How have metabolic constraints affected human evolution?
In the 2002 Annual Reviews in Anthropology, Leslie Aiello and Jonathan Wells provide a synopsis of the ways that morphological evolution in the human lineage have affected the energy utilization of our species and its ancestors. These considerations focus on body size, because it is tightly correlated with metabolic rates among mammals. Secondarily, they focus upon the relative sizes and proportions of different organs, especially the relative sizes of the brain and of the gut.
Aiello and Wells begin with the origin of early humans (which they assign to Homo ergaster). The most important change to happen at this time was an increase in body mass, likely to nearly twice the mass of female australopithecines. But there was also a complex of other changes that occurred at this time, including a change to more humanlike body proportions, with longer legs, and a change in diet toward higher energy food resources, probably including meat. One aspect of this change that the review summarizes is this our regulatory benefits of longer limbs, more linear physiques, and the effects of heat load upon a birthweight and energy expenditure during pregnancy, following the work of Wheeler (e.g. 1991), Ruff (1991), and Wells. From the increase in body mass, they calculate the necessary increase in resting metabolic rate following Kleiber's equations. They estimate that compared to Australopithecus afarensis, early humans would have required 39 percent more energy to meet resting metabolic requirements, with a much larger increase in females than males (resulting from the marked decrease in sexual dimorphism).
The authors spend a section considering what the dietary balance of these early humans must have been. They note that modern hunter gatherers with especially high energy requirements, such as Eskimos, meet these requirements by including a very high proportion of meat in their diets. Interestingly, they argue against this dietary model for the earliest humans, not on the basis of ecological reconstruction or arguments about scavenging vs foraging, but instead on the basis of the thermoregulatory requirements of meat digestion. They argue that digestion of meat produces more heat than the digestion of other kinds of foods, especially if the meat is protein-rich and fat-poor. They also note that the digestion of protein requires a great deal of water, which would be relatively scarce for savanna-based hominids. They do not use these arguments to suggest that early humans lacked meat in their diets, but instead emphasize that a balance between different dietary sources would be more advantageous, particularly if dietary fat were relatively unavailable.
Aiello and Wells then turn to the expensive tissue hypothesis. In brief, this hypothesis builds on the observation that some tissues require more energy for their resting metabolism than others. In particular nervous tissue is very expensive and digestive tissue is also quite expensive. The relative sizes of most body tissues are relatively constrained by functional requirements. But a reduction in dietary bulk might allow natural selection to pare away digestive tissues that were less necessary for food absorption, making energy available for the expansion of other tissues such as brain tissue (Aiello and Wheeler 1995). A novel element in this review is the inclusion of body fat and its potential complication in the estimation of resting metabolic rate. Aiello and Wells hypothesize that later members of the genus Homo were relatively fatter than earlier fossil hominids. It is well recognized that living humans in Westernized societies have a higher percentage of body fat than most mammals in wild populations. Fat tissue, called adipose tissue, has a relatively low contribution to overall metabolic rate. This means that an a fatter person will have a relatively lower metabolic rate than a leaner person of the same mass. If it is true that recent humans generally have been fatter than earlier humans, then even if their mass remained unchanged, the resting metabolic rates of human populations may have actually increased relative to their fat-free mass. This is a bit of a convoluted argument, dedicated to a single problem. Considering that recent humans have larger brains than their ancestors, the expensive tissue hypothesis predicts that either human metabolic rates must have increased over time, or that the relative mass of some other expensive tissues must have decreased. If humans became fatter at the same time that their brains increased in size, then the increase in fat mass might contribute to a relative reduction in the energetic requirements of the overall body mass. This reduction would have allowed an increase in the metabolic requirements of brain tissue. Aiello and Wells propose that these two opposing forces may have balanced each other, with the change in body composition underwriting the increase in size of the human brain.
Needless to say this vision is complicated by the fact that we have no evidence of soft tissue proportions in fossil humans. Likewise, there is no special reason to believe that recent humans--except for people in industrialized societies--actually are much fatter than their fossil ancestors. Aiello and Wells cite a study (Lawrence et al. 1987) that estimates body fat percentage in women in harsh environments at around 20 percent. This estimate would of course be higher for women than for men, considering the increased fat storage available in breast tissue and other sources in women. But it is far from clear that even human women have higher fat storage than females in other primate species. This is a subject that clearly needs further study.
