Evolution of hypsodonty in equids: testing a hypothesis of adaptation

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Paleobiology, 32(2), 2006, pp. 236–258

Evolution of hypsodonty in equids: testing a hypothesis of adaptation Caroline A. E. Stro¨mberg

Abstract.—The independent acquisition of high-crowned cheek teeth (hypsodonty) in several ungulate lineages (e.g., camels, equids, rhinoceroses) in the early to middle Miocene of North America has classically been used as an indication that savanna vegetation spread during this time. Implicit in this interpretation is the untested assumption that hypsodonty was an evolutionary response to feeding in open habitats, either due to a change in food source (from browse to graze) or to increased incorporation of airborne grit in the diet. I examined the adaptive explanation for hypsodonty in equids using criteria pertaining to process and pattern of adaptations set up in the comparative-methods literature. Specifically, I tested whether hypsodonty appeared coincident with or just after the spread of open, grass-dominated habitats in the Great Plains of North America. Phytolith (plant opal) analysis of 99 phytolith assemblages extracted from sediment samples from Montana/Idaho, Nebraska/Wyoming, and Colorado were used to establish the first continuous record of middle Eocene–late Miocene vegetation change in the northern to Central Great Plains. This record was compared with the fossil record of equids from the same area in a phylogenetic framework. The study showed that habitats dominated by C3 grasses were established in the Central Great Plains by early late Arikareean ($21.9 Ma), at least 4 Myr prior to the emergence of hypsodont equids (Equinae). Nevertheless, the adaptive hypothesis for hypsodonty in equids could not be rejected, because the earliest savanna-woodlands roughly co-occurred with members of the grade constituting the closest outgroups to Equinae (‘‘Parahippus’’) showing mesodont dentition. Explanations for the slow evolution of full hypsodonty may include weak and changing selection pressures and/or phylogenetic inertia. These results suggest that care should be taken when using functional morphology alone to reconstruct habitat change. Caroline A. E. Stro¨mberg. Departments of Palaeobotany and Palaeozoology, Swedish Museum of Natural History, Box 50007, SE-104 05 Stockholm, Sweden. E-mail: [email protected] Accepted:

6 September 2005

Introduction The early to middle Miocene of North America saw the independent evolution of high-crowned cheek teeth (hypsodonty), long legs, and large size in several ungulate lineages (e.g., rhinoceroses, oreodonts, camels, equids) (Webb 1977; Jacobs et al. 1999). Over the past 100 years it has become standard to view these evolutionary changes as an indication that savanna or grassland vegetation spread during this time (Osborn 1910; Scott 1937; Simpson 1944; Stirton 1947; Webb 1977, 1983; Janis 1984, 1993; Webb and Opdyke 1995). Implicit in this interpretation is that hypsodonty and associated traits were evolutionary responses to life in a new habitat and to a new diet: grasses. In particular, the late early Miocene radiation of horses in Equinae, with modified locomotory and masticatory apparati, and cementum-covered, highcrowned teeth—what Simpson (1951) referred q 2006 The Paleontological Society. All rights reserved.

to as ‘‘The Great Transformation’’—has long been regarded as the classic story of adaptation to a changing environment (Fig. 1) (e.g., Kowalevsky 1873; Osborn 1910; Matthew 1926; Huxley 1953; Mayr 1963; Gould 2002; MacFadden 2005). Some authors have gone further, citing the supposed parallel evolution of horses and grasses as a co-evolutionary ‘‘arms race’’ (Stirton 1947; Stebbins 1981; McNaughton and Tarrants 1983). In this context, specific focus has been put on a single character, namely hypsodonty (Fig. 2) (e.g., Van Valen 1960; Janis 1988; Janis et al. 2000, 2002; Jernvall and Fortelius 2002). Mammalian tooth shape is generally thought to reflect feeding ecology (see Butler 1983; Hiiemae 2000) and paleontologists routinely use tooth morphology to infer diet in fossil taxa (Janis 1984, 1997/98; Fortelius et al. 1996; Jernvall et al. 1996; but see MacFadden et al. 1999; Feranec 2004). Modern analogs would 0094-8373/06/3202-0006/$1.00

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FIGURE 1. Phylogeny of North American Equidae. Boxes mark the fossil occurrences of equid genera and (selected) species. Based on McFadden (1998) and Hulbert and MacFadden (1991). NALMA 5 North American Land Mammal Age; BAR 5 Barstovian, BLA 5 Blancan, BRIDG 5 Bridgerian, CHAD 5 Chadronian, CLARE 5 Clarendonian, DUCH 5 Duchesnean, HEM 5 Hemingfordian, HEMPH 5 Hemphillian, ORELL 5 Orellan, PE 5 Pleistocene, PLIO 5 Pliocene, WASAT 5 Wasatchian, WHIT 5 Whitneyan, E 5 early, M 5 middle, L 5 late. ‘‘M.’’ 5 ‘‘Merychippus.’’ Lineages of hypsodont horses (in the Equinae clade) are marked with heavier lines.

