The Biology of the Colonizing Ape - Binghamton...

The Biology of the Colonizing Ape

Jonathan C.K. Wells1* and Jay T. Stock2

1Childhood Nutrition Research Centre, Institute of Child Health, London WC1N 1EH, UK2Leverhulme Centre for Human Evolutionary Studies, Department of Biological Anthropology,University of Cambridge, Cambridge CB2 1QH, UK

KEY WORDS adaptation; plasticity; human evolution; migration; dispersal

ABSTRACT Hominin evolutionary history is charac-terized by regular dispersals, cycles of colonization, andentry into novel environments. This article considers therelationship between such colonizing capacity and homi-nin biology. In general, colonizing strategy favors rapidrates of reproduction and generalized rather than special-ized biology. Physiological viability across diverse envi-ronments favors a high degree of phenotypic plasticity,which buffers the genome from selective pressures. Colo-nizing also favors the capacity to access and process infor-mation about environmental variability. We propose thatearly hominin adaptive radiations were based upon thedevelopment of such capacities as adaptations to unstablePliocene environments. These components came together,along with fundamental changes in morphology, behavior,and cognition in the genus Homo, who exploited them insubsequent wider dispersals. Middle Pleistocene homi-nins and modern humans also show development of fur-ther traits, which correspond with successful probing of,and dispersals into, stressful environments. These traitshave their precursors in primate or ape biology, but havebecome more pronounced during hominin evolution.

First, short interbirth intervals and slow childhoodgrowth allow human females to provision several off-spring simultaneously, increasing the rate of reproductionin favorable conditions. This allows rapid recovery frompopulation crashes, or rapid population growth in newhabitats. Second, despite high geographical phenotypicvariability, humans have high genetic unity. This isachieved by a variety of levels of plasticity, includingphysiology, behavior, and technology, which reduce theneed to commit to genetic adaptation. Hominin behaviormay increasingly have shaped both the ecological nichesoccupied and the selective pressures acting back on thegenome. Such selective pressures may have been exacer-bated by population dynamics, predicted to both derivefrom, and favor, the colonizing strategy. Exposure to eco-logical variability is likely to have generated particularselective pressures on female biology, favoring increasingsteering of offspring ontogeny by maternal phenotype. Wepropose that the concept of hominins as ‘‘colonizing apes’’offers a novel unified model for interpreting the suite oftraits characteristic of our genus. Yrbk Phys Anthropol50:191–222, 2007. VVC 2007 Wiley-Liss, Inc.

The tendency of humans and their ancestors to dis-perse, migrate, and colonize new habitats and territoriesis well-known to academics of many disciplines. Paleon-tologists, archeologists, anthropologists, geographers, andhistorians have accumulated considerable evidence of theextent to, and the manner in, which individuals and pop-ulations have moved and interacted (Villaflor and Sokol-off, 1982; Clark, 1986; Mascie-Taylor and Lasker, 1988;Anthony, 1990; Gamble, 1993; Robinson, 1996; Diamond,1987, 1998; Lahr and Foley, 1994, 1998; Kingdon, 2001;Shennan, 2002). The movement of individuals is one ofthe principal forces of evolution, along with natural selec-tion, mutation, and genetic drift, and hence has been ofmajor interest to population geneticists (Fix, 1999). Suchdispersals may also be considered within a broader bio-logical context (Baker, 1978; Chepko-Sade and Halpin,1987; Dingle, 1996; Clobert et al., 2001).

Many authors emphasize two major migrations inhuman evolution—the dispersals of Homo erectus andanatomically modern Homo sapiens, both from Africa.These are merely the most large-scale migrations amonga continuum of population movements within and be-tween specific regions, habitats, and territories, whichoccurred throughout hominin evolution, commencingwith the emergence of hominins and the subsequentadaptive radiation of Australopithecines. Contrastingwith this evolutionary history, it is important to notethat most ethnographies of contemporary or recent popu-lations record low levels of population movement. Con-temporary human populations tend to be relatively phil-

opatric, where migration concerns only short range mari-tal movements (Fix, 1999). Regional warfare or economichardship within an increasingly globalized human com-munity are important contemporary factors promotingperiodic dispersals over longer distances; however, theseconcern movements between territories already popu-lated. In themselves, therefore, modern population move-ments have limited capacity to inform about any broadertendency to colonize and its contribution to our biology.

Dispersal is one of a range of strategies whereby organ-isms can improve their environmental conditions, in termsof food supplies, access to mates, and the risk of predation(Fix, 1999). One challenge is that there has never been asingle ‘‘real’’ population structure of humans. Rather, pop-ulation structure and movement are just one more way inwhich humans adapt to the broader environment (Fix,1999). The movement of DNA between gene pools, and thepenetration of gene pools into novel environments, havetherefore been consistent features of hominin evolution,although their relative influences may have fluctuatedover time. Such adaptive strategies in turn are subject toconstraints that limit the regional and total availability of

*Correspondence to: J.C.K. Wells, Childhood Nutrition ResearchCentre, Institute of Child Health, 30 Guilford Street, London WC1N1EH, UK. E-mail: [email protected]

DOI 10.1002/ajpa.20735Published online in Wiley InterScience

(www.interscience.wiley.com).

VVC 2007 WILEY-LISS, INC.

YEARBOOK OF PHYSICAL ANTHROPOLOGY 50:191–222 (2007)

resources. As predicted by Malthus (1798/1976), popula-tions tend therefore to grow, spread, decline, or contractover time, according to the availability of resources.

Diamond (1987) noted that humans are similar to manyother species in undergoing cycles of colonization, whileFoley (1987) considered hominin colonization within thebroader context of mammalian and geophysical trends,and suggested that successful colonization would befavored by both the retention of generalist physiologicaltraits, and the evolution of behavioral and cultural prac-tices aiding adaptation to novel environments. Lahr andFoley (1998) further emphasized the importance of disper-sals in the recent evolutionary history of the genus Homo.The term ‘‘colonizing ape’’ was applied to humans by Hilland Hurtado (1996) following their detailed demographicanalysis of the Ache, a foraging population from Paraguay.Gamble (1993) considered humans and their ancestors as‘‘timewalkers’’ continually encountering new habitats,while Shennan (2002) reviewed the implications of popula-tion expansions and crashes for interpreting the archeo-logical record. These authors have all addressed thefundamental role of colonization in human evolution andhistory. However, despite such awareness among paleoan-thropologists and archeologists that humans are and havebeen colonizers, it can be argued that few human biolo-gists have appreciated the extent to which ‘‘getting there’’is as relevant to our biology as ‘‘being there.’’

The themes of colonization and dispersal are prevalentin the genetics, archeological, and paleoanthropologicalliterature. In contrast, the aim of this review is to con-sider contemporary issues in human biology within theintegrative framework of colonization, and to examinethe extent to which hominins and humans fit the profileof ‘‘colonizing apes.’’ The second section offers a briefreview of the migratory history of apes and hominins. Inthe third section, the broad biology of colonization isdescribed, to provide a template against which homininand human biology can be compared. The next sectiondescribes hominin life history and population dynamics,while the final section reviews evidence for the hypothe-sis that, relative to apes, humans have traits thatimprove the capacity to colonize.

THE HISTORY OF DISPERSALS IN THEHOMININE LINEAGE

Dispersals and adaptive radiations have characterizedhominin evolution in its entirety (Foley, 2002). They havearisen both as habitat ranges have expanded andcontracted in relation to climatic variability, and thro-ugh the exploitation of novel environmental niches (Lahrand Foley, 1998). Increasing environmental fluctuationthroughout the Pliocene and Pleistocene has been high-lighted as a major factor in the evolution of the homininlineage by selecting for species to be able to accommodateenvironmental variability and exploit a diversity of envi-ronments (Foley, 1987; Potts, 1998a). Recent literature isreplete with characterizations of hominin dispersal eventsas Out of Africa 1 and 2 models, referring to dispersals ofHomo erectus1 and modern Homo sapiens, respectively,

although the pattern of hominin dispersal throughout thelast 1.8 million years is likely to be more complex thanthese characterizations would suggest. Regardless, thereis little doubt that recent human populations have colon-ized novel environments on a scale not seen in earlier spe-cies, and that this proposition is not an artifact of fossilpreservation. While these patterns of hominin dispersalwould merit several reviews in themselves, the aim hereis only to identify the main events and protagonists, toprovide a foundation for discussion of the biological andbehavioral factors, which underpin these dispersals.

Primates and apes

Significant movement of species between continentsand ecological zones is not unknown for nonhuman pri-mate species. Hamadryas baboons have crossed a landbridge at the Bab el Mandab strait between Africa andArabia on a number of occasions over the past severalhundred thousand years (Winney et al., 2004). While thishighlights intercontinental dispersals among a primatespecies, environmental conditions in Arabia and EastAfrica would have been relatively consistent with oneanother, even if there were fluctuations in time. There isalso evidence for dispersal events amongst apes. Althoughextant apes exist only within Africa and southeast Asia,where Miocene fossil apes are scarce, there is abundantfossil evidence for apes within Eurasia during the Miocene(Begun, 2002). Phylogenetic analyses of Miocene apes sug-gest that the common ancestor of hominins and extantAfrican apes was Eurasian (Begun, 1997, 2000; Stewartand Disotell, 1998), which indicates a minimum of two dis-persal events of Miocene apes between Africa and Eura-sia. These appear to have been associated with the disper-sal of other mammalian taxa including carnivores (Nar-golwalla and Begun, 2005; Folinsbee and Brooks, 2007),and thus to be based upon movements within relativelyconsistent ecological niches, following patterns observedin other mammals, while drying conditions in sub-Saharan Africa led to extinctions (Begun et al., 2003).

Early hominin species

Late Miocene and early Pliocene hominin origins canbe considered as the beginning of an adaptive radiation,possibly based upon the origins of bipedalism, which mayhave followed shortly after a Eurasian dispersal of apesinto Africa (Foley, 2002). Of key importance at this timeis not a dispersal event per se, but the evidence that newphenotypic traits within the emergent hominin lineagecorresponded with a general trend toward more xeric con-ditions and ecologically diverse habitats. Climatic oscilla-tions that occurred both on seasonal scales and withinthe lifespan likely defined the selective environments ofhominins (Foley, 1987), but such variability may havebeen important across a broader temporal scale. Potts(1998a,b) proposed the term Variability Selection to referto the selection of characteristics, which favored the abil-ity of hominins to exploit a range of habitats across majorlonger term climatic fluctuations. In this model, thecapacity for adaptive versatility evolves when there arelarge inconsistencies in selective conditions. Such a mech-anism could operate on the shorter time scales proposedby Foley, which would correspond to selective pressurewithin the lifespan rather than across generations. Fromthe late Miocene through the Pleistocene, environmentalvariability was increasing from seasonal to multimillen-

1While recent usage has favored the distinction between Homoergaster from Africa and Homo erectus from east Asia, we will useHomo erectus (sensu lato) as a generic term to include both Asianand African variants. This simplifies the discussion and allows thefocus to be placed on biological characteristics related to thecapacity for dispersal within this grade of hominins, rather thantaxonomic issues associated with relationships between fossils.

192 J.C.K. WELLS AND J.T. STOCK

Yearbook of Physical Anthropology—DOI 10.1002/ajpa

nial time scales (Foley, 1987; Potts, 1998a). This resultedin increasing fragmentation of ecological niches, whichwould have emphasized local selective pressures onorganisms and evolutionary novelty. In this context, apespecies could either maintain a general frugivore adapt-ive strategy within the reducing areas of rain forest, orexploit the new and expanding savannah habitat (Foley,1987).

Ancestral chimpanzees and gorillas appear morphologi-cally similar to contemporary species (McBrearty andJablonski, 2005; Suwa et al., 2007) suggesting similaradaptive niches to contemporary representatives of thespecies. Proposed early hominin species such as Sahelan-thropus tchadensis (Brunet et al., 2002), Orrorin tugene-sis (Senut et al., 2001), and Ardipithecus ramidus (Whiteet al., 1994) are found in a range of habitats. However,fossil chimpanzee remains from the Kapurthin formationin the Rift Valley system place middle Pleistocene chim-panzees beyond their current distribution and contempo-rary with early Homo or Homo erectus (McBrearty andJablonski, 2005). Although the origin of bipedalism is of-ten interpreted as a response to increasing resourcepatchiness and expanding grassland in a mixed woodlandsavanna environment, it is difficult to determine whetherindividual species are associated with multiple habitattypes due to the time averaging effect of many fossilassemblages. However, the data available suggest thatlate Miocene and early Pliocene species filled differentadaptive niches within the hominin adaptive radiation,including forest, woodland, savanna, and mosaic habitats(Reed, 1997; Potts, 1998a). It is therefore likely that thefoundation of hominins’ tendency to colonize can betraced to early hominin and australopithecine biology,whereby populations entered new and unstable environ-ments, which in turn imposed localized selective pres-sures. When previously separated populations encoun-tered each other, each species is likely to have formed acomponent of the selective pressures acting on the other.

While the adaptive radiation of hominins provides thebasis for the exploitation of a range of habitats in thehuman lineage, it is often assumed that this would berelated to an increase in home range. Recent evidencefor very large home range sizes ([63 km2) and the ex-ploitation of a variety of ecological niches amongst themosaic savanna chimpanzees at Fongoli (Pruetz andBertolani, 2007) provides corroborative evidence thatsimilar patterns of diverse habitat exploitation wouldlikely have resulted in greater home ranges amongstearly hominins.

Early Homo

The location of the origin of the genus Homo, and thetaxonomy of early Homo remain controversial. Althoughthe earliest evidence for fossils typically assigned to thegenus Homo date between 2.6 and 2.4 MYA (Wood andCollard, 1999a), some now regard Homo erectus gradehominins, whose earliest appearance is about 1.89 MYAin Eastern Africa, as the first convincing member of thegenus (Wood and Collard, 1999b). The predominant viewof the relationship between African, Eurasian, and EastAsian Homo erectus is described by the ‘‘longer chronol-ogy’’ Out of Africa 1 model (Anton and Swisher, 2004).This model suggests that Homo erectus evolved withinAfrica, and rapidly dispersed to Eurasia, by 1.7 MYA atDmanisi, Georgia (Gabunia et al., 2000) and Indonesia,by as early as 1.8 MYA (Swisher et al., 1994).

Several assumptions central to the longer chronologyOut of Africa 1 model have been challenged. The lack ofboth a clear ancestor of Homo erectus and diagnostic cra-niodental material amongst early larger bodied postcra-nial remains tentatively assigned to the taxa (McHenryand Coffing, 2000) remain problems. Others have sug-gested that Asia is a plausible alternative source of theevolution and dispersals of Homo erectus (Dennell andRoebroeks, 2005), although there is a current lack of fos-sil evidence to support this hypothesis. However, what isrelevant to the current review is that there is unequivo-cal evidence for a large-scale intercontinental dispersalpreceding or following the emergence of Homo erectus,regardless of its point of origin. A rapid emergence anddispersal of Homo erectus is not implausible. Othermammal species are known to have evolved rapidly inresponse to a novel niche, and Homo erectus may haveundergone a similar process (Kingdon, 2001) in responseto dramatic aridifcation at around 1.8 MYA (Wynn,2003). At this time, an ecological zone of savanna andsteppe stretched from Eastern and Northern Africathrough the Levant and central Asia (Dennell, 2003).While early Homo erectus fossils from eastern Africa andDmanisi were found within this environmental context,those from Indonesia and Eastern Asia were clearlyassociated with forest environments.

The early Pleistocene dispersal of Homo erectus wasachieved using Oldowan (Mode 1) lithic technology(Anton, 2003), which has a deep chronology within Africa(Semaw et al., 2003). By 1.5 MYA, a more advanced Mode2 Acheulean technology developed and is subsequentlyfound associated with Homo erectus in the Middle Eastand Europe, but its distribution did not extend fully intoAsia (Anton, 2003). As such, lithic technology appears tohave played little role in the early dispersal of Homo,which suggests that other mechanisms may have beenimportant to the evolution of the colonizing strategy.

