin 1 receptor (MC1R), mutations of which are known to result in pale skin andred hair (Lalueza-Fox et al. 2007). Recent developments in the amplification of ancient DNA have

enabled researchers to look at this gene in both H. sapiensand H. neanderthalensis.Lalueza-Foxet al. (2007) recognized a mutation on theMC1Rgene in the two Neanderthal specimens that was

not observed in the 3,700 modern humans they analyzed. They argue that the mutations inMC1R



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arose independently in each lineage and became fixed in the populations as a result of converge

evolution.

GENE REGULATION AND EXPRESSION

Investigations into gene expression patterns have thus far identified differences between Homand Pan in roughly 100 genes (Marques-Bonet et al. 2009). For example, the coding regiforprodynorphin(PDYN),a precursor molecule with a role in regulating behavior, memory, an

perception, shows a strong positive selection signal (Rockman et al. 2005). It has been suggestthat many of the observed differences in gene expression can be explained by changes in gen

regulation (Caceres et al. 2003, Gilad et al. 2006).

Human Accelerated Region 1F and HACNS1

Human accelerated regions (HARs) are segments of the genome that are highly conserved in t

vertebrate genome but have evolved in modern humans more rapidly than can be explained drift alone. Pollard et al. (2006a,b) recognized 49 HARs, of which only two code for proteins. O

of the 49, HAR1, is part of a novel RNA gene, HAR1F, that is expressed in the brain and involvin neurodevelopment. In addition, the gene enhancer HACNS1 (human-accelerated conserv

noncoding sequence 1) is strongly conserved in terrestrial mammals and has accrued 16 modehumanspecific mutations sinceit diverged fromPan (Prabhakar et al. 2008).HACNS1 is express

in the developing limb bud and may have a role in the development of the thumb and wrist regio

Thrombospondin 2 and Thrombospondin 4

Proteins known as thrombospondins (THBSs) play a role in the formation of synapses and neur

growth, and a higher expression rate of THBS genes and their resultant proteins in the adumodern human brain has been suggested as a mechanism for synaptic remodeling of mode

humans. Microarray studies indicate a sixfold increase in the expression ofTHBS4 mRNA aa twofold increase inTHBS2mRNA in the cerebral cortex of modern humans when compar

with chimpanzees or macaques (Caceres et al. 2007). This increase in expression has promptthe suggestion that enhanced synaptic plasticity may be a defining feature of the adult mode

human brain (Sherwood et al. 2008).

GENE LOSSES AND DUPLICATIONS

The loss or gain of a gene in the genome has the potential to greatly affect the phenotype atherefore the fitness of an organism. Genes are lost as a result of gene deletions or mutatio

leading to a loss of function, and they can be gained as a result of duplications. Many of the gen

known to have been either gained or lost in the modern human genome since humans divergfrom chimpanzees/bonobos are involved in olfaction and/or taste (Hahn M. et al. 2007, Wan

et al. 2006).

MOXD2 and S100A15A

An exon deletion resulted in the inactivation of Monooxygenase, DBH-Like 2 (MOXD2)andcalcium-binding protein (S100A15A) in the modern human lineage since its divergence fromP(Chou et al. 1998, Hahn Y. et al. 2007). MOXD2is highly conserved in mammals and encod

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an enzyme chiefly expressed in the olfactory epithelium. Hahn Y. et al. (2007) have identified

an exon deletion and a polymorphic nonsense mutation in this gene that they posit could have

changed the olfactory sensory organs of modern humans. In contrast, S100A15Aplays a role inskin physiology. Modern humans are missing the necessary start codon, and its inactivation may

have played a role in the physiological distinctiveness of modern human skin (Hahn Y. et al. 2007).

Copy-Number Variants

Copy-number variants (CNVs) are heritable changes in the genome that have been either du-

plicated or deleted on certain chromosomes. Their importance to human evolution and geneticvariation is reflected in their common occurrence in the human genome as well as in observed

differences in CNVs between modern human populations (Redon et al 2006). Comparisons ofCNVs between humans and other primates have begun to identify portions of the genome under

selective pressure for CNV changes during evolution (Perry et al. 2008).

