Evolution in The Genus Homo

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Evolution in the Genus Homo

Bernard Wood1 and Jennifer Baker1,2
1
Center for the Advanced Study of Hominid Paleobiology and 2 Hominid Paleobiology
Graduate Program, Department of Anthropology, George Washington University,
Washington, DC 20052; email: bernardawood@gmail.com
Annu. Rev. Ecol. Evol. Syst. 2011. 42:4769
Keywords
First published online as a Review in Advance on

August 11, 2011
clade, grade, Homo habilis, modern human genome
The Annual Review of Ecology, Evolution, and

Systematics is online at ecolsys.annualreviews.org
Abstract
This articles doi:

10.1146/annurev-ecolsys-102209-144653
c 2011 by Annual Reviews.
Copyright
All rights reserved
1543-592X/11/1201-0047$20.00
We review the fossil and genetic evidence that relate to evolution in the
genus Homo. We focus on the origin of Homo and on the evidence for taxonomic diversity at the beginning of the evolutionary history of Homo and
in the last 200,000 years. We set out the arguments for recognizing a second early Homo taxon, Homo rudolfensis, and the arguments for and against
including Homo habilis sensu stricto and Homo rudolfensis within Homo. We
end by reviewing recent genomic evolution within Homo. The challenge of
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 of the phenotypic and behavioral developments we see within the genus Homo.
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INTRODUCTION
Carl Linnaeus introduced the genus Homo to zoological nomenclature in 1758, including it in
his Order Primates along with monkeys and lemurs. As originally conceived by Linnaeus, Homo
included two species, Homo sapiens (i.e., modern humans) and Homo troglodytes, a taxon based on
a melding of de Bondts (1658) Homo sylvestris Orang Outang that may have been based on a
real orangutan or an unusually hirsute modern human and contemporary Swedish descriptions
of albino people living in caves in the Moluccas. This review focuses on the interpretation of the
genus Homo implied by the inclusion of only H. sapiens of these two; consideration of H. troglodytes
is best left to historians of science.
The history of the various ways the genus Homo has been interpreted since its introduction in
the tenth edition of Linnaeuss Systema Naturae has been reviewed elsewhere (Wood 2009). The
quick and dirty version of that review is that there have been episodic relaxations, some explicit
and some implicit, of the criteria used to decide which taxa should be included within the genus
Homo. Each episode has resulted in the addition of one or more extinct taxa to the list of species
recognized within Homo (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 genus Homo was 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 humans
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 are

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 torus;
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
interpreted H. habilis as being dexterous, upright,
and bipedal as well as capable of spoken
language, but fresh evidence and fresh
interpretations of existing evidence have led
others 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 are
more anteriorly situated, and the premolars and
molars are larger and have more complex cusps.
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Homo
heidelbergensis
Homo
neanderthalensis
Homo
Homo
habilis rudolfensis
Australopithecus
sediba
Homo
erectus Homo
ergaster
Australopithecus
bahrelghazali
Paranthropus
boisei
Australopithecus
garhi
Kenyanthropus
platyops
Mya
Paranthropus
robustus
Homo
antecessor

Homo floresiensis
Australopithecus
africanus
Paranthropus
aethiopicus
Australopithecus
afarensis
Australopithecus
anamensis
Ardipithecus ramidus
5
Anatomically modern Homo
6
Premodern Homo
Transitional hominins
Ardipithecus
kadabba
Orrorin tugenensis
Archaic hominins
7
Megadont archaic hominins
Sahelanthropus
tchadensis
Possible early hominins

8
Figure 1
The taxa recognized in a typical speciose hominin taxonomy; the species conventionally included within Homo are emphasized in bold.
The taxa are sorted into grades (see Wood 2010a for details); the three grades that contain Homo taxa are in bold. The height of the
columns reects either uncertainties about the temporal age of a taxon, or in cases in which there are well-dated horizons at several
sites, it reects current evidence about the earliest, called the rst appearance datum (FAD), and the most recent, called the last
appearance datum (LAD), fossil evidence of any particular hominin taxon. However, the time between the FAD and the LAD is likely
to be represent the minimum time span of a taxon, for it is highly unlikely that the fossil record of a taxon, and particularly the relatively
sparse 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 genus Homo
than the one set out in Figure 1. For example, John Robinson (1972) proposed that Australopithecus
be sunk into Homo. Curnoe & Thorne (2003) went even further, suggesting that only three species
should be recognized in the hominin clade and including all three in Homo (i.e., Homo ramidus,
Homo africanus, and H. sapiens). This review will focus on the more mainstream interpretation of
the genus Homo set out in Figure 1.
DEFINING HOMO
Genus denitions applicable to the fossil record use two different categories of inference (Wood
2010b). The rst employs phenotypic evidence to generate hypotheses about the closeness, or
otherwise, 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 of
contemporary genus denitions, but most researchers who focus on the hominin fossil record
implicitly, if not explicitly, subscribe to a genus denition that combines information about clades
and grades. This is certainly the case for the way most researchers interpret the genus Homo.
It is widely assumed, but rarely articulated, that the species included in Homo should comprise a
monophyletic group or a clade; in other words, they should share a most recent common ancestor
that is not shared with taxa belonging to a different monophyletic group. But although all genera
should be clades, not all clades are necessarily genera. This is because most paleoanthropologists
assume (but also rarely articulate) that the taxa within a genus should share the same functional
characteristics or competencies. In the case of Homo, suggested shared competencies include the
ability to use complex language; to make the only type of tools, stone tools, that can be reliably
detected in the early archeological record (as in Man the toolmaker); and to hunt (as in Man
the hunter). Therefore, the search for the origin of the genus Homo is a search for the origin of an
entity that is both a clade (sensu Hennig 1966) and a grade (sensu Huxley 1958) (Wood & Collard
1999).
There are two options for applying the two main criteria for genus identication (i.e., monophyly and adaptive coherence). One can start in the present and work back in time, or one can
start in the past and work toward the present. The former top-down approach focuses on the
type species of the genus Homo (i.e., H. sapiens). It involves taking stock of hypotheses about the
nature of its derived morphology and behavior, deciding on the cardinal features and behaviors
that dene the adaptive zone of H. sapiens, and deciding on the characters that will be used to generate hypotheses about the relationships among the extinct taxa that are candidates for inclusion
in Homo. Then one works backward into the tree of life, applying the same tests to each hominin
taxon encountered. Is there reliable evidence (i.e., the same cladogram is generated even if one
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 reliable
evidence (i.e., reliable quantitative proxies of behaviors) that the taxon is in the same adaptive
zone as H. sapiens? The bottom-up approach involves making a subjective judgment about when
in the past one starts to pick up the trail leading to Homo. One then works toward the present,
applying the tests set out above to all the hominin taxa encountered. The difference between this
approach and the top-down option is that, in general, the deeper into the past the sparser the
fossil evidence, thus making it more difcult to generate reliable evidence about monophyly and
adaptive similarity.
Most researchers apparently consider the hypothesis that later Homo taxa (i.e., H. sapiens, Homo
neanderthalensis, Homo heidelbergensis, Homo erectus; we discuss Homo oresiensis separately) form a
monophyletic group to be so obviously correct that it does not require formal testing, for there
have been few attempts to assess the relationships of those taxa. For example, although Eldredge
& Tattersall (1975, gure 4) included H. neanderthalensis, H. heidelbergensis, and H. erectus in their
pioneering application of cladistic methods to hominin relationships, they did not carry out any
formal analysis of the relationships among these taxa.