Current perspectives attribute the dispersing capabil-ities of Homo to a more complete adaptation to the sa-vannah niche, in contrast to ancestral species that weremore suited to forest margin niches. The dramatic shifttoward grassland habitats offered more niches for terres-trial fauna, including both herbivores and their preda-tors (Anton, 2003). Homo erectus may have followed ageneral dispersal of mammalian fauna from Africa(Turner, 1984; Anton et al., 2002). A shift to dependenceupon carnivory through hunting may have helped Homoerectus capitalize on the dispersal of suitable prey speciesand may have been a central component of the dispersalof this species (Foley, 2002). Thus, climate change to-gether with the generalized Homo physique and biology(see below) could have allowed the continued expansionof territory and occupation of new locations by descend-ant groups. Anton et al. (2002) developed a model ofHomo erectus colonization in which increased diet qualityand body size are shown to result in both larger esti-mated home range size and greater rates of dispersal,when compared to living primates and earlier hominins.They view environmental conditions, such as habitatconnectivity and biomass distribution, as fundamental todriving this shift, both in terms of the direct influence ofchanging resource distribution on population movements,but also through changing patterns of foraging behavior,a shift to higher quality foods, and possibly technology.Increased brain size may have further contributed to thecapacity to exploit such ecological changes through asso-ciated improvements in cognitive flexibility.

193THE BIOLOGY OF THE COLONIZING APE


Middle Pleistocene Homo

The link between Homo erectus and subsequent spe-cies is a challenging issue, illustrated by the difficulty oflinking Homo erectus with both Homo sapiens and Nean-derthals in Europe (Lahr and Foley, 1998). Most authorsnow recognize a transitional species, Homo heidelbergen-sis (Groves, 1994), which may have evolved either inAfrica or Europe. Lahr and Foley (1998) recognize afurther transitional species, intermediate between hei-delbergensis and sapiens, Homo helmei. There is biogeo-graphical evidence that contact between African andEurasian biomes occurred regularly through glacialcycles, promoting a number of dispersal events in humanevolution. Despite open questions about the taxonomicrelationships of species, it is clear that by the middlePleistocene (ca. 780 KYA), hominins were in temperateregions of Europe (Carbonell et al., 1995; Bermudez deCastro et al., 1997; Manzi et al., 2001). While fossil evi-dence is sparse, there is lithic evidence for occupation ofnorthern latitudes by 700 KYA (Parfitt et al., 2005).

This evidence for the colonization of Europe and north-ern latitudes raises important questions concerning thetechnological and biological characteristics associatedwith this dispersal. There is clear evidence for thecontrolled use of fire in northern Europe by 400 KYA,associated with Homo heidelbergensis (Gowlett, 2006)suggesting that such technological innovation, if not asso-ciated with the dispersal of this species (Foley, 2002), wasat least necessary for the colonization of northern lati-tudes. It has traditionally been argued on the basis of ar-cheological assemblages that a heavy reliance upon meatwas an integral part of Neanderthal technical and phys-iological adaptations (Mellars, 2004), an interpretationsupported by isotopic evidence (Richards et al., 2000b).

Anatomically modern Homo sapiens

Fossil, genetic, and archeological evidence points to arecent African origin of modern humans (Howells, 1976;Day and Stringer, 1982; Stringer and Hublin, 1984; Lahrand Foley, 1994, 1998; Lahr, 1994), with the commonancestor dating from �150 to 200 KYA (Cann et al.,1987; Tishkoff et al., 1996; Harpending and Rogers,2000; Ingman et al., 2000; Ke et al., 2001; Kivisild et al.,2001; Excoffier, 2002). The earliest modern human fossilsfrom Omo Kibish, and Herto date between 200 and 120KYA (Day, 1969; Day and Stringer, 1982, 1991; Lahr,1996; White et al., 2003; McDougall et al., 2005). Evi-dence for the first dispersal of modern humans out ofAfrica places them in the Levant by 100–90 KYA (Bar-Yosef et al., 1986; Stringer et al., 1989; Stringer, 1992;Mercier et al., 1993; Turbon et al., 1997; Holliday, 2000),although there is no strong fossil evidence for subse-quent dispersals until after �60 KYA. Modern humanscolonized Europe between 46 and 41 KYA (Mellars,2006a), while early modern human remains have beenidentified in Southeast Asia as early as 44 KYA at NiahCave (Barker et al., 2002). Humans may have occupiedAustralia by 62 KYA (Thorne et al., 1999), but are moreconservatively dated to 50 KYA at Lake Mungo (Bowleret al., 2003). These remains help to place minimum timeestimates on the pattern of modern human dispersal,which may be extended in some regions if we associ-ate microlithic technologies with anatomically modernhumans (James and Petraglia, 2005).

Dispersals out of Africa may have taken advantage offluctuating environmental conditions, which opened anorthern route of dispersal through the Levant duringinterglacials, allowing a migration of African fauna intoEurasia (Tchernov, 1992). Conversely, if dispersals fol-lowed a southern route across the Bab al Mandab Strait,and along the coasts of Arabia and South Asia to Aus-tralia, marine resources would have been the key behav-ioral adaptation enabling this migration (Foley andLahr, 1992; Lahr and Foley, 1994; Stringer, 2000). Thesemodels have importance beyond their geographic impli-cations, as a northern dispersal may have been corre-lated with faunal movements, while the southern routeis clearly dependent upon behavioral innovation througha shift toward marine resource exploitation. While arche-ological evidence to test these models is sparse, mtDNAamong contemporary Asian and Australasian popula-tions has unique derived lineages of the M, N, and Rhaplogroups, which coalesce between 70 and 50 KYA(Quintana-Murci et al., 1999; Macaulay et al., 2005;Thangaraj et al., 2005). The northern dispersal routewas inhospitable at this time (Van Andel and Tzedakis,1996), lending indirect support for the southern disper-sal hypothesis.

Closely related to the pattern of dispersals is the issueof ancestral bottlenecks arising due to local extinctions.Genetic analyses indicate an early bottleneck in the pop-ulation ancestral to all contemporary humans between200 and 130,000 years ago, with a population size as lowas around 10,000 individuals (Rogers, 1995; Rogers andJorde, 1995; Takahata et al., 1995); however, this wasfollowed by significant expansion of population sizebetween 80 and 60,000 years ago (Mellars, 2006b),resulting in a degree of population subdivision prior toevidence for the primary dispersals out of Africa (Har-pending et al., 1993; Rogers and Jorde, 1995).

Dispersals also spread northward through the easternAsian continent, supported by genetic variability insouthern compared to northern Chinese populations (Jinand Su, 2000). Although Paleolithic populations mightalso have spread eastward from the Levant area intoAsia, genetic contributions from this source appear to berelatively minor (Kivisild et al., 1999). The chronology ofhuman dispersals into the Americas remains controver-sial, as the traditional interpretation that all populationsin the New World derived from early and/or successivemigrations from northeast Asia are challenged by evi-dence that paleoamericans may have originated fromSouth Asia or the Pacific rim, followed by subsequentreplacement by migrations from northeast Asia (Neveset al., 1999; Gonzalez et al., 2003).

The pattern of dispersal of modern humans has clearlyinfluenced human diversity, because of local selectiveenvironments, the history of colonization, and subse-quent local isolations (Lahr, 1996; Lahr and Foley, 1998).This would increase intergroup differences, a hypothesissupported by regional variability in local assemblages inthe archeological record (Phillipson, 2005; Klein, 1999),and global patterns of morphological variability (Stocket al., 2007). Overall, genetic evidence is consistent withat least two primary dispersals out of Africa (Joblinget al., 2004), and a series of subsequent dispersals fromthese initial lineages. This produced considerable geneticdiversification (Watson et al., 1997), some of which hasbeen negated by more recent gene flow (Lahr, 1996).

These dispersals equate to substantial and continualentrance into new ecological niches, even taking into



account that populations are initially likely to have fol-lowed ‘‘corridors’’ of favorable geography, climate, andfauna. As humans settled in an increasing proportion ofthe world’s land masses, exploratory or invasive disper-sals would have been accompanied or replaced by culturaldiffusion of subsistence practices. Although such informa-tion transfer could have involved many aspects of technol-ogy and behavior, the most important in terms of shapinghuman biology and environmental interactions is thespread of agriculture. There has been considerable debateas to whether the Neolithic spread of agriculture intoEurope was due to demic diffusion of Near Eastern farm-ers or cultural diffusion. Genetic evidence suggests thatonly one-fifth of contemporary mtDNA can be attributedto Neolithic farmers (Sykes, 1999), while most lineageswithin Europe can be traced back to Upper Paleolithicmigrations from the Near East (Richards et al., 2000a).Similar patterns of genetic continuity from Paleolithicdispersals have been found in Australia (Pellekaan et al.,2006) and South Asia (Macaulay et al., 2005). While thereis evidence for relatively recent large scale populationmovements in many areas of the world, for example theBantu expansions in sub-Saharan Africa (Pereira et al.,2001), initial patterns of dispersal out of Africa were offundamental importance in shaping the biological diver-sity found within the human species today.

Summary

Hominin evolution is very much a story of adaptiveradiations, dispersals, colonization, and local extinctionsresulting in population expansions and contractions(Lahr and Foley, 1998). Intercontinental dispersals ofMiocene apes appear to have exploited similar forestniches. Increasing environmental variability across spa-tial and temporal scales played a key role in both extinc-tion events and the selective landscape, which drove theadaptive radiations of early hominins (Foley, 1987; Potts,1998b). The exploitation of varied niches appears to havebeen a component of the success of the dispersal ofHomo erectus and possibly other early Homo species.However, behavioral, social, and technological innova-tions enabled the colonization of a wider range of envi-ronments and niches in the Middle and Upper Paleo-lithic (Lahr and Foley, 1998), augmenting the scale andsuccess of dispersals into more diverse environments,including northern latitudes.

THE BIOLOGY OF DISPERSALAND COLONIZATION

This section provides a broad summary of the biologyof dispersal, against which hominins and humans can beevaluated. It is first necessary to clarify several relatedterms. Gamble (1993) distinguished migration (a discreteshort-term movement), dispersal (a more general processstill small-scale in time and space), and colonization (aprocess occurring on a larger temporal and geographicscale). Using these definitions, colonization is merelydispersal systematically enacted on a broader scale(Gamble, 1993). Migration is a term commonly appliedto human population movements, and yet is inappropri-ate as a broader model: when a population expands itsrange on a large scale, individual organisms may moveonly short distances. This review uses Gamble’s terminol-ogy and focuses on colonization. However, any evaluationof the process of colonization requires understanding

of the general biology of dispersal. Unlike seasonalmigrations, or the movement of individuals betweensocial groups, one-way population movements into newterritories or niches predispose to unpredictable environ-ments (Dingle, 1996). It is the greater risk inherent indispersal as opposed to small-scale migration that under-pins its effects on biological traits.

Diamond (1987) has described three stages in coloniza-tion cycles: an expanding phase, a phase of local adapta-tion by colonist populations, and a retreating phase ofspecialization. Selective pressures are predicted to differduring these stages, but collectively they may act toincorporate the capacity to colonize into the organism’sbiology.

Why disperse?

Dispersal has been described as a process across a land-scape characterized by opportunities and risks (Wiens,2001). Relevant factors include the state of both environ-ment and organism. Risks during dispersal may begreater than those in the old environment, while the newenvironment may also hold many unknowns. Dispersalshould be favored when the benefits of entering and colo-nizing new habitats exceed the costs of migrating andadapting to the new environments (Baker, 1978). Severalcontexts are relevant to these costs and benefits.

Organisms can be assumed to select habitats to maxi-mize fitness, a concept known as the ideal free distribu-tion (Fretwell and Lucas, 1970) where individuals indifferent habitats would have equal average fitness.However, conspecific competition favors dispersal toexploit new resources, such that those displaced fromthe optimum environment may have poorer fitness (Fret-well, 1972). Conspecific competition merges into kin com-petition when dispersal results in relatives being aggre-gated in space. Even in stable habitats, avoidance of kincompetition favors dispersal (Hamilton and May, 1977),and genetic studies reveal high levels of heterozygositywithin primate social groups (Pusey and Packer, 1985).

Bet-hedging refers to a scenario where strategies foravoiding penalties in bad conditions are favored overstrategies for maximizing fitness in good conditions (Phi-lipi and Seger, 1989). This can be achieved either byreducing variance in fitness over generations, or byincreasing phenotypic expression of a single genotypeamong individuals within generations (Philipi and Seger,1989). The enforced dispersal of offspring represents pa-rental bet-hedging, since it distributes risk across envi-ronments with different selective pressures (Den Boer,1968; Ronce et al., 2001).

r- and K-reproductive strategies

Organisms’ reproductive strategies are conventionallyevaluated on a continuum (May and Rubenstein, 1984).At one extreme are opportunistic r-strategists, with highrates of reproduction but short life spans. They dispersewidely and do not necessarily persist in a given environ-ment, but breed rapidly in favorable conditions. Localextinctions are common, but the ‘‘hit and run’’ strategyremains successful because dispersal and fast turnoverrate allow rapid exploitation of new environments. Suchorganisms produce large numbers of offspring but investminimally in each one (May and Rubenstein, 1984).

At the other extreme are K-strategists, which tend tooccupy more stable environments with reduced mortality



risk, allowing the benefits of increased size to be real-ized. However, larger organisms require relatively moreresources and must compete with conspecifics, both forthemselves and for their offspring. K-strategists there-fore grow and reproduce more slowly, and reproductiverate is sensitive to population density. Species persist ina given area, to which they become specialized, and dis-perse slowly to other areas. Organisms adopting thisstrategy produce few offspring at a slow rate, but investconsiderable parental effort in each one. In practice, fewspecies fall at the extremes of the r-K continuum, andmany can merely be placed nearer one or other ideal(May and Rubenstein, 1984). More generally, the K-con-cept has been criticized (Hawkes, 2006a), but the notionthat organisms vary in life-cycle ‘‘pace,’’ and that bodysize is strongly associated with life-history variables, isnot contested (Hawkes, 2006a).

Although humans are often portrayed as K-strategistspar excellence, due to their long lifespans and extendedperiods of parental care, this perspective is not fully sup-ported by evidence. Humans can breed more rapidlythan other apes and are capable of manipulating paren-tal investment to maximize fitness. Furthermore, over-exploitation of environmental resources is increasinglyconsidered a factor in human population dynamics.

Who disperses?

Dispersal tends not to be randomly distributed in apopulation. Even in plants, dispersal is imposed by onegeneration on another, such that movement takes placeprior to breeding. Natal dispersal is also found in manyanimal species, while organisms may also move betweenbreeding areas or social groups (Clobert, 2001). Allknown primates are characterized by intergroup transfer(Pusey and Packer, 1985).

In some species, dispersal is undertaken by groups ofanimals, which may be more successful in competing inthe new environment. Examples include social carni-vores (Doolan and MacDonald, 1996) and some species ofprimate (Pusey and Packer, 1985), and humans fit withthis trend. Colonization of empty sites reduces the costsof kin competition, as does recolonization when extinc-tions occur due to natural events or intrapopulation com-petition. Given the sexual division of labor known in allcontemporary human foraging societies, this pattern ofcolonization must itself have imposed different stresseson each sex.

The genetics of dispersal

Where genes are not randomly distributed, the totalpopulation may be considered as a metapopulation di-vided into several subpopulations. To the extent thatthose dispersing differ from those remaining, dispersalmust influence such genetic variability. Although modernhumans represent a single biological species, they cannotbe considered a single interbreeding population. Ratherhumans comprise ‘‘an array of locally interconnectedpopulations (demes) whose social relations with ourneighbors include an exchange of mates’’ (Weiss, 1988).Genes can move between populations either by theexpansion of one group into the territory of another orby the exchange of mates between groups. The termdemic diffusion has been used to refer to a mixture ofthese processes (Wijsman and Cavalli-Sforza, 1984).

