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Nonhuman Primate Hybridization and the Taxonomic Status of Neanderthals

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Nonhuman Primate Hybridization and the Taxonomic Status of Neanderthals AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 115:157–166 (2001) Nonhuman Primate Hybridization and the Taxonomic Status of Neanderthals Michael A. Schillaci* and Jeffery W. Froehlich Department of Anthropology, University of New Mexico, Albuquerque, New Mexico 87131 KEY WORDS Sulawesi macaques; Neanderthals; hybridization; modern human origins; genetic distance; R matrix; FST ABSTRACT The present study examines the taxo- nificantly greater than those observed both between hy- nomic status of Middle Paleolithic Neanderthals by com- bridizing and noninterbreeding Sulawesi macaque paring their observed minimum genetic divergence from species, suggesting that mate recognition and the possi- Upper Paleolithic modern humans in Europe with that bility of gene flow between Neanderthals and Upper Pa- observed between macaque species from Sulawesi that are leolithic modern humans might have been greatly re- known to hybridize and fully intergrade in the wild. The duced. These results support a species-level taxonomic genetic divergence, and differentiation between Neander- distinction for the Neanderthals as suggested by propo- thals and Upper Paleolithic modern humans, as indicated nents of the replacement model. Furthermore, assump- by pairwise minimum genetic distances and FST values tions regarding the monophyletic origin of modern hu- calculated from the estimated minimum genetic relation- mans from outside Europe are likely valid. Am J Phys ship (R) matrix derived from craniometric data, are sig- Anthropol 115:157–166, 2001. © 2001 Wiley-Liss, Inc. The origin of anatomically modern humans has placement model, however, requires a relatively been the subject of considerable recent debate in the abrupt displacement of regional archaic human pop- anthropological literature (for overview, see Frayer ulations in Europe and Asia by morphologically, cul- et al., 1993; Smith et al., 1989; Straus, 1995; turally, and behaviorally distinct anatomically mod- Stringer, 1992; Wolpoff, 1992). Much of this debate ern humans, presumably from Africa (Stringer and centers on the various interpretations of morpholog- Andrews, 1988; Stringer and Gamble, 1993). Hy- ical (i.e., genetic) affinity among the Middle and potheses regarding mate recognition and gene flow Upper Paleolithic hominid fossils, and the origin(s) between Middle Paleolithic Neanderthals and Up- of anatomically modern humans in Europe. Deter- per Paleolithic modern humans are typically re- mining to what extent, if any, the Middle Paleolithic jected by supporters of the replacement model Neanderthals of Europe contributed to the Upper (Cann, 1987, 1988; Cann et al., 1987). The third Paleolithic modern human gene pool has been a model allows for the possibility of limited admixture, subject of recent investigation by Turbo´n et al. or hybridization, between Neanderthal populations (1997). The answer to this particular question has and modern humans dispersing into Europe (cf. obvious taxonomic and phylogenetic implications. Bra¨uer, 1984; Duarte et al., 1999; Simmons, 1994, Using a species definition fostered by the biological 1999; Smith and Trinkaus, 1991). species concept, any gene flow between Middle Pa- The debate fostered by the replacement and mul- leolithic Neanderthals (Homo neanderthalensis) and tiregional models has incorporated archaeological anatomically modern humans (Homo sapiens) would (d’Errico et al., 1998; Hublin et al., 1996; Klein, imply they were conspecific. Conversely, the absence 1992; Mellars, 1989), morphological (Pearson, 2000), of measurable gene flow implies a species-level dis- molecular (Krings et al., 1997, 1999; Ovchinnikov et tinction for the Neanderthals, allowing for a mono- al., 2000; Scholz et al., 2000), and quantitative ge- phyletic origin for anatomically modern humans netic (Relethford, 1998; Relethford and Harpending, outside of Europe. Briefly, the participants in this debate typically lend support to one of three models: 1) the multire- Grant sponsor: Sigma Xi; Grant sponsor: University of New Mexico gional model, 2) the replacement model, and 3) an School of Graduate Studies; Grant sponsor: University of New Mexico admixture model. The multiregional model assumes Student Research Allocation Committee. phyletic gradualism from archaic Homo sapiens to *Correspondence to: Michael A. Schillaci, Department of Anthro- anatomically modern humans, with continuing gene pology, University of New Mexico, Albuquerque, NM 87131. flow between Neanderthals and Upper Paleolithic E-mail: [email protected] modern human populations likely (e.g., Frayer et al., 1993; Wolpoff, 1989; Wolpoff et al., 1984). The re- Received 19 November 1999; accepted 15 