suggest that hypsodonty evolved coincident with, or in rapid response to, the emergence of open, grass-dominated habitats, specifically to cope with abrasive, silica-rich grasses or, alternatively, windblown dust that became incorporated into the diet in these environments (Osborn 1910; Matthew 1926; Simpson 1951; Janis 1988; Wang et al. 1994; MacFadden 1997, 2000). The advent of phylogenetic systematics has brought a novel perspective on adaptations, emphasizing the historical context of the evolution of functional traits (e.g., Gould and Vrba 1982). There is also increasing awareness that adaptive hypotheses must be tested using strict functional and phylogenetic criteria (e.g., Coddington 1988; Harvey and Pagel

1991). In light of this, the validity of assumptions regarding the adaptive nature of hypsodonty must be reexamined. It can no longer be assumed that the evolution of highcrowned cheek teeth during the early to middle Miocene was an adaptive response to changes in vegetation—it must be verified through rigorous testing. Historically, a scarcity of direct, paleobotanical data from areas with abundant vertebrate fossils has prevented paleontologists from challenging the notion that faunas transformed along with the spread of grasslands (reviews in Jacobs et al. 1999; Stro¨mberg 2002). However, an alternative record of vegetation change has recently become available through fossilized plant opal (phytoliths; Stro¨mberg

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FIGURE 2. Cheek tooth crown height in extant and fossil equids. A, B, Basic tooth morphology, redrawn from Janis and Fortelius (1988). A, Brachydont, or lowcrowned (human) tooth. The crown is defined as the enamel-covered part of the tooth above the gum line (Peyer 1968). B, Hypsodont, or high-crowned, (horse) tooth in which the height of the crown is increased through ontogenetically delayed root formation and finite tooth crown growth. Eruption of the crown occurs gradually in hypsodont teeth as the exposed part of the crown wears away (worn away crown marked by dashed lines). Note that the enamel is often present in most of the tooth, blurring somewhat the distinction between crown and root. C, Relative cheek tooth crown heights for fossil equids, redrawn and modified from MacFadden (1992: Fig. 11.6). Hypsodonty Index (HI) 5 M1MSTHT/M1APL (MacFadden 1992, 1998). Abbreviations (genera and species referred to in the text and in Fig. 1): ar 5 Archaeohippus; co 5 Cormohipparion; de 5 Desmatippus; di 5 Dinohippus; ep 5 Epihippus; eq 5 Equus; hi 5 Hipparion; hp 5 Hypohippus; hy 5 Hyracotherium; ka 5 Kalobatippus; meg 5 Megahippus; mes 5 Mesohippus (bairdii); mi 5 ‘‘Merychippus’’ insignis; mio 5 Miohippus; mp 5 ‘‘Merychippus’’ primus; na 5 Nannippus; ne 5 Neohipparion; on 5 Onohippidium; or 5 Orohippus; pc 5 ‘‘Parahippus‘‘cognatus; pl 5 ‘‘P.’’ leonensis; pr 5 Protohippus.

serve information about vegetation type, such as degree of habitat openness (Stro¨mberg 2004). Through this new record of habitat change, the assumption of adaptation for hypsodonty becomes a testable hypothesis. The aim of this paper is to evaluate critically the hypothesis that hypsodonty in equids evolved as an adaptation to grass-dominated habitats, using criteria set up by phylogeneticists. To provide background, I first review tests of adaptive hypotheses in the modern comparative-methods literature and discuss to what degree these tests can be applied to the evolution of hypsodonty (see ‘‘Testing a Hypothesis of Adaptation,’’ below). In the section that follows (‘‘Adaptive Explanation for Hypsodonty’’), I use current knowledge in relevant fields (tooth development, population dynamics, paleontology) to scrutinize each of the criteria for the adaptive hypothesis for hypsodonty. The remainder of the paper focuses on testing one of the phylogenetic criteria for adaptations, namely that which states that hypsodonty had to evolve coincident with or just after a change in vegetation. In this test, described in ‘‘Materials and Methods’’ and ‘‘Results,’’ I compare the timing of the evolution of hypsodonty in equids, as estimated from first occurrences of hypsodont taxa, with the timing of the emergence of grass-dominated habitats, as indicated by phytolith assemblage data. This is done in a phylogenetic framework, essentially following the phylogenetic comparative methods laid out by Greene (1986) and later authors (cited in Grandcolas and D’Haese 2003; see below). To detect geographic variation, I conduct the test for three separate areas (Nebraska/eastern Wyoming, northeastern Colorado, and southwestern Montana/Idaho). In the ‘‘Discussion’’ section, the outcome of the test and its implications for the hypothesis of adaptation for hypsodonty in horses are evaluated, and contrasted with previous studies. Testing a Hypothesis of Adaptation