Random migration promotes genetic homogeneity ofpopulations, whereas selective migration promotes ormaintains differences between populations (Mascie-Taylor and Lasker, 1988). Colonization may induce foun-der effects and increase genetic variability, especiallythrough reaching ‘‘islands’’ of difficult access (Neel andSalzano, 1967). Likewise, differential extinction mayresult in genetic bottlenecks through which few variantspass. Genetic variability is further favored by any tend-ency for groups of kin to disperse. However, inter-breeding preserves gene flow between populations andcounterbalances these effects.

The hominin pattern of dispersal likewise influencesthe capacity for genetic adaptation to occur. If adults dis-perse, they are adapted to the old rather than the newenvironment, whereas the offspring encounters the newenvironment from early in the life course. Such a scenariofavors two types of phenotypic plasticity as an alternativemechanism for accommodating environmental stressesand stochasticity. In adults plasticity derives from behav-ior (altering the niche to fit physiology), whereas in theoffspring plasticity derives from physiological flexibilityduring ontogenesis (altering physiology to fit the niche).While plasticity appears to oppose genetic adaptation, theprocesses are in fact closely related.

Whether genetic variability is expressed or repressedis determined by the balance between two forces. Canali-zation maintains phenotypic stability in the face ofenvironmental change, and hence maintains genetic var-iation (even allowing mutations to accumulate) by buf-fering against selection. In this way, different genotypesare constrained to produce similar phenotype regardlessof environmental conditions (Flatt, 2005). In contrast,phenotypic plasticity refers to sensitivity of a single ge-notype to environmental variability, such that the samegenes allow the possibility of different phenotypesaccording to environmental conditions (Flatt, 2005).These processes influence each other, so that plasticity ofone trait may be associated with canalization of another.Equally, a canalized trait is less plastic.

Severe environmental stresses may cause ‘‘decanali-zation,’’ resulting in the emergence of new phenotypes(Rutherford and Lindquist, 1998). This concept may beof particular importance in considering the rapid emer-gence of new species. In general, canalization is pre-dicted to be favored where optimal phenotype is similaracross a range of environments; in contrast if optimalphenotype differs in relation to different environments,then plasticity is predicted to be favored (De Visseret al., 2003). The relative plasticity of an organism’s biol-ogy therefore provides information about the stability ofits evolutionary environment.

Dispersal and plasticity

Critical to plasticity is the concept that the environ-ment acts on the organism in two ways. First, the envi-ronment influences development and hence phenotype,while second, the environment comprises the selectivepressures to which the organism is the subject (Scheiner,1993). Some factors act both as cues in development andas selective agents, but necessarily operate during differ-ent time periods. The time lag between these influencesis a consequence of the inability of producing phenotypesinstantaneously (Moran, 1992). In general, dispersalcapacity is positively associated with plasticity, and colo-nizing species tend to show little local genetic differen-



tiation (Levin, 1988; Bazzaz, 1996). Models suggest thatthe greater the environmental heterogeneity, the lessaccurate plastic types need be to outcompete local spe-cialists (Sultan and Spencer, 2002). Nevertheless, plas-ticity becomes disadvantageous with longer time lagbetween initial cue and later selective pressure (Padillaand Adolph, 1996).

The benefits of plasticity comprise producing a betterphenotype in any given environment (Via et al., 1995),and in the absence of costs, plasticity would allow opti-mal phenotype in all environments (De Witt, 1998). Pen-alties may include maintenance and production costs,costs of acquiring information about environmentalstate, costs of unstable development imposed by environ-mental fluctuations, and adverse impacts on relatedgenetic traits (Relyea, 2002). Plasticity enables individu-als to accommodate changes in their natal environment,but also enables low-cost adaptation to a new environ-ment (Murren et al., 2001).

At the broadest level, the ability to migrate is itself aform of plasticity, and its success is significantlyincreased by complementary physiological plasticity. Ingeneral, physiological plasticity is greater during earlyontogenesis, implying that the process has greatest valueif the offspring encounters its new environment duringearly life. Older organisms with less physiological plas-ticity may be able to draw on behavioral options notavailable to young individuals, manipulating their envi-ronment to their advantage.

Information

Information enables organisms to evaluate their envi-ronments and adjust their development and behaviorappropriately (Dall et al., 2005). As discussed above, in-formation acquired during ontogenesis can guide physio-logical development. Information transmitted throughbehavior likewise provides a critical resource for reduc-ing environmental uncertainty (Dall et al., 2005). Inmany species, behavior is organized in the form ofinstinct and has little capacity for modification accordingto the state of the environment (Plotkin, 1994). In morecomplex organisms, however, the processing of informa-tion allows the accommodation of environmental unpre-dictability (Plotkin, 1994).

The processing of information, whether through plas-ticity or behavior, requires gene-based capacities toextract information from the environment and incorpo-rate them into guiding mechanisms conferring homeosta-sis or adaptation on the phenotype, and they are efficientat this process because they already contain some infor-mation about what requires processing or learning(Plotkin, 1994). Sophisticated information-processingrequires not only access to environmental cues or signalsbut also the capacity to assess the possible consequencesof pursuing alternative options (Dall et al., 2005).

Broadly, the information that programs behavior maybe acquired by organisms in three different ways (Avitaland Jablonka, 2000). Some behaviors may be innate, andrelatively impervious to experience. Some behaviors maybe learned through trial and error by an individual orga-nism during its lifetime; and some behaviors may besocially acquired from conspecifics. The relative impor-tance of these pathways is directly related to the stabil-ity of the environment. Innate behavior is valuable whenthe environment is relatively stable, and when there islittle benefit of, or time available for, learning. Trial and

error learning is favored when the experience of an indi-vidual organism is more useful than ancestral experi-ence. Social learning is favored when an individual orga-nism is unlikely to acquire appropriate informationthrough its own experience and can instead benefit fromthe experience of conspecifics. This is particularly sowhen the rate of environmental change precludes suffi-cient time or opportunity to gain appropriate experience.

Transgenerational plasticity and learning

Biological mechanisms for nongenetic transgenera-tional heritability include hormonal and immunologicalprogramming, epigenetic inheritance, and behavior.While heritability confers a degree of stability, thesemechanisms also offer increased flexibility compared togenomic transmission due to their capacity to respondfaster to environmental variability.

The transgenerational transmission of phenotype viahormonal programming is well illustrated by the effect oflitter placement of females on the phenotype of their off-spring in gerbils (Clark et al., 1993). Immunological pro-gramming is a similar transgenerational mechanism,whereby the transmission of antibodies in breast-milk isinfluenced by maternal exposure to pathogens, hence pre-paring the offspring for likely disease experience (Avitaland Jablonka, 2000). Epigenetic inheritance refers toalterations in gene chromatin structure by mechanismsthat do not involve mutation of DNA, such as methylationstatus. These changes can result in heritable variabilityin gene function without alterations to the DNA itself(Cooney et al., 2002; Waterland and Jirtle, 2003).

Behavior produces transgenerational transmissionthrough the mechanisms of social learning and culturalevolution. Studies of mice for example illustrate how off-spring learn their mother’s diet through accompanyingher on foraging trips and consuming her faeces (Avitaland Jablonka, 2000). Such behavioral transmission isnow termed culture, which refers to socially transmittedbehavior patterns or products of animal activities. Im-portant differences between cultural and genetic trans-mission are first, that behaviors can only be transmittedif they are displayed (Avital and Jablonka, 2000), andsecond, that novel behaviors can be transmitted tofuture generations as soon as they emerge in any gener-ation. These characteristics increase the flexibility andspeed of cultural transmission, but at the cost of thepotential loss of any adaptive information that is notused every generation.

Acquiring information socially has many advantages.Unlike material resources, information does not becomedepleted through sharing, though it may be copied withpoor fidelity. Learnt information may also be generaliz-able to other contexts in the future, though it mayequally constrain the organism to a specific set of condi-tions. However, if all information were acquired throughsocial learning, the resulting knowledge might cease torelate to experience, and hence confer no fitness benefit(Richerson and Boyd, 2005). Other potential costsinclude the time and energy required (Avital andJablonka, 2000).

Regular entry into novel environments increases thepremium on the nongenetic transmission of information.Colonization mimics environmental instability, reducingthe ability of organisms directly to acquire sufficient in-formation about the environment. This is particularlythe case where offspring are born into a different



environment from that in which their parents matured.The social transfer of information, whether by program-ming, epigenetics, or cultural transmission, facilitatesrapid adaptation to new territory.

Niche construction

Niche construction refers to the way in which organ-isms influence, manufacture, and maintain their envi-ronment, thus manipulating the selective pressures towhich they are exposed (Laland et al., 2001; Odling-Smee et al., 2003). Through such ecosystem engineering(Jones et al., 1994, 1997), organisms construct not onlytheir own physical environment but also that of otherorganisms. In humans, niche construction is often ahighly intentional activity, and although the details varylocally, the tendency itself is universal.

In general, larger colonizing organisms retain moregeneralist biology, since with increasing generation time,genetic adaptation is too slow to accommodate ecologicalvariability. In the absence of specialized physiology,behavior takes on two functions in niche construction.First, behavior may act on the niche to make it moreamenable, and hence fit it to the organism, e.g., mamma-lian mothers buffering external energy perturbationsthrough lactation (Dall and Boyd, 2004). Second, throughbehavior organisms may converge on an optimum modeof exploiting the niche, and hence fit the organism to theniche.

Niche construction may be particularly important inhominin evolution due to the tendency of adults to dis-perse to new environments, a time in the life coursewhen physiological plasticity is reduced. Although manyspecies manipulate their niche through social or physicalmeans, humans clearly influence their ecological envi-ronment more than other species. This is most evidentin relatively recent behavior, however earlier homininslikewise constructed diverse niches using rudimentarytechnology and a scale of social cooperation not seen inother species.

Summary

In summary, this brief review of the biology of coloni-zation emphasizes a number of related features, includ-ing (a) the retention of a generalist anatomy and phy-siology and (b) the accommodation of environmentalvariability and uncertainty through physiological, behav-ioral, and technological plasticity. As will be described inmore detail in the last section of this paper, humans fitclosely with this broader pattern.

LIFE HISTORY AND DEMOGRAPHY

It is life cycles rather than organisms that evolve(Bonner, 1965). Life history theory addresses the strat-egies pursued by organisms as they harvest energy fromthe environment and invest it in various vital functions(Hill and Hurtado, 1996), and is essential for under-standing how a colonizing capability has emerged. Thecapacity of Homo to colonize and experience rapid popu-lation growth emerged from broader demographic flexi-bility, allowing population size and structure to accom-modate ecological fluctuations.

Human demography

Relative to mammals in general, humans have largesize, a long period of growth, and a long interbirth inter-val (Promislow and Harvey, 1990). Relative to otherapes, humans likewise live longer, breed later, and de-velop more slowly during childhood (Hill and Hurtado,1996; Bogin, 2001). However, the paradox is thathumans breed more rapidly than contemporary ape spe-cies. Average interbirth interval is around 5 years inchimpanzees (Goodall, 1983; Nishida et al., 1990) and7 years in orangutans (Galdikas and Wood, 1990), butaround 3–4 years in foraging human populations(Howell, 1979; Blurton Jones et al., 1992) and as low as2 in farming populations. Adult ape mortality rateappears to be an order of magnitude greater than that inforaging human populations (Goodall, 1986), though ju-venile mortality is more similar between species (Table 1).Contemporary humans therefore live for longer andbreed for longer than other ape species, and yet havehigher fertility rates and similar or higher offspring sur-vival rates.

Population size in hominin evolution

Contemporary positive population growth rates arenot thought to be characteristic of the majority of homi-nin evolution. Rather, the reproductive strategy of Homomay be considered to have evolved under a set of con-straints, and to have recently been released from themby encountering new circumstances. By convention, theglobal population of humans is generally assumed tohave shown negligible long-term growth throughout thevast majority of hominin evolution, and then to haveescalated from the Neolithic, and especially rapidly fromthe 16th century onward. The extraordinary shift in av-erage population growth rates is illustrated by thechange in estimated doubling time from 8,000 to 9,000years prior to the Neolithic to 40 years since 1950, suchthat over the last 10,000 years the human populationhas multiplied by a factor of �1000 (Livi-Bacci, 1992).

Ignoring short-term fluxes, these population sizesequate to a long-term growth rate of \0.001% per yearduring the paleolithic (Polgar, 1972; Hassan, 1973). Aver-age growth rate is estimated to have risen to 0.1% dur-ing the early period of food production (Carneiro andHilse, 1966; Hassan, 1973), albeit with probable markedfluctuations over shorter time periods. The nature of ex-ponential growth is such that even relatively low growth(1%–2% per year) induces population increases of ordersof magnitude within a few centuries. For example, Hilland Hurtado (1996) calculated that at the 2.5% per yeargrowth observed in 20th century Ache, a population of20 individuals would increase to 3.9 3 1055 people in5,000 years.

It is clear that the current distribution of humans overthe majority of the Earth’s surface is itself no explana-tion for the characteristics of human reproductive strat-egy, since such a distribution could have occurred over ashort period of time at very low rates of populationgrowth. Rapid human population growth in recent mil-lennia is therefore a product of a particular reproductivestrategy in a particularly favorable environment.

Fertility rate and ecological conditions

In recent decades, anthropologists have developed anumber of optimal foraging models intended to generate



and test hypotheses concerning how best to captureresources from the environment (Belovsky, 1988; Kelly,1995; Winterhalder et al., 1998). Such models have pro-ven useful in a variety of circumstances, but perhaps themost important conclusion is that no single model canexplain the diversity of foraging behavior across a rangeof ecological conditions (Kelly, 1995). As illustrated bycontemporary foragers, a key strategy for accommodat-ing ecological stress is mobility. Such mobility, inresponse to climate trends and fluctuations in resourceavailability, would alter the selective pressures impact-ing on populations, and favor plasticity over specializa-tion. However, even modest changes in population sizeand structure will influence foraging returns with anygiven territorial range (Kelly, 1995); hence homininbehavior may itself have contributed to such pressuresand favored mobility. The relative importance of ecologi-cal stresses versus hominine behavior remains unknownfor the majority of Homo evolution, but in contemporarypopulations some studies demonstrate population sizeplateauing in relation to resource availability (Attenbor-ough, 2002).

Ecological conditions impact on fertility rate at a num-ber of different levels. First, physiological mechanismsconnect the age of menarche and the probability of con-ception with energy availability and flux (Slyper, 1998;Ellison, 2001). Second, lactation is well established as acritical determinant of the probability of conception(Short, 1984), with its duration explaining the majorityof variability in total fertility rates between populations(Campbell and Wood, 1988). Third, these mechanismsare further influenced by a variety of social factors.Unlike other apes, humans ‘‘stack’’ their offspring, con-tinuing to provision one postweaning while gestating orbreast-feeding the next (Robson et al., 2006). Alloparent-ing has been identified as critical for this strategy, andrapid rates of reproduction typically require high levelsof alloparental investment (Hrdy, 2005). Without suchcooperation, the high cost of reproductions act as a con-straint on female fertility. The effect of energy availabil-ity on female fertility is illustrated by differences in totalfertility rate between the !Kung, Hadza, and Ache (Hrdy,1999), and both alloparenting and technological develop-ments impact on the interbirth interval (Hassan, 1981;Bogin, 2001; Sellen, 2006).

At some point, hominin interbirth interval appears tohave decreased relative to that of apes, possibly with theemergence of Homo erectus (Aiello and Key, 2002). How-

ever, comparison of contemporary foraging, horticultural-ist, and agricultural societies indicates broad similaritiesin fertility rates, though with a tendency for the highestrates in intensive agriculturalists (Campbell and Wood,1988; Hewlett, 1991; Bentley et al., 1993). Substantialchanges in fertility rates are thus unrealistic as the pri-mary driver of population dynamics.

Mortality

Mortality patterns play a key role in population dynam-ics, by determining the likelihood of those born breeding,and the duration of adult reproductive careers. The sim-plest explanation for the long-term stability of homininpopulations despite short interbirth intervals and longreproductive careers is that high fertility was balanced byjuvenile and adult mortality. Data on juvenile mortalityfrom a variety of primate species are illustrated in Table1. The species listed include other apes from a variety ofenvironments, and baboons who occupy a savannah nichesimilar to that in which much hominin evolutionoccurred. Juvenile mortality is high in all species, thoughalso variable in relation to ecological conditions.