There are several interrelated forces that do suggest that increased fat storage may have been an important human adaptation, possibly as early as the earliest fossil evidence of humans. One of these is the relatively high reproductive rate of humans compared to other hominoids. The short birth intervals of humans, combined with the rapid transition from weaning to new pregnancies among human mothers is significantly enhanced by the ability to store energy and smoothe out fluctuations in dietary resource availability. This hypothesis is supported by the observations that female reproductive fitness appears to depend on fat stores to some extent, and very thin women have a higher rate of miscarriage and a higher likelihood of low birthweight babies. Another is the fact that humans modify their group sizes with much less seasonal variation that is observed in chimpanzees.
Another novel element of this review is the consideration of energy costs as they change during early ontogeny. Aiello and Wells note that the metabolic costs of the brain are especially high very early in life, because of the early growth of the brain. They cite an estimate that the brain requires up to 70 percent of the total energy costs of the individual (Holliday 1986), although this sounds like an overestimate. They suggest that human children meet these energy requirements in part by compromising their rate of growth, especially during the time period between 2 and 12 years of age. The unique ontogeny of human growth in includes this time span during which chimpanzees actually have faster growth rates than humans, followed by the "adolescent growth spurt" in humans, when childhood growth rates continue and may even increase (Ulijaszek 1995). This alteration in rates may reflect the increased resting metabolic requirements of tissue proportions in human children. The authors also note that parent-offspring conflict provides another explanation for slowed growth rates in human children, considering that parents and children must both depend on the same resources, collected by parents. I might add to that the competition between children and new siblings, considering that at the weaning age it is likely that most human children would very shortly have seen their mothers investing their energetic resources in growing pregnancies and the care of subsequent offspring.
In the final section, the authors make suggestions about the relationship between energetic evolution and social organization. Citing Aiello and Key (2002), they provide estimates that indicate that lactating early humans would have had energy requirements 45 percent higher than lactating australopithecines, and "almost 100 percent higher than for a nonlactating and nongestating smaller-bodied hominin" (333). That paper argues that a reduction in the birth interval would have reduced the energy costs per offspring, at the same time that it increased overall reproductive output. The reduction is most noted in the length of lactation, which is the most expensive part of direct maternal investment. In that paper, they note that only a major shift in diet could allow this change to happen, because the resources lost to children by a reduction in lactation length would have to be replaced by other foods, presumably high-energy foods like meat. But they also note that other individuals besides the mother might be involved in providing these resources to children. They focus on the possible effects of grandmothers, following Kristin Hawkes and colleagues (1997). One might include on this list the possibility of paternal investment, or the contributions of other group members. In any event, the social changes necessary for effective hunter-gatherer foraging strategies, which necessitate the sharing of both risks and benefits of hunting, would help to support this strategy.
These energetic ideas leave several questions unanswered, mostly based around assumptions that cannot be verified. For example, what was the birth interval of australopithecines? If this birth interval were short, as in recent humans, then the transition to a more human-like body size might not been accompanied by such extensive social changes. And were the predecessors of early humans--such as Homo habilis--themselves fat? One might expect that the origins of tool use corresponded with the origins of some of the dietary changes that Aiello and Wells argued characterized early humans. If so, then energy storage must have been an integral element of this toolmaking adaptation. Indeed, the evidence the brain size first increase in Homo habilis or another small-bodied hominid directly detracts from the idea that energetic changes were the principal driving factors of changes in body size, sociality, or other early human characteristics. It goes without saying that we don't directly know what the proportion of different "expensive" tissues in australopithecines or any other early hominid might have been, beyond the suggestion that the reconstructed skeleton of Lucy had a broad gut and pelvic cavity.
References:
Aiello LC, Key C. 2002. The energetic consequences of being a Homo erectus female. Am J Hum Biol 14:551-565.
Aiello LC, Wells JCK. 2002. Energetics and the evolution of the genus Homo. Annu Rev Anthropol 31:323-338.
Aiello LC, Wheeler P. 1995. The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199-221.
Hawkes K, O'Connell JF, Blurton-Jones NG, Alvarez H, Charnov EL. 1998. Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci U S A 95:1336-1339.
Holliday MA. 1986. Body composition and energy needs during growth. In: Falkner F, Tanner JM, editors, Human growth: A comprehensive treatise, 2 edition. New York: Plenum. p 101-107.
Ruff CB. 1991. Climate and body shape in hominid evolution. J Hum Evol 21:81-105.
Ulijaszek SJ. 1995. Energetics and human evolution. In: Ulijaszek SJ, editor, Human energetics in biological anthropology. Cambridge, UK: Cambridge University Press. p 166-175.