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WHEN DOES HOMO BEGIN?

Some researchers (e.g., Kimbel et al. 2004, Strait & Grine 2004) have presented what they interpret
to be compelling cladistic evidence that Homo habilis sensu stricto and Homo rudolfensis should be
included along with H. sapiens, H. neanderthalensis, H. heidelbergensis, and H. erectus within the
genus Homo, and many researchers concur with this judgment. However, we suspect that the
authors who support the inclusion of H. habilis sensu stricto and H. rudolfensis within Homo also
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Sahelanthropus tchadensis
Ardipithecus ramidus
Australopithecus anamensis
Australopithecus afarensis
Australopithecus garhi
Australopithecus africanus
Kenyanthropus platyops

Paranthropus robustus
Paranthropus boisei
Paranthropus aethiopicus
Homo habilis sensu stricto
Homo rudolfensis
Homo erectus sensu lato
Homo sapiens
Figure 2
A cladogram presenting one hypothesis regarding the relationships among early hominins. The nodes 1 and
2 represent two hypotheses for the lower boundary of the Homo clade. If Homo were to include node 1, it
would embrace the species presently included in early Homo (i.e., H. habilis sensu stricto and H. rudolfensis). If
Homo was dened so as to exclude node 1, and to include just node 2, then it would be conned to early
African H. erectus and temporally later, more derived Homo species (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, and H. 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 the
boundary so that it includes H. habilis sensu stricto and H. rudolfensis (Figure 2, node 1), or to
draw it beneath early African H. erectus so that it excludes H. habilis sensu stricto and H. rudolfensis
(Figure 2, node 2).
GRADE CRITERIA FOR INCLUDING TAXA WITHIN HOMO