Greater adult mortality rates in humans compared tononhuman primates is implausible as the only factorcounterbalancing high fertility, since reduced adult mor-tality is directly implicated in the lengthening of thehuman lifespan compared to the primate species(Hawkes, 2006b). Any counterbalancing would thereforehave to incorporate a strong influence of juvenile mortal-ity. In traditional societies, only around 50% of live bornoffspring survive to adulthood (Lancaster and Lancaster,1983). Figure 1 illustrates total fertility rates in 40 for-aging societies. The median is 5.4 offspring, and if theanalysis is restricted to populations from tropical/sub-tropical forests, the median is a similar 5.2 (Kelly, 1995).Figure 2 illustrates mortality rates for individuals aged\15 years in 22 foraging societies. The median is 42.5%mortality, and given that females in foraging populationsrarely reproduce until in their twenties, around 50% pre-adult mortality is not implausible. Combining these me-dian fertility and mortality rates still allows for popula-tion growth, but this would be lost if precontemporarypopulations had slightly longer interbirth intervals and/or slightly higher adult mortality rates. A contribution offemale adult mortality is also plausible on account ofstrong selective pressures on female reproductive ener-getics (see below).

TABLE 1. Key life history variables in baboons, great apes, and humans

Species LocationObservationperiod (yr)

Age at1st birth

(yrs)

Interbirthinterval

(yr)

Juvenilemortality

(%)

Mortalityin 1st year

(%) Reference

Chacma baboon Botswana 10 6.75 2.0 61 38 Cheney et al., 2004Mountain baboon South Africa 2 – 3.2 – 7 Lycett et al., 1998Hamadryas baboon Ethiopia 5.5 6.1 2.0 36 (5 yrs) 24 Sigg et al., 1982Olive baboon Kenya 4 – 2.1 48.7 (2 yrs) 22 Smuts and Nicolson, 1989Orangutan Sumatra 32 15.4 9.3 33 (11 yrs) 6.9 Wich et al., 2004Mountain gorilla Rwanda 24 10 3.9 34 (4 yrs) 26.2 Watts, 1991Bonobo Congo 20 15 4.8 27.3 (6 yrs) 4.5 Furuichi et al., 1998Chimpanzee Tanzania 15 14.5 5.5 38.2 (5 yrs) 27.3 Goodall, 1983, 1986

Tanzania 22 14.6 6 53 28 Nishida et al., 1990Human* Foragers 20th century 19.6 11 37.0 (15 yrs) 20.3 Kelly, 1995

Juvenile mortality assessed over varying proportions of the juvenile period, noted in years (yrs).All species based on one sample, except humans where data were derived from 22 populations.*Sample size for human data 9 for age at first birth, 11 for interbirth interval, 20 for mortality to 15 years, and 14 for mortality infirst year.



Although contemporary populations use a number ofcultural methods to constrain fertility, infanticide is theonly such method likely to have made a major contribu-tion to hominin demography. Studies of foragers suggestthat earlier estimates over-emphasized the level of infan-ticide (Kelly, 1995); however, among recent or contempo-rary populations, infanticide has been used at a low levelto manipulate the sex ratio and to optimize birth spacing(Morales, 1987; Hewlett, 1991). It may likewise havecontributed to marginally higher infant/juvenile mortal-ity rates in the past, particularly in times of resourcescarcity.

The negligible population growth prior to the currentmillennium described above is very much an estimationwith wide confidence intervals, and an apparent lineartrend may conceal significant short-term fluctuations.Until recently, archeologists emphasized a ‘‘wave ofadvance’’ model of population movement and expansion,implying the steady occupation of, or diffusion into, adja-cent territory (Boserup, 1965). More recent analyses sug-gest that, although cultural diffusion may have operatedin such fashion (Shennan, 2002), population expansionitself may have had very different dynamics. Four plausi-ble scenarios for the evolution of human demographyhave been presented (Shennan, 2002). The conventionalview assumes high stability, with a recent marked popu-lation increase. Other possibilities, within this same over-all pattern, are constant, increasing or decreasing sto-chastic variability over time. The most likely scenariocomprises fluctuations in global population decreasingover time in relation to the aggregate of many specificpopulations. Thus small discrete populations distributedin few regions across a mosaic of habitats would be sub-ject to considerable impact of local population crashes inresponse to climatic stresses such as glaciations. There istherefore no reason why high population growth ratesmay not have occurred regularly in the past, even if long-term average growth was negligible (Boone, 2002).

Demographic stochasticity

Regular population fluctuations might arise for a num-ber of reasons, including climate-induced ecologicalchange, predation, disease, famine, and conspecific vio-

lence. Each of these might induce local extinction andtherefore merits consideration.

Hominins evolved in and adapted to unstable niches.Climatic trends, inducing ecological shifts and trans-forming foraging returns, must inevitably have acted ondemography through influencing both fertility and mor-tality patterns. Thus, the simplest model of demographicstochasticity would consider hominins to have occupiedsuitable territory when available, and to have retreatedwhen subsistence became untenable. These pressuresare still, in very broad terms, a consequence of homininbehavior, through the probing of and dispersing intosuch unstable environments.

In recent millennia, the movement of diseases betweenpreviously isolated populations has often exerted devas-tating demographic effects. For example, native SouthAmerican populations were decimated in the 16th cen-tury by diseases brought in by colonizing Europeans(Livi-Bacci, 1992; Diamond, 1998). Notably, the Acherecovered their population size less than 20 years afteralmost half of them died (Hill and Hurtado, 1996), a phe-nomenon also reported in other populations (Thorntonet al., 1991). This clearly illustrates the capacity ofhuman populations to ‘‘bounce back’’ from significantcrashes. However, the relevance of such diseases for pre-agricultural populations is probably limited, given thatmany modern infectious diseases followed animal domes-tication (Diamond, 1998).

Data from populations such as the !Kung and Achedemonstrate that predation is a significant source ofmortality, but less so than homicide or disease (Hill andHurtado, 1996). Hominins were relatively large animalsand would have had few predators, particularly afterdeveloping the control of fire. Their sociality would alsohave discouraged predation. An intriguing possibility isthat predator–prey cycles may have induced fluctuationsin contexts where humans were the predator, ratherthan the prey. Such a hypothesis clearly depends ona major role of hunting in subsistence, and might berelevant to specific periods of human evolutionary his-tory. Hunting has been proposed as a convergent nicheallowing colonization of new habitats without the needfor physiological specialization to local vegetable foods(Foley, 2001). Furthermore, there is considerable evi-

Fig. 1. Total fertility rate in 40 foraging societies. Based ondata from Kelly (1995).

Fig. 2. Mortality rate up to 15 years in those live-born in 22foraging societies. Based on data from Kelly (1995).



dence from recent human prehistory of over-hunting onmost continents (Stuart, 1991; Klein, 1992; Steadman,1995; Diamond, 1998). Thus, once large scale huntingbecame common, humans may have inflicted demo-graphic cycles on themselves through over-exploitationof particular prey species.

More generally, fluctuations in energy supply per seare a plausible cause of population crashes. Data fromcontemporary nonindustrialized populations demonstrateregular food shortages, of sufficient severity to contributeto mortality. In addition to over-hunting, the archeologi-cal record shows numerous examples of over-exploitationof resources, including shellfish. Recent research sug-gests that resource over-use led to social collapse onEaster Island over a remarkably short time period (Huntand Lipo, 2006), and archeologists now consider this sce-nario relevant to the collapse of recent civilizations (Mor-rison, 2006).

In small-scale societies, conspecific violence is an im-portant cause of mortality, and the ethnographic recorddemonstrates the extinction of social groups due tosmall-scale warfare. For example, of 28 societies fromNew Guinea, 25 (89%) were reported to have experi-enced either group extinction or forced migration (Soltiset al., 1995). However, it is difficult to extrapolate fromsuch data to earlier periods of human evolution, whenhumans were colonizing unpopulated territory, and incontemporary societies there is no close correlationbetween population density and the likelihood of warfare(Guilane and Zammit, 2005).

Niche construction and population dynamics

While the above factors may have imposed stochastic-ity on hominin demography, we suggest that active nicheconstruction may have made an increasingly importantcontribution. Characteristics aiding survival during eco-logical instability will overlap with those favoring theprobing of new territory and novel niches. In this way,hominin strategies must increasingly have contributedto the selective pressures acting back on them. Entryinto novel niches, initially characterized by plentiful newresources, would allow increased population growth;however over-exploitation of these resources could leadto either renewed impetus to colonize new environmentsor it would bring about a population crash. Furthermore,any association between opportunistic niche appropria-tion and overexploitation would increase vulnerability toclimatic variation.

The archeological record is replete with examples ofrecent populations over-exploiting local resources; thisprocess results in a steady decrease in the quality ofresources available (Shennan, 2002). The notion thatnonindustrialized populations are better at maintainingthe sustainability of their resource bases has been chal-lenged (Alvard, 1995, 1998), while archeologists havealso found the concept of population crashes useful inaccounting for the apparent fluctuating occupation, orabandonment, of specific sites over centuries or millenia(Matson et al., 1988; Jones et al., 1999). Trade networksbetween populations emerged in response to differentialaccess to key resources, and trade has been considered arecently-evolved counterbalance to local overexploitation(Shennan, 2002).

The relative importance of climatic trends versus hom-inin behavioral strategy as selective pressures favoringthe traits that permit colonization remains unclear and

is an important topic for further research. We suggest atrend of positive feedback, such that initially tentativecolonizing aided by climatic variability led to more proac-tive colonizing. Whatever be the cause of population sto-chasticity, it would have favored increasing r-selection ofhominin reproductive strategy.

Colonizing through agriculture

The combination of 41 year interbirth intervals, highjuvenile mortality, and population cycles is likely to havebeen the norm for the vast majority of hominin evolution,offering little opportunity for any systematic global popu-lation growth. Agriculture represents a new niche inhominin evolution with substantially increased productiv-ity from a given area of land. There is considerable evi-dence to suggest that agriculture initially increasedrather than resolved nutritional stress (Cohen and Arme-lagos, 1984; Larsen, 2002), and only became viable infavorable climatic conditions that appeared in the Holo-cene (Richerson et al., 2001). However, as it developed itappears to have stimulated fertility rate by decreasingthe interbirth interval while also increasing the motiva-tion to produce offspring, since intensive agriculturefavors increased family size (Hassan, 1981). Thus, ratherthan stemming from systematic population growth(Boserup, 1965), agriculture appears to have both enabledit and stimulated it.

From this perspective, agriculture represents a nicheripe for colonizing in the same way that new territorycan be exploited. Populations expose themselves to eco-logical stresses not by entering a new habitat, but byaltering their subsistence strategy. Despite short-termpopulation crashes arising from regular famines and ter-ritorial conflicts associated with access to land, the nicheof food production has been associated with an extraordi-nary global population increase, with an estimatedfivefold increase in global population by the end of theNeolithic (Hassan, 1981). According to more recent fig-ures, swidden agriculturalists in New Guinea wereobserved to have a population density of 288 persons persquare kilometer in 1972 (Sahlins, 1972). Although theNile valley in upper Egypt had an estimated 0.11–0.27persons per square kilometer in the paleolithic (Hassan,1973), the density in 1960 was 755 persons per squarekilometer (Hassan, 1981).

Figure 3 illustrates two proposed shifts in populationdynamics, deriving from changes in both mortality andfertility (Deevey, 1960). The first of these shifts occurredwith the origins of agriculture. A second shift occurredwith the intensification and industrialization of agricul-ture that resulted from the industrial revolution. Rapidpopulation increases in modernizing countries are cur-rently sustained by the ‘‘green revolution’’ that, in theshort term, boosts productivity.

Summary

The human capacity to colonize has emerged fromassumed ancestral life history patterns through changesin the typical birth interval, in the duration of femalereproductive careers, and the age-pattern of mortality.These changes are associated with an extended period ofoffspring growth and development, which in turn hasimpacted on the requirements for maternal care. Evi-dence from different sources implicates the emergence ofthe genus Homo as particularly important in this devel-



opment; however, further work is required to addressthis evolutionary history in greater detail and to eluci-date how important human behavior itself may havebeen as a selective pressure favoring a generic colonizingreproductive strategy.

THE BIOLOGY OF HUMAN DISPERSAL

This section considers in greater detail the role of spe-cific components of hominin and human biology in thecapacity to colonize. Although Hill and Hurtdado’s (1996)description of humans as ‘‘colonizing apes’’ derived fromtheir focus on fertility rates, this section addresses manybroader aspects of human anatomy, physiology, andbehavior. For each trait, evidence on primates, homininsand humans is evaluated where available, (a) to test thehypothesis that hominins and humans have an enhancedcolonizing capability compared to nonhuman apes, and(b) to identify likely selective pressures favoring thiscapability.

Speciation

Nonhuman apes have traditionally been considered tobe the chimpanzee, gorilla and orangutan, and gibbons;however, recent molecular research indicates greaterspeciation, with two species each of chimpanzee, gorillaand orangutan (Butynski, 2001; Warren et al., 2001;Won and Hey, 2004) along with further proposed subspe-cies of chimpanzee and gorilla. Such speciation indicatesboth adaptation to local conditions and geographical iso-lation, and the accommodation of environmental stressesby genomic change as opposed to plasticity.

Early hominins show consistency with this pattern,with considerable evidence of environmental change as asignificant factor contributing to speciation (Vrba, 1988;Foley, 1994). Pliocene environments in the African riftvalley system included both forest and savanna until�2.5 MYA; however, a drying trend produced highly vari-able habitats from 2.3 to 1.8 MYA, at which point therewas a major shift toward grassland ecology by 1.5 MYA(Potts, 1998a). The shifting mosaic of habitats in centraland eastern Africa is considered to have favored evolu-tionary novelty (Foley, 1987; Potts, 1998a,b) and contrib-

uted to extinctions (Foley, 1994), adaptive radiation, andspeciation (Wood, 1992; Potts, 1998a; Bobe and Behrens-meyer, 2004). Successful Pliocene hominins appear tohave been species, such as Australopithecus afarensis,who could successfully exploit resources across a numberof biomes (Potts, 1998a; Bonnefille et al., 2004).

Selective pressures resulting from such rapid ecologi-cal change can pre-empt rapid genetic evolution in smallpopulations, through decanalization of traits that previ-ously resisted change (Flatt, 2005). Thus, the increasingphenotypic variability observed in the late Pliocene maybe seen as related to environmental instability anddiversification (Potts, 1998a). This process may havebeen particularly important in the evolution of earlyHomo (2.4–2.2 MYA) and Homo erectus (2.0–1.8 MYA),as these periods are associated with faunal turnover andecological heterogeneity (Bobe and Behrensmeyer, 2004).While Homo erectus is notoriously considered ‘‘the fossilwithout ancestors’’ (Walker and Shipman, 1996), itsseemingly rapid development in response to new selec-tive pressures might be due to the release of previouslyaccumulated genetic variability for phenotypic expres-sion in a new environment.

While environmental variation appears to be stronglycorrelated with speciation in the hominin fossil record, theincreased hominin diversity that resulted may have fur-ther influenced selective environments. Homo erectus mayhave invoked selective pressures by probing the emergingsavannah niche, since rapid evolutionary change canoccur under the influence of behavioral changes [the Bald-win effect (Baldwin, 1909), now considered a component ofniche construction (Odling-Smee et al., 2003)]. While therelative importance of niche construction to Early Pleisto-cene radiations is for the time being speculative, it clearlyplayed an important role in modern human dispersals andthe colonization of higher latitudes.

At present, there is little evidence for correspondencebetween modern human origins and climatic fluctua-tions; however, the dispersal (Mellars, 2006a) of tropi-cally adapted (Holliday, 1997) modern humans intoEurope suggests that behavioral flexibility (Mellars,2004) may have been required. While behavior will bediscussed in greater detail later, the main contrast hereis that the speciation of anatomically modern humansdoes not appear to correspond directly with their disper-sal, as it did with Homo erectus. This in turn impliesgreater buffering of the later Homo genome by a varietyof levels of plasticity.