Wheeler PE. 1991. The thermoregulatory advantages of hominid bipedalism in open equatorial environments: the contribution of increased heat loss and cutaneous evaporative cooling. J Hum Evol 21:107-115.
A revised chronology for early Homo
In case you haven't been paying attention, the chronology of early African Homo has been completely turned upside-down this year. Well, "upside-down" isn't precisely right; "displaced younger by a quarter-million years" is better.
The redating has come from Frank Brown's group, which in a series of papers has defined and dated stratigraphic units between the major tuffs of the Koobi Fora formation, between the KBS Tuff at 1.87 Ma and the Chari tuff at around 1.38 Ma. Gathogo and Brown (2006) outline the consequences of this redating for fossils of early Homo. Their paper focuses on the fossils from area 123 at Koobi Fora, but discusses the likely consequences of redating on other localities.
Fossils of Homo now estimated to be 1.65 +/- 0.15 myr in age in the Koobi Fora region are currently assigned to at least two taxa on the basis of both crania and mandibles. Homo habilis is represented by specimens KNM-ER 1501, 1502, 1805, and 1813, and H. ergaster is represented by specimens KNM-ER 730, 1812, and 3733 (for attributions, see Wood, 1991, 1992; Wood and Richmond, 2000). The ages of specimens KNM-ER 1501, 1502, 1812, and 1813 have been discussed above, and although not the main focus of this paper, a few notes are offered below on the others.
Specimen KNM-ER 730 derives from a level 5 m below the Koobi Fora Tuff Complex in Area 103 (Feibel et al., 1989), and is thus ca. 1.6 myr old. Feibel et al. (1989) gave an age of 1.85 myr for KNM-ER 1805, but this specimen lies "just below the base of the Okote Tuff" in Area 130 (Leakey et al., 1978), and is more likely closer in age to that of the base of the Okote Tuff Complex (ca. 1.6 myr) than it is to that of the KBS Tuff (1.87 myr). On the basis of mollusc-packed sandstones and algal horizons correlated from Area 102 to Area 104, Feibel et al. (1989) estimated that KNM-ER 3733 was 1.78 myr in age. Although the age of KNM-ER 3733 cannot be confirmed without additional fieldwork, the White Tuff, with an estimated age of 1.63 myr (Brown et al., 2006), is the nearest unequivocally identified unit in the local section in Area 104. This tuff is exposed <300 m from the location of KNM-ER 3733, and Tindall (1985) records only 8 m of section below the White Tuff nearby. Therefore KNM-ER 3733 should be approximately the same age as KNM-ER 1813. Indeed, all specimens from Koobi Fora assigned to H. aff. H. erectus by Wood (1991), many of which are now referred to H. ergaster (Wood and Richmond, 2000), are now estimated to be 1.45 to 1.65 myr old with the exception of KNM-ER 2598. The latter specimen, which is a partial occipital bone from Area 15, was placed 4 m below the KBS Tuff by Feibel et al. (1989) and estimated to be about 1.9 myr old. This age estimate is reasonable because strata do not extend more than 7 m above or below the KBS Tuff at the recorded location of KNM-ER 2598 (Gathogo and Brown 2006:7-8, emphasis added).
This raises a question: Just how much evidence is left for large-bodied H. erectus-like hominids earlier than 1.65 Ma?
Wood (1991) didn't diagnose postcrania, and Gathogo and Brown (2006) don't comment on them. At least KNM-ER 1808 would seem to fall under this umbrella, since Wood (1991) did diagnose that. But more important in bracketing the evolution of large body size is KNM-ER 3228, a hip bone previously dated to 1.95 Ma. It's pretty big for a human, let alone an australopithecine. On the other hand, McHenry and Coffing (2000) suggested that KNM-ER 3228 might belong to H. rudolfensis. To my eyes, this would make it a pretty big specimen compared with femora like KNM-ER 1472 and KNM-ER 1481, but who knows?
Another uncomforable fit in an H. rudolfensis would be KNM-ER 2598. It sure looks like a large-brained, thick-boned specimen. It doesn't look much like KNM-ER 1470. But then, maybe 1470 is the unusual specimen...
Gathogo and Brown (2006) take on directly the issue of KNM-ER 1470 and KNM-ER 1813. The two were formerly considered contemporaries at around 1.89 Ma, but now KNM-ER 1813 is only 1.65 Ma.