As far as the grade criterion is concerned, Wood & Collard (1999) suggested that adaptive similarity should be judged on the basis of data (preferably quantitative) taken directly from the
hard tissue evidence rather than on secondary inferences generated from the hard tissue evidence. The adaptive criteria they suggested included body size and shape (as reected in long
bone lengths, limb proportions, etc.), posture and locomotion (as reected in the morphology of
the limbs and the bony labyrinth), circumstantial evidence of cognitive ability (as reected in
absolute and relative brain size, etc.), evidence of dexterity (as reected in digit proportions,
carpal bone morphology, etc.), diet (as reected in mandibular corpus area, postcanine crown
area, enamel thickness, enamel microwear, etc.) and life history (as reected in the only available
proxies 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 limb
proportions of OH (Olduvai Hominid) 62, the only associated skeleton securely assigned to
H. habilis sensu stricto, are not statistically signicantly different from the limb proportions of
A.L. (Afar Locality) 288-1 (also known as Lucy), the best-preserved associated skeleton belonging
to Australopithecus afarensis. However, Reno et al. (2005) have suggested that any estimate of the
length of the OH 62 femur (and thus the estimated value of the humerofemoral index of OH
62) must be treated with caution. Haeusler & McHenry (2004, 2007) also investigated the limb
proportions of early Homo by looking at OH 62 and a second probable H. habilis sensu stricto
associated skeleton, KNM-ER (Kenyan National Museums-East Rudolf ) 3735, from Koobi Fora
in Kenya. They concluded that the limb proportions of both of these skeletons are more modern
humanlike than chimpanzee-like. However, their use of OH 34 to derive the limb proportions of
OH 62 is controversial, as are their conclusions with respect to KNM-ER 3735. Thus, although
there is still doubt about the precise limb proportions of the individuals represented by OH 62
and KNM-ER 3735, it is fair to say that most informed observers subscribe to the view that the
limb proportions of OH 62 are more similar to those of archaic hominins (i.e., Australopithecus)
than to the limb proportions of modern humans and extinct later Homo taxa such as H. erectus.
No limb bones are assigned to H. rudolfensis, but what can be concluded about the posture
and locomotion of H. habilis sensu stricto? The only postcranial material from Olduvai Gorge
that can be securely attributed to H. habilis sensu stricto is the OH 62 associated skeleton. As we
have seen above, what can be inferred about its limb proportions would argue against a later
Homo-like posture and locomotion. Ruff (2009) compared cross-sectional bone strength measurements at two locations in the femur and humerus of OH 62 with those taken at what were judged
to be equivalent locations in modern humans and chimpanzees as well as in two early H. erectus
specimens: KNM-WT (Kenyan National Museums-West Turkana) 15000 and KNM-ER 1808.
For each combination of section locations, the femoral to humeral strength proportions of OH
62 fall below the 95% condence interval of modern humans, but for most comparisons they
are within the 95% condence interval of chimpanzees. In contrast, the two H. erectus specimens
both fell within or above the modern human distributions. This indicates that load distribution
between the limbs and by implication, locomotor behavior, was signicantly different in H. habilis
sensu stricto from that seen in H. erectus and modern humans. When considered along with other
postcranial evidence, Ruff (2009) suggests that the most likely interpretation is that H. habilis,
although bipedal when terrestrial, still engaged in frequent arboreal behavior, while H. erectus was
a completely committed terrestrial biped (Ruff 2009, p. 90). Larson (2007) reached comparable
conclusions about the shoulder.
Evidence from the size and shape of the bony labyrinth, which houses the receptors that monitor
movement and posture, of early hominins has also been used to make inferences about posture
and locomotor mode (Spoor et al. 1994); this method has the obvious advantage that it uses data
obtained from crania, which are usually more condently assigned to a taxon than are isolated
limb bones. Among the early hominin specimens considered in that study were Stw (Sterkfontein
Witwatersrand) 53, assigned by some to H. habilis, and SK (Swartkrans) 847, which some assign
to H. habilis and others to H. erectus. The semicircular canal morphology of the former was so
different from that of modern humans that Spoor et al. (1994) suggested that Stw 53 relied less
on bipedal behavior than the australopithecines (p. 648). They also suggested that the extreme
differences in labyrinthine morphology between SK 847 and Stw 53 make attribution of both
specimens to the same species, on this evidence alone, highly unlikely (p. 648). In an analysis of
the labyrinthine morphology of Sangiran 2 and 4, OH 9 (i.e., H. erectus) and SK 847, Spoor (1994)
suggested that the dimensions of the semicircular canals (of these taxa) are similar to those in
modern humans (p. 254). Thus, whatever taxon Stw 53 belongs to, be it H. habilis or a different

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early Homo taxon (e.g., Grine et al. 1996, Curnoe & Tobias 2006), these results suggest that the
locomotor repertoire of Stw 53 was very different from that of H. erectus and modern humans.
Brain size as reected in the volume of the endocranial cavity is an obvious but imperfect
proxy for cognition. The difference between the endocranial volumes of chimpanzees and modern humans apparently match the markedly different cognitive capacities of the two taxa, but
at a ner 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 of
cognitive 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 and H. 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 that
the morphology of the type specimen of H. habilis sensu stricto (OH 7) resembles the carpal morphology seen in archaic hominins such as A. afarensis. Although they make the point that this
primitive 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 of H. habilis sensu
stricto certainly 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 two
comparative 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 rst molar (M1 ). The authors used the height of the mandibular corpus at M1 and 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-based
body 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. rudolfensis were, respectively, 75% and 100% larger than the
estimates of body mass based on the nonmandibular evidence. Similar discrepancies were seen for
A. afarensis and Australopithecus africanus (Wood & Aiello 1998, gures 3 and 5). In contrast, the
hominoid mandible-based body mass predictions for early African H. erectus matched those based
on the nonmandibular evidence. Thus, H. habilis sensu stricto and H. rudolfensis have 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 & Cofng (2000) showed that the ends
of the range of the MQ for hominin taxa are 0.9 for H. sapiens and 2.7 for Paranthropus boisei.
The body mass estimates they use for H. rudolfensis are almost certainly too large, but the MQ
estimate for H. habilis sensu stricto of 1.9 is likely to be closer to the mark. When compared with
the MQs of 1.7 and 2.0 for A. afarensis and A. africanus, respectively, H. habilis sensu stricto shows
no evidence of any reduction in relative postcanine tooth crown area compared with the two
archaic hominins with the largest hypodigms. Indeed, its MQ is only a little smaller than the
MQ (2.2) of Paranthropus robustus, whereas the MQ of early African H. erectus (0.9) is the same
as that for H. sapiens. Thus, both sets of results (i.e., mandibular corpus cross-sectional area and
the surface area of the postcanine dentition) suggest that signicant reduction in the size of the
masticatory 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 more
discriminating about the specimens they judge to contain evidence about microwear. This is
because trampling or rolling in the beds of streams and rivers produces microscopic damage to
the tooth enamel that could be confused with the microscopic damage produced when teeth
make contact with food during chewing. When Ungar et al. (2006) and Ungar & Scott (2009)
applied these more stringent criteria to their initial sample of 83 early Homo specimens from three
southern African and seven east African sites, the sample size decreased to just 18 specimens.
Ungar et al. (2006) concluded that H. erectus and individuals from Swartkrans Member 1 ate, at
least occasionally, more tough or brittle foods than did H. habilis and individuals from Sterkfontein
Member 5C (p. 91). This is more, albeit tenuous, evidence that the diet of early African Homo
differed from that of H. habilis sensu stricto (see also Ungar et al. 2011).
The life history of a taxon is a reection of the way the individual members of a taxon adapt
to their ecological context by dividing their energy among the tasks of maintenance of their
milieu interieur, production of offspring, and maintenance of offspring prior to them becoming
independent. As far as fossil taxa are concerned, the rate of development of the hard tissues is a
proxy for the tempo of ontogeny. Several recent studies have examined the rate of dental development (as judged from dental microstructure) in later hominins (Bermudez de Castro & Rosas
2001, Bermudez de Castro et al. 2003, Macchiarelli et al. 2006, Ramirez Rozzi & Bermudez de
Castro 2004). These studies suggested that the enamel formation rates of the anterior teeth of
Neanderthals were faster than those in H. sapiens, but subsequent investigations of the development
of Neanderthal postcanine teeth suggested that the developmental tempo of H. neanderthalensis
was modern human-like (Dean et al. 2001, Guatelli-Sternberg et al. 2005, but see Smith et al.
2010). Clearly, larger samples are needed, and researchers should cross-validate their methods, but
Smith et al. (2007) recently demonstrated that the distinctively slow dental development seen in
living modern humans can be traced back to at least 160 ka. Even if the developmental schedule of
H. heidelbergensis (see above) was not like that of modern humans, it was almost certainly more
similar to the developmental schedule of H. sapiens than to those of chimpanzees and gorillas. In
contrast, preliminary results suggest that the developmental schedules of H. erectus sensu stricto,
early African H. erectus, H. habilis sensu stricto, and H. rudolfensis were more like those of chimpanzees
and 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 periodicity of
9 days to estimate enamel formation times, and then they plotted the latter against enamel thickness. These analyses show that archaic hominins take, on average, 100 fewer days than modern
humans to reach an enamel thickness of 1,000 m. The authors conclude that none of the
trajectories of enamel growth in apes, australopiths or fossils attributed to Homo habilis, Homo
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. habilis),
Dean (1995) identied a nonmodern humanlike pattern.