Bipedalism

The fossil evidence increasingly indicates that bipedal-ism was not a characteristic exclusive to the human an-cestral line, but a locomotor capacity related to a numberof morphological characteristics found amongst someground dwelling apes from at least 4.4 to as much as7 million years ago. Early proposed hominin speciesSahalanthropus tchadensis (Brunet et al., 2002), Orrorintugenensis (Senut et al., 2001), and Ardipithecus ramidus(White et al., 1994) show changes in locomotor anatomyin the absence of significant expansion of the brain, acharacteristic of subsequent Australopithecines. The loca-tion of the Sahalanthropus tchadensis discovery, 2,500km west of the Rift Valley (Brunet et al., 2002), suggeststhat either (a) hominin origins may have taken place out-side of the east Africa or (b) early hominins dispersedquite widely, perhaps as a consequence of bipedalism.

Fig. 3. Long-term trends in human population size. Thedata are presented on a logarithmic scale and emphasize theeffect of major shifts in subsistence strategy on populationgrowth rate. Adapted and redrawn from Deevey (1960).



The diversity of bipedal species in the Pliocene suggeststhat bipedal locomotion helped hominin species to exploitthe diversity of environments in sub-Saharan Africa thatwere occurring as a result of climatic fluctuations and atrend toward more xeric environments through the Plio-cene (Potts, 1998a). Species adapting more successfully tovariable and open savannah habitats developed more effi-cient bipedalism, incorporating adaptation to heat stress,and resolving the need for greater energy efficiency inoccupying larger home ranges.

While a diverse range of bipedal hominins are knownfrom the late Pliocene and early Pleistocene, there arekey morphological differences in bipedal morphologybetween australopithecines and Homo erectus. Australo-pithecus afarensis has a broad thorax and pelvis, consid-erably smaller acetabulum, relatively robust humeri andshort femora. While primitive features have been notedfor australopithecine and Homo habilis feet (Clarke andTobias, 1995; Kidd et al., 1996), what is perhaps mostrelevant is the accumulated evidence for a range ofbipedal adaptations amongst Pliocene hominin species(Harcourt-Smith and Aiello, 2004). Although there areno well preserved and clearly taxonomically identifiedHomo erectus feet, the 1.85 MYA KNM-ER 813 talusappears to be quite human-like (McHenry and Coffing,2000). The transition from a diversity of bipedal homi-nins with varying locomotor adaptations within the Plio-cene to one remaining lineage (Homo erectus) in thePleistocene suggests that this was the first to arrive athighly efficient locomotion for a biped. While the dramat-ically different body size and physique of Homo erectushas been interpreted in this context (Jungers, 1988;Wood and Collard, 1999b), the capacity for efficient en-durance running may have also been a part of this mor-phological package (Bramble and Lieberman, 2004). Fur-thermore, changes in inner ear anatomy shown in fossilsof Homo erectus imply the development of improved bal-ance (Spoor et al., 1994).

The fossil evidence suggests that bipedalism was ageneralized trait that facilitated hominin entry intodiverse environments associated with increasing envi-ronmental variability. In this context, bipedalism is thefoundation of the hominin adaptive radiation. It is diffi-cult at present to link it specifically to any large scaledispersals of particular hominin species in the Pliocene.However, the emergence of the genus Homo clearly rep-resents a morphological grade shift. As such, it can beseen as a fundamental component of colonizing adapta-tion, as it is associated with the emergence of an ener-getically efficient, obligate biped capable of considerableendurance and home range. It remains worth notingthat associated improvements in manual dexterity are acorrelate of encephalization and central to the evolutionof hominin behavioral strategies, which include unparal-leled niche construction.

Size and physique

Body size correlates with numerous physiological,energetic, behavioral, and life history traits, and repre-sents one of the most fundamental biological characteris-tics of a species. Greater body size can only be realizedthrough faster growth or the extension of the growth pe-riod, and requires either increased energy availabilityfor the former, or a reduced risk of preadult mortality.The benefits of body size include improved thermoregula-tory capacity and increased competitiveness, and greater

energetic and reproductive efficiency. Larger femalesaccommodate the energy demands of their offspringmore successfully, and it is notable that sexual dimor-phism decreased in Homo erectus due to a substantialincrease in female size (Aiello and Key, 2002). However,the increase in body size and brain size is associatedwith compensations elsewhere. For example, humanmuscle mass is reduced compared to that of other apespecies (Leonard et al., 2003), while trade-offs betweenorgans has also occurred (Aiello and Wheeler, 1995).

Both stature and body mass have shown systematicchange during hominin evolution. This trend emergedfrom a relatively modest baseline, with australopithecinesconsidered to have been similar in size to contemporarychimpanzees but smaller than orangutans and gorillas(McHenry and Coffing, 2000). While body breadth hasbeen relatively constant throughout hominin evolutionin the tropical latitudes (Ruff, 1991), there were majorchanges in stature and body mass. Despite the adaptiveradiation of bipedal hominins in the Pliocene, the cur-rent evidence for stature and body mass amongst thesespecies suggests relative homogeneity, with staturesranging from �130 to 150 cm, and body mass estimatesfrom 29 to 50 kg (McHenry and Coffing, 2000). By 1.6MYA, the most complete Homo erectus skeleton demon-strates a marked increase in both stature and body mass(Ruff and Walker, 1993), comparable to modern humans.There is evidence for such large bodied hominins asearly as 1.95 MYA, yet these remains are of uncertaintaxonomic status (Wood and Collard, 1999a; McHenryand Coffing, 2000). The available evidence suggeststhere was a major shift in body size with Homo erectus,and possibly Homo rudolphensis. While there is evidenceto suggest that this increase in body size led to a greaterhome range and capacity for dispersal in Home erectus(Anton et al., 2002), the small body size of some of theremains from Dmanisi fall within the range of somemodern human hunter-gatherers, and their derived mor-phology appears to be well adapted to long-distance loco-motion (Lordkipanidze et al., 2007). The intercontinentaldispersals of Miocene apes demonstrate that larger bodysize was not necessary for major migrations within eco-logical zones. The broad range of mosaic grassland envi-ronments may have also contributed to dispersals at thistime (Dennell, 2003).

Contemporary humans and hominins show significantvariability in size and physique, some of which corre-sponds with adaptations to climate (Ruff, 1994, 2002).Much of this variation has been assumed to be geneticand to reflect local physical environmental factors suchas heat stress (Roberts, 1953; Katzmarzyk and Leonard,1998). However, the effect of thermal load on growth hasbeen proposed to commence in utero, when growth rateis more plastic (Wells and Cole, 2002). More generally, aconvergence of evidence from different fields suggeststhat plasticity in body size can occur on intergenera-tional scales, in response to factors such as resourceavailability and patterns of mortality (Bateson et al.,2004); see Plasticity in Growth and Metabolism sectionbelow. Although it is difficult to determine whether bodysize variability among fossil hominins reflects a range ofplasticity, this may have been an important componentof hominin adaptability with particular relevance toenergy requirements and environmental variability. Bymaintaining plasticity in size and physique, the homoge-neity of more fundamental physiology and anatomicalstructure is preserved.



The larger body size of Homo would have offered arange of benefits in the context of colonizing, includingdecreased risk of predation of adults, increased homerange and hence dietary range, and increased efficiencyin the energetics of reproduction. These benefits aid inthe exploitation of novel environments with minimalphysiological specialization.

Diet

Hominin evolution appears to have been characterizedby a series of increases in dietary quality. A complemen-tary trend comprises decreasing physiological specializa-tion, with dietary adaptability conferred instead bybehavior and technology. The combination of these strat-egies has conferred on humans the capacity to access awide variety of habitats while retaining a generalized di-etary physiology.

The ecology and diet of Miocene apes was dominatedby forested environments and frugivory, which havebeen argued to favor social and cognitive means of foodprocurement (Potts, 2004). Extant apes tend to eat‘‘what there is’’ (mostly vegetable material) and avoid ahigh degree of physiological and anatomical specializa-tion (Rodman, 2002). However, chimpanzees exhibit sig-nificant sex-differences in diet, with females consumingless animal meat than males, but greater quantities ofsocial insects (McGrew, 1992). Recent observations ofchimpanzees indicate that the use of sharpened sticks tohunt was primarily conducted by adult females, but alsoby juvenile males (Pruetz and Bertolani, 2007), whilefemale bonobos share food to a greater extent than males(Hohmann and Fruth, 1996). These traits may be anala-gous to the sex-differences in foraging strategy amongcontemporary humans, indicative of sex-differentialselective pressures.

Early hominin foraging likely remained broadly con-sistent with these strategies with the environmentalshift to more fragmented forests and open habitatsthrough the Miocene and Pliocene. Ardipithecus ramidusand subsequent australopithecines shared a dentitioncharacterized by moderate to small incisors, large molarswith relatively flat occlusal surfaces, and thick dentalenamel, suggesting a dietary shift near the stem of hom-inin evolution (Teaford and Ungar, 2000). Analyses ofAustralopithecine dental microwear suggest the con-sumption of contrasting hard/soft and abrasive/nonabra-sive material, consistent with a range of food seed andsoft fruit eating, which has been interpreted as an adap-tation to habitat diversity from gallery forest to savanna(Teaford and Ungar, 2000). This is supported by isotopicevidence for a greater consumption of C4 plants, or ani-mals that feed upon these, in australopithecine diets(Lee-Thorp and Sponheimer, 2006).

The trend toward a generalized diet continued in Homo,with increased quality considered important for accommo-dating the needs of larger brains (Leonard and Robertson,1994). A recent review of masticatory biomechanics, den-tal morphology, and microwear suggests that early Homo(habilis, rudolphensis) and Homo erectus were welladapted to at least periodic exploitation of a wide range ofresources in different environments (Ungar et al., 2006a).While evidence for meat consumption as early as 2.6 MYA(Dominguez-Rodrigo et al., 2005) cannot be linked toa particular species, microwear evidence for an increasein food toughness makes meat consumption probableamongst Homo erectus (Ungar et al., 2006b).

Exploiting the increase in herbivore numbers thatoccurred at this time is a plausible strategy for meetingincreased energy requirements (Anton et al., 2002).While chimpanzees hunt with relative frequency (Boeschand Boesch, 1989; Stanford, 1996), there is considerableevidence for increased consumption of meat in the genusHomo (Blumenshine et al., 1994; Bunn, 1994; Domin-guez-Rodrigo, 1997; Hoberg et al., 2001; Anton andSwisher, 2004). Since the composition of meat varies lessthan that of plant matter between ecosystems, huntinghas been proposed to allow convergence on a commonniche (Foley, 2001), a phenomenon indicated by theapparent reduction in hominin speciation in the earlyPleistocene with the adaptive success of Homo erectusand its occupation of an enormous geographical range.Isotopic evidence also provides further support fordietary specialization toward very high levels of meatconsumption amongst the Neanderthals (Richards,2000b; Lee-Thorp and Sponheimer, 2006), which is likelyto have been a central feature of their behavioral andmetabolic adaptations.

Nevertheless, hunting is not the only possible strategyfor buffering dietary physiology and allowing niche ho-mogeneity in diverse habitats. Conklin-Brittain et al.(2002) have proposed the exploitation of undergroundstorage organs (roots, tubers, rhizomes, and corms),which savannah baboons and geladas eat during leanperiods, as a key fallback food for early hominins. A dietrich in such matter has similar protein but substantiallyless fiber than the chimpanzee diet, and therefore couldhave allowed increases in energy intake (Conklin-Brittain et al., 2002). However, this strategy may havebeen constrained by limitations in tuber digestibility,with O’Connell et al. (2002) arguing that cooking wasrequired for their maximal exploitation. The practice ofcooking renders a wide variety of plant foods such astubers more edible (Wrangham and Conklin-Brittain,2003), and tubers have been proposed as a high qualityalternative to meat for Homo erectus (O’Connell et al.,1999). There is limited empirical support for these inter-pretations at present; however, the reduction in bodysize dimorphism that occurred with the emergence of H.erectus (Aiello and Key, 2002) suggests increased selec-tive pressures on female foraging activities.

Whatever the relative importance of meat versus plantproducts in the Homo diet, it is clear that behavioraland technological flexibility dominated over physiologicalspecialization (Leonard and Robertson, 1994; Milton,2002). The shift to a more versatile, generalized dietamong Pliocene hominins appears to have been height-ened in the early Pleistocene, and represented the mostversatile approach to subsistence yet found in the pri-mate or hominin lineages. It would allow for the exploi-tation of an unprecedented range of habitats, increasedhome range, and the potential to colonize new territo-ries. There are clear ecological differences between thepaleoenvironments at fossil bearing sites of Georgia,Java, and the East African and Levantine sites in theRift valley system (Anton and Swisher, 2004), whichdemonstrate that early Pleistocene dispersals necessi-tated considerable dietary flexibility.

In addition to accommodating greater adult energyrequirements, dietary adaptations were likely of particu-lar importance in early life. Human development departsfrom the general primate pattern whereby offspring areweaned directly to the adult diet. Instead, from mid-infancy through to childhood, humans uniquely require



specialized ‘‘supplementary’’ foods (Sellen, 2006), pro-vided either by the mother or other adults. Such foodsallow shortening of lactation, decreasing the interbirthinterval. Aiello and Key (2002) suggested that a decreasein the duration of lactation was a fundamental compo-nent of the evolution of Homo erectus, arguing that itsincreased brain size would have made lactation too ex-pensive to continue for a duration compatible with otherape species. Bogin (2001) concurs that a brief childhoodphase of growth may have emerged 2 MYA, and length-ened subsequently (see below).

The ‘‘releasing’’ of offspring energy demand from mater-nal physiological constraint has been further exacerbatedsince the origins of agriculture. First, crop agricultureprovides materials for cereal weaning foods (Hassan,1981). Second, pastoralism has provided alternative sour-ces of milk. In mammals in general, activity of theenzyme lactase is turned off during weaning (Avital andJablonka, 2000). However, with animal domestication,and the availability of milk beyond infancy, it benefits theoffspring to preserve activity of the lactase gene. In theminority of populations, which have practiced pastoral-ism over many generations, activity of the gene is main-tained throughout the life course, allowing ingestion ofmilk at all ages (Aoki, 1986; Durham, 1990).

Accompanying behavioral trends in dietary adaptation,differences in metabolic physiology must also haveoccurred. The switch from a diet based on complex carbo-hydrates to one containing substantial quantities of meatwould have required changes in insulin metabolism, tomaintain appropriate blood glucose concentrations (McMi-chael, 2001). Such metabolic versatility again allows con-vergence on a common physiological phenotype in a widevariety of nutritional settings. Although such convergenceinitially required moderate anatomical adaptation, in thegenus Homo this was achieved primarily through meta-bolic, behavioral, and technological adjustments. Dietarysex-differences also consolidated, indicative of selectivepressures on maternal reproductive strategies.

Growth rate

Growth may be considered from two perspectives, thegeneric shape of the human growth curve and within-individual plasticity therein. This section considers onlythe first of these perspectives, the second beingaddressed in Plasticity in Growth and Metabolism sec-tion below.

In many species, growth rate is fairly consistent acrossthe entire developmental period, and individuals simplygrow until they reach adult size and start breeding.Many social species interpose a slower growth periodbetween birth and adulthood (Bekoff and Byers, 1985;Bogin, 1994), and most primates are consistent with thispattern. Contemporary ape species show such extendedgrowth, with infant and juvenile periods. Humans dis-play a more complex version of growth-slowing, with dis-tinct infant, childhood, juvenile, and adolescent stages(Bogin, 2001). Humans are not unique in having growthspurts, but differ from other primates in delaying themin the growth process (Leigh, 1996). This patternextends the total growth period, and also alters the rela-tive rates at which different body components develop.

The human ontogenetic profile has been attributedpreviously to more than one underlying mechanism.Evolution occurs when ontogeny alters in timing (hetero-chrony) or incorporates new characters (Gould, 1977).