KNM-ER 1813, lateral view
The real offshoot of this is that there are no longer any early small-skulled habilines. The question of whether KNM-ER 1470 and KNM-ER 1813 were too different to belong to a single species has drawn a lot of ink, but it was always a non sequitur, because the two weren't the only crania to consider. The more interesting observation had been that Olduvai Gorge preserved only small-skulled habilines, while Koobi Fora had both small and large ones. This was not only a geographic problem but also a temporal one, since the Olduvai habilines were all relatively late (less than around 1.8 Ma) and the Turkana habilines were mostly earlier.
Now the situation has changed. The small Turkana habiline, KNM-ER 1813, is now contemporary with the Olduvai sample. There are no longer any small-skulled early Turkana habilines. KNM-ER 1805 makes sense as a male of the later, small-skulled sample because it is relatively small-brained but robustly built (e.g., with a sagittal crest). That leaves KNM-ER 1470, KNM-ER 1590, KNM-ER 3732, and KNM-ER 3735 as plausible habilines before 1.85 Ma.
This seems like a nice sample as a possible ancestor for both later large-bodied Homo and later habilines. Heck, Wood (1991) even wrote this in his description of KNM-ER 3735:
Some features (e.g. vault thickness) ally it with a Homo erectus-like hominid, but in other areas (e.g. the frontal) it is more like crania such as KNM-ER 1813, a conclusion endorsed by Walker (1987) and by Leakey et al. (1989). Tobias (1989) includes KNM-ER 3735 within H. habilis (Wood 1991:134-135).
What more could you ask of a common ancestor? But then if some of this ancestral population would be expected to resemble later H. erectus-like specimens, then why not KNM-ER 2598?
And what, exactly, would make such a population -- with its mixture of H. erectus-like and habiline-like features -- different from Dmanisi? The answer, of course, is KNM-ER 1470. It's still the odd one in this lineup. But then, it does have the largest brain in this set, which might help to explain the rounded occiput.
Looking at what is left in the early part of the sequence is certainly interesting, but just as interesting is how all the H. erectus-like specimens are all bunched together between 1.65 and 1.45 Ma. This is the time interval that already held KNM-WT 15000, KNM-ER 3883, and KNM-ER 42700, and is just older than OH 9. Now we can add KNM-ER 3733, KNM-ER 730, KNM-ER 1808, and KNM-ER 1821. Isn't this an interesting sample? Don't you wish we knew about the other postcrania?
It seems to me that the hypothesis that H. erectus-like hominids first appeared in Africa around 1.65 Ma has interesting archaeological consequences. This isn't long before the appearance of the earliest Acheulean, and it plausibly makes the Developed Oldowan-Acheulean sequence a correlate of this evolution.
It is markedly not coincident with the earliest such evidence in Asia. But that raises the Dmanisi question again, doesn't it?
References:
Brown FH, Haileab B, McDougall I. 2006. Sequence of tuffs between the KBS Tuff and the Chari Tuff in the Turkana Basin, Kenya and Ethiopia. J Geol Soc 163:185-204.
Gathogo PN, Brown FH. 2006. Revised stratigraphy of Area 123, Koobi Fora, Kenya, and new age estiamtes of its fossil mammals, including hominins. J Hum Evol (in press) DOI link
McDougall I, Brown FH. 2006. Precise 40Ar/39Ar geochronology for the upper Koobi Fora Formation, northern Kenya. J Geol Soc 163:205-220.
Wood B. 1991. Koobi Fora Research Project, Volume 4, Hominid Cranial Remains. Clarendon Press, Oxford.
Dental growth in early Homo
Dean and colleagues (2001) present a study of perikymata counts of anterior teeth (incisors and canines) in early humans and australopithecines, compared to extant apes and humans. The basic microanatomy of teeth and their process of development is briefly described in this write-up about Afropithecus.
The operating assumption that makes this study interesting is that "brain size, age at first reproduction, lifespan and other life-history traits correlate tightly with dental development" (628). Of course, this is true not only of dental development but all these other traits with each other and with others (most notably, body mass), since these kinds of "correlations" are really interspecies allometries of one kind or another. But the interesting thing is the apparent deviation of dental development rates in humans from other hominoid species. We take longer to grow our dental enamel, and this difference is likely to reflect a difference in the rate of growth or maturation:
Modern human enamel develops along a slower trajectory because the earliest-formed enamel, closest to the enamel dentine junction, is secreted in smaller increments for a longer time period. None of the trajectories of enamel growth in apes, australopiths of fossils attributed to Homo habilis, Homo rudolfensis or Homo erectus falls within that of the sample from modern humans (628-629).
