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FULL TITLE:
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The role of character displacement in the molarization of hominin mandibular premolars
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RUNNING TITLE:
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Character displacement in fossil hominin premolars
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AUTHORS:
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KES SCHROER1,2 and BERNARD WOOD3
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Dartmouth, 6047 Silsby Hall, Hanover NH 03755, USA, 3Center for the Advanced Study of
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Hominid Paleobiology, The George Washington University, 2110 G St NW, Washington DC
Neukom Institute for Computational Science, Dartmouth, 2Department of Anthropology,
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20052, USA.
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CORRESPONDING AUTHOR: kes.schroer@gmail.com
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CONTACT FOR OTHER AUTHORS: bernardawood@gmail.com
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KEYWORDS: competition, morphological evolution, paleobiology, Paranthropus, primate,
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sympatry
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DATA ARCHIVAL LOCATION: http://dx.doi.org/10.6084/m9.figshare.1243200
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The authors declare no conflict of interest.
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Word count: 5,069
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Table count: 1
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Figure count: 3
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ABSTRACT:
Closely related species are likely to experience resource competition in areas where their
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ranges overlap. Fossil evidence suggests that hominins in East Africa c.2-1.5 million years ago
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may have lived synchronically and sympatrically, and that competition may have contributed to
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the different tooth sizes observed in Homo and Paranthropus. To assess the likelihood that these
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taxa overlapped, we applied a character displacement model to the postcanine tooth size of fossil
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hominins and validated this model in populations of living primates. Mandibular fourth premolar
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(P4) crown size was measured from fossil taxa and from living primate species where dietary
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overlap is established. Dimensions of the P4 crown were fitted to a character matrix and
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described as the response variables of a generalized linear model that took taxon and location as
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input variables. The model recovered significant divergence in samples of closely related, living
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primates. When applied to fossil hominins the same model detected strong indications of
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character displacement between early Homo and Paranthropus (P=0.002) on the basis of their P4
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crown size. Our study is an example of how ecologically-informed morphologies measured in
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appropriate extant referents can provide a comparative context for assessing community and
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ecological evolution in the fossil record.
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Introduction
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Species rarely exist in isolation and overlapping species can exert strong selective
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pressures on one another (Schoener 1982; Goldberg and Barton 1992; Webb et al. 2002; Kneitel
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and Chase 2004; Dayan and Simberloff 2005; Burger et al. 2006, Slingsby and Verboom 2006;
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Johnson and Stinchcombe 2007; Emerson and Gillespie 2008; Cavender-Bares et al. 2009).
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While range overlap in living species can be readily observed, such overlap in fossil species is
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harder to detect. Time-averaging in fossil sites makes it difficult to be sure that members of a
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paleoecological community were synchronic (Flessa et al. 1993; Kidwell and Flessa, 1996;
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Kowalewski, 1996; Roy et al. 1996; Olszewski 1999; Behrensmeyer et al. 2000) and while
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taphonomic investigations have greatly improved the temporal resolution of paleontological sites
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through the analysis of preservation conditions (Kidwell and Brenchley 1996; Behrensmeyer et
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al. 2000), these methods cannot explicitly test hypotheses regarding evolutionary pressures in a
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paleoecological community. This study offers a computational framework validated in extant and
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overlapping taxa that can be used to assess the likelihood of species overlapping in deep time.
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Our study targets the likelihood of overlap between two groups of hominins living in
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Africa c. 2-1.5 million years ago. Fossil evidence belonging to two fossil hominin genera,
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Paranthropus and Homo, has been found in synchronous deposits at several Plio-Pleistocene
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fossil localities in East Africa, most explicitly in the Turkana Basin. Though separated from their
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proposed Australopithecus-like ancestor (Strait et al. 1997; Strait and Grine 2004) by less than a
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million years, the two taxa have remarkably different postcanine tooth morphologies. The
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postcanine tooth crowns of Paranthropus boisei are absolutely and relatively large compared to
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earlier hominin taxa, and together with the molarization of the P4 crown, this is one of the most
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extreme points of contrast between the dentition of P. boisei and Homo (Hillson 1996; Wood and
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Strait 2004; Bailey and Wood 2007; Wood and Constantino 2004). In contrast, the postcanine
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tooth crowns – including the P4 – of Homo are reduced in size compared to earlier hominins
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(Wood 1991; Hillson 1996; McHenry and Coffing 2000; Lucas et al. 2008). The close ecological
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relationship between mammalian dental morphology and diet (Kay 1975; Lucas and Luke 1984;
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Lucas et al. 1985, 1986; Teaford and Ungar 2000; Lucas 2004) suggests that the increase in
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premolar crown size probably reflects pressure to process large volumes of mechanically
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challenging foods (Jolly 1970; Walker 1981; Lucas et al. 1985, Kay and Grine 1988). Evidence
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from isotopes and dental wear supports the suggestion that differences in the postcanine tooth
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crowns of Paranthropus and Homo may relate to their different diets, with P. boisei becoming
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heavily dependent on a diet of tough, C4 resources and Homo consuming a more generalized diet
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of C3 resources that lacks extremely hard or tough foods (Ungar et al. 2008, 2011; Cerling et al.