March 2001. © 2001 WILEY-LISS, INC. 158 M.A. SCHILLACI AND J.W. FROEHLICH 1994) perspectives. Results presented by recent mo- per Paleolithic modern humans from Europe and lecular and morphometric studies seem to indicate recent modern human samples. The divergence of that Neanderthals were genetically distinct from Neanderthals, the authors argued, supports the re- anatomically modern humans, and that gene flow placement model by indicating a monophyletic ori- between these congeners was curtailed (Krings et gin for Upper Pleistocene modern humans in Eu- al., 1997, 1999; Ovchinnikov et al., 2000; Scholz et rope, independent (genetically) of Neanderthals. al., 2000; Turbo´n et al., 1997; but see Norborg, Although Turbo´n et al. (1997) presented a cogent 1998). argument for the distinctiveness of the Neander- thals, what is unclear from their discussion is how MORPHOMETRIC DATA AND BIOLOGICAL morphological distinctiveness is deemed taxonomi- DISTANCE cally significant. Moreover, how much observed mor- phological divergence is needed to demonstrate rel- The use of morphometric data to assess genetic ative genetic isolation between Neanderthals and relationships among human and nonhuman primate Upper Paleolithic modern humans? populations is common within biological anthropol- Questions such as these regarding morphology ogy. Although measurement values for metric traits and genetic isolation in the human and nonhuman are a product of both hereditary and environmental primate fossil record should be addressed through factors, research presented in the anthropological empirical study of reproduction and morphology literature concerning human quantitative genetics among extant primate taxa (see Prat, 2000a,b; Sim- indicates a moderate degree of genetic control for mons, 1994, 1999). Determining what level of mor- many head and face measurements (Hiernaux, phological divergence corresponds to genetic isola- 1963; McHenry and Giles, 1971; Osborne and De- tion among hominid fossils can be accomplished by George, 1959; Devor, 1987; Susanne, 1977). Susanne evaluating the level of divergence between morpho- (1977), for example, presents narrow-sense herita- logically distinct extant primate species with, and bility values (h2) ranging between 0.391–0.715 for without, known hybrids. The anthropological litera- 19 head and face measurements, based on a study of ture is replete with reports of natural hybridization Belgian families. Devor (1987) reports an average occurring between morphologically and genetically narrow-sense heritability of 0.55 for head and face distinct primate taxa, such as the reported hybrid- measurements. This relatively high level of herita- ization between Papio hamadryas anubis and bility demonstrates the utility of craniometric vari- P. h. hamadryas (Phillips-Conroy and Jolly, 1986; ables in genetic distance studies. Phillips-Conroy et al., 1991), between Hylobates Previous research muelleri and H. albibarbis (Marshall and Sugard- jito, 1986), between H. lar and H. pileatus (Brockel- Multivariate and quantitative genetic analyses of man and Srikosamatara, 1984), and between karyo- morphometric data are increasingly being used in typically distinct subspecies of Lemur fulvus human paleontology to investigate the origins of (Tattersall, 1993). modern humans and to estimate historical relation- Hybridization has also been reported among the ships among Pleistocene hominids (e.g., Donnelly et highly variable Sulawesi macaque taxa (Bynum et al., 1998; Kidder, 1999; Kidder et al., 1992; Releth- al., 1997; Ciani et al., 1989; Froehlich and Supri- ford and Harpending, 1994; Turbo´n et al., 1997). atna, 1996; Groves, 1980; Watanabe and Ma- Recently, Turbo´n et al. (1997) claimed a monophy- tsumura, 1991; Watanabe et al., 1991a,b). The ex- letic origin for modern humans in Europe, “indepen- amples of macaque hybridization from Sulawesi are dent of the Neanderthals, whose morphological particularly interesting because the morphological traits in the face are clearly distinct from those variation among the seven macaque taxa endemic to modern human populations analyzed,” based on a this island (Fig. 1) equals or exceeds that of all other discriminant analyses of Lower, Middle, and Upper non-Sulawesi macaque species according to Albrecht Paleolithic fossils, as well as Iberian Mesolithic and (1978). Despite significant differences in character recent modern human samples. This study was traits such as pelage patterning, size and shape of based on a discriminant analysis of the first three the gluteal fields, female sexual swelling, body size, principal components calculated from a covariance and various facial measurements (Bynum et al., matrix derived from the measurement values of 25 1997; Froehlich and Supriatna, 1996; Froehlich et craniofacial variables. Because the raw data were al., 1999; Supriatna, 1991), all of which
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