Despite considerable variation in external tooth morphology, early fossil hominins share a common and fundamental enamel growth trajectory with the African ape clade that is derived in modern humans. (629).
It is now generally held that a prolonged life-history schedule reflects a reduction in the mortality rate of adults, triggered perhaps by behavioural, dietary or other changes. An increase in brain size (and cognitive ability) is associated with this reduction, but does not necessarily drive it, even in the human lineage. The size of key brain components associated with learning and cognition correlates with the timing of dental development in primates as the cost in time needed to grow and learn to use a larger brain increases. In this context a slower trajectory of enamel growth in permanent teeth, one of the basic determinants of tooth formation time, can be regarded as a life-history attribute associated with the extended, or prolonged, growth period of modern humans. The first evidence for a shift in enamel growth rates in the hominin fossil record seems to be with the origin of the larger-brained Neanderthals (at least by 100 kyr ago; see Tabun specimen C1 in Fig. 1) and modern humans (629-630).
Dean and colleagues also posit that the dental development data for specimens attributed to Homo habilis and/or Homo rudolfensis are consistent with an assignment to Australopithecus. Certainly the data do not contradict such an assignment, since there is no apparent difference between australopithecines, early humans, or any of the habilines in the study. Of course, the data also do not contradict the assignment of KNM-WT 15000 to Australopithecus -- they are just uninformative about taxonomic assignment. The key here is that the enamel formation times of the teeth show that early humans were essentially australopithecine-like in their dental development; and that both kinds of hominids were basically apelike.
The authors promote an interesting linkage between dental development times and brain size expansions:
If correct, these estimates of molar emergence times have shifted a little, in step with brain size, from those known for African great apes and australopiths. Nevertheless, it now seems increasingly likely that a period of development truly like that of modern humans arose after the appearance of H. erectus, when both brain size and body size were well within the ranges known for modern humans (630).
This is not to say that dental development times determine brain sizes or vice versa, but that the processes that promote delayed maturation connect both of these features. I would suggest that this connection might involve a genetic correlation between dental maturation and brain size that altered both characters with selection on overall maturation rate. If a prolongation of juvenile growth was a product of selection acting on social learning, then both slower growth and larger brains may have emerged in concert with each other.
The interesting part of this potential linkage is that growth may not have reached its modern rate 2 million years ago, but instead may have continued to change as brain sizes increased during the Middle and Late Pleistocene. That scenario is consistent with the dental development patterns in this study. In that perspective, this study can be chalked up in a list of ways early Homo was not very much like modern humans in its adaptive pattern.
References:
Dean C, Leakey MG, Reid D, Schrenk F, Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern humans from Homo erectus and earlier hominins. Nature 414:628Ð631. Nature online
Tilting at absent Asian australopithecines
In Nature a couple of weeks ago, Robin Dennell and Wil Roebroeks had a provocative paper exploring the possibility that early humans (i.e. Homo erectus) originated in Asia rather than Africa.
The paper is all speculation of course; there is no evidence of any earlier hominid in Asia.
But it is the good kind of speculation. Although maybe not quite this big:
Most probably, we are on the threshold of a profound transformation of our understanding of early hominin evolution that might prove as far-reaching as the demise of the notion of Man the Hunter in the early 1960s (Dennell and Roebroeks 2005:1103).
Here's the abstract:
The past decade has seen the Pliocene and Pleistocene fossil hominin record enriched by the addition of at least ten new taxa, including the Early Pleistocene, small-brained hominins from Dmanisi, Georgia, and the diminutive Late Pleistocene Homo floresiensis from Flores, Indonesia. At the same time, Asia's earliest hominin presence has been extended up to 1.8 Myr ago, hundreds of thousands of years earlier than previously envisaged. Nevertheless, the preferred explanation for the first appearance of hominins outside Africa has remained virtually unchanged. We show here that it is time to develop alternatives to one of palaeoanthropology's most basic paradigms: 'Out of Africa 1' (Dennell and Roebroeks 2005:1099).
It is worth reviewing exactly what "Out of Africa 1" is supposed to be. The paradigm is that emergence of hominids from Africa required increases in brain size and/or body size, coincident with the emergence of hominids like KNM-ER 3733, KNM-WT 15000, and others. The motivation for this hypothesis is simple: australopithecines have not been found outside of Africa. Nor has anything like Homo habilis, which is australopithecine-sized but has larger brains.