CONCLUSION

Not long ago a review of the evolution of the genusHomowould have been confined to a reviewof the fossil evidence. The past two decades have seen important additions to the fossil record of

Homo, but we remain ignorant about the evolutionary history of important aspects of the modernhuman phenotype such as the substantial increase in brain size and the changes in brain shape that

occur within the genusHomo.Third-generation sequencing technology will provide researcherswith ever-larger volumes of data from which we must hope we can better understand the molecular

basis of the key adaptations associated with the emergence of modernH. sapiens. The challengeof the upcoming decades is to meld innovations in molecular genetic methods and technology

with evidence from the fossil record to generate hypotheses about the developmental bases ofthe phenotypic and behavioral developments we see within the genus Homo. We must hope that

before too long we will understand not just what happened during the course of our evolution butalso how it happened.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings that

might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

B.W. thanks the George Washington (GW) University Provost for research support, and J.B.acknowledges the support of a GW Presidential Graduate Fellowship. We also thank Chet

Sherwood for valuable comments and Brenda Bradley for permission to adapt her 2008illustration.

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Annual Review

Ecology, Evolu

and Systematic

Volume 42, 201

Contents

Native Pollinators in Anthropogenic Habitats

Rachael Winfree, Ignasi Bartomeus, and Daniel P. Cariveau 1

Microbially Mediated Plant Functional Traits

Maren L. Friesen, Stephanie S. Porter, Scott C. Stark, Eric J. von Wettberg,

Joel L. Sachs, and Esperanza Martinez-Romero 23

Evolution in the GenusHomo

Bernard Wood and Jennifer Baker 47

Ehrlich and Raven Revisited: Mechanisms Underlying Codiversification

of Plants and Enemies

Niklas Janz 71

An Evolutionary Perspective on Self-Organized Division of Labor

in Social Insects

Ana Duarte, Franz J. Weissing, Ido Pen, and Laurent Keller 91

Evolution ofAnopheles gambiaein Relation to Humans and Malaria

Bradley J. White, Frank H. Collins, and Nora J. Besansky

111Mechanisms of Plant Invasions of North America and European Grasslands

T.R. Seastedt and Petr Pysek 133

Physiological Correlates of Geographic Range in Animals

Francisco Bozinovic, Piero Calosi, and John I. Spicer 155

Ecological Lessons from Free-Air CO2Enrichment (FACE) Experiments

Richard J. Norby and Donald R. Zak 181

Biogeography of the Indo-Australian Archipelago

David J. Lohman, Mark de Bruyn, Timothy Page, Kristina von Rintelen,

Robert Hall, Peter K.L. Ng, Hsi-Te Shih, Gary R. Carvalho,

and Thomas von Rintelen 205

Phylogenetic Insights on Evolutionary Novelties in Lizards

and Snakes: Sex, Birth, Bodies, Niches, and Venom

Jack W. Sites Jr, Tod W. Reeder, and John J. Wiens 227

v


25/25

The Patterns and Causes of Variation in Plant Nucleotide Substitution Rates

Brandon Gaut, Liang Yang, Shohei Takuno, and Luis E. Eguiarte 24

Long-Term Ecological Records and Their Relevance to Climate Change

Predictions for a Warmer World

K.J. Willis and G.M. MacDonald 2

The Behavioral Ecology of Nutrient Foraging by Plants

James F. Cahill Jr and Gordon G. McNickle

2

Climate Relicts: Past, Present, Future

Arndt Hampe and Alistair S. Jump 3

Rapid Evolutionary Change and the Coexistence of Species

Richard A. Lankau 3

Developmental Patterns in Mesozoic Evolution of Mammal Ears

Zhe-Xi Luo 3

Integrated Land-Sea Conservation Planning: The Missing Links

Jorge G. Alvarez-Romero, Robert L. Pressey, Natalie C. Ban, Ken Vance-Borland,Chuck Willer, Carissa Joy Klein, and Steven D. Gaines 3

On the Use of Stable Isotopes in Trophic Ecology

William J. Boecklen, Christopher T. Yarnes, Bethany A. Cook, and Avis C. James 4

Phylogenetic Methods in Biogeography

Fredrik Ronquist and Isabel Sanmartn 44

Toward an Era of Restoration in Ecology: Successes, Failures,

and Opportunities Ahead

Katharine N. Suding 4

Functional Ecology of Free-Living Nitrogen Fixation:A Contemporary Perspective

Sasha C. Reed, Cory C. Cleveland, and Alan R. Townsend 4

Indexes

Cumulative Index of Contributing Authors, Volumes 3842 5

Cumulative Index of Chapter Titles, Volumes 3842 5

Errata

An online log of corrections toAnnual Review of Ecology, Evolution, and Systematics

articles may be found at http://ecolsys.annualreviews.org/errata.shtml

evolution in the genus homo

Documents