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THE LOWER BOUNDARY OF HOMO

How well does this evidence about adaptive coherence match the cladistic evidence? On the basis
of adaptation, is it possible to distinguish H. habilis sensu stricto and H. rudolfensis from potential
precursor archaic hominins such as A. afarensis? We suggest that, taken overall, the evidence
reviewed above suggests that the adaptive regimes of both H. habilis sensu stricto and H. rudolfensis
have as much, if not more, in common with those of archaic hominin taxa (e.g., A. afarensis and
A. africanus) as they do with premodern Homo taxa such as H. erectus. This is why we prefer
to include these taxa in a separate grade of transitional hominins rather than including them
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with H. erectus in premodern Homo (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 for Homo, then the boundary of Homo would be set so that it includes
H. heidelbergensis but not H. 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 that Homo
includes early African H. erectus but not H. 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, that H. habilis sensu stricto and H. rudolfensis are included in
Homo (i.e., node 1 in Figure 2), what can be concluded about evolution within the genus Homo? Do
new species arise primarily through anagenesis, or is there evidence of cladogenesis within Homo?
Are species within Homo always time successive, or do the temporal ranges of Homo taxa 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 an
inevitable, 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 pattern
that 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
Homo clade, one at the beginning of the clade and one in the most recent 200 ka of its history.
EVIDENCE FOR TAXONOMIC DIVERSITY IN EARLY HOMO