Gould proposed human growth to have been character-ized by a particular type of heterochrony, neoteny,whereby developmental rates are slowed and develop-mental stages found in juveniles of ancestral populationsbecome adult features. Others including McKinney andMcNamara (1991) and Vrba (1996) have argued thathypermorphosis, whereby growth phases are extended,accounts for the human growth pattern. Bogin (1999)has followed Shea (1989) in arguing that neither of theseprocesses alone can produce human adult size andshape. Additional genetic changes are likely to haveoccurred, and there is evidence that these have influ-enced the endocrine system (Bogin, 1999).

Such developmental changes can be attributed to theeffect of the relatively few genes controlling the rate ofdifferent developmental processes. These changes appearto be associated with the increase in brain volume. Rela-tive to the chimpanzee, human body growth is similarwhereas brain growth is markedly different. Apes ingeneral have a rapid rate of brain growth before birthbut a slow one afterward. In contrast, human braingrowth is rapid both before and after birth, such thatthe large human brain size relative to other apes canbe attributed primarily to postnatal growth patterns(Martin, 1983). This is achieved through a derived pat-tern of brain allometry and moderate extension of theduration of brain growth coupled with a decrease inearly postnatal somatic growth (Vinicius, 2005).

The strongest contrast between humans and otherapes comprises discrepancy in the significance of wean-ing. In apes, viable weaning requires eruption of the firstpermanent molar, allowing access to the adult diet(Bogin, 2006), while the offspring must also be capableof foraging. The duration of the interbirth intervals ofextant apes can be related to these variables; howeveralthough the first human molar erupts at about 6 yearsof age, and humans at this age are still incapable of for-aging for themselves, humans wean their offspring at 3–4 years in natural fertility societies (Bogin, 2006).Between the end of infancy and the beginning of juvenilegrowth, humans are therefore characterized by an un-usual childhood period in which the slow-growing off-spring is provisioned by adults but not through lactation,and not necessarily entirely by the mother. This reducesthe cost of childhood growth, allowing the high costs ofbrain growth to be met without adverse impact on thematernal energy budget or reproductive schedule (Bogin,2001). Hrdy (2005) has also emphasized humans as ‘‘co-operative breeders,’’ using investment from kin to subsi-dize offspring growth.

In contrast with apes, this pattern allows each humanmother to ‘‘stack’’ several offspring at the same time(Robson et al., 2006), breast-feeding one while still provi-sioning several that are older. When unconstrained byjuvenile mortality, the low-cost human growth pattern isparticularly suitable for rapid population growth, allow-ing either rapid recovery from population crashes, orrapid population expansion in new habitats. While thebenefits to maternal fitness are clear, this same growthpattern is also powerfully protective of offspring pheno-type, with the slow growth rate protecting the off-spring from severe physiological responses to ecologicalfluctuations.

Dental eruption and formation have been used asmarkers of the tempo of development among ancestralhominins (Smith, 1991; Bogin, 1999). Bogin suggests thatthe childhood period may have emerged around 2 MYA,



with the Homo genus, and then lengthened subsequently.Recent analyses of dental formation provide evidencethat both australopithecines and early Homo more closelyresemble apes (Dean et al., 2001; Moggi-Cecchi, 2001).While the modern pattern of growth was in place amonganatomically modern humans by 160 KYA (Smith et al.,2007), the question of when it arose remains controver-sial. Studies of anterior dentition have identified evidencefor both a rapid (Ramirez Rozzi and Bermudez de Castro,2004) and slow (Guatelli-Steinberg et al., 2005) rate ofdental development among Neanderthals. Recent analy-ses of Neanderthal molar crown and root formationsupport the interpretation that their development wassimilar to modern humans (Macchiarelli et al., 2006).While broader interpretation of these studies requires theassumption of a direct relationship among dental forma-tion, eruption, and somatic growth, they collectively sug-gest that the modern human growth pattern evolved afterthe increase in body size with Homo erectus but prior tothe large bodies and brains found among Neanderthals. Ifso, the unique pattern of life history developed within thetime interval of the greatest encephalization of the homi-nin lineage (Ruff et al., 1997), indicating a close relation-ship between these characteristics.

Human growth patterns are consistent with generalmodels relating growth rates to the risk of mortality, andwith primate patterns of slow growth rates. Humansnevertheless stand out for the extent to which growth isslowed, and for the ‘‘stacking’’ of multiple offspring,increasing the independence of growth from ecologicalstresses.

Adiposity

Adipose tissue, unique to vertebrates, provides a meansof accommodating imbalances in the intake and utiliza-tion of energy. Fat is a slow release fuel, appropriate forlonger term imbalances, whereas short-term energybursts are fuelled by glycogen (Pond, 1998). In mammals,metabolic flexibility is of particular importance in meet-ing the energy costs of lactation, substantially higherthan those of pregnancy (Clutton Brock et al., 1989;Pond, 1997). The literature contains frequent referencesto the role of fat in accommodating cycles of feast andfamine (Prentice et al., 1992; Chakravarthy and Booth,2004), yet this is insufficient as an explanation of theselective pressures favoring human fat stores.

The available evidence on adiposity in primates ispatchy, and derives primarily from captive animals.Nevertheless, many species demonstrate a capacity toaccumulate fat, indicative of its role in buffering uncer-tainty in energy supply (Dufour and Sauther, 2002).Reported body fat ranges include 8%–41% in lemurs (Pe-reira and Pond, 1995), 5%–16% in baboons (Rutenberget al., 1987), and 19%–44% in gorillas (Zihlman andMcFarland, 2000). An elegant study of orangutans in thewild demonstrated seasonal metabolism of fat stores dur-ing times of energy stress (Knott, 1998). Wheatley (1982)has estimated that such stores allow orangutans toaccommodate substantially longer periods of low energyintake than crab-eating macaques, which occupy thesame region but exploit a habitat with more predictableenergy supply. Primates therefore fit with the generalmammalian pattern of using energy stores to bufferunpredictability in energy intake; however in the wild,periodical seasonal energy stress and the need to main-tain mobility for predator avoidance tend to constrain

absolute body fat levels (Pond, 1997), with, e.g., 2% fatobserved in wild-living baboons (Altmann et al., 1993).

As reviewed by McFarland (1997) and Dufour andSauther (2002), primates also tend to show higher levelsof body fat in females relative to males. This sex differ-ence is likely to be most closely associated with theenergy costs of reproduction, but may also be related insome species to sexual selection in relation to cues of fit-ness (Pond, 1997). The study of orangutans showedgreater metabolism of ketones in females compared tomales, with the highest rate in a female that had both anursing infant and an accompanying older juvenile(Knott, 1998).

Humans show consistency with this general primatepattern, but appear to stand out in two respects. First,adult female humans have higher typical body fat con-tent than any nonaquatic mammal (Dufour and Sauther,2002; Wells, 2006a), and even in harsh conditions womentend to maintain �20% of body weight as fat (Lawrenceet al., 1987), while adult males tend likewise to havehigher body fat content than other species occupyingsimilar environments (Wells, 2006a). Second, humanneonates have unusually high levels of body fat com-pared to the small number of species with data available(Kuzawa, 1998). The extent to which humans genuinelydiffer from other ape species is uncertain, because of thelack of equivalent data. However, unlike humans, obser-vations of primate neonates suggest minimal body fatcontent at birth (Schultz, 1969). The life-course profile ofhuman body composition is shown in Figure 4.

Reconstructing the emergence of adiposity in homininsis not possible on the basis of direct evidence, since softtissue does not fossilize. An indirect approach highlightsthree plausible factors (Wells, 2006a), each favoringselection for energy stores.

First, energy stores are predicted to benefit both sexesin relation to stochastic variability in energy supply.Data from contemporary populations inhabiting highlyseasonal environments illustrates the capacity of bodyfat stores to buffer regular fluctuations in energy supply.For example annual body weight fluctuations of 6 kg aretypical in Gambian farmers (Prentice et al., 1992), withthe majority of this variability attributable to changes inadiposity (Lawrence et al., 1987). The australopithecineradiation exposed hominins to increasingly seasonalenvironments, characterized by longer dry seasons thanthose experienced by ancestral gorilla and chimpanzeepopulations (Foley, 1993). Body fat stores may haveaided adaptation to such conditions, along with otherstrategies such as dietary adaptations.

The dispersals of Homo erectus and sapiens fromAfrica, exposing populations to new environments andstresses, are likely to have further increased stochastic-ity in energy supply. Even adjacent territories may haveproblematic features only evident after arrival, whiledispersing over longer distances increases such risk.Many species rely on fat stores to fuel their migratoryjourneys (Dingle, 1996; Pond, 1998). Early hominins areunlikely to have regularly undertaken lengthy disper-sals, however with increasingly opportunistic foragingsuch as hypothesized for Homo erectus, fat stores mayhave become important for buffering periods of accom-modation to new territories, habitats, and dietary niches.The metabolic sensitivity of some contemporary popula-tions has been attributed to strong selective pressuresduring specific recent migrations (McMichael, 2001),though this remains controversial.



Second, the enhanced adiposity in reproducing femalesand neonates strongly implicates the impact of the largeHomo brain on reproductive energetics. The high andobligatory energy demands of brain tissue favor fatstores in the neonate to buffer uncertainty during theestablishment of lactation and the onset of weaning(Kuzawa, 1998). As a proportion of body weight, the con-tribution of the brain is greatest at birth (Stratz, 1909),accounting for almost 90% of basal metabolic energy uti-lization at this time compared with only 25% in adult-hood (Leonard and Robertson, 1992). Consistent withKuzawa’s hypothesis, malnourished human neonateshave been shown to metabolize fat stores efficiently(Kerr et al., 1978). Since the offspring’s fat stores mustbe acquired via maternal nutrition, selection is also pre-dicted to favor fat stores in adolescent and adult females.Although incomplete, the available evidence indicates asubstantially higher energy cost of the neonatal brain inhumans relative to other apes. Extending the approachof Dufour and Sauther (2002), Table 2 estimates therelationship between neonatal brain weight and bodycomposition in apes and humans. Although all speciesshow similar ratios of neonatal brain weight to bodyweight, humans have substantially higher brain weightin relation to nonbrain lean body mass. These greatercosts must ultimately be met by the mother. Greaterfemale fatness may also have been shaped by sexualselection (Pond, 1997). However, such pressures aremore likely to have acted on regional fat distribution,and its visibility to males, than the amount per se.

It has been proposed that the trajectory of braingrowth in Homo erectus was similar to that of Homo

sapiens (Leigh, 2006); however, this argument is basedon reanalysis of data originally claimed to refute suchsimilarity (Coqueugniot et al., 2004). Thus, it remainsunclear when the characteristic human fatness profileevolved, and whether patterns of growth and develop-ment are similar between Homo sapiens and erectus(Bogin, 1999). Nevertheless, the fact that Homo erectusdemonstrated both larger adult brain and an increasedcapacity to disperse, hence potentially encounteringgreater environmental uncertainty, favors the hypothesisof greater adiposity in both females and neonates emerg-ing in related fashion.

The third significant factor concerns the increasingtendency of Homo to influence its niche, and hence theselective pressures acting on it. Relevant aspects of suchniche construction may have included improved foragingreturns and the development of supplementary foods,but also greater exposure to over-exploitation of resour-ces. Mobility represents a key solution to energy uncer-tainty (Binford, 2001); however nomadic behavior mayimpose its own energy stress, and inevitably loses effi-cacy as population density rises (Kelly, 1995). Increasedefficiency in energy extraction may thus paradoxicallyhave increased the risk of population cycles, with fatstores both aiding the growth and buffering any subse-quent dietary energy stress.

With the emergence of agriculture, exposure to foodshortages and famine is assumed to have increasedrather than decreased (Cohen, 1990; Larsen, 2002; Beny-shek and Watson, 2006). The archeological record con-tains evidence of periodic growth interruptions amongearly agricultural populations (Starling and Stock,

Fig. 4. Ontogenetic profile of body composition in humans. (a) Relative fat mass (y-axis: fat mass adjusted for height) and (b)relative lean mass (y-axis: lean mass adjusted for height) are plotted against age. During childhood, the two sexes increasinglydiverge, with the male gaining lean mass rather than fat, and the female pursuing the opposite strategy. These differences can beattributed to the role of fat in reproductive energetics. [Compiled from figures in Wells, 2007. Sexual dimorphism in body composi-tion. Best Practice and Research: Clinical Endocrinology and Metabolism 21:415–430. Reprinted with permission from Elsevier.]

TABLE 2. Estimations of brain size relative to lean mass in neonatal apes

Body weight(g)

Brain weight(g) % Adipose fat

Nonbrainlean weight (g)

Brain/nonbrainlean weight

Orangutan 1,728 170.3 2 1,526 0.112Gorilla 2,110 227.0 2 1,845 0.123Chimpanzee 1,756 128.0 2 1,595 0.080Homo sapiens 3,300 384.0 16.6 2,432 0.158

Data on body and brain weight from Dufour and Sauther (2002). Assumptions for % adipose tissue based on descriptions of Shultz(1969) for apes, and data of Harrington et al. (2002) for humans.



2007), and recent genetic analyses reveal a global distri-bution of polymorphisms attributable to localized formsof energy stress (Kagawa et al., 2002). In addition toreproductive energetics, fat stores are critical forimmune function, and we suggest that the emergence ofagriculture may further have shaped the adiposity ofcontemporary humans through exposure to novel infec-tious diseases, many of which derived from newly domes-ticated animals before crossing the species barrier tohumans (Diamond, 1998). Recent research has empha-sized the energy costs of mounting an immune response(Demas et al., 1997; Lochmiller and Deerenberg, 2000;McDade, 2003), while the metabolic control of blood glu-cose has also been linked to the availability of substratesfor immune response (Fernandez-Real and Ricart, 1999).Infectious diseases account for high mortality in earlylife, and may have contributed in particular to selectionfor infant fatness.

The occupation of more variable environments by Aus-tralopithecines, followed by the tendency of Homo to col-onize new territory and probe new niches, is likely tohave contributed significantly to the unique profile of ad-iposity in our genus. Fat stores are an efficient source ofplasticity on the organism throughout the life course andrepresent a further dimension of maintaining a general-ized physiology across diverse environments.

Plasticity in growth and metabolism

Phenotypic plasticity is observed across a broad rangeof organisms (Bateson et al., 2004), and many componentsof human plasticity are clearly derived from a muchbroader baseline. In mammals, in general, the most plas-tic period comprises fetal life and infancy, when growth isprimarily under nutritional regulation. Such plasticityallows adaptation to nutritional supply, a proxy for eco-logical conditions. Primate studies indicate a powerfuleffect of energy supply on growth rate (Janson and vanSchaik, 1993; Johnson, 2002; Altmann and Alberts,2005), and also the capacity for catch-up if short-termnutritional insufficiency is resolved (Fleagle et al., 1975;Rutenberg and Coelho, 1988), though this may beachieved at a longer-term cost (Metcalfe and Monaghan,2001). In contrast, prolonged nutritional insufficiencyinduces long-term effects on size and metabolism, andlater growth is more strongly canalized (Tanner, 1963).Primate studies also highlight the importance of mater-nal biology in regulating such early growth, with forexample earlier weaning of offspring in good conditions(Lee et al., 1991; Bowman and Lee, 1995). To some extent,humans exhibit similar plasticity, but are also notable fordistributing it across an extended growth period, and alsolimiting the exposure of sensitive offspring to ecologicalperturbations in early life.