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2011, 2013; Ungar and Sponheimer, 2011). Some authors have suggested that the very different
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postcanine tooth morphology of Paranthropus and Homo in East Africa may have been driven
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by competition for resources (Schaffer 1968; Wood and Strait 2004).
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The propensity of closely related overlapping,species to compete was first noted by
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Darwin in The Origin of Species, where he wrote that overlapping species were engaged in an
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“incessant struggle” and that “more living beings can be supported on the same area the more
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they diverge in structure, habits, and constitution” (Darwin 1859; Pfenning and Pfenning 2010).
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The evolutionary consequences of range overlap were formalized by Gause’s “competitive
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exclusion” principle (Gause 1934). This principle, which was devised using evidence from the
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study of bacteria, suggests that two taxa overlapping in space and competing for the same
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resources cannot coexist in the long-term. Instead, one of two scenarios will play out. Either one
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competitor will evolve some advantage over the other and drive its competitor to extinction, or
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the two taxa will evolve to occupy non-competing ecological niches. The competitive exclusion
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principle may be extrapolated to describe evolutionary relationships in two closely-related taxa
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sharing the same habitat, in which case the scenario of divergence is more specifically called
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character displacement (Brown and Wilson 1956).
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Diet is a common source of resource competition in overlapping, closely related species
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(Schluter 2000, Ackerly et al. 2006, Grant and Grant 2006), although other kinds of competition
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are possible (West-Eberhard 1983; Boughman 2002; Clutton-Brock 2007; Richie 2007; Sobel et
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al. 2010). Due to the dietary and taxonomic information retained in gnathic and dental
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morphologies, these anatomical structures feature frequently in previous studies of character
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displacement (Dayan et al. 1989, 1990, 1992; Yom-Tov 1991; Reig 1992; Dayan and Simberloff
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1994; Werdelin 1996), and the occurrence of exaggerated morphologies has been linked with
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character displacement (Lack 1947, Martin and Harding, 1981; Losos 1990). It is for these
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reasons that we decided to test whether the contrast between the large molarized mandibular
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premolars of P. boisei, and the smaller, less complex, crowns of early Homo might be the
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consequence of character displacement.
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Although there are reservations regarding the strength of experimental evidence for
character displacement (Grant 1972; Wiens 1977; Strong et al. 1979; Slatkin 1980; Rundle et al.
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2003; Bo1nick and Fitzpatrick 2007; Meiri et al. 2011; Stuart and Losos 2013), character
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displacement continues to be widely applied toward understanding morphological divergence in
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overlapping and potentially overlapping taxa (Schoener 1982, Taper and Case 1985; Abrams
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1986; Schluter and McPhail 1992; Schluter 2000; Dayan and Simberloff 2005, Rando et al.