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). The
announcement of a small-brained species attributed to Homo caused considerable controversy,
largely because the date of 1.75 Ma for H. habilis extended the age for the earliest evidence of
Homo by 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 (for
no particularly compelling reason) between 700 and 800 cm3 .
Although Tobias (1991) made a persuasive case that all of the nonmegadont archaic hominins
from Bed I and Lower Bed II at Olduvai Gorge could be subsumed in a single taxon, H. habilis
sensu stricto, during the rst half of the 1970s, it became clear that the early Homo cranial (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 easy
to 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 of H. habilis sensu lato (e.g.,
Miller 1991, Suwa et al. 1996), others supported a two-taxon solution (Grine et al. 1996, Kramer
et al. 1995, Lieberman et al. 1988, Prat 1997, Stringer 1986, Wood 1985). For example, Wood
(1991, 1993) showed that variation within the hypodigm of H. habilis sensu lato exceeded the degree
of variation in comparative samples of Gorilla and H. sapiens and within other generally accepted
early hominin species (e.g., A. africanus and H. erectus). He also suggested that the pattern of the
variation within the hypodigm of H. habilis sensu lato was unlike that seen in other taxa in the African
ape clade. Finally, he showed that the hypodigm of H. habilis sensu lato subsumes more variability
in some nonmetrical features (e.g., mandibular premolar root morphology) than is seen in the
comparative samples. Various two-taxon schemes for early Homo have been proposed, but the one
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that has received most support sorts the material into H. habilis sensu stricto and H. rudolfensis (see
below and Figures 1 and 2).
In 1972 the KNM-ER 1470 cranium was found in Area 131 at Koobi Fora in strata below the
KBS (Kay Behrensmeyer Site) Tuff. Its at, tall, and wide midface and relatively large brain appeared to distinguish it from specimens from Olduvai named as paratypes of H. habilis sensu stricto
(e.g., OH 13). In 1986 the Russian anthropologist Valery Alexeev named a new species Pithecanthropus rudolfensis (Pithecanthropus is a genus that was sunk into Homo in 1940) for KNM-ER 1470;
he suggested this was justied because of the morphological differences between the Koobi Fora
cranium and the fossils from Olduvai Gorge allocated to H. habilis sensu stricto (Alexeev 1986).
Groves (1989) later suggested that P. rudolfensis should be transferred to the genus Homo such
that its formal name would be Homo rudolfensis. Some claimed that when Alexeev established
P. rudolfensis, he violated the rules of The International Code of Zoological Nomenclature
(Kennedy 1999), but although Alexeevs proposal was idiosyncratic and did not follow all of the
recommendations of the Code, it did comply with its rules (Wood 1999). Thus, if H. habilis sensu
lato does subsume more variability than is consistent with it being a single species, and if KNM-ER
1470 is judged to belong to a different species than the type specimen of H. habilis sensu stricto (i.e.,
OH 7), then H. rudolfensis is available as the name of a second early Homo taxon.
Those who subscribe to a two-taxon solution with H. rudolfensis as the second taxon have
claimed that H. rudolfensis and H. habilis sensu stricto show a different mix of primitive and derived
features (e.g., Wood 1991). For example, the face of KNM-ER 1470 is widest at its mid-part,
whereas the faces of OH 13 and KNM-ER 1813 are widest superiorly. The absolute size of the
brain case of KNM-ER 1470 (approximately 750800 cm3 ) suggests that the cranial capacity of at
least one H. rudolfensis individual is greater than that estimated for OH 7 (approximately 670 cc),
but when the absolute size of the brain of KNM-ER 1470 is related to estimates of body mass, it is
not signicantly larger than the estimated sizes of the brains of OH 13 or KNM-ER 1813. It has
been suggested that the more primitive face of H. rudolfensis is combined with a robust mandibular
corpus and postcanine teeth with larger crowns and more complex premolar root systems (e.g.,
KNM-ER 1802) than those seen in most specimens of H. habilis sensu stricto (Wood 1991).
In his comparative analysis of the variation subsumed in the separate and combined Tanzanian
and Kenyan/Ethiopian samples of early Homo, Wood (1991) made it plain that the hypodigm
from Koobi Fora most probably samples more than one, and probably two, taxa of early Homo,
the same data suggest that these two taxa are marginally more likely to be synchronic than time
successive (p. 250). He was also careful to suggest that the hypothesis of distinct early and late
Homo taxa cannot be condently falsied, nor can these data categorically exclude a single taxon
solution (Wood 1991, p. 250). Clearly, additional specimens are needed to test the two-taxon
hypothesis and existing proposals for allocating individual specimens to the hypodigms of the two
hypothetical taxa. New material recently discovered at Koobi Fora and currently under study may
help resolve some of these issues.
Most of the fossil evidence for H. erectuslike fossils comes from sites in the Turkana Basin.
Fossils recovered from Koobi Fora have provided well-preserved crania (e.g., KNM-ER 3733,
3883, 24700) and mandibles (e.g., KNM-ER 730, 820, 992); there is also a fragmentary but diseased
associated skeleton, KNM-ER 1808, and a second less complete associated skeleton, KNM-ER
803. A morphologically distinctive occipital fragment, KNM-ER 2598, from 4 m below the KBS
Tuff has also provided the current approximately 1.87-Ma rst appearance datum for H. erectus.
There is debate about whether H. habilis and H. erectus are time successive (i.e., allochronic) or
synchronic taxa. In 2001, KNM-ER 42700, a 1.55-Ma cranium lacking the face, was recovered
from the Koobi Fora Formation at Ileret. Its size overlaps some of the earlier nonmegadont
crania included in H. habilis sensu lato, but it displays morphology typical of Asian H. erectus. Early

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African H. erectus had been given the name Homo ergaster after 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 in H. erectus (as does the magnicent collection
of hominins from Dmanisi), and when compared with other H. erectus skulls such as OH 9, Spoor
et al. (2007) suggest it is consistent with a high degree of sexual dimorphism and with African
and Asian Homo erectus belonging to the same species. The Koobi Fora material also provided
evidence pertinent to the origins of H. erectus, for the discovery of a maxilla, KNM-ER 42703,
dated at 1.44 Ma, which represents the youngest H. habilis known, indicates these two hominin
taxa coexisted for close to half a million years. This makes it less likely (but not impossible) that
the latter evolved into the former and is evidence in favor of cladogenesis within early Homo.
EVIDENCE FOR TAXONOMIC DIVERSITY IN LATER HOMO

