Levels of the genealogical hierarchy and the problem of hominoid phylogeny

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 94:81-88 (1994)

Levels of the Genealogical Hierarchy and the Problem of Hominoid Phylogeny

JEFFREY ROGERS Department of Genetics, Southwest Foundation for Biomedical Research, Sun Antonio, Texas 78228

KEY WORDS analysis

Molecular systematics, Evolution, DNA sequence

ABSTRACT Molecular data are widely used to reconstruct phylogenetic relationships among species, and these phylogenies are often used as the basis for inferences about the history of evolutionary change in other nonmolecular characters. This approach is an appropriate and powerful one in many circumstances. But when several lineages diverge over a relatively short period of time, the assumption that a molecular (gene) tree will always be a valid basis for such inferences may not hold. Empirical evidence from humans, nonhuman primates, and other mammals indicates that the relationships among molecular divergence, morphological differentiation, and the origin of reproductive isolation between diverging lineages are complex. The simple dichotomously branching trees that result from molecular systematic studies of Homo, Gorilla, and Pan may be a misleading basis for reconstruc- tions of evolutionary change in nonmolecular characters. 0 1994 Wiley-Liss, Inc.

There is general agreement that the last common ancestor of the genera Homo, Go- rilla, and Pan lived in Africa 5-10 million years ago. However, detailed knowledge of this ancestor and the historical processes that caused it to differentiate into three separate lineages continues to elude biological anthropologists. Reconstruction of the morphology of the last common ancestor depends on inferences from both the anatomy of the known hominoid taxa (living and ex- tinct) and the phylogenetic relationships among those taxa.

However, the phylogeny of the living Afri- can hominoids continues to inspire debate and disagreement. Several studies have suggested that chimpanzees are more closely related to humans than to gorillas (e.g., Koop et al., 1989; Caccone and Powell, 1989; Ruvolo et al., 1991; Begun, 1992; Ho- rai et al., 1992). Others have concluded that chimpanzees and gorillas are the most closely related, with the human lineage the outgroup (e.g., Andrews, 1987; Djian and Green, 1989). I have argued that the avail-

able data are not yet sufficient to support any definitive conclusion, and that the best reconstruction may be a trichotomy (Rogers, 1993; see also Smouse and Li, 1987; Hase- gawa and Kishino, 1991; Saitou, 1991). The acceptance of one phylogenetic tree over the others has implications for reconstruction of the ancestral morphology and other historical questions regarding the radiation of this clade. In the following discussion I address a question related to but separate from the issue of hominoid phylogenetic relationships: Regardless of the true branching order of the Gorilla, Pan, and Homo lineages, can molecular systematic data provide a reliable basis for inferences about the history of evolutionary change in nonmolecular characters during the earliest phases of this radiation?

Received February 1,1993; accepted July 21,1993

0 1994 WILEY-LISS, INC.

J. ROGERS 82

THE GENERAL PRACTICE OF MOLECULAR SYSTEMATICS

Until recently, DNA sequencing studies have been labor-intensive projects. As a result, most studies of hominoid molecular systematics have examined one copy of a given segment of DNA from each of several species (but see Ruano et al., 1992 for an exception). After determining a nucleotide sequence for each species, a tree relating these sequences to one another is con- structed using one or another analytical method (e.g., maximum parsimony or neigh- bor joining). The phylogeny of the species is then inferred directly from that reconstructed tree.

This standard approach addresses the question of phylogeny by investigating two hierarchical levels within biological systems: genes (or noncoding DNA sequences) and species. In essence, the phylogeny for several extant species is inferred directly from the reconstructed genealogy of ortholo- gous DNA sequences derived from a single sequence present in the common ancestor. There should be little doubt that this approach to molecular systematics is a powerful tool for evolutionary biology. In many circumstances, moderate amounts of nucleotide sequence from one individual of each of a number of taxa will be enough to determine the phylogenetic relationships among those taxa. For example, the relationships among Pongo, Homo, and Pan can be established with great confidence using this approach (Koop et al., 1989).