Human growth comprises three distinct components(fetal/infant, childhood, and adolescent periods) that areto some extent additive (Karlberg, 1989). Most attentionhas focused on the first of these periods, emphasizing howfetal/infant growth rate varies in relation to energy sup-ply (Wells, 2007). Associations between birth-weight andthermal environment (Wells and Cole, 2002) likewiseindicate adaptation to broader climatic conditions. Child-hood growth can also exhibit more minor fluctuations inrelation to ecological pressures such as climatic condi-tions (Weitz et al., 2004). Studies of exposure to chroniclow energy intake have demonstrated adaptability in me-tabolism, ergonomics, mechanical efficiency, and muscle

structure (Waterlow, 1999), illustrating the capacity tomaintain function across a range of ecological conditions.Equally, the 20th century showed a major secular trendin growth in industrialized populations (Cole, 2003), espe-cially during the first 2 years after birth, with girls inparticular reaching puberty and ceasing growth at sub-stantially earlier ages (Garn, 1987; Karlberg, 2002). In astudy of 22 small-scale nonindustrial societies, favorableconditions were associated with faster growth and earliermaturation (Walker et al., 2006). Through such plasticity,the pace of human life history can quicken when ecologi-cal constraints relax.

However, consistent with theoretical models, the samestudies of small-scale societies showed that higher juve-nile mortality risk was likewise associated with fastermaturation (Migliano, 2005; Walker et al., 2006). Thesedata suggest that growth rate is sensitive to differenttypes of cues, enhancing the capacity to match life-coursedevelopment to ecological conditions. Despite infantgrowth being the most plastic, recent studies have dem-onstrated the capacity for adolescent growth to continueinto the third decade of life in some populations (Satya-narayana et al., 1980, 1981; Little et al., 1983; Steckel,1987), indicating the capacity for early deficits to be par-tially resolved through plasticity later in the life course.

Some have claimed that early life plasticity represents‘‘predictive adaptive responses’’ anticipating the likelyenvironment during adulthood (Gluckman and Hanson,2005). Others have argued instead that the human fetusadapts to information about the past rather than thefuture (Wells, 2003, 2007; Kuzawa, 2005). Biomedicalstudies demonstrate a powerful capacity for maternalphysiology to buffer the fetus against external ecologicalperturbations during pregnancy and lactation (Wells,2007), and maternal birth-weight predicts offspringbirth-weight better than does pregnancy weight gain(Emanuel et al., 2004; Hypponen et al., 2004).

According to this perspective, phenotype of the humanneonate is strongly influenced by the ecological condi-tions experienced by matrilineal ancestors, and the ma-jority of adaptation to contemporary external conditionscommences during infancy, when the capacity for mater-nal physiological buffering decreases. Such guiding ofoffspring by maternal phenotype has been termed ‘‘inter-generational phenotypic inertia’’ (Kuzawa, 2005). Its sig-nificance for a colonizing organism is profound: offspringare initially protected from the severe stresses thatderive from entry into novel ecological niches and canpreserve high phenotypic quality inherited from theirmothers, regardless of short term ecological fluctuationsduring early development. However, during childhood,the offspring can adapt to more consistent ecologicalstresses, and in successive generations matrilineal guid-ing increasingly softens, as shown by migration studies(Boas, 1912; Bogin and Rios, 2003).

Overall, this mechanism means that human phenotypeis slow to relinquish high quality attained over severalpreceding generations, but at the cost that there is alsoa time-lag on the capacity to recover from chronic matri-lineal exposure to poor conditions. This slow transge-nerational response to ecological change is illustrated bylong-term secular trends in human growth (Steckel,2004, 2005), showing the depression of stature over sev-eral generations in mediaeval Europe, and a consistentrecovery during the 20th century (Steckel, 2004).

The importance of maternal phenotype in guiding off-spring growth rate is emphasized by a recent UK cohort



study. Shorter, fatter mothers gave birth to daughterswho grew rapidly in the first 2 years of life, but then atthe same rate as the daughters of other mothers. Thesefast-growing infants reached puberty early, as had theirown mothers, and were fatter at that time (see Fig. 5).Their earlier puberty is likely to reduce the total growthperiod and result in short final height, thus reproducingmaternal phenotype (Ong et al., 2007). Although thisassociation could plausibly derive from genetic trans-mission, it is notable that the fast growth occurred onlyduring infancy, the period primarily under nutritionalregulation. It is more likely that the fetuses of early-maturing mothers detect the large maternal energystores, and are programmed to exploit them by growingfast during lactation. This interpretation is supported bythe fact that these mothers’ sons also grew faster duringinfancy (Ong et al., 2007).

Human adults have an extraordinary capacity toaccommodate ecological variability through behavioral,technological, and social mechanisms (see The ExtendedPhenotype section). These mechanisms allow them both toshape their niche, and to avoid long-term physiologicaladaptation. Adults entering new environments can there-fore buffer a range of stresses. In contrast, the offspringhas high physiological plasticity in early life, and canmatch physiological phenotype to prevailing conditions.However, this matching is strongly manipulated bymaternal phenotype, so that the offspring adapts to themother as well as the external environment. While somestresses are consistent (e.g., thermal load), others areunpredictable (e.g., energy supply). The combination ofoffspring physiological plasticity and maternal bufferingoptimizes overall adaptation of the offspring to novel envi-ronments. The profile of earlier hominin plasticity is diffi-cult to reconstruct. Nevertheless, awareness of the plas-ticity of growth in contemporary humans may be of partic-ular value when evaluating the fossil record (see Size and

Physique section above). Overall, human plasticity accom-modates the impact of ecological pressures and depressesthe rate of genetic adaptation. However, more fundamen-tal aspects of human biology (e.g., long life-span, largebrain) remain strongly canalized and are therefore pre-served across a great diversity of environments.

Cognition and information processing

After infancy, ecological accommodation is increasinglyachieved via the brain rather than physiological systems.Encephalization is characteristic of modern humans, andits emergence is central to our evolutionary history. It hasbeen argued that a general trend toward the evolution ofcognitive development in the Cenozoic is the result ofadaptations to increasing environmental variability(Richerson and Boyd, 2000). In this context, homininscontinue a more general trend toward increased brainvolume found amongst primates compared to other verte-brates, and amongst hominids compared to other pri-mates (Begun, 2004). The relative brain volume of Aus-tralopithecines was within a continuum with contempo-rary ape species (McHenry and Coffing, 2000). With theevolution of the genus Homo, and in particular, Homoerectus, brain size underwent significant expansion(Leonard et al., 2003) followed by general stability andfurther significant increases in encephalization between600 and 150 KYA (Ruff et al., 1997). In sum, the fossil evi-dence suggests that, building upon the relatively largebrains found amongst all apes compared to other species,significant periods of brain expansion and hence cognitiveability occurred with the hominin adaptive radiation, theorigins of Homo, and throughout the evolutionary historyof Homo heidelbergensis, neanderthalensis, and sapiensin the middle Pleistocene (see Fig. 6).

Increasingly, however, attention is directed to particu-lar components of the brain rather than its total size.Recent comparisons of ape frontal lobes show them tohave much greater similarity to humans than to nonapeprimates (Semendeferi, 1999; Semendeferi et al., 2002).Table 3 provides figures for total cranial capacity, frontalcortex as a percentage of volume of cortex of cerebralhemispheres, and relative volume and neuronal densityof two specific brain regions. While non-ape primateshave relatively smaller frontal cortexes than apes, thetable shows that apes and humans have very similarvalues (Semendeferi et al., 2002). More detailed cyto-architectonic studies remain very rare; however, Seme-nedeferi et al. (1998, 2001) have shown that the brainsof all extant apes exhibit the regions known as Brod-man’s areas 10 (considered to be important in decision-making, strategy formulation, and planning) and 13(considered relevant to emotional responses to socialstimuli). Table 3 shows that humans have a relativelylarge area 10 (though the magnitude of the difference ismodest: Holloway, 2002), but a relatively small area 13.However, complementary to these size differences is sys-tematically lower neuronal density in both regions, acharacteristic associated with greater brain connectivity(Armstrong, 1990). Relatively greater prefrontal whitematter (Schoenemann et al., 2005) and relatively largerand more abundant ‘‘spindle neurons’’ (Allman et al.,2002) are two further traits indicative of greater connec-tivity between brain regions in humans. Area 10 isemerging as a particularly interesting aspect of thehuman brain, associated with comparing current andpast experience, estimating likely pay-offs, and formulat-

Fig. 5. Schematic diagram illustrating growth patterns inthe offspring of mothers characterized by early versus late men-arche. Daughters of early-menarche mothers grow faster ininfancy, and reach menarche earlier themselves, a trajectory thatis associated with greater fatness but reduced final height. Off-spring of late-menarche mothers reach menarche later and growfor longer, ending up taller. These data represent the guiding ofoffspring phenotype by maternal phenotype, most likely throughin utero programming. Based on data from Ong et al. (2007).



ing strategies, and has been proposed to be of impor-tance in the context of food sharing (Allman et al., 2002).Comparative research on brain structure, though still atan early stage, therefore suggests that hominin cognitivecapacities emerged from a sophisticated ape baseline,and that the human brain is as notable for its greaterconnectivity between regions, aiding the evaluation ofproblems, as its size.

Colonization represents a plausible stress favoringsuch greater brain connectivity. Figure 7 illustrates theassociation between major colonization expansions andstepwise increases in encephalization. Across a broadrange of species, there is a clear general trend of increas-ing encephalization from A. afarensis to living humans;however, when we consider the pattern of hominin

encephalization in the context of colonization and selec-tive environments, we can see some correlations. Brainsize increases amongst early bipedal hominins corre-spond with adaptive radiations and exploitation of a va-riety of niches. While further encephalization amongstearly Homo is noted, and may be associated with thebroad dispersal event characterized as Out of Africa 1, itremains relatively stable from 1.8 to 0.6 MYA (Ruffet al., 1997). The subsequent rapid increase noted byRuff et al. in the Middle Pleistocene is associated withthe first consistent hominin occupation of Northern Lati-tudes, which was dependent upon unprecedented cul-tural buffering, such as the use of fire (Gowlett, 2006).Relatively modern encephalization quotients are foundin the record from circa 150 KYA, at which point modern

Fig. 6. Theoretical relation-ship between Hominin Encephal-ization, adaptive radiations, andmajor dispersal events. The en-cephalization data were derivedfrom data presented in Ruff et al.(1997) and McHenry and Coff-ing (2000), using Martin’s (1981)equation: EQ 5 brain mass/(11.223 body mass0.76).

TABLE 3. Comparison of selected brain characteristics across contemporary apes

Orangutan Gorilla Chimpanzee Bonobo Human

Cranial capacity (cc)Both sexesa 434.4 534.5 398.5 1,345Maleb 415 550 410 355 1,435Femaleb 370 460 380 339 1,325

Relative frontal cortex volume (%)c 37.6 35.9 35.4 34.7 37.7Area 10

Relative volume (%)d 0.45 0.54 0.57 0.74 1.22Neuronal density per ccd 78,182 47,300 60,468 55,690 34,014

Area 13Relative volume (%)e 0.09 0.08 0.07 0.03 0.03Neuronal density per cce 42,400 54,783 50,686 44,111 30,351

Spindle cell volume (lm3)f 6,648 5,684 8,796 7,743 20,822

cc 5 cm3.a Tobias, 1971.b Apes: Pilbeam and Gould; humans: Filipek et al., 1994.c Semendeferi et al., 2002.d Semendeferi et al., 2001.e Semendeferi et al., 1998.f Nimchinsky et al., 1999.



human behavior was developing on spatio-temporallymosaic scales (McBrearty and Brooks, 2000). This tech-nological and cultural evolution would become the basisfor the success of modern human dispersals.

While these correlations are intriguing, brain pheno-type is associated with various physiological and behav-ioral traits, and as such it is difficult to tease out thecauses and consequences of its changes during homininevolution. Given the expense of brain tissue, larger brainsvolumes could only be selected if benefits exceed costs.What factors might have conferred such benefits in homi-nins? Amongst the factors proposed to have favoredincreased cognitive capacity are technology, hunting, diet,increased home-range, and sociality. Of these, the strong-est candidate is generally considered to be the last—forexample, across primates in general, neocortex size isassociated with social group size (Dunbar, 2003).

Humphrey (1986) argued that the primary factorfavoring increased intelligence in our own genus was thebenefit of predicting and manipulating the behavior ofothers in the social group. This argument was expandedby Byrne and Whiten (1988) in their treatise on Machia-vellian intelligence. Thus ‘‘manipulating people ratherthan their genes or the objects they wield is whatrequires high intelligence’’ (Gamble, 1993, p 102), andthe formation and maintenance of alliances has beenproposed to favor a large working memory, able to pro-cess large amounts of both recent social data and priorsocial interactions (Byrne and Whiten, 1988). A relatedissue comprises the benefits of transmitting cultural in-formation (Richerson and Boyd, 1998). However, entryinto volatile niches offers a new perspective on the bene-fits of enhanced cognitive capacities, and recent researchfurther implicates female reproductive behavior as a keyarea of importance in this context.

As noted by Popper (1982), increased cognitivecapacity allows thoughts rather than the organism itselfto be risked in difficult circumstances. Gamble (1993)has suggested that the acquisition and use of informa-tion about nearby habitats was critical to hominin dis-persal and colonization. In many foraging populations,males only acquire proficiency in hunting during theadult years (Kaplan et al., 2000), and prior to this periodthey may have been unlikely or unable to provide infor-mation of sufficient value to underpin migration deci-sions. Furthermore, primate studies have indicated theimportance of females in driving both cognitive and tech-nological evolution (Boesch and Boesch, 1984), andfemale foraging strategy may have been important fordetermining the viability of dispersal.

Traditionally, evolutionary models have consideredfemales as burdened with the costs of parental care.Washburn’s notion of fathers provisioning nuclear fami-lies with meat is now considered unlikely, and huntersare thought more likely to have used their skills to com-pete for mating opportunities (Hawkes et al., 2001). Thereproductive strategy of ‘‘stacking’’ several dependent off-spring of differing maturity therefore results in extremerequirements for offspring care. These high demandswould in turn have induced powerful selective pressureboth on female foraging behavior itself, and also the cog-nitive basis of allocating resources and delegating paren-tal care. Allomothering is widely practiced amongst pri-mates, and relieves the burden of care on mothers whileproviding experience to nulliparous females who subse-quently benefit from increased reproductive success(Hrdy, 1999). Hrdy’s (2005) notion of humans as coopera-

tive breeders with high levels of allomaternal care repre-sents a highly plausible socio-cognitive solution to thehigh female burden of care. The flexibility of the approachis particularly suited to accommodating the exposure toecological diversity that dispersal generates—allomother-ing strategy can be tailored to local circumstances, whilenulliparous females can learn about new environments.Consistent with such flexibility, contemporary foragersdisplay no particular social solution to the dilemma ofparental care, and rather show a range of different mar-riage strategies, including polygamy, monogamy, polyan-dry, along with varied paternal care contributions (Kelly,1995). While the burden of maternal care is high, femalesmay also be considered disproportionately empoweredwith control over offspring development, such that it ismales that are disadvantaged through having little op-portunity to exert influence (Waage, 1997). Female biol-ogy involves transgenerational transmission of informa-tion at several levels unavailable to the male.

Clearly, intelligence provides an alternative means ofadaptation to anatomical or physiological adaptation,and is a major source of plasticity in our species. We sug-gest that initially, increased cognitive capacities mayhave been favored on account of the benefits of adaptingto unstable environments per se. The increased cognitivecapacity may then have allowed more proactive dispersaland niche construction, rapidly inducing further selec-tive pressures in a positive feedback cycle. Such pres-sures may have targeted female reproductive behavior inparticular, and it is notable that a high proportion ofgenes related to intelligence are found on the human X-chromosome (Zechner et al., 2001). One of the benefits ofthis model is that it offers a plausible explanation forthe sustained changes in brain phenotype that occurredover the last 2 million years, with the colonizing Homogenus increasingly provoking the selective pressuresthat favored more sophisticated cognition.

The extended phenotype

The evolution of human cognition is clearly related toa number of other characteristics, which could be seenas extrosomatic adaptations, which contribute to anextended phenotype, which would contribute to coloniz-ing ability. Foremost amongst these are technology, cul-tural evolution, and language. While these have beendiscussed extensively in the literature, their relevance tocolonizing will be explored briefly below.