There is also evidence of taxonomic diversity, but not necessarily sympatry, much more recently
within the Homo clade. It has long been accepted that H. sapiens and H. neanderthalensis overlapped
in time if not in space, but more recently Grun
et al. (1997) suggested that H. erectus persisted much
later 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. oresiensis, a novel dwarfed H. erectus-like species (Morwood & Jungers 2009).
The species H. oresiensis was 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 and
evidence 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 that
are 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 in
Southeast 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), its
especially small brain (approximately 417 cm3 ) for an adult hominin, and its primitive morphology,
they have suggested that the collection of fossils is most parsimoniously interpreted as evidence
of a novel endemically dwarfed premodern Homo. A vociferous minority claims that no new taxon
needs to be erected because it considers H. oresiensis to sample a population of H. sapiensmost
likely related to the small-statured Rampasasa people who live on Flores todayaficted by either
an endocrine disorder or one, or more, of a range of syndromes that include microcephaly (i.e., a
pathologically 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 what
pathology results in an early Homo-like cranial vault; primitive mandibular, dental, carpal and pedal
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 that H. oresiensis was a dwarfed H. erectus, but the burden of subsequent analyses (Argue
et al. 2009, Brown & Maeda 2009, Morwood & Jungers 2009, Tocheri et al. 2007) suggests that
it may be more closely related to a transitional hominin such as H. 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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in Africa. The earliest fossil evidence for anatomically modern humans comes from Ethiopia at
Omo Kibish (approximately 190 ka) (McDougall et al. 2005) and from Herto (approximately 160
154 ka) (White et al. 2003). Although these crania are more robust and exhibit an overall more
archaic appearance than later H. sapiens, their features do not warrant allocation to a premodern
Homo species.
There is a long-standing debate about whether H. sapiens arose in Africa and then migrated across the globe, replacing any and all premodern Homo populations, or whether these
various migrations of modern humans engaged in signicant levels (i.e., detectable genetically
or morphologically) of interbreeding with the preexisting premodern Homo populations (e.g.,
Relethford 2001, Stringer 2002). The multiregional continuity hypothesis argues that once
H. sapiens left Africa, signicant gene ow took place between them and the hominins they encountered (Wolpoff et al. 2000) and that, moreover, this gene ow inuenced the nature of regional
variations in morphology seen among extant populations of H. sapiens. The strong version of the
recent out-of-Africa model also posits that H. sapiens arose in Africa, but it suggests that no signicant gene ow took place between them and the hominins they encountered beyond Africa.
In the past two decades most of the genetic evidence has favored the recent out-of-Africa hypothesis. A seminal study from Allan Wilsons lab (Cann et al. 1987) suggested that the common
ancestor of all (maternally inherited) modern mitochondrial DNA (mtDNA) lived in Africa approximately 200 ka, and studies investigating the evolutionary history of the paternally inherited
Y chromosome suggested that the last common ancestor of modern humans lived well within
the past 100 ka (Karafet et al. 2008, Thomson et al. 2000). Investigations of single nucleotide
polymorphisms (SNPs) and autosomal microsatellites indicate that genetic diversity is highest in
Africa and steadily decreases as the distance from the continent increases (Prugnolle et al. 2005,
Ramachandran et al. 2005), and prior to 2010 research on mtDNA had not revealed any evidence
of admixture (Briggs et al. 2009, Jakobsson et al. 2008, Krings et al. 1997, Serre et al. 2004, Tishkoff
et al. 2009).
This perspective was challenged in 2010 with the publication of the draft sequence of the
nuclear genome reconstructed from DNA recovered from three H. neanderthalensis fossils from
Vindija Cave in Croatia (Green et al. 2010). This study also found that all of the H. sapiens
DNA samples tested (with the notable exception of those from Africa) contained between 1%
and 4% of the distinctive DNA sequence recovered from Neanderthal fossils. By identifying and
analyzing SNPs between the two groups of genomes, the researchers discovered that Neanderthal
DNA is signicantly closer to non-African modern human DNA than it is to African DNA, and
statistical analysis of the gene ow led the researchers to argue that the gene ow was from
Neanderthals to the ancestors of non-African modern humans. This evidence suggests that once
early anatomically modern humans left Africa, some interbreeding did occur with the indigenous
groups of Neanderthals they encountered, conceivably in the Middle East before modern humans
moved into Eurasia and prior to the divergence of the European, East Asian, and Papuan groups.
These new data are consistent with the assimilation hypothesis espoused by Fred Smith (Smith
1985; Smith et al. 1989, 2005; Trinkaus & Smith 1985). As new evidence accumulates, the theory of
modern human origins will most likely move away from a simple recent out-of-Africa explanation
to a more intricate and sophisticated account in which several different groups of ancestors lived
in pockets around the globe.
More evidence for taxonomic complexity in later Homo (see above) came from an unexpected
source. In 2008 a taxonomically undistinguished hominin distal manual phalanx was recovered
from layer 11 (approximately 5030 ka) at the cave site of Denisova in southern Siberia. Its
geographical location plus the subterranean location of the sediments provided near-optimal conditions for DNA preservation, and in April 2010 the complete mitochondrial genome of that

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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 afnities 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 of H. sapiens
share approximately 46% of their DNA with the Denisovans. These landmark papers suggest
there is evidence of gene ow from premodern Homo species to modern H. sapiens at two different 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 possibility 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 supplement 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 to
have taken place since the divergence of the separate lineages leading to modern humans and
Neanderthals.
Possible genetic modications range from single-nucleotide substitutions to extensive chromosomal transformations. Three mechanisms have been put forward to explain the phenotypic
differences between modern humans and chimpanzees/bonobos. The rst stresses modications
to protein-coding genes, and thus many genomic studies have focused on detecting protein-coding
sequences that have undergone accelerated evolution, i.e., a greater rate of nonsynonymous amino
acid 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 focuses 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 observation
by 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 regulatory regions of the genes result in signicant changes in gene expression. There has been
considerable debate about the relative contributions made by these three mechanisms, but evidence increasingly indicates that regulatory differences have played a major role in the evolution
of 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 balanced view of the variation between the two genomes is to be obtained. The modern human and
chimpanzee genomes were sequenced using different methods, and therefore direct comparison
of the coverage of the two is difcult. Because the chimpanzee sequence is not sequenced to
the same standard as the modern human genomethe chimpanzee draft sequence has only 6
coverage, compared with the 30 coverage of the modern human sequencedifculties have
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Neanderthal
Human
Skin physiology RPTN (Green et al. 2010)
Sperm motility SPAG17 (Green et al. 2010)
Wound healing PCD16 (Green et al. 2010)
rRNA regulation TTF1 (Green et al. 2010)
Hair and skin color MC1R (Lalueza-Fox et al. 2007)
Hair and
skin color
Pathogen resistance CMAH (Chou et al. 2002),
MC1R (LaluezaFox et al. 2007)
Skeletal
development
CASP12 (Wang et al. 2006)
Hair protein KRTHAP1 (Winter et al. 2001)
(Clark et al. 2003)

Hearing (Clark et al. 2003)