Of course, it is questionable just how basic this paradigm is. Consider what I (and my colleagues) were able to write only seven years ago:
The problem is that significant range expansion out of Africa occurred a half million years or more later than the first H. sapiens [corresponding to others' H. erectus or H. ergaster]. Population size before then may have remained small, and this is not an inconsequential time span, being one quarter of the time H. sapiens has existed. An important date in behavioral evolution is 1.5 MYA because it is marked by the earliest appearance of the Acheulean, the ubiquitous hand-axe industry of the Early and Middle Pleistocene.... Before this time, humanity was limited to Africa and immediately adjacent sections of Asia such as the Levant (Hawks et al. 2000:7).
Evidence for large body size in Late Pliocene humans (notably KNM-WT 15000 but also many others) made it very plausible that larger bodies were necessary for dispersal from Africa. But without good evidence for such dispersal before around 1.4 million years ago (and arguably not before 1 million years), larger bodies could not be assumed to be a sufficient condition for dispersal. Writing about the origin of humans, we had to consider all these alternatives -- at a time when the Dmanisi sample consisted of a single uncertainly dated mandible and the Mojokerto date stood alone with very questionable provenience.
Now we know that hominids did leave Africa by at least 1.8 million years ago. Dmanisi has almost singlehandedly changed the perspective.
And in doing so, it made much more convenient the hypothesis that large body size was both necessary and sufficient for dispersal from Africa. If the date of dispersal and the date of human origins are the same, then it is natural to propose that the coincidence is more than chance.
I would say this is more of a convenient hypothesis (and an easy story to tell) than it is a basic paradigm. The idea that large body size caused dispersal from Africa may have been a local minimum in terms of parsimony (at least as long as the body size of the Dmanisi fossils was not known), but it was only one alternative among many still in play.
And it remains a plausible hypothesis -- after all, the Dmanisi remains are a bit larger than australopithecines, and they might well have shrunk from a larger early-human-like size after reaching Asia instead of before.
But Dennell and Roebroeks give motivations for examining some alternatives.
The only reason why the earliest tool assemblages in Asia are attributed to H. erectus s.l. is that palaeoanthropologists have already decided that, in effect, it was the only hominin capable of migration out of Africa, and with sufficient Wanderlust to do so (Dennella and Roebroeks 2005:1099).
Homo erectus sensu lato (s.l.) means Homo erectus "in the loose sense", which would include not only the "strict sense" (sensu stricto) H. erectus. from Java and China, but also hominids like OH 9 and KNM-ER 3733 from Africa, and presumably the Dmanisi hominids.
A long passage reviews the total faunal evidence from Asia during the Late Pliocene. The thrust of the passage is that there are very few sites with extensive fauna, and of these most preserve mainly large-bodied herbivores. There are a few hints that a hominid-friendly fauna may have existed, including the presence of baboons. But there are no hominids of any kind at the vast majority of Asian localities -- Dmanisi is a real exception in the Plio-Pleistocene record.
This is the key taphonomic argument: if we have only found Early Pleistocene humans from continental Asia within the past ten years, then how can we preclude there having been australopithecines there? Dennell and Roebroeks argue that if there were australopithecines, we shouldn't necessarily expect to have found them yet -- we just haven't looked extensively enough.
A close read of the section raises a caution, though. One of the main arguments for the incompleteness of the Asian record is that sites don't preserve each others' fauna.
It is also likely that the full range of taxa is incomplete for the Indian subcontinent, because Megantereon and Pachycrocuta are not recorded in India but are present in Pakistan; in Pakistan, there is no evidence of Camelus and small primates, and in neither country is Homotherium recorded, although this is present to the west at Dmanisi, to the north at Kuruksay, central Asia and to the east at Longuppo, south China (Dennell and Roebroeks 2005:1100).
Of course, all of these species are recorded in Asia taking all the sites in aggregate; this is hardly an argument for the overall weakness of the record -- just an argument that no individual site is an adequate record of the continent's fauna.
To me, the important question is not whether australopithecines as currently known from Africa were in Asia. A more troubling possibility is that the australopithecines that we now know from Africa were not the only (or main) manifestations of early hominids in Africa. Large parts of Africa that we might expect to be congenial to hominids, like the Zambesi basin, have few or no fossils at all. The recovery of the Bahr el Ghazal mandible (Brunet et al. 1994) certainly makes clear that hominids were living across a much larger area than we have adequately sampled. But that mandible is, although not identical, certainly very similar to known contemporary hominids in its adaptation.
