Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa

Abstract

Recent discoveries of new fossil hominid species have been accompanied by several phylogenetic hypotheses. All of these hypotheses are based on a consideration of hominid craniodental morphology. However, Collard and Wood (2000) suggested that cladograms derived from craniodental data are inconsistent with the prevailing hypothesis of ape phylogeny based on molecular data. The implication of their study is that craniodental characters are unreliable indicators of phylogeny in hominoids and fossil hominids but, notably, their analysis did not include extinct species. We report here on a cladistic analysis designed to test whether the inclusion of fossil taxa affects the ability of morphological characters to recover the molecular ape phylogeny. In the process of doing so, the study tests both Collard and Wood's (2000) hypothesis of character reliability, and the several recently proposed hypotheses of early hominid phylogeny. One hundred and ninety-eight craniodental characters were examined, including 109 traits that traditionally have been of interest in prior studies of hominoid and early hominid phylogeny, and 89 craniometric traits that represent size-corrected linear dimensions measured between standard cranial landmarks. The characters were partitioned into two data sets. One set contained all of the characters, and the other omitted the craniometric characters. Six parsimony analyses were performed; each data set was analyzed three times, once using an ingroup that consisted only of extant hominoids, a second time using an ingroup of extant hominoids and extinct early hominids, and a third time excluding Kenyanthropus platyops.

Results suggest that the inclusion of fossil taxa can play a significant role in phylogenetic analysis. Analyses that examined only extant taxa produced most parsimonious cladograms that were inconsistent with the ape molecular tree. In contrast, analyses that included fossil hominids were consistent with that tree. This consistency refutes the basis for the hypothesis that craniodental characters are unreliable for reconstructing phylogenetic relationships. Regarding early hominids, the relationships of Sahelanthropus tchadensis and Ardipithecus ramidus were relatively unstable. However, there is tentative support for the hypotheses that S. tchadensis is the sister taxon of all other hominids. There is support for the hypothesis that A. anamensis is the sister taxon of all hominids except S. tchadensis and Ar. ramidus. There is no compelling support for the hypothesis that Kenyanthropus platyops shares especially close affinities with Homo rudolfensis. Rather, K. platyops is nested within the Homo + Paranthropus + Australopithecus africanus clade. If K. platyops is a valid species, these relationships suggest that Homo and Paranthropus are likely to have diverged from other hominids much earlier than previously supposed. There is no support for the hypothesis that A. garhi is either the sister taxon or direct ancestor of the genus Homo. Phylogenetic relationships indicate that Australopithecus is paraphyletic. Thus, A. anamensis and A. garhi should be allocated to new genera.

Introduction

The phylogenetic relationships of the earliest hominids remain a point of contention (Wood, 1991, Wood, 1992, Skelton and McHenry, 1992, Skelton and McHenry, 1998, Lieberman et al., 1996, Strait et al., 1997, Strait and Grine, 1998, Strait and Grine, 1999, Strait and Grine, 2001). The discovery of new species (White et al., 1994, Leakey et al., 1995, Brunet et al., 1996, Asfaw et al., 1999a, Senut et al., 2001, Ward et al., 2001, Leakey et al., 2001, Brunet et al., 2002) has fueled, rather than resolved, this debate, although a common assumption shared by these studies is that the pattern of early hominid phylogeny can be ascertained through analysis of craniodental morphology. Recently, however, this premise has been questioned (Collard and Wood, 2000), and consequently, doubts have been raised about the reliability of all phylogenetic hypotheses pertaining to early hominids. Collard and Wood (2000) have argued that the generally accepted molecular phylogeny of hominoids (Fig. 1a) (e.g., Goodman et al., 1994, Ruvolo, 1997, Shi et al., 2003, Wildman et al., 2003, Salem et al., 2003; but see Marks, 1993, Bailey, 1993, Deinard et al., 1998, Deinard and Kidd, 1999) can be used to test the phylogenetic reliability of morphological characters, and that craniodental characters produce cladograms that are grossly inconsistent with the molecular tree (Fig. 1b,c). The implication of Collard and Wood's (2000) study is that because craniodental characters are inadequate indicators of phylogeny in living hominoids, they will also be inadequate to the task of resolving the relationships among our extinct ancestors and relatives.

The observation of incongruence between molecular and morphological data is not unique to the hominoids. A variety of studies have revealed that molecular and morphological data do not show complete congruence with regard to a number of disparate taxonomic groups, including primates (e.g., Shoshani et al., 1996, Baker et al., 1998, Horowitz et al., 1998, Liu and Miyamoto, 1999, Wiens and Hollingsworth, 2000, Gatesy and Arctander, 2000, Gatesy and O'Leary, 2001, Yoder et al., 2001, Masters and Brothers, 2002, Freudenstein et al., 2003). This raises the question of how incongruence is to be interpreted. Collard and Wood (2000) took the position that, with respect to the hominoids, molecular data should be preferred and can be used to evaluate morphological data.

A factor not considered by Collard and Wood (2000), however, is the role that fossil taxa may play in resolving apparent incongruencies between morphological and molecular data sets. Fossil species preserve unique suites of primitive and derived characters, and therefore have a strong influence on patterns of character transformation (Eernisse and Kluge, 1993, Springer et al., 2001). In particular, fossils can play a key role in establishing phylogenetic linkages between morphologically derived extant species (Gauthier et al., 1988). As aptly noted by Gatesy et al. (2003:409):

Certain fossils are expected to preserve ancestral morphologies that have been radically altered in extant taxa and might allow more precise hypotheses of homology in divergent anatomical systems. By including fossils, more characters and taxa (especially primitive taxa with unique combinations of morphological character states) can be utilized in phylogenetic analysis.

Thus, fossils serve to extend taxon sampling (Gauthier et al., 1988), which has been shown to increase overall phylogenetic accuracy (Wheeler, 1992, Zwickl and Hillis, 2002). Studies of quite disparate taxonomic groups have demonstrated that fossil taxa generally stabilize relationships and elucidate otherwise ambiguous patterns of character evolution (Eernisse and Kluge, 1993, O'Leary, 1999, Gatesy and O'Leary, 2001, Springer et al., 2001, Gatesy et al., 2003, Mallat and Chen, 2003).

Over a decade ago, Begun (1992) argued that morphological characters can recover the molecular phylogeny of apes so long as extinct species are included. To date, however, no study has reconstructed the phylogeny of both early hominids and living hominoids. In this paper, we test Collard and Wood's (2000) hypothesis by determining whether parsimony analysis of craniodental characters can yield a phylogeny of extant hominoids and extinct early hominids that is consistent with the ape molecular tree. As a result of testing Collard and Wood's (2000) hypothesis, it is also possible to test several recently proposed hypotheses of hominid phylogeny.

Regarding the fossil hominid taxa included herein, it is worth noting that, with the exception of Australopithecus anamensis (Ward et al., 2001), none of the recently discovered early hominid species has been comprehensively described, and the relevant specimens are not yet available for study. Thus, the present analysis of these species relies heavily on their initial published descriptions. In this regard, the proposed reconstruction of early hominid phylogeny relies on the accuracy of these initial descriptions and interpretations, some of which have been called into question. In particular, the validity of the species diagnosis of Kenyanthropus platyops has been questioned by White (2003), who implied that many of the defining features of the type specimen are artifacts of post-depositional distortion. We have no independent means of evaluating this claim, and thus we performed analyses that both included and excluded this taxon.