Brain development PDYN (Rockman et al. 2005),
Y genes
HAR1 (Pollard et al. 2006a,b), THBS2 and THBS4 (Ccares et al. 2007)
(Hughes
et al. 2005)
Limb development HACNS1 (Prabhakar et al. 2008)

Nervous system (Dorus et al. 2004)
Speech FOXP2 (Enard et al. 2002)
Jaw musculature MYH16 (Stedman et al. 2004)
Olfactory organs MOXD2 (Hahn Y. et al. 2007)
Skin physiology S100A15A (Hahn Y. et al. 2007)
Brain size ASPM (Evans et al. 2004b), MCPH1 (Evans et al. 2004a)
Aerobic energy metabolism AEM genes (Uddin et al. 2008)
Gene
regulation
evolution
Protein
evolution
Gene
loss
Figure 3
Examples of potentially functionally important genetic changes along the human and chimpanzee lineages. Genetic changes of all types
(protein evolution, gene regulation evolution, gene loss) have been identied. As current research largely focuses on modern human-,
rather than ape-, specic changes, fewer changes along the chimpanzee lineage are known. The placement does not indicate any
chronological 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 techniques
used.
PROTEIN EVOLUTION
Sequence comparisons between modern human and chimpanzee genomes provide evidence for
genes that have been positively selected in modern humans since the divergence of the two lineages.
Now, with the publication of the Neanderthal genome, it is possible to compare the modern human
and the Neanderthal genomes to hunt for genetic changes that have occurred recently. Thus far,
78 substitutions in protein-coding genes have been noted between the two, and in each case the
Neanderthals possessed the ancestral state and modern humans the derived condition (Green et al.
2010). The modications in the modern human lineage include changes to RPTN, which encodes
for the protein repetin involved in skin physiology; SPAG17, which encodes for a protein involved
in sperm motility; TTF1, which is involved in ribosomal gene transcription control; PCD16, a
cell-cell adhesion molecule that has a likely role in wound healing; and CAN15, which encodes
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 and
their immediate ancestors would have evolved mechanisms that allowed for the evolution of these
larger brains. Mitochondria are fundamental to efcient production of aerobic energy, and any
genetic changes that would have allowed for their more efcient functioning most likely would
have been positively selected for with time. Studies have shown that the genes that code for
the 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 ape
evolution. 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, AEM
genes 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 of abnormal spindlelike microcephaly associated (ASPM) and Microcephalin (MCPH1) and either brain size or intelligence,
individuals possessing loss-of-function mutations in these genes have pathologically small (i.e., microcephalic) brains owing to effects on the dynamics of mitotic division in neuroprogenitor cells of
the cerebral cortex (Evans et al. 2004a,b; Mekel-Bobrov et al. 2007; Timpson et al. 2007). There is
evidence of positive selection on MCPH1 prior to the MRCA of chimpanzees/bonobos and modern humans and on ASPM in the modern human lineage since the MRCA (Goodman & Sterner
2010, Goodman et al. 2009). One study suggested that haplogroup D, the derived form of MCPH1,
developed in an earlier hominin lineage that subsequently separated from modern humans at approximately 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 identied as a possible source of the movement of haplogroup D back
into H. 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 these
and other known microcephaly genes (CENPJ, CDK5RAP2) suggests a sex-specic association in
each microcephaly gene except CENPJ during neurogenesis (Rimol et al. 2010).
Melanocortin 1 Receptor
The evolution of skin color has generated great interest in the scientic community, and one of
the outcomes of the publication of the draft chimpanzee genome sequence was the nding 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 physiology
are 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 and
red hair (Lalueza-Fox et al. 2007). Recent developments in the amplication of ancient DNA have
enabled researchers to look at this gene in both H. sapiens and H. neanderthalensis. Lalueza-Fox
et al. (2007) recognized a mutation on the MC1R gene in the two Neanderthal specimens that was
not observed in the 3,700 modern humans they analyzed. They argue that the mutations in MC1R
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arose independently in each lineage and became xed in the populations as a result of convergent
evolution.
GENE REGULATION AND EXPRESSION

Investigations into gene expression patterns have thus far identied differences between Homo
and Pan in roughly 100 genes (Marques-Bonet et al. 2009). For example, the coding region
for prodynorphin (PDYN), a precursor molecule with a role in regulating behavior, memory, and
perception, shows a strong positive selection signal (Rockman et al. 2005). It has been suggested
that many of the observed differences in gene expression can be explained by changes in gene
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 the
vertebrate genome but have evolved in modern humans more rapidly than can be explained by
drift alone. Pollard et al. (2006a,b) recognized 49 HARs, of which only two code for proteins. One
of the 49, HAR1, is part of a novel RNA gene, HAR1F, that is expressed in the brain and involved
in neurodevelopment. In addition, the gene enhancer HACNS1 (human-accelerated conserved
noncoding sequence 1) is strongly conserved in terrestrial mammals and has accrued 16 modern
humanspecic mutations since it diverged from Pan (Prabhakar et al. 2008). HACNS1 is expressed
in the developing limb bud and may have a role in the development of the thumb and wrist region.
Thrombospondin 2 and Thrombospondin 4

Proteins known as thrombospondins (THBSs) play a role in the formation of synapses and neurite
growth, and a higher expression rate of THBS genes and their resultant proteins in the adult
modern human brain has been suggested as a mechanism for synaptic remodeling of modern
humans. Microarray studies indicate a sixfold increase in the expression of THBS4 mRNA and
a twofold increase in THBS2 mRNA in the cerebral cortex of modern humans when compared
with chimpanzees or macaques (Caceres et al. 2007). This increase in expression has prompted
the suggestion that enhanced synaptic plasticity may be a dening feature of the adult modern
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 and
therefore the tness of an organism. Genes are lost as a result of gene deletions or mutations
leading to a loss of function, and they can be gained as a result of duplications. Many of the genes
known to have been either gained or lost in the modern human genome since humans diverged
from chimpanzees/bonobos are involved in olfaction and/or taste (Hahn M. et al. 2007, Wang
et al. 2006).
MOXD2 and S100A15A