2002, 2004, 2005). Phytoliths are highly suitable for paleoecological studies, because (a) they can preserve in the same sediment types as, and often in direct association with, mammal fossils (Stro¨mberg 2002), and (b) they pre-

The definition of adaptation in evolutionary biology as ‘‘any feature that promotes fitness and was built by selection for its current role’’ (Gould and Vrba 1982: p. 6; see also Williams 1966) emphasizes the historical component of

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FIGURE 3. Phylogenetic patterns extrapolated from different models of evolution. Black bar, appearance of trait (hypsodonty); gray bar, appearance of the demand for the function (feeding on grass/grit); plus sign, presence of trait/demand in an organisms; minus sign, absence of trait/demand. A, Demand for function and trait coincide; the trait is an adaptation. B, Demand for function appears much before trait; the trait is irrelevant to the task/ environment or an adaptation. C, Demand for function appears after trait; the trait is an exaptation. D, Demand for function occurs after trait. The trait appears to be an adaptation if parsimony methods are used to reconstruct ancestral selective factors, but is an exaptation in each lineage that possesses it. See text for further explanation.

the adaptation concept by making a clear distinction between current utility of a trait (‘‘adaptedness’’; Brandon 1990; Burian 1992) and its historical origin. Gould and Vrba (1982) formalized this view by coining the term ‘‘exaptation’’ for traits shaped by selection to perform a different function than they are presently serving, or that result from processes other than natural selection (e.g., genetic drift, sorting due to genetic/epigenetic linkage or pleiotropy) (Fig. 3). Using this historical definition, several authors have set up criteria for recognizing adaptations (e.g., Greene 1986; Padian 1987; Coddington 1988, 1990, 1994; Mishler 1988; Brandon 1990; Baum and Larson 1991; Edwards and Naeem 1993). These criteria fall into two classes, pertaining to selection (process) and phylogeny (pattern), respectively (Grandcolas and D’Haese 2003). The two sets of criteria work on different phenomenological levels—the population level and the clade level, respectively—which cannot be considered in a single approach (de Pinna and Salles 1990; Grandcolas and D’Haese 2003). The selection criteria specify that a trait fixed through natural selection has to be shown to (1) be heritable, (2) signify a solution to a problem that the environment presents (i.e., there

has to be a performance [functional] advantage to possessing the trait; Arnold 1983, 1994; Greene 1986; Brandon 1990), and (3) confer increased fitness on the organism that possesses it (e.g., Mishler 1988; Brandon 1990). The phylogenetic criteria involve statements about the direction of evolution across a clade; they predict that the purported adaptation will represent the derived (apomorphic) state (Greene 1986; Padian 1987; Coddington 1988, 1990, 1994; Mishler 1988). They also require that the problem to which the feature is a solution—a particular task or property of the environment—be manifested prior to the appearance of the trait (Fig. 3) (Baum and Larson 1991; Lauder et al. 1993; Blackburn 2002). Greene (1986) put it differently, stating that the trait has to occur coincident with a performance advantage of that trait; if the advantage appears much before the trait, the trait can be considered irrelevant to the task. The two views can be logically connected if variation for the trait exists in the population when the task appears. Given variation in the population, functional advantage and fitness advantage (leading to selection) of the trait should occur coincident with or just after the appearance of the demand for the function/task (but note that Greene [1986] did not include natu-

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ral selection in his definition of adaptation). In the fossil record then, the trait should be manifested coincident with or just after the task (Fig. 3). Although these criteria are clearly stated, tests of them have proven less straightforward (see Martins 2000 for a review). On a theoretical level, it is now widely recognized that an adaptive hypothesis can never be decisively tested if only the phylogenetic criteria are used (e.g., Carpenter 1989; Brooks and McLennan 1991; Grandcolas and D’Haese 2003). Rather, phylogenetic patterns should be used as null-models against which to test predictions from population level studies of process. On a practical level, phylogenetic tests of adaptive explanations are hampered because they are usually limited to extant organisms and environments. Ancestral character states are then reconstructed using modern distributions (parsimony methods; e.g., Baum and Larson 1991; Kohlsdorf et al. 2001) under the questionable assumption that traits and selective factors (task/environment) have changed at a slow rate relative to cladogenesis (see discussion in Frumhoff and Reeve 1994; Schluter et al. 1997; Cunningham et al. 1998; Losos 1999) (see Fig. 3D). This problem would partly be solved if fossil taxa were considered in tests of adaptation, an approach that is rarely practiced today (but see Hopkins 2005). However, even if the evolution of the trait across a clade can be reconstructed in detail from the fossil record, the issue of mapping the distribution among taxa of the demand for the function remains. Tasks such as behavior (climbing, herding etc.) seldom leave a fossil record that can be studied. Although environmental alterations creating new selective landscapes may be preserved in the fossil record (as a change in floras, paleosols, or various climate proxies), it is often difficult to demonstrate unequivocally an association between task and trait. For example, plants and animals are seldom preserved together. In addition, the temporal and spatial resolutions of different fossil records often differ substantially (e.g., Mess et al. 2001), and comparisons among them can never produce meaningful or definitive tests of adaptive hypotheses. Owing to the newly established record of