But biological systems consist of a genealogical hierarchy that has more than two levels: genes, individual organisms, demes or populations, species, and monophyletic groups (Vrba and Eldredge, 1984; Eldredge, 1985). The standard procedure of molecular systematics ignores the levels of individual organisms and populations, treating all systematic questions as issues of macroevolution, while drawing its basic data from the hierarchical level of genes (or DNA sequences). Ignoring the levels of organisms and populations is perfectly acceptable if analysis of one copy of one DNA sequence from each species will lead to correct conclu-

sions. However, since the intention is generally to use the phylogeny derived from molecular comparisons in subsequent analysis of nonmolecular characters, it is critical to be aware of the limitations of this strategy.

When a phylogenetic tree takes the form of several dichotomous branching events separated by relatively long internodal distances, the standard molecular approach will generally lead to robust conclusions. Mi- croevolutionary processes can be safely ignored. But if multiple branching events occur close together in time, then reconstruction of phylogenetic history is more difficult (Nei, 1987; Pamilo and Nei, 1988; Dut- rillaux et al., 1988; Rogers, 1993). In the case of the hominoids, one goal of molecular studies is to provide a basis for inferences about the last common ancestor and the earliest members of the descendent lineages. As a result, the value of any given gene tree (phylogenetic tree for a single segment of DNA) depends on a critical assumption that is not often explicitly acknowledged. The standard approach assumes that the branching order among lineages established by the analysis of DNA sequences is true for other characters (morphological, behavioral, etc.) that will be analyzed. Monophyletic groups established by the molecular data are accepted as valid for all other character state analyses.

This assumption of congruence across characters will be valid in many but not all cases. When the internodal distances in the phylogenetic tree are relatively short, the assumption will often be violated. One reason is that different biological processes occur a t the different levels of the genealogical hierarchy. Genes or short DNA sequences (short enough to preclude recombination as a significant process) evolve through mutation, either basepair substitution, insertion, or deletion. A gene tree will reflect the history of mutational changes that have occurred in the sampled descendents of a given DNA sequence. But populations undergo a wider variety of evolutionary changes, including genetic drift, gene flow, and others. A simple dichotomously branching tree can adequately represent the process of diversification of DNA sequences, but

GENEALOGICAL HIERARCHY AND HOMINID PHYLOGENY 83

populations can undergo reticulate evolution as a result of gene flow among partially isolated demes within a species.

In addition, the timescale of evolutionary change differs in the various hierarchical levels. A new mutation instantly creates a new lineage in a gene tree, but at the population level, replacement of one neutral allele for another requires an average of 4N generations, where N is the effective population size (Nei, 1987). Furthermore, the variance of this time to fixation for allelic substitutions is large, so that about 7.5N generations are required before there is a 95% probability that a new neutral allele will be fixed in a population by drift. For hominoids with effective population sizes on the order of 10,000 and generation times of about 20 years, a basepair mutation will cre- ate a new allele immediately, but it will take hundreds of thousands of years for that allele to become a fixed derived character of that lineage. This disparity means that a single population or species can simultaneously contain both ancestral and derived alleles at a locus, and that different populations of a species can have different combi- nations of ancestral and derived alleles in varying proportions. Analysis of a gene tree cannot fully reconstruct the potentially complex patterns of geographic and temporal population genetic structure in ancient taxa.

POTENTIAL COMPLEXITIES IGNORED BY GENERAL PRACTICE

This distinction between the hierarchical levels of genes and populations would not be a concern if the goal of molecular systematics were only to determine gene trees, i.e., to determine the relationships among DNA sequences. But in most cases the results of sequence comparisons will be used to make inferences about relationships among higher-level entities, populations, and species in various diverging evolutionary lineages. Furthermore, those inferences about population-level relationships will in turn be used as the basis €or conclusions about the history of other characters that were not investigated directly. There are four reasons to be skeptical of such conclusions when two

or more divergence events occur in a brief period, i.e., less than about 4N to 8N generations.

First, when branching events are close together in time, gene trees can contradict one another (Pamilo and Nei, 1988; Rogers, 1993). Consequently, even if the correct gene tree is established for one locus, that tree cannot be assumed to apply to all loci. The examples of mitochondrial DNA (Ru- volo et al., 1991; Horai et al., 1992) and involucrin (Djian and Green, 1989) or the pseudoautosomal regions of the X- and Y-chromosomes (Ellis et al., 1990) in the hominoids illustrate this process. Compari- sons of karyotypes across species of Cerco- pithecus also demonstrate this phenomenon (Dutrillaux et a]., 1988). The potential for inconsistency across loci means that several genes or loci should be examined before any inferences about population- or species-level relationships can be attempted (Rogers, 1993).