An exon deletion resulted in the inactivation of Monooxygenase, DBH-Like 2 (MOXD2) and a
calcium-binding protein (S100A15A) in the modern human lineage since its divergence from Pan
(Chou et al. 1998, Hahn Y. et al. 2007). MOXD2 is highly conserved in mammals and encodes
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an enzyme chiey expressed in the olfactory epithelium. Hahn Y. et al. (2007) have identied
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, S100A15A plays a role in
skin 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 duplicated or deleted on certain chromosomes. Their importance to human evolution and genetic
variation is reected 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 of
CNVs 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 genus Homo would have been conned to a review
of 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 modern
human phenotype such as the substantial increase in brain size and the changes in brain shape that
occur within the genus Homo. Third-generation sequencing technology will provide researchers
with 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 modern H. sapiens. The challenge
of 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 of
the 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 but
also how it happened.
DISCLOSURE STATEMENT
The authors are not aware of any afliations, memberships, funding, or nancial 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 2008
illustration.
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Alexeev V. 1986. The Origin of the Human Race. Moscow: Progress
Arbiza L, Dopazo J, Dopazo H. 2006. Positive selection, relaxation, and acceleration in the evolution of the
human and chimp genome. PLoS Comput. Biol. 2:e38
Argue D, Morwood MJ, Sutikna T, Jatmiko, Saptomo EW. 2009. Homo oresiensis: a cladistic analysis. J. Hum.
Evol. 57:62339
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Bakewell MA, Shi P, Zhang JZ. 2007. More genes underwent positive selection in chimpanzee evolution than
in human evolution. Proc. Natl. Acad. Sci. USA 104:748994
Bermudez
de Castro JM, Ramirez Rozzi F, Martinon-Torres M, Sarmiento Perez S, Rosas A. 2003. Patterns
of dental development in Lower and Middle Pleistocene hominins from Atapuerca (Spain). In Patterns
of Growth and Development in the Genus Homo, ed. JL Thompson, GE Krovitz, AJ Nelson, pp. 24670.
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Contents
Annual Review of
Ecology, Evolution,
and Systematics
Volume 42, 2011
Native Pollinators in Anthropogenic Habitats

Rachael Winfree, Ignasi Bartomeus, and Daniel P. Cariveau p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p23
Evolution in the Genus Homo
Bernard Wood and Jennifer Baker p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p47
Ehrlich and Raven Revisited: Mechanisms Underlying Codiversication
of Plants and Enemies
Niklas Janz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p71
An Evolutionary Perspective on Self-Organized Division of Labor
in Social Insects
Ana Duarte, Franz J. Weissing, Ido Pen, and Laurent Keller p p p p p p p p p p p p p p p p p p p p p p p p p p p p91
Evolution of Anopheles gambiae in Relation to Humans and Malaria
Bradley J. White, Frank H. Collins, and Nora J. Besansky p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 111
Mechanisms of Plant Invasions of North America and European Grasslands
T.R. Seastedt and Petr Pysek p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 133
Physiological Correlates of Geographic Range in Animals
Francisco Bozinovic, Piero Calosi, and John I. Spicer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 155
Ecological Lessons from Free-Air CO2 Enrichment (FACE) Experiments
Richard J. Norby and Donald R. Zak p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 227
ES42-FrontMatter
ARI
11 October 2011
16:5
The Patterns and Causes of Variation in Plant Nucleotide Substitution Rates

Brandon Gaut, Liang Yang, Shohei Takuno, and Luis E. Eguiarte p p p p p p p p p p p p p p p p p p p p p 245
Long-Term Ecological Records and Their Relevance to Climate Change
Predictions for a Warmer World
K.J. Willis and G.M. MacDonald p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 267
The Behavioral Ecology of Nutrient Foraging by Plants
James F. Cahill Jr and Gordon G. McNickle p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 289
Climate Relicts: Past, Present, Future
Arndt Hampe and Alistair S. Jump p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 313
Rapid Evolutionary Change and the Coexistence of Species

Richard A. Lankau p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 335
Developmental Patterns in Mesozoic Evolution of Mammal Ears
Zhe-Xi Luo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 355
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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 381
On the Use of Stable Isotopes in Trophic Ecology
William J. Boecklen, Christopher T. Yarnes, Bethany A. Cook, and Avis C. James p p p p 411
Phylogenetic Methods in Biogeography
Fredrik Ronquist and Isabel Sanmartn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 441
Toward an Era of Restoration in Ecology: Successes, Failures,
and Opportunities Ahead
Katharine N. Suding p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 465
Functional Ecology of Free-Living Nitrogen Fixation:
A Contemporary Perspective
Sasha C. Reed, Cory C. Cleveland, and Alan R. Townsend p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 489
Indexes
Cumulative Index of Contributing Authors, Volumes 3842 p p p p p p p p p p p p p p p p p p p p p p p p p p p 513
Cumulative Index of Chapter Titles, Volumes 3842 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 517
Errata
An online log of corrections to Annual Review of Ecology, Evolution, and Systematics
articles may be found at http://ecolsys.annualreviews.org/errata.shtml
vi
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Evolution in The Genus Homo

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Annu. Rev. Ecol. Evol. Syst. 2011.42:47-69. Downloaded from www.annualreviews.org

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