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The Context of Human Genetic Evolution Robert Foley1 Downloaded from genome.cshlp.org on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press PERSPECTIVE The Context of Human Genetic Evolution Robert Foley1 Human Evolutionary Biology Research Group, Department of Biological Anthropology, and King’s College Research Centre Human Diversity Project University of Cambridge, Cambridge, CB2 3DZ, UK The debate on modern human origins has often focused on the relationship between genes and fossils. Although more and more genetic evidence has been accumulating in favor of a recent African origin for modern humans, it has been assumed by many that the fossil evidence remains ambiguous. On the contrary, it has been clear for some time that the fossil evidence does not support the multiregional model: Fossils and archeology indicate a pattern of multiple dispersals from and beyond Africa, against which the genetic data can be compared. The continuing value of paleobiology is in complementing genetic information by revealing the context of human evolution: locating the dispersals and extinctions of populations in time and space, correlating these events with the environmental forces that shaped them, and providing an increasingly detailed understanding of the morphology and technology of early humans. Molecular biology has revolutionized the study of relatively small population (effective population human evolution. The importance of fossils as the size between 5000 and 50,000 individuals) (Rogers primary source of information about our past has and Harpending 1992; Harpending et al. 1993; Nei been steadily undermined as it has become possible and Takahata 1993; Harpending 1994). That size to infer detailed aspects of recent human history represents a bottleneck in the hominid lineage dat- from the distribution and frequency of genes found ing back no more than 200,000 years (Cann et al. around the world today. To some extent, a fusion of 1987; Stoneking et al. 1992), with evidence of de- paleontological and genetic approaches came about mographic expansion occurring in the last 70,000 last year with the extraction and sequencing of an- years (Rogers 1995). cient DNA from an extinct hominid, the Neander- This emerging consensus has been interpreted thal type specimen (Krings et al. 1997), but this is in evolutionary terms as evidence for a recent Afri- likely to remain a rarity. Ancient DNA, however, has can origin (i.e., ∼200,000 years ago) for modern hu- been able to confirm that humans and Neander- mans, followed by a dispersal out of Africa, with thals belonged to different populations over the last little or no interbreeding with other populations of quarter of a million years and that Neanderthals did hominid. Many anomalies and further details re- become effectively extinct. main to be sorted out. The geographical clades of These results fit in with an increasingly consis- the mtDNA have been questioned (Maddison 1991; tent interpretation of human evolutionary genetics. Maddison et al. 1992), and it has been suggested Compared with chimpanzees and other apes, the that much of the genetic evidence is consistent with human population is relatively lacking in genetic a number of different models (Templeton 1992, diversity (Ruvolo et al. 1993); such genetic variation 1993). Furthermore, tree building and mismatch as does exist occurs primarily within populations techniques, the primary means of turning genetic rather than between (Relethford and Harpending information into evolutionary history, have been 1994); African populations are more diverse geneti- subject to dispute (Templeton 1992, 1993). Finally, cally than those found anywhere else in the world estimates of the coalescence time of human b- (Vigilant et al. 1991; Cavalli-Sforza et al. 1994; Wat- globin genes (∼800,000 years) have also been used son et al. 1997); and for the most part, non-African to argue against a recent African origin for modern patterns of genetic variation can be treated as a sub- humans (Fullerton et al. 1997), but they are not, in set of African ones. The chronological and demo- fact, inconsistent with the recent-origin model, as graphic context of the processes of diversification the coalescence time for a neutral autosomal locus has been strongly disputed, but several genetic sys- would be expected to be roughly four times that of tems indicate that living populations derive from a a mitochondrial gene, and selection may also play a confounding role. Such disputes, though, should perhaps not dis- 1E-MAIL [email protected]; FAX 44 (0) 1223-335460. tract from the general pattern: Genetics supports a 8:339–347 ©1998 by Cold Spring Harbor Laboratory Press ISSN 1054-9803/98 $5.00; www.genome.org GENOME RESEARCH 339 Downloaded from genome.cshlp.org on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press FOLEY single recent African origin for modern humans. gional model and have allowed the debate on the This consensus leads to two important questions: origin of modern humans to persist. However, it is First, what is the relationship between this evidence