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2010). In its most straightforward form, character displacement can be quantified as the
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displacement statistic DS-DA, where DS denotes the divergence between sympatric (i.e., shared
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location) populations of two taxa and DA denotes the divergence between allopatric (i.e.,
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different locations) populations of the same taxa (Schluter and McPhail 1992). The term DS
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quantifies the difference between two taxa in areas where they may potentially be in competition
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(i.e., sympatric locations), while DA quantifies the difference between the two taxa in the absence
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of competition (i.e., allopatric locations). When the value of DS exceeds the value of DA, this is
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an indication that competition has contributed to any differences between the two taxa (Figure
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1). Character divergence may involve several kinds of variation, including behavioral and
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reproductive (Waage 1979; Armbruster 1985; Levin 1985; Marshall and Cooley 2000; Geyer and
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Palumbi 2003; Adams 2004; Allen et al. 2014), but in general the term has been applied to
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morphological divergence (i.e., ecological character divergence; Slatkin 1980; Schluter and
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McPhail 1992; Adams and Rohlf 2000; Losos 2000). Although the displacement statistic has
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been applied to morphological variation in many sympatric vertebrate species (Dayan et al. 1989,
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1990, 1992; Losos 1990; Dayan and Simberloff 1994; Simberloff et al. 2000; Davies et al. 2012),
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it has only once been applied to the fossil hominin record (Schaffer 1968).
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One way to apply the character displacement statistic to observed morphological
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differences is to use a generalized linear model (GLM) that can approximate the relationship
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between the observed morphologies and the ecological relationship between the two taxa. GLMs
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are widely used in studies of species distribution models (Guisan and Zimmermann 2000; Scott
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et al. 2002) because they can be used to interpret the strength of the fit between response (i.e.,
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morphological) variables and explanatory (i.e., ecological) variables (Austin 1987; Yee and
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Mitchell 1991; Guisan et al. 2002). The use of general linear models is especially common in
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character displacement studies (Bolnick 2004; Collyer and Adams 2007; Russo et al. 2007).
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The GLM we propose builds on one for multivariate phenotypic change proposed by
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Collyer and Adams (2007). The Collyer and Adams model tests the likelihood of character
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displacement as an explanation for divergent morphologies against a null hypothesis of randomly
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assorted individuals pulled from observed populations. This model is especially suitable for this
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study because it does not presume a specific taxonomic level. Early character displacement
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studies only considered sympatric and allopatric populations of the same species (i.e., Schluter
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and McPhail 1992), but character displacement may account for morphological divergence at the
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species level (Dayan et al. 1990; Dayan and Simberloff 1994), the family level (Monroe, 2012)
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and at the level of the ecological guild (Schluter 1986).
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The Collyer and Adams model, which was developed and tested in salamanders and
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pupfish, has not previously been tested in mammals. Nonhuman primates, which are the closest
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living relatives to fossil hominins, have observable degrees of geographic overlap and dietary
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competition, and many primate populations – including species of strepsirrhines (Tan 1999),
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platyrrhines (Puertas and Bodmer 1993), and catarrhines (Fleagle 1977; Sterck and Steenbeek
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1997; Lambert 2004; Allen et al. 2014) – live in sympatry and potentially provide extant
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referents for understanding the pressures of overlap during human evolution. Thus, we reasoned
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that validating the Collyer and Adams model in sympatric primate populations would increase its
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suitability for assessing the likelihood that Paranthropus and Homo in East Africa were
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sympatric and synchronic.
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Materials and Methods
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Sample
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The fossil hominin sample is composed of Paranthropus and Homo. Representatives of
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these taxa are potentially sympatric in East Africa but unlikely to be sympatric in southern
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Africa. Two species of Paranthropus recognized at East African sites, Paranthropus aethiopicus
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and P. boisei, and they are generally considered close relatives (Strait et al. 1997; Wood and
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Richmond 2000; Constantino and Wood, 2007; Wood and Lonergan 2008). Some authors have
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argued that these two taxa represent, respectively, the early and later phases of a chronospecies
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(Foley 1991; Bobe et al. 2007; Schroer and Wood 2013), but in this analysis they are combined
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as P. boisei sensu lato. The allopatric Paranthropus taxon, Paranthropus robustus, is only
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known from southern Africa.
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The East African sample of early Homo that is potentially sympatric with Paranthropus
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includes remains allocated to three early Homo taxa, Homo habilis, Homo rudolfensis, and Homo
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ergaster. The allopatric sample of Homo includes remains of Homo found outside of East Africa
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that are more recent (< 0.5 million years) than the East African sample of Homo. The Homo
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specimens found at the site of Dmanisi in Georgia have been affiliated with H. ergaster, Homo
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erectus, or a close relative (Rosas and Bermudez de Castro 1998; Gabunia et al. 2000; Vekua et
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al. 2002; Lordkipanidze et al. 2013), those at Rabat have been assigned to H. ergaster or H.