The question is whether hominids had adapted to other ecologies that are much less satisfactorily sampled than the East African rift. They probably weren't living where chimpanzee and gorilla ancestors did, but where else might they have been? Some such ecologies -- like the coasts -- would make early dispersal very plausible.
(In this regard, early humans are not the only hominids who lack a satisfactory ancestor. Who was the ancestor of A. aethiopicus? In what ecology did the first robust hominid arise?)
So what is the broader set of hypotheses that we should consider? Dennell and Roebroeks suggest:
If the above taphonomic review suggests that we cannot show the absence of hominins from areas in Asia at a time before the little evidence we have indicates their presence, we need to consider alternatives to the current Out of Africa [that is, their "Out of Africa 1"] model. There are three issues here. The first is when hominin(s) first left Africa -- might they, for example, have left shortly after they acquired the ability to make stone tools, the earliest of which are currently 2.6 Myr old? Or could they have left even earlier, about 3.0Ð3.5 Myr ago, when some australopithecines were already living in the African grasslands? The second issue is whether we yet know the full range of hominins that inhabited both Africa and Asia in the Late Pliocene and Early Pleistocene. Even in east Africa, several new taxa have been claimed in the past decade (for example, A. anamensis, A. garhi, Ardipithecus ramidus and Kenyanthropus platyops) and doubtless more will be found. (An indication of how little we know about Pleistocene east Africa is that only recently has the first fossil evidence for chimpanzee been found.) In Asia, the recent discoveries of H. georgicus and H. floresiensis should make us very wary of assuming that H. erectus s.l. was the only player on the Asian stage in the Early Pleistocene. Third, Asia might not have been the passive recipient of whatever migrated out of Africa but might have been a major donor to speciation events, as well as dispersals back into Africa. Such two-way traffic is well documented for other mammals in the Pliocene and Early Pleistocene, such as Equus and bovids, with more taxa migrating into than out of Africa. There is no reason why hominin migrations were always from Africa into Asia, and movements in the opposite direction might also have occurred, as has been suggested for the Olduvai OH9 (refs 13, 58) and Daka specimens. We should even allow for the possibility that H. ergaster originated in Asia and perhaps explain its lack of an obvious east African ancestry as the result of immigration rather than a short (and undocumented) process of anagenetic (in situ) evolution (Dennell and Roebroeks 2005:1100-1101).
Of course, most of the evidence indicating the presence of hominids is not fossil but archaeological. On this topic, Dennell and Roebroeks have much to say:
Any stone tool assemblage in Asia dated as older than 1.9 Myr ago (the earliest date that Homo is supposed to have left Africa) is either dismissed or (more usually) ignored; undated Oldowan tools are assumed to date from after 1.9 Myr ago and not from 2.6 Myr ago (the date of their first appearance in east Africa); and stone tool assemblages in Asia dated to the Olduvai Event (1.77Ð1.95 Myr ago) and not associated with hominin remains are automatically attributed to Homo erectus s.l. However, there is no reason why Oldowan assemblages in Arabia cannot be older than 1.9 Myr old, or why the tools from Ain Hanech (Algeria) or Erq el Ahmar (Israel) were made by H. erectus s.l. [instead of other hominids] (ibid:1102, references omitted).
There is a section about what exactly absence of evidence can tell, a short critique of using continents as proxies for biogeographic units:
As noted earlier, Pliocene grasslands extended all the way from west Africa to north China, and 'Savannahstan' might prove a more useful spatial unit for modelling early hominin adaptations and dispersals within them than simply an undifferentiated 'Africa' or 'Asia'. For example, the African hominins 1.9Ð1.7 Myr ago at Koobi Fora (Kenya) and Ain Hanech (Algeria), and their slightly later counterparts in Asia at 'Ubeidiya (Israel), and Majuangou (north China) were all living in broadly comparable grassland environments, and it makes sense to place them within the same frame of reference.
I think there is much of value to consider here; but it is less a revolution and more a statement of the field in transition. There are also alternatives that are not considered in this paper but that may be equally plausible -- most notably, the idea that early humans themselves may have been substantially polymorphic (witness KNM-ER 42700), or that brain size rather than body size may have been a prerequisite to dispersal (since habilines, Dmanisi, and H. erectus s.l. are all allometrically similar in brain size).
National Geographic News also has an article about the paper.
References:
Dennell R, Roebroeks W. 2005. An Asian perspective on early human dispersal from Africa. Nature 438:1099-1104. Full text (subscription)
Hawks J, Hunley K, Lee S-H, Wolpoff M. 2000. Population bottlenecks and Pleistocene human evolution. Mol Biol Evol 17:2-22.