Second, genetic variability among populations within species can influence the topology of species-level phylogenetic trees. Smouse et al. (1991) analyzed mitochondrial DNA haplotypes in three populations from each of three species of North American fish, genera Luilus and Notropis. In all cases, genetic distances between populations were greater than variation within populations, though the latter was not trivial, and distances between species were larger than distances among populations within a species. Nevertheless, the species-level tree obtained for these taxa differed depending upon which population of each species was used. Clearly, inferences about historical relationships among evolutionary lineages must address issues of variability at several levels of the genealogical hierarchy.

Third, within species and between closely related species, molecular and overall genetic divergence among populations may not be a reliable reflection of the degree of morphological differentiation. Vigilant et al. (1989) examined mitochondrial DNA sequences in several human populations including two populations of African pygmies. The eastern pygmies from Zaire are more similar to Europeans in mitochondrial DNA

84 J. ROGERS

sequences than they are to western pygmies from the Central African Republic. Ruano et al. (1992) sequenced a segment of the HOX2B locus from humans, chimpanzees (Pan troglodytes), gorillas, and orangutans. There is greater DNA sequence difference between alleles found in various Gorilla individuals and between alleles found among individuals of Pan troglodytes than between one allele found in Pan and the only sequence found in humans. Both these studies indicate that divergence among DNA sequences at a single locus is not correlated in any simple manner with morphological sim- ilarity among the individuals or populations represented.

As more primate molecular data become available, more examples of high diversity within some species and smaller distances between species appear. Pongo pygrnaeus (Ferris et al., 19811, Macaca mulatta, Macaca nemestrina and Macaca assamensis (Melnick et al., 1992) all exhibit intraspecific mitochondrial DNA differences of 4.5% or more, yet the differences between Pan troglodytes and Pan paniscus (Ferris et al., 1981) and between rhesus macaques and Japanese macaques (Hayasaka et al., 1988) are less than 4%. Papio baboons are another group that exhibit no simple relationship between genetic and morphological divergence across populations (Williams-Blangero et al., 1990; Jolly, 1993). Levels of molecular variability are high in natural populations of baboons (Rogers and Kidd, 1993) and the available evidence regarding other species suggests that substantial DNA sequence diversity exists within many primate species.

Fourth, genetic divergence in general and DNA sequence divergence in particular are not necessarily reliable predictors of the possibility of genetic exchange between populations, i.e., of species boundaries as indicated by reproductive isolation. Thomomys townsendii is a species of pocket gopher na- tive to the southwestern United States. While the two are closely related, Thorno- mys townsendii is reproductively isolated from Thornornys bottae (Patton and Smith, 1989). Protein data suggest that several populations of Thomornys bottae are more closely related to Thomomys townsendii than to other populations of Thomornys bot-

tae, making Thomomys bottae paraphyletic (Patton and Smith, 1981). Hafner et al. (1987) have shown that Thomomys umbri- nus is probably also a paraphyletic species, demonstrating reproductive isolation between populations that are closely related while maintaining gene flow among less related ones. Avise et al. (1983) found that mitochondrial DNA haplotypes from southern and western populations of Perornyscus maniculatus are more similar to haplotypes from Peromyscus polionotus than they are to haplotypes from eastern populations of Per- omyscus rnaniculatus.

Though only a few groups have been examined in detail, such paraphyly seems to occur in primate species as well. Eastern populations of Macaca mulatta are more similar in mitochondrial DNA to Macaca fuscata than to western Macaca rnulatta, de- spite the high levels of nuclear gene flow that are believed to occur between eastern and western rhesus (Melnick et al., 1993). Similar discordance between mitochondrial phylogeny and species boundaries may occur in other macaques (Melnick et al., 1992). Analyses of chromosome evolution in species of the genus Cercopithecus suggest a complex history of population differentiation and genetic exchange during its evolutionary radiation (Dutrillaux et al., 1988). Given the observed differences among chromosomes, no simple bifurcating tree can represent the relationships among Cercopithecus species without very high levels of ho- moplasy. Harrison (1991) presents a review of the relationship between molecular differentiation and species boundaries, and God- frey and Marks (1991) have summarized information concerning discordance between morphological differentiation and genetic isolation among primate populations.