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erectus (Martinon-Torres et al. 2007; Gomez-Robles et al. 2008), and Homo fossils from
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Sangiran and Zhoukoudian have been assigned to H. erectus. These specimens represent the
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most reliably allopatric sample of Homo compared to the East African sample, for there is no
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evidence of Paranthropus or a Paranthropus-like lineage at these sites. The inclusion of younger
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Homo specimens increases the morphological and geographic variation in the allopatric sample,
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will inflate the value of DA, and will make character displacement less likely to detect (i.e., an
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increased Type II error).
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Some southern African hominin fossils have been assigned to Homo, but they are not
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included in this analysis. because either there is no consensus over their taxonomy, or because
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the evidence for geological age is weak. Some of these specimens, such as Stw 53 and SK 847,
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have been assigned to early Homo (Hughes and Tobias 1977; Howell 1978; Tobias 1978, 1991;
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Corruccini 1980; Chamberlain 1987; Grine et al. 1993; 1996; Clarke 1990, 1994), but they have
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also been linked with later Homo (Robinson 1960, 1967; Clarke 1977; Tobias 1978; Groves and
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Mazak 1975; Walker 1981; Dean and Wood 1982; Spoor et al. 1994) or with non-Homo taxa
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(Mann 1970; Wolpoff 1970, 1971; Krantz 1977; Wood and Abbott 1983; Wood and
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Uytterschaut 1987; Ferguson 1989; Kuman and Clarke 2000; Berger et al. 2010). The allopatric
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population of Homo was restricted to individuals in areas with no known overlap with any non-
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Homo hominin.
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Mandibular dental crown measurements were obtained from photographs of precision
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casts in the collections of The George Washington University and the University of Arkansas, or
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they were taken from high-resolution photos of the original fossil specimens (B.A. Wood, pers.
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comm.). Photographs were taken with a Canon Digital Rebel XT camera fitted with a macro lens
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and then digitized in TPSDig (Rohlf 2009). Measures of the P4 included maximum mesiodistal
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and buccolingual diameters; occlusal area was calculated using 20 semilandmarks of equal
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distance fitted from a curve around the occlusal margin. Although mesiodistal (MD) and
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buccolingual (BL) length are correlated with occlusal area, these are the three most common
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measures of premolar crown size in fossil studies and were used to construct the matrix of
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observable traits in Paranthropus and Homo. The morphology of the P4 has been used for fossil
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hominin alpha taxonomy (Biggerstaff 1969; Wood and Uytterschaut 1987; Bailey 2000; Bailey
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and Lynch 2005) and it has been used to identify isolated specimens of Paranthropus and Homo.
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However, most of our specimens were from mandibular remains for which there is additional
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evidence for taxonomic assignment (Table S1).
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Measurements were taken from the literature in cases where photographs and casts were
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unavailable (Table S1), and when occlusal areas were not available an approximation of occlusal
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area (MD x BL) was used in its place. This method tends to overestimate the occlusal area in
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molars (Schmidt et al. 2011), but its effect on premolars is unknown. This method was
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distributed evenly across the taxa represented in the fossil hominin sample. Extensively worn
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specimens (i.e., occlusal wear great enough to mask the identification of individual cusps and
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interproximal wear that affected an estimated >20% of the occlusal margin) were not included in
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the sample. For teeth with moderately worn margins, the margin was reconstructed by
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approximating the curvature of the margin from overall crown shape (Wood and Uytterschaut
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1987; Bailey and Lynch 2005). All of the fossil specimens are adult, but sex was not controlled.
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The locations of fossil sites are given in Figure 2.
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Living primates were included in this study to provide an independent assessment of the
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robusticity of the Collyer and Adams model of character displacement. In all of the extant
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primate groups examined here there is evidence of dietary overlap and ecological competition
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(Rodman 1991; Ungar 1993; Wahungu 1998; Bentley-Condit 2009; Yamagiwa and Basabose
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2009; Vogel et al. 2009; Harrison and Marshall 2011). The living primate groups chosen include
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taxa previously proposed as comparative models for the unusual morphology of
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Paranthropus(Jolly 1970; Vogel et al. 2008; Wood and Schroer 2012). Additionally, dental wear
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and craniodental morphology suggest that P. boisei was adapted to a more mechanically
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challenging diet than Homo (DuBrul 1977; Rak 1983; Grine 1986, 1987; Kay and Grine 1988;
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Hylander 1988; Teaford and Ungar 2000; Scott et al. 2005, Constantino and Wood 2007; Ungar
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et al. 2008) and the extant primate groups examined here are known to differ in the mechanical
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properties of their diet. Gorilla consumes more tough foods than sympatric Pan populations
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(M’Kirera and Ungar 2003), and Pongo and Cercocebus eat food that is much harder than
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sympatric primates in their regions (Vogel et al. 2009; Daegling et al. 2011). Macaca nemestrina
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is also durophagous (Caldecott, 1986).