Technology. Technological developments are often con-sidered to be a central component of human evolution,and certainly from the emergence of Homo, stone toolsare associated with all populations in the fossil record. Itremains more difficult to identify patterns of tool useamongst australopithecines and other Pliocene hominins.Those studying chimpanzees have noted that many sim-ple tools are made of vegetable material and would nothave survived the process of fossilization. Despite this,we know that there is considerable variation in chimpan-zee material culture (McGrew, 1992, 2004), much ofwhich is based upon degradable organic material(McGrew, 1992; Whiten et al., 1999). New discoveries con-tinue to illuminate the ways in which chimpanzees useorganic materials as tools, including the first documenteduse of spears (Pruetz and Bertolani, 2007). Despite thefrequency of use of organic tools among chimpanzees,their use of stone anvils and percussive technology tocrack nuts has been documented not only among living



chimpanzees, but has also produced an archeological re-cord with some antiquity (Mercader et al., 2002, 2007).

Of particular interest are chimpanzee sex-differencesin tool use. While the use of tools in hunting by males isnegligible, a sophisticated toolkit has been observedapplied to the gathering of social insects (McGrew, 1992)and vertebrates (Pruetz and Bertolani, 2007). This hasled to increasing interest in the hypothesis that the ori-gins of hominin tool use may be most closely associatedwith female gathering (McGrew, 1981; Zihlman, 1981;Tanner, 1987). Compared to humans, chimpanzees arenotable for their lack of use of containers to transportfood items, and their tendency to consume foods whereacquired (McGrew, 1992). Collectively, the ape evidencehighlights the importance of tool use in the gathering ofvegetable, invertebrate, and occasionally mammalianfoods by females, and again highlights selective pres-sures acting disproportionately on females.

Technology clearly plays a key role in opening upnovel niches. Since rudimentary technology contributesto a wide variety of subsistence activities among chim-panzees, aiding in the capture of animals, access to plantresources, the transport of materials, and the processingof foods, it is reasonable to predict it would have playeda similar role in early hominins. Interpretations have of-ten been based upon perceived associations betweenmajor evolutionary transitions and material culture(Leakey et al., 1964; Klein, 1999); however, evidence forstone tools as early as 2.6 MYA (Semaw et al., 1997;Semaw et al., 2003), which were used to butcher animals(Dominguez-Rodrigo et al., 2005), leaves the question ofthe association between Oldowan tools and hominin spe-cies open. Disparity between the dates of the earliestHomo erectus fossils (Anton, 2003) and the first Acheu-lean tools (Asfaw et al., 1992), and the chronology of dis-persals characterized as Out of Africa 1 (Gabunia et al.,2000), further highlights this issue.

Despite the disparities noted above, technology mayhave been important in some aspects of the adaptiveradiation of Pliocene hominins in response to environ-mental instability (Potts, 1998a) and the dispersal ofHomo erectus (Morwood et al., 1998), and has clearlyplayed an important role in subsequent population move-ments. Stone tool technologies developed throughout theOldowan and Achelean (between 2.5 and 0.3 MYA), andraw material transport distances were low; however,both the rate of technological change and transport dis-tances increased considerably by the Middle Stone Age(Ambrose, 2001). More recent developments, includingthe production of clothing and shelter and the inventionof watercraft, would have been essential technologi-cal components of the dispersal of modern humans.Although the package of technological components thatwe consider to relate to ‘‘modern human behavior’’ devel-oped over a considerable time in Africa (Lahr and Foley,1998; McBrearty and Brooks, 2000), much of this techno-logical package was in place by the time of the first per-manent dispersal of anatomically modern humans out ofAfrica (Lahr and Foley, 1998; Underhill et al., 2001;Stringer, 2002). While the benefits of technology requireno elaboration here, we emphasize the capacity for mod-ern technological flexibility to facilitate entry into andexploitation of a wide variety of niches while preservinga common physiology and anatomy. Technology appearsparticularly important in colonizing higher latitudes(Torrence, 1983), indicating its capacity to mediate moreextreme environmental conditions. Consistent with that

hypothesis, chimpanzees exploit tools to a greater extentin harsher environments (McGrew, 1992).

In addition to its obvious practical implications, tech-nology also represents an important component of thebiology of human migration for its capacity to store in-formation extrasomatically (Pfaffenberger, 1992). As ma-terial artefacts are created, they encapsulate in them-selves information about their design and often theirutility. Artefacts overcome a major limitation of morpho-logical adaptation, namely that they can be discardedwhen not wanted (Petraglia et al., 2005). Thus thecapacity to make technology when required is as impor-tant as the technology itself. This benefit comes at thecost that such knowledge may be lost if both the articles,and those who know how to produce them, fail to bereplaced over time.

Cultural evolution. Recent evaluations highlight thegreat ape clade as the source of a novel cultural reper-toire from which subsequent hominin evolution drew(van Schaik et al., 2003; Whiten et al., 2003; McGrew,1992, 2004). The role of culture in chimpanzee biologyhas been clarified by a detailed evaluation of local grouppractices and variability in their within-group transmis-sion over time (Whiten et al., 1999). Experimental stud-ies have demonstrated both the emergence of local tradi-tions, and conformity bias maintaining their integrityover time (Whiten et al., 2005). Such learned behaviorhas been shown to be adaptive, including exploiting al-ternative resources during seasons of poor fruit avail-ability, and swallowing leaves to treat nematode infec-tions (Whiten, 2006). However, unlike in humans, thereis very little evidence of direct teaching among apes(McGrew, 1992; Whiten, 1999).

Contemporary human populations illustrate extraordi-nary cultural variability, in which social learning is com-plemented by individual learning, ensuring thatacquired information has ecological validity (Richersonand Boyd, 2005). Providing this validity is preserved,culture becomes increasingly adaptive when learning isdifficult and the environment is unpredictable. Underthese conditions, it is beneficial to accumulate the cultur-ally acquired knowledge of many others, providing astore of information impossible for any individual to ac-quire alone (Richerson and Boyd, 2000; Wells, 2006b).Compared to genetic inheritance, the speed of culturaltransmission combined with a broad pool of potential in-formation confers markedly high phenotypic plasticity.

There are two potential mechanisms through whichcultural evolution can influence human adaptation tonew environments. One is as a simple buffering system,through which environmental stresses are mediatedthrough cultural mechanisms that passively conferadvantages to survivorship and reproduction, thusensuring genetic survival (Dawkins, 1976). A more activerelationship between culture and evolution is proposedby models of niche construction (Laland et al., 2001;Odling-Smee et al., 2003) and gene-culture coevolution(Durham, 1990), in which culture directly changes theselective environment of the species and thus in partdetermines the trajectory of evolution within the species.

There is substantial evidence that cultural transmis-sion is encouraged by psychological mechanisms predis-posing individuals to favor information from more memo-rable or common sources, or those considered prestigious(Richerson and Boyd, 2005). These traits allow not onlyadaptation but also systematic maladaptation; hence,



culture tends to be most adaptive when it incorporatesaccurate emulation and teaching. However, rapid cul-tural adaptation may favor mechanisms protecting in-group members from receiving information from othergroups. This scenario may account for the emergence ofstrong group identities among human populations, par-ticularly at their boundaries (Richerson and Boyd, 2005),and some apparently maladaptive behaviors may bedirected toward such group identity rather than fitnessper se. The concept of bet-hedging may also meritgreater attention in this context: when prior experienceoffers a poor guide to novel problems, behavioral diver-sity within and between groups may represent a viablelonger-term survival strategy.

The question of how cultural evolution relates tohuman evolution is challenging to address (Foley andLahr, 2003). Cumulative cultural change is a necessarycomponent of human survival in a variety of stressfulenvironments, although it is difficult to identify in theearly archeological record (Henrich and McElreath,2003). While cultural transmission is clearly a part ofthe adaptive phenotype of great apes, at present it can-not be firmly linked to the ability to colonize specifichabitats, and certainly not to the extent found withinmodern humans. The cognitive differences between otherspecies and humans may relate to the combination ofontogenetic factors such as the ability to infer thethoughts of other individuals (theory of mind) and anunderstanding of other individuals as intentional agents(Tomasello and Rakoczy, 2003). While there is evidencethat chimpanzees possess aspects of a theory of mind(Hare et al., 2001), the extension from individual to col-lective intentionality may underpin human culture andcognition (Tomasello and Rakoczy, 2003). Our under-standing of this change remains speculative, althoughthe cognitive capacity for collective intentionality musthave been greatly enhanced by language, and thus canonly confidently be said to have been in place withinHomo sapiens (see Communication and Language sec-tion below).

Cognitive developments can be seen as a major compo-nent of dispersals within our species and may have cor-responded with the early occupation of higher latitudes(Parfitt et al., 2005); however, cultural diversity showssignificant associations with ecological parameters suchas temperature and rainfall in contemporary humanpopulations (Collard and Foley, 2002). There is also evi-dence of increasing cultural differentiation in more pro-ductive regions, suggesting that such differentiation isconstrained in harsher environments due to the greaterneed for interaction between populations (Nettle, 1998),and constraints of resource availability. Equally, moreproductive environments may favor niche constructionand associated cultural differentiation, leading to greaterdiversity (Collard and Foley, 2002). Cultural evolutioncan therefore be considered to have played a key role inthe behavioral adaptations that have been central to col-onizing within our species, while relieving selective pres-sures on anatomy and physiology.

Communication and language. Language is a defin-ing feature of our species and has attracted considerableattention from evolutionary biologists. While human lan-guage appears to have evolved in parallel with otherforms of communication such as calls and gestures, itwas likely preceded by the capacity for some form ofsymbolic thought and representation (Deacon, 1997).

However, the development of vocal language must beconsidered as a separate process, linked with anatomicaland neurobiological changes. Patterns of basicranial flex-ion (Lieberman et al., 1992), hyoid (Arensburg et al.,1989), and hypoglossal canal morphology (Kay et al.,1998) provide controversial evidence for languageamongst Neanderthals and possibly Homo heidelbergen-sis, but not early Homo or australopithecines. However,the discovery of the normal human variant of theFOXP2 gene, which differs between humans and othermammalian species and corresponds with fine motor con-trol of the mouth, appears to have arisen between 50and 200 KYA (Enard et al., 2002). Thus, the full symbol-izing capabilities of modern humans appear to have hada relatively recent emergence, perhaps linked with thisgenetic change (Fisher, 2005). This time period coincideswith the mosaic pattern of origins of modern humanbehavior (McBrearty and Brooks, 2000) and suggeststhat a complete linguistic and cultural package facili-tated the expansion of modern humans across the globe.

The symbolism afforded by the origins of language isan inherently social process and would have conferredthe ability of individuals to share a ‘‘virtual commonmind’’ (Deacon, 1997). It also would have been a neces-sary precursor for the rapid technological evolutionfound within our species by enhancing the transmissionof information between individuals and minimizing trialand error. Symbolism may therefore have been of partic-ular value in the most recent disposals of Homo sapiens,where sea crossings and expansion into previously unin-habited and ecologically stressful niches required agreater degree of planning and evaluation. Likewise lan-guage may have offered significant benefits to socialgroups as they consolidated niches, competed for re-gional resources and emphasized local cultural identity.In contrast, the morphological and genetic evidence sug-gests that earlier dispersals of Homo erectus must havebeen achieved with much simpler forms of communica-tion, perhaps providing one of the mechanisms restrict-ing dispersal of this species within tropical regions.

Summary

In this section, we have reviewed evidence concerningthe characteristics of hominin and human biology thatfacilitate the capacity to enter new territory, habitats,and ecological niches. Comparisons between humans andapes demonstrate a markedly greater degree of plasticityand behavioral flexibility, and support the hypothesisthat at many levels, humans have the biology of a ‘‘colo-nizing ape.’’ Plio-pleistocene adaptive radiations appearto have been contingent upon the morphological andtechnological ability to exploit a diverse range of habi-tats, leading to the dispersal events resulting in adistribution of Homo erectus from southern Africa toSouth-East Asia, within a band of tropical latitudes. Thecolonization of the broad range of habitats, including peri-arctic environments, was most accessible with a completepackage of human body size, cognition, culture, physiol-ogy, and plasticity. Despite this, there remain open ques-tions about whether these characteristics only came to-gether within modern humans, or arose in a mosaic fash-ion amongst Pleistocene hominins, thus enabling theoccupation of northern Europe by Homo heidelbergensisand neanderthalensis. It is important to note the poten-tial feedback and selective environments that may haveresulted from colonizing. These may be important in



driving much of the directional change in the homininphenotypes, in particular regarding the Homo brain.

CONCLUSIONS

Although all organisms have the potential to repro-duce in geometric ratio (Malthus, 1798/1976), suchpotential is balanced in practice by mortality and con-straints on resources. These balancing factors shapeeach organism’s biology and reproductive strategy. Whenorganisms inhabit stochastic environments, and experi-ence regular demographic cycles, natural selection willfavor traits that promote the potential for rapid popula-tion growth, allowing the capacity to bounce back. Suchtraits comprise not only reproductive strategy, but manyother components of biology. In this paper, we consideredhow life cycles [identified by Bonner (1965) as the pri-mary target of selection] may be considered as a form ofrisk management, and evolve by varying a set of life his-tory strategies. The story of hominin evolution over thelast 6 million years represents the adaptation of lifecycles to increasingly stochastic environments, favoringgreater plasticity in many aspects of phenotype. Wehighlight a number of related issues, and argue thatsuch plasticity has played a key role in the emergence ofthe genus Homo as a colonizing ape.

First, we suggest that the radiation of Australopithe-cines into more variable niches initiated the exposure ofearly hominins to selective pressures favoring thecapacity to accommodate fluctuating ecological condi-tions. These capacities then played a key role in theemergence of the genus Homo. Plasticity both protectsgenetic variation and also releases it under strong envi-ronmental stresses. The rapid shift in phenotype thatcharacterizes Homo relative to australopithecines may,we argue, be considered the product of such a decanaliz-ing release. Phenotypic plasticity subsequently remainedpreserved in Homo and was fundamental to its success-ful dispersal across diverse habitats.

Second, the high level of plasticity relative to otherapes allows humans to opt out of genetic adaptation. Weare an animal that above all refuses to commit to specificlong-term strategies. Adults use a combination of behav-ior and technology to alter their environments to suittheir anatomy and physiology. Offspring show greatercapacity to improve the fit between their physiology andecological conditions during the ontogenetic process, butadapt to parental experience rather than the environ-ment directly. Human biology therefore displays anextraordinary capacity for behavior and technology tohomogenize diverse habitats and construct a narrowerrange of ecological niches, further accommodated by met-abolic plasticity, thus buffering selective pressures onthe human genome.

Third, we suggest that the tendency to probe new ter-ritories, habitats, and niches has generated, throughpositive feedback, sustained selective pressures favoringtraits that accommodate environmental variability.Increasingly, Homo colonized niches rather than terri-tory, but also homogenized these niches to fit anatomyand physiology. Bursts of colonizing success may havepromoted selection for the very traits that predispose tosuch niche-probing. When during Homo evolution thisbegan to induce positive feedback selection remains opento debate, but we suggest that the notion of the genusHomo as increasingly contributing to its own selectivepressures through niche-probing and dispersal would

explain continued genetic change over 2 million years,demonstrated in particular by the systematic expansionand increasing sophistication of the Homo brain. Thisissue merits further investigation, through both thepaleoanthropological record and simulation models.

Fourth, we emphasize the powerful impact of selectivepressures on females in particular. Research in bothhumans and primates increasingly highlights the impor-tance of female reproductive strategy for the evolution ofcognitive capacities, and recent studies break with tradi-tion in suggesting that females rather than males mayalso have driven key aspects of technological evolution.Understanding the challenges of buffering vulnerableoffspring from the stresses of stochastic environmentsand new habitats, despite maintaining fast rates ofreproduction, is relevant not only to our conception ofhominin evolution, but also to the sensitivity of contem-porary health to social and metabolic perturbations(Kuzawa, 2005; Wells, 2007).

Human reproductive strategy is notable for itscapacity for rapid bursts in population growth. Today,humans are applying their colonizing reproductive strat-egy to the highly productive niche of modern agriculture.This latest population boom is exerting its own selectivepressures on human biology, and as noted by Shennan(2002), further population crashes are not unlikely.

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