The four issues or problems described above demonstrate that the distinction between data at the level of gene trees and inferences about population relationships, morphological differentiation, or species boundaries is critical in analyses of hominoid evolution. It is clear that differentiation at one level is not perfectly correlated with differentiation at the others. Of course, there is one true species-level phylogenetic tree, and one true historical process of differ-

GENEALOGICAL. HIERARCHY AND HOMINID PHYLOGENY 85

entiation among populations. But while the species-level tree must be divergent, the population-level tree may be reticulate. Each independent gene or locus will also have its one true diverging tree, but it may not have the same topology as the species- level tree. Assuming perfect correspondence between trees at different levels when multiple branching events occurred close together may lead to spurious, or at least premature, conclusions.

IMPLICATIONS FOR THE STUDY OF THE HOMlNOlD DIFFERENTIATION

The molecular evidence suggests to some researchers that the time between the two divergence events that gave rise to the three African hominoid lineages may have been relatively short (Smouse and Li, 1987; Ha- segawa and Kishino, 1991; Saitou, 1991; Rogers, 19931, though several investigators have argued otherwise (Caccone and Powell, 1989; Ruvolo et al., 1991). Studies of comparative anatomy also suggest that the time separating the divergences was not long (Groves, 1986). If the time between the two branching events was in fact less than about 4N t o 6N generations (about 0.8-1.2 million years), then reconstruction of the true branching order of particular DNA sequences may not provide a reliable basis for inferences about the history of character state change during and subsequent to the separation of the three lineages.

In order to investigate clades whose con- stituent lineages are separated by short internodal distances, we will need to know much more about the relationships among molecular divergence, morphological differentiation, and the origin of reproductive isolation. Without such information, inferences about patterns of evolutionary change in nonmolecular characters that are based on the branching order of DNA sequences should be considered preliminary and sub- ject to revision. In other words, to reconstruct details of the evolutionary history of a clade consisting of several very closely related lineages, we must explicitly adopt a model of cladogenesis or speciation, a description of the mechanisms and correlates of the formation of new evolutionary lineages. Over the years, a number of specia-

tion models have been proposed (see Tem- pleton, 1980; Provine, 1989; Otte and Endler, 1989). But the debate concerning the diversification of the African hominoids has only rarely included discussion of the speciation process (e.g., Foley, 1989; Van Valen, 1989). On the other hand, the population-level processes involved in the origin of anatomically modern Homo sapiens have received considerable attention (see Temple- ton, 1993; Frayer et al., 1993; Aiello, 1993 for recent reviews).

With regard to the late Miocene differentiation of the modern Homo, Gorilla, and Pan lineages, different speciation models have different implications for the relationships among genetic divergence, morphological differentiation, and the origin of reproductive isolation. If we adopt one or another type of founder-effect speciation model (Car- son and Templeton, 19841, and add the assumption that morphological change occurs during the speciation process (see Gould, 19821, then we would predict a strong corre- lation between the timing of molecular divergence, morphological divergence, and the appearance of reproductive isolation. How- ever, vicariance speciation may be a more common process (Lynch, 19891, and the implications of this model for the correlations among genetic and anatomical differentiation are not so clear. Vicariance seems to be an attractive speciation model for the Afri- can hominoid case (Groves, 19861, especially if the last common ancestor was a forest- or woodland-living species with a geographic range that was fragmented by climatic changes. (I consider vicariance speciation to include the possibility that one widely dis- tributed species can be simultaneously di- vided into more than two isolated incipient lineages.) If the three lineages separated through habitat change and vicariance speciation, the true phylogeny may be a “hard” trichotomy (Maddison, 19891, rather than two separate divergences that have not yet been fully resolved (Smouse and Li, 1987; Rogers, 1993 and references therein). Of course, a variety of speciation models have been proposed (Otte and Endler, 1989; Provine, 1989) and should be considered.