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Ideally, the taxa included within each group of living primates should approximate the
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phylogenetic distance that separates Paranthropus and Homo, but few sympatric living primate
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genera separated such a short time ago. Therefore, intervals both longer and shorter than
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Paranthropus and Homo were used in the analyses. We undertook both species-level (Macaca)
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and genus-level (Gorilla-Pan, Hylobates-Pongo, Cercocebus-Papio) comparisons. For the
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Hylobates-Pongo and Cercocebus-Papio groups, congeners were examined while in Gorilla-Pan
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sympatric and allopatric populations of the same species were examined (i.e., sympatric and
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allopatric Gorilla gorilla and sympatric and allopatric Pan troglodytes). Genus-level distinctions
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are probably the most relevant comparisons for the ecological context of Paranthropus and
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Homo (Strait et al. 1997; Wood and Richmond 2000), but there is controversy surrounding the
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definition of a hominin genus (Wood and Collard 1999) as well as questions about the
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monophyly of both Paranthropus and Homo (Wood 1988).
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The samples of the extant primate taxa were taken from the collections of the National
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Museum of Natural History in Washington, DC, the American Museum of Natural History in
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New York City, and the Natural History Museum in London. Photographs were taken in the
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same manner as the fossil specimens. The left side of the mandible was used unless that side was
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missing, in which case the right side was substituted. The extant primate samples were confined
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to wild adults of mixed-sex. Taxa were sampled equally within each comparative group, with
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specimens randomly selected from each taxon via a custom R script that simultaneously drew
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equal representation of male and female specimens without replacement (S2). Maps showing the
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relative ranges of overlap for the extant primate taxa are shown in Figure 3.
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To calculate intra-observer error, a sample of 45 individuals representing all of the taxa
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in the extant primate sample were measured again two months after their initial measurement.
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Technical error for linear measurements was ±0.4 mm for all taxa. Technical error for area
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measurements was ±6.10 mm2 for all taxa.
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Analytical methods
Measurements of premolar crown size were log-transformed to normalize variance
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among hominin and primate taxa. Individuals were analyzed separately in the following
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comparative groups: fossil hominins, African apes, Asian apes, macaques, and papionins. We
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examined sympatric and allopatric pairs of taxa within each comparative group. The observed
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variation in each fossil or living group was fitted to the general linear model:
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Y = BX + U,
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where Y is the morphological matrix, X is the design matrix, B is the estimate of the parameters,
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and U is the residual error (Collyer and Adams 2007).
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The design matrix encodes each individual by taxon and allocates it to either a sympatric
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or allopatric location. The taxon is denoted by one of two categorical designations, encoded as 1
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or -1 in this analysis. For location, 1 denotes sympatry and -1 denotes allopatry. The design
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matrix also includes a third variable, which is the interaction variable of taxon and location. This
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is obtained by multiplying the values of taxon and location. Thus, the sympatric population of
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the first taxon is (1 x 1 = 1), the allopatric population of the first taxon is (1 x -1 = -1), the
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sympatric population of the second taxon is (-1 x 1 = -1), and the allopatric population of the
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second taxon is (-1 x -1 =1). Sample matrices are described in the supplementary information
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(S1).
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The Y-matrix is constructed from the log-transformed morphological values of the three
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premolar crown size variables considered for each individual. The untransformed matrix for the
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five groups is can be found at [http://dx.doi.org/10.6084/m9.figshare.1243200]. The model
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parameters, B, are the regression coefficients describing the relationship between the design
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matrix and the observed morphological values for each individual. After the application of a
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least-squares regression, U is minimized so that theoretically B describes all of the relationship
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between the design and observed matrices (Guisan et al. 2002). After determining B, it is applied
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to the least squares means for each population, deriving four vectors – two describing the two
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taxa in sympatry and two describing each the two taxa in allopatry. The vectors for the sympatric
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and allopatric taxa are subtracted to derive two phenotypic change vectors, one describing the
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change between the sympatric taxa (DS) and one describing the change between the allopatric
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taxa (DA). Subtracting the lengths of these vectors results in the DS-DA statistic.