FIGURE 4. Geographic spread of floral (and faunal) localities included in this study (Stro¨mberg 2005). Biogeographical regions are from Janis et al. (1998). See text for further explanation.

vegetation change based on phytoliths (Figs. 4, 5) (Stro¨mberg 2004, 2005), I am able to conduct the first complete test of the phylogenetic criteria for a hypothesis of adaptation involving extinct organisms. Several other fortunate circumstances contribute to making the adaptive explanation for hypsodonty testable. First, multiple clades of ungulates (and rodents) evolved hypsodonty independently during the early Miocene (Janis et al. 1998; MacFadden 1997). This represents a ‘‘class’’ of events rather than a unique instance, potentially providing power to an adaptive explanation (e.g., Lauder et al. 1993; Leroi et al. 1994; Martins and Hansen 1996). Second, many of these ungulate clades, including equids, were endemic to North America for large parts of the Cenozoic (Janis et al. 1998), making possible a rough sampling of the environment in which the trait evolved. Third, the Cenozoic fossil record of North American ungulates is rich and well studied, providing temporal as well as spatial control on changes

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FIGURE 5. Phytolith assemblage data used in this study. A, B, Interpretation of fossil phytolith assemblages (represented as pie charts). A, Phytolith assemblage generally interpreted as representing closed forest. B, Phytolith assemblage interpreted as reflecting a relatively open, grass-dominated habitat (savanna or woodland). C. Vegetation patterns in the Northern and Central Great Plains of North America, based on phytolith assemblages. Adapted from Stro¨mberg (2005). Pie charts: black, forest indicator phytoliths (from dicotyledons, conifers, palms etc.); black with white dots, closed-habitat grass short cell assemblage (typical of bamboos and basal grasses); white, open-habitat short cell assemblage (from pooids, panicoids, chloridoids etc.); stippled dots, short cell assemblage from grasses with unknown autecology (open or closed habitat), but potentially related to open-habitat grasses. Rectangular area with oblique dotted lines indicates timing of the spread of grass-dominated habitats based on phytolith data; the height of the areas reflects the degree of uncertainty in timing for each region due to missing data and problems with relative and absolute age assignment (marked as black dashed arrows bracketing phytolith assemblages).

in character states and environments (Woodburne 1987, 2004; Janis et al. 1998). Finally, some of the clades that evolved high-crowned cheek teeth have living members, allowing a better understanding of factors pertaining to selection (e.g., physiology, behavior) (Potts and Behrensmeyer 1992). Adaptive Explanation for Hypsodonty Selection Criteria Heritability. Heritability of hypsodonty has not been explicitly investigated, but a body of work attests to the genetic basis of dental morphology (see Butler 1983; Fortelius 1985 for review).

Performance Advantage. Hypothetically, hypsodonty solves the problem of increased tooth wear resulting from various dietary factors, namely (a) silica phytoliths (particularly in grass tissue), (b) grit adhering to the surface of plants, or (c) lowered nutritive value of the food, which determines the amount that has to be consumed to satisfy basic metabolic needs (Simpson 1951; Baker et al. 1959; Walker et al. 1978; Covert and Kay 1981; Kay and Covert 1983; Fortelius 1985; Janis and Fortelius 1988; Williams and Kay 2001). The performance advantage of hypsodonty (and hypselodonty, or ever-growing teeth) is that it ‘‘increases the wear life of the dental battery, or allows more

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abrasive material to be processed without shortening the functional life of the teeth’’ (Radinsky 1984: p. 12; see also Fortelius 1985). Three observations in modern ungulates support the (lifetime) performance advantage of hypsodonty. First, non-hypselodont ungulates have a finite amount of tooth material. Once this is worn down, the animals cannot chew effectively and, hence, are unable to maintain nutritional status (e.g., Skogland 1988; Kojola et al. 1998; Pe´rez-Barberı´a and Gordon 1998a). Starvation appears to be a common cause of death in adult ungulates