Tooth wear in early Homo
Discovery News has an article summarizing some of Peter Ungar's recent work on tooth anatomy and wear in early Homo.
The study suggests Homo habilis, which some researchers have nicknamed "the handy man" because this species made the first known stone tools, was more of a fruit and veg eater than the apparent omnivore Homo erectus.
Teeth for the latter had greater numbers of pits, while handy habilis teeth had more striations suggestive of pulling down on fruit and leaves.
"Both of the species would probably have focused on high energy-yield, easy-to-consume foods, such as soft fruits when they could get them," Ungar told Discovery News. "The differences between H. habilis and H. erectus suggest that the latter may have focused a bit more on tough foods. They could have been meat, tough tubers or other items."
This is the most-studied dietary transition in human evolution, and it looks like the answers are getting more solid.
Mojokerto site rediscovered?
An upcoming paper in Journal of Human Evolution by O. F. Huffman and colleagues reports on a possible location for the Mojokerto skull. A 1994 paper by Carl Swisher and colleagues dated rock from the supposed site to 1.81 million years ago.
This paper finds that the real site is a bit above that dated horizon. The abstract:
The fossil calvaria known as the Mojokerto child's skull was discovered in 1936, but uncertainties have persisted about its paleoenvironmental context and geological age because of difficulties in relocating the discovery site. Past relocation efforts were hindered by inaccuracies in old base maps, intensive post-1930s agricultural terracing, and new tree and brush growth. Fortunately geologic cross sections and site photographs from 1936-1938 -- not fully utilized in past relocation fieldwork -- closely circumscribe site geography and geology. These documents match the conditions at just one sandstone outcrop. It is situated on the southern margin of a topographic nose at the upper end of a 18 m-wide gully (0663760 m E, 9183430 m N, UTM Zone 49M), 15 m southeast of the Kumai et al. (1985) relocation. The relocated discovery bed is 3.3 m of fossiliferous pebbly sandstone, a river-channel deposit cut into tuffaceous mudstone. The sandstone and mudstone beds correspond to original site descriptions. Pebbly sandstone is also found within the skull.
The calvaria is well-preserved and taphonomically similar to large and fragile specimens found among several hundred vertebrate fossils excavated from the sandstone in 2001-2002. Since no well-preserved fossils were found intact at the surface of the sandstone, the good condition of the Mojokerto skull suggests that it was buried fully when discovered. The relocated hominin bed is the uppermost fluvial sandstone of a marine-deltaic sequence in the upper Pucangan Formation. The Mojokerto child probably died along the ancient seacoast, judging from the large extent of the deltaic facies and evidence that the calvaria experienced minimal transport. The relocated discovery bed is 20 m stratigraphically above the horizon from which the widely cited 1.81 +- 0.04 Ma 40Ar39Ar date for the skull (Swisher et al., 1994, Science 263, 1118) was obtained. Additional field and laboratory results will be required to determine the skull's age.
The paper gives a good history of attempts to find the original excavation site. An interesting heterogeneity of the matrix fill inside the skull (assessed by CT) also factors in the story.
After a long discussion of the complexities in dating the site, they conclude:
In summary, additional field and analytical results are needed to date the Mojokerto fossil more exactly than latest Pliocene or early-mid Pleistocene in age. The 0.3 Ma difference between the 40Ar/39Ar and fission-track age determinations must be resolved. For any of these radioisotopic dates to be considered other than a maximum age, better evidence must be advanced to show that the dated material was erupted shortly before deposition at Perning. Additional paleontological and magnetostratigraphic control and radioisotopic dating would seem to be required. Geochronological conclusions have to be evaluated further in terms of the potential for temporal stratigraphic breaks in the section, rates of deposition, and the regional stratigraphic (including sequence stratigraphic) context.
I don't suppose there will ever be a very good date for the specimen. But it's impressive the amount of work there has been on it in the past several years.
References:
Huffman OF, Zaim Y, Kappelman J, Ruez DR Jr, de Vos J, Rizal Y, Aziz F, Hertler C. 2006. Relocation of the 1936 Mojokerto skull discovery site near Perning, East Java. J Hum Evol (in press). DOI
Swisher CC 3rd, Curtis GH, Jacob T, Getty AG, Suprijo A, Widiasmoro. 1994. Age of the earliest known hominids in Java, Indonesia. Science 263:1118-1121. PubMed
John Hawks Department of Anthropology
University of Wisconsin—Madison
Copyright © 2007 John Hawks