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To evaluate the significance of the DS-DA value obtained from this model, a distribution
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list was generated from permutations of randomized values for each group. To generate a
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randomized list of DS-DA values, the interaction variable (i.e., taxon by location) was stripped
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from the design matrix so that individuals were no longer encoded by their taxon and location
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information. From this randomized design matrix, and holding the Y-matrix constant, new
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parameters were generated. The vectors of sympatric and allopatric morphological difference
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were subtracted to obtain the randomized DS-DA statistic and this process was reiterated 999
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times to generate the distribution list. Probability was obtained through encoding each DS-DA
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result as either 1 (greater than or equal to the observed DS-DA) or 0 (less than the observed DS-
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DA). The results were summed and divided by the number of iterations to generate the likelihood
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that the observed DS-DA was significant. The greater the observed difference in sympatry and
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allopatric populations, the less likely the randomization will obtain an equal or greater value of
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DS-DA. Non-random variation was assumed at the P<0.5 level and statistical significance was
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assumed at the P<0.05 level. This analysis was performed using R (R Development Core Team
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2010) through a script modified from Collyer and Adams (2007) and provided in the
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supplementary information (S2 & S3, Table S2).
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Results
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Although sympatric and allopatric divergence vectors differ, the means of the three traits
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of P4 crown size are similar in populations of the same genus or species (Table S3). This appears
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especially true for the MD and BL measurements. For example, in the case of the sympatric (i.e.,
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East African) and allopatric (i.e., southern African) populations of Paranthropus, tooth size of
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the two Homo groups is more similar to one another than either is to Paranthropus. However,
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there is greater divergence in P4 crown size between the East African sympatric groups (i.e., P.
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boisei and Homo) than in the allopatric groups (i.e., P. robustus and Homo). The difference
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between these fossil hominin populations, tested against randomized distributions of premolar
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dimensions, is significant (P=0.002). That is to say, within the 999 randomly generated DS-DA
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values from a Paranthropus/Homo matrix, less than 1% of the random values were greater than
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the DS-DA value obtained when sympatric and allopatric populations are encoded in the design
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matrix. These results suggest that shared location had an effect on premolar size differences in
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East African hominins and provides support for previous suggestions that the extremely large
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postcanine teeth, and in particular the molarized premolars, of P. boisei may relate to
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competitive pressures resulting from geographic overlap with members of Homo in that region
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(Schaffer 1968; Wood and Strait 2004).
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Results are similar in extant primate groups and indicate that changes in premolar
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dimensions relate to competition in living populations. The dimensions of the P4 in populations
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experiencing sympatryy are generally more divergent (i.e., DS>DA) than in comparative
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allopatric populations (Table 1). The probability of observing a higher divergence in sympatric
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populations compared to allopatric populations is nonrandom in all groups except the Hylobates-
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Pongo group (which has the largest phylogenetic distance between taxa), and the results from
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both African apes and macaques reach significance. The highest significance in the study
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(P=0.001) belongs to the only genus-restricted group in the sample, the macaques.
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Discussion
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In the five groups studied here, DS-DA is generally positive and its magnitude is unlikely
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to be replicated by randomized populations. This result indicates a trend for more difference in
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the size of the P4 crowns between sympatric populations than between allopatric populations.
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This trend holds regardless of whether species- or genus-level differences are examined, and
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both species- and genus-level groups achieve statistical significance. Dimensions of the P4 crown
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appear to carry signals of character displacement in fossil hominin and living primate
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populations.
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In the case of fossil hominins, the DS-DA difference in this group may be indicative of
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competition generated by geographical overlap in East Africa at, or prior to, c.2 million years
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ago. Divergence in synchronous East African populations is greater than the divergence between
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allopatric, non-overlapping hominin populations, despite the separation of allopatric populations
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by greater geographic and phylogenetic distances. One explanation of these observations would
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be character displacement between two closely-related taxa driven by dietary competition, such
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as is observed in comparable living primate populations and in other organisms (Guillotin et al
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1994; Kamilar and Ledogar 2011; Stroik 2014). This explanation appears statistically likely
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compared to random assortment, although it cannot pinpoint the time of divergence in P4 size
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between Paranthropus and Homo. Overlap may have co-occurred with the appearance of P.