Molecular studies generally depict the phylogeny of the African hominoids as a

86 J. ROGERS

simple dichotomously branching tree. The one ancestor is portrayed as differentiating into three descendent lineages, without ac- knowledgement of the potential complexity of the speciation process at the population level. Phylogenetic analyses tend to gener- ate simple tree structures. But should we assume that this aspect of hominid evolution occurred in a more simple manner than the evolutionary radiations of Cercopithecus (Dutrillaux et al., 19881, Papio (Jolly, 19931, Macaca (Melnick et al., 1992,1993), or other primate taxa?

Even if we set aside analogies to other primate lineages, should we assume the differentiation of the last common ancestor was simpler than later aspects of hominid evolution for which a substantial fossil record is available? A good deal of paleontological evidence is available regarding the origin of Homo and the relationships among hominids extant between 4.5 and 1.5 million years ago (Wood, 1992). There is also substantial material documenting the differentiation of and change within Homo sapiens from 300,000 years ago to the present (Mel- lars and Stringer, 1989; Smith et al., 1989; Frayer et al., 1993). These periods of human evolution suggest complex mosaic change in which geographic and temporal patterns of variation are difficult to collapse into simple, dichotomously branching phylogenetic trees. As the paleontological record provides more complete documentation of cladogenic events, these events appear more complex, and all characters do not present concordant distributions in time and space. There is no reason to assume that the diversification of the living African hominoids occurred in a much simpler manner.

Our historical description of the African hominoid divergence will differ depending on the speciation model adopted: vicariance (Lynch, 1989) or or some other process. Since conclusions from molecular systematics will inevitably be used to infer morphological character states for the last common ancestor of humans, chimpanzees, and gorillas, the relationship among morphological change, molecular change, and the origin of reproductive isolation is central to the debate about hominoid phylogeny. At this point the data and theory of hominoid molec-

ular systematics are not sufficient to estab- lish a definitive molecular population-level phylogenetic tree that can be used to make reliable inferences about the history of changes in morphology or other characters.

Our phylogenetic conclusions will be strongest when they make use of the largest amount of relevant data possible. Ideally, analyses should include molecular data from several independent loci along with morphological comparisons. Primate phylo- genetics would benefit from development of models that can combine data from molecular studies with data from polygenic morphological traits. This is not possible today, but as the genetic architecture of morphological traits becomes known through devel- opmental genetic and gene mapping studies, such models may become possible. Until more data and theory are developed, it is premature to build inferences about the biology of the last common ancestor of Homo, Gorilla, and Pan on existing molecular systematic data.

ACKNOWLEDGMENTS I wish to thank A.G. Comuzzie, C.J. Jolly,

K.K. Kidd, J . Marks, and T. Preuss for many valuable discussions of these issues. I also thank two anonymous reviewers for their comments and suggestions.

LITERATURE CITED Aiello L (1993) The fossil evidence for modern humans

origins in Africa: A revised view. Am. Anthropol. 95: 73-96.

Andrews P (1987) Aspects of hominoid phylogeny. In C Patterson (ed.): Molecular and Morphology in Evolu- tion: Conflict or Compromise. Cambridge: Cambridge University Press, pp. 23-53.

Avise JC, Shapira JF, Daniel SW, Aquadro CF, and Lansman RA (1983) Mitochondria1 DNA differentiation during the speciation process in Peromyscus. Mol. Biol. Evol. 1 :38-56.

Begun D (1992) Miocene fossil hominids and the chimp- human clade. Science 257:1929-1933.

Caccone A, and Powell JR (1989) DNA divergence among hominoids. Evolution 43:925-942.

Carson HL, and Templeton AR (1984) Genetic revolu- tions in relation to speciation phenomena: The found- ing of new populations. Ann. Rev. Ecol. System. 15: 97-131.

Djian P, and Green H (1989) Vectorial expansion of the involucrin gene and their relatedness of the hominoids. Proc. Natl. Acad. Sci. USA 86:8447-8451.