worth summarizing the results of some recent stud- and the fossil evidence that it has been claimed, ies that bear on this issue. supports the so-called multiregional model? And more broadly, what can paleoanthropology contrib- ute to a field where the bulk of the resources is being Australian Populations and Homo erectus in put into genetics? The answer to the first question is Southeast Asia that it has been clear for a long time that the mor- The most often cited evidence for continuity out- phological evidence does not support a multire- side Africa is that between modern Australian popu- gional view. However, this has not percolated lations and the later specimens of Homo erectus, the through to the genetic community. This apparent Ngangdong sample from Java (Fig. 1). Australians lack of communication between the two disciplines are supposed to share with the late-surviving H. erec- can be used to help provide an answer to the second tus a number of cranial traits (Larnach and Macin- question: that paleobiology provides a different sort tosh 1974; Wolpoff et al. 1984). Upon superficial of evidence, one that focuses specifically on the visual comparisons, Ngangdong and some recent context in which human genetic evolution oc- Australian specimens may appear similar, but it is curred. These themes will be developed below. misleading to interpret this as part of a unique evo- lutionary relationship. First, the earliest known Aus- Multiregional Evolution tralian fossils, those from Mungo, are quite gracile and do not show these traits (Brown 1987). The later The multiregional model of human evolution has a ones, like Kow Swamp and Keilor, are very diverse, long history. It was first proposed by Franz Weiden- implying that some became more robust with time reich (1943) in relation to his analyses of the Peking (Lahr 1996). Second, new dates indicate that Ngang- Man fossils but has been further developed and pro- dong may be as young as 50,000 years; if this is the moted in recent years by Milford Wolpoff and Alan case, then the supposed source population persisted Thorne (Wolpoff et al. 1984). The essence of this unchanged long after the origins of the Australians. model is that since the origin of Homo some two Third, the few characters that Australian popula- million years ago, the human lineage has evolved as tions do share with with Southeast Asian H. erectus a single lineage, without speciation events (Wolpoff are also found in the early modern human fossils of and Caspari 1997). Within this lineage there would Eastern Africa (Omo Kibish) and the Levant (Skhul, have been universal directional trends in characters Qafzeh) (Lahr 1996), and metrically, the most such as brain size, but regional differences in popu- ‘‘primitive’’ of the Australian fossils (the Willandra lations would have persisted. Over time, therefore, Lakes specimen WLH50) falls closest to the African some specific morphological traits would persist in transitional or early modern specimens (Stringer particular regions, regardless of other global trends; 1998). These African specimens, however, also have the human lineage thus evolved in several regions modern proportions of the skull, unlike those found (multiregionality). This continuity has been seen to in Ngangdong that are essentially archaic and thus extend to the transition from archaic to modern fall closer to Australians and represent a better an- hominids in Africa, Asia, and Europe, the last of cestral model (Groves and Lahr 1994). In other these being the link between Neanderthals and words, where Australian populations look like ar- modern Europeans. The multiregional model is chaic ones, it is those on the cusp of modernity in therefore largely inconsistent with the general in- Africa that they resemble most (Fig. 1). terpretation of the genetic evidence, requiring that the effective population size of the human lineage was always large enough for gene flow to occur glo- Regional Continuity Traits bally and that coalescence times for most genes Central to the support for multiregional evolution is would be in excess of a million years. the notion that certain anatomical traits show a per- sistence and uniqueness within regions, regardless Paleontological Support for a Single-Origin Model of the time of the specimens. These are the so-called continuity traits (Wolpoff et al. 1984). Three re- A number of paleontological observations have gional groups are usually discussed: Australian, East been consistently quoted as supporting the multire- Asian, and European. In practice, it is the first two of 340 GENOME RESEARCH Downloaded from genome.cshlp.org on October 3, 2021 - Published by Cold Spring Harbor Laboratory Press CONTEXT OF HUMAN GENETICS EVOLUTION Figure 1 Fossil modern hominid skulls from Australia and Africa, com- pared with the H. erectus Ngangdong skull from Java. (A) Cast of Ngang- dong, (B) Lake Mungo 3 (Australia); (C) Willandra Lakes 50 (WLH-50, Aus- tralia); (D) Kow Swamp (Australia): (E) Keilor (Australia); (F) Ngaloba (African transitional); (G) Omo Kibish (early modern African).
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