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boisei and early Homo, or it may predate their appearance. In this case, the divergence observed
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in the P4 size of Paranthropus and Homo may be a “ghost” of past competition past (Connell
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1980; Hairston 1980; Pacala and Roughgarden 1985; Pritchard and Schluter 2001).
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Numerous other evolutionary processes (e.g., seasonal diets, intraspecific competition,
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niche conservatism, etc.) could have contributed to the differences in P4 morphology, and the
344
model does not address the counterpart of character displacement, hybridization. Hybridization is
345
observed in several overlapping and closely related primate species, including some taxa
346
included in this analysis (Jolly et al 1997; Ackermann et al. 2006; Burrell et al. 2009; Ackermann
347
and Bishop 2010), and some have proposed that it may have occurred during human evolution
348
(Tattersall and Schwartz 1999; Holliday 2006; Sankararaman et al. 2012). While hallmarks of
349
hybridization, such as the frequent emergence of supernumerary teeth (Ackermann et al. 2006)
350
are infrequent among the fossil evidence for Paranthropus and Homo, this study does not
351
explicitly test the hypothesis that hybridization occurred between these taxa and contributed to
352
the evolution of extreme dental morphologies. The differences in P4 size could be the result of
353
reticulate evolution in which populations repeatedly diverge and hybridize (Arnold 1992; Sosef
354
1997; Holliday 2003; Larsen et al. 2010), in which case character displacement would be nearly
355
impossible to detect.
356
Despite these caveats, comparative evidence from living primates suggests that character
357
displacement remains a likely hypothesis to explain the divergence in P4 size between
358
Paranthropus and Homo. In three of the four primate groups we examined, the results suggest
359
that sympatric and allopatric populations have significantly greater divergence than random
360
assortments. The results from living primate also suggest that both phylogenetic closeness and
361
dietary competition contribute to the strength of the signal of character displacement. Although
362
Hylobates can share up to 95% of its diet with Pongo (Vogel et al., 2009), there is no significant
363
character displacement indicated in this group. This may relate to their substantial phylogenetic
364
distance, or to the wide variety of other foodstuffs eaten by Pongo. Conversely, the highest
365
significance levels are found in macaques, the group where the phylogenetic distance is the least
366
and for which evidence from field studies suggests that substantial dietary overlap only occurs
367
during the wet season (Singh et al., 2011). Generally, the genetic closeness of pairs of taxa
368
predicts how well the model will perform in each group, with dietary overlap accounting for the
369
discrepancy between papionins and African apes. African apes show a stronger signal of
370
character displacement than papionins although African apes have twice the phylogenetic
371
distance (Page et al. 1999; Scally et al. 2012). A study of one sympatric G. gorilla and P.
372
troglodytes troglodytes group in the Lope Reserve of Gabon found that gorillas shared 73% of
373
the chimpanzee food items and the chimpanzees shared 57% of the gorilla food items (Tutin and
374
Fernandez 1992). Another study in Kahuzi-Biega National Park, Zaire showed that gorillas
375
consume 50% of the fruit species preferred by chimpanzees (Yamagiwa et al. 1996). Information
376
from overlapping papionin populations is limited and dietary overlap is difficult to compare
377
between research sites, but evidence suggests that sympatric Papio and Cercocebus near the
378
Tana River feed at different canopy heights (Wahungu 1998) and experience less competition
379
than Gorilla and Pan. These data point to the intriguing suggestion that phylogenetic distance
380
and dietary competition both contribute to character displacement in primate premolars.
381
This study is an illustration of one way in which fossil species and fossil morphologies
382
can contribute to understanding how competitive overlap, via character displacement, might have
383
promoted evolution within closely related lineages. Our application of the Collyer and Adams
384
model overcomes some of the problems created by possible time-averaging at fossil sites 1) by
385
establishing the likelihood that extinct species overlapped through a test against random
386
assortment, and 2) through comparison with observable closely-related living populations. In
387
essence, computational frameworks such as the one presented here put fossil species “back in
388
play” when reconstructing the dynamic and complex evolutionary pressures that operate when
389
taxa overlap geographically and temporally.