GENEALOGICAL HIERARCHY AND HOMINID PHYLOGENY 87

Dutrillaw B, Muleris M, and Couturier J (1988) Chro- mosomal evolution of Cercopithecinae. In A Gautier- Hion, F Bourliere, and J-P Gautier (eds.): A primate radiation: Evolutionary biology of the African gue- nons. Cambridge: Cambridge University Press, pp. 150-159.

Eldredge N (1985) Unfinished Synthesis: Biological Hi- erarchies and Modern Evolutionary Thought. Oxford: Oxford University Press.

Ellis N, Yen P, Neiswanger K, Shapiro U, and Goodfel- low PN (1990) Evolution of the pseudoautosomal boundary in Old World monkeys and great apes. Cell 63:977-986.

Ferris SD, Brown WM, Davidson WS, and Wilson AC (1981) Extensive polymorphism in the mitochondrial DNA of apes. Proc. Natl. Acad. Sci. USA 78t6319- 6323.

Foley R (1989) The ecological conditions of speciation: A comparative approach to the origins of anatomically modern humans. In P Mellars and C Stringer (eds.): The Human Revolution: Behavioral and Biological Perspectives in the Origins ofModernHumans. Prince- ton, NJ: Princeton University Press, pp. 298-318.

Frayer DW, Wolpoff MH, Thorne AG, Smith FH, and Pope GG (1993) Theories of modern human origins: The paleontological test. Am. Anthropol. 95t14-50.

Godfrey L, and Marks J (1991) The nature and origins of primate species. Yrbk. Phys. Anthropol. 34:39-68.

Gould SJ (1982) The meaning of punctuated equilibrium and its role in validating a hierarchical approach to macroevolution. In R Milkman (ed.): Perspectives on Evolution. Sunderland, MA: Sinauer Associates, Inc.,

Groves CP (1986) Systematics of the great apes. In DR Swindler and J Erwin (eds.): Systematics, Evolution and Anatomy, Volume 1, Comparative Primate Biol- ogy. New York: Alan R. Liss, Inc., pp. 187-217.

Hafner MS, Hafner JC, Patton JL, and Smith MF (1987) Macrogeographic patterns of genetic differentiation in the pocket gopher Thomomys urnbrinus. Syst. Zool. 36:18-34.

Harrison RG (1991) Molecular change at speciation. Annu. Rev. Ecol. Syst. 22:281-308.

Hasegawa M, and Kishino H (1991) DNA sequence analysis and evolution of Hominoidea. In M Kimura and N Takahata (eds.): New Aspects of the Genetics of Mo- lecular Evolution. Berlin, Springer-Verlag, pp. 303- 317.

Hayasaka K, Horai S, Gojobori T, Shotake T, Nozawa K, and Matsunaga E (1988) Phylogenetic relationships among Japanese, rhesus, Formosan and crab-eating monkeys, inferred from restriction-enzyme analysis of mitochondrial DNAs. Mol. Biol. Evol. 5:270-281.

Horai S, Satta Y, Hayasaka K, Kondo R, Inoue T, Ishida T, Hayashi S, and Takahata N (1992) Man’s place in Hominoidea revealed by mitochondria1 DNA genealogy. J. Mol. Evol. 35t32-43.

Jolly CJ (1993) Species, subspecies and baboon systematics. In WH Kimbel and LB Martin (eds.): Species, Species Concepts and Primate Evolution. New York, NY Plenum Press, pp. 67-107.

Koop BF, Tagle DA, Goodman M, and Slightom J L (1989) A molecular view of primate phylogeny and

pp. 83-104.

important systematic and evolutionary questions. Mol. Biol. Evol. 6:580-612.

Lynch J D (1989) The gauge of speciation: On the fre- quencies of modes of speciation. In D Otte and JA Endler (eds.): Speciation and Its Consequences. Sunderland, MA: Sinauer Associates, lnc., pp. 527- 553.

Maddison WP (1989) Reconstructing character evolution on polytomous cladograms. Cladistics 5:365-377.

Mellars P, and Stringer C (eds.) (1989) The Human Rev- olution: Behavioral and Biological Perspectives in the Origins of Modern Humans. Princeton, NJ: Princeton University Press.

Melnick DJ, Hoelzer GA, and Honeycutt RL (1992) Mito- chondrial DNA: Its uses in anthropological research. In E J Devor (eds.): Molecular Applications in Biologi- cal Anthropology. Cambridge: Cambridge University Press, pp, 179-233.