390
That is not to say that fossil species can replace experimental evidence. Indubitably,
391
observations of character displacement in action contribute most to our understanding of how
392
competitive overlap results in predictable selective pressures that result in morphological
393
divergence (Schoener 1982; Goldberg and Barton 1992; Grant and Grant 2006; Bailey and
394
Kassen 2012; Stuart and Losos 2013). However, rapid evolution is never observable and rarely
395
detectable in fossil lineages. Computational models allow us an additional opportunity to
396
synthesize information from experimental, living, and extinct populations within probability
397
frameworks and could, in the future, be generalizable to include other species interactions and
398
ecological variables.
399
400
401
Conclusion
Within the hominin clade, premolar crown size is known to differ markedly between the
402
megadont and hyper-megadont dentitions of species belonging to the genus Paranthropus and
403
the reduced postcanine dentition of species within the genus Homo. This study applied the
404
Collyer and Adams model of character displacement to the P4 crown size of fossil hominins to
405
test the probability that competition may have influenced the morphological divergence of
406
sympatric East African early Homo and Paranthropus taxa. In order to validate the model’s
407
potential for detecting signals of character displacement, the model was also applied to living
408
primate populations where range overlap is directly observable.
409
In the extant groups examined, the difference between the P4 crown size of sympatric
410
populations generally exceeds the difference between the P4 crown size of allopatric taxa. In taxa
411
within 10 million years of their inferred genetic divergence, including fossil hominins, this
412
difference was always significant at P<0.05. The results of this study are unable to falsify the
413
hypothesis that character divergence occurred at some point during the evolution of East African
414
early Homo and Paranthropus taxa, and they are consistent with the hypothesis that sympatric
415
overlap and competition may have played a role in the evolution of hominin premolars.
416
The results of this study suggest that ecological modeling can provide insights into
417
reconstructing the evolution of our hominin relatives. Most studies of character displacement
418
consider only contemporary populations in relatively restricted geographic areas, and many only
419
examine variation in populations of the same species. This study expands the application of
420
character displacement both hierarchically and geographically, and demonstrates that the same
421
theoretical frameworks that account for variation in living taxa can be applied to variation
422
observed in the fossil record. By considering the importance of species and location interactions
423
in the evolution of morphological adaptations, studies such as this one move us closer to
424
understanding the processes that lie behind the morphological patterns we observe in the fossil
425
hominin record.
426
ACKNOWLEDGMENTS
427
The manuscript was greatly improved by comments from Drs. Patricia Hernandez, Mark
428
Grabowski (George Washington University), Matthew Skinner (University of Kent), Paul
429
Constantino (St. Michael’s College), P. David Polly (Indiana University), and two anonymous
430
reviewers. Dr. Peter Ungar (University of Arkansas) provided access to many fossil casts. Access
431
to extant species was made possible through Linda Gordon, Darrin Lunde, and Dr. Matthew
432
Tocheri (NMNH), Eileen Westwig (AMNH), and Roberto Portela Miguez (BMNH). Kristen
433
Ramirez (CUNY) and Christine Foltz assisted with photography. David Otten (University of
434
Arkansas), Michael Frick, Teresa Girolamo, and David Cobey provided hospitality during
435
museum visits. Funding for this research was provided by the NSF-IGERT DGE-0801634, an
436
NSF-GRF to KS, and a Cosmos Club Scholars Award to KS.
437
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FIGURE LEGENDS
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Figure 1. Schematic of character displacement, measured through the DS-DA statistic. DS denotes
847
the difference between two taxa that overlap in geographic location while DA denotes the
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difference between the same two taxa in non-overlapping populations. When DS>DA, character
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displacement is indicated. Figure is modified from Pfenning et al. (2006).
850
Figure 2. Map indicating the sites of fossil specimens examined in this analysis. Fossil sites are
851
labeled according to whether they provide sympatric or allopatric population samples.
852
Figure 3. Maps showing the approximate ranges of living primates used as comparative models
853
for the fossil hominins. Groups are divided into A) African apes, B) papionins, C) Asian apes,
854
and D) macaques. Ranges are derived from data from the IUCN RedList.