Melnick DJ, Hoelzer GA, Absher R, and Ashley MV (1993) mtDNA diversity in rhesus monkeys reveals overestimates of divergence time and paraphyly with neighboring species. Mol. Biol. Evol. 10t282- 295.

Nei M (1987) Molecular Evolutionary Genetics. New York: University of Columbia Press.

Otte D, and Endler JA (1989) Speciation and its Conse- quences. Sunderland, MA: Sinauer Associates, Inc.

Pamilo P, and Nei M (1988) Relationships between gene trees and species tress. Mol. Biol. Evol. 5:56%583.

Patton JL, and Smith MF (1981) Molecular evolution in Thomomys: Phyletic systematics, paraphyly and rates of evolution. J . Mammal. 62,493600.

Patton JL, and Smith MF (1989) Population structure and the genetic and morphological divergence among pocket gopher species (genus Thomomys). In D Otte and JA Endler (eds.): Speciation and its Conse- quences. Sunderland, MA: Sinauer Associates, Inc., pp. 284-304.

Provine WB (1989) Founder effects and genetic revolu- tions in microevolution and speciation: An historical perspective. In LV Giddings, KY Kaneshiro, and WW Anderson (eds.): Genetics, Speciation and the Founder Principle. Oxford: Oxford University Press,

Rogers J (1993) The phylogenetic relationships among Homo, Pan and Gorilla: A population genetics perspective. J. Hum. Evol. 25t201-215.

Rogers J , and Kidd KK (1993) Nuclear DNA polymor- phisms in a wild population of yellow baboons (Papio hamadryas cynocephalus) from Mikumi National Park, Tanzania. Am J. Phys. Anthropol. 90t477-486.

Ruano G, Rogers J, Ferguson-Smith AM, and Kidd KK (1992) DNA sequence polymorphism within hominoid species exceeds the number of phylogenetically infor- mative characters for a HOX2 locus. Mol. Biol. Evol. 9575-586.

Ruvolo M, Disotell TR, Allard MW, Brown MW, and Honeycutt RL (1991) Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proc. Natl. Acad. Sci. USA 88t1570-1574.

Saitou N (1991) Reconstruction of molecular phylogeny of extant hominoids from DNA sequence data. Am. J . Phys. Anthropol. 84r75-85.

pp.43-76.

88 J. ROGERS

Smith FH, Falsetti AB, and Donnelly SM (1989) Modern human origins. Yrbk. Phys. Anthropol. 32r35-86.

Smouse P, and Li W-H (1987) Likelihood analysis of mitochondria1 restriction-cleavage patterns for the human-chimpanzee-gorilla trichotomy. Evolution 41 ;

Smouse PE, Dowling TE, Tworek JA, Hoeh WR, and Brown WM (1991) Effects of intraspecific variation on phylogenetic inference: A likelihood analysis of mtDNA restriction site data on cyprinid fishes. Syst. Zool.40:393409.

Templeton AR (1980) Modes of speciation and inferences based on genetic distances. Evolution 34:719-729.

Templeton AR (1993) The “Eve” hypothesis: A genetic critique and reanalysis. Am. Anthropol. 9 5 5 - 7 2 .

1162-1 176.

Van Valen LM (1989) Our ancestors. Nature 338:304. Vigilant L, Pennington R, Harpending H, Kocher TD,

and Wilson AC (1989) Mitochondria1 DNA sequences in single hairs from a southern African population. Proc. Natl. Acad. Sci. USA 86:9350-9354.

Vbra E, and Eldredge N (1984) Individuals, hierarchies and processes: Towards a more complete evolutionary theory. Paleobiology 10; 146-1 71.

Williams-Blangero S, VandeBerg JL, Blangero J , Konigsberg L, and Dyke B (1990) Genetic differentiation between baboon subspecies: Relevance for biomedical research. Am. J. Primatol. 20:67-81.

Wood B (1992) Origin and evolution of the genus Homo. Naure 355383-790.

Levels of the genealogical hierarchy and the problem of hominoid phylogeny

Documents

Transcript of Levels of the genealogical hierarchy and the problem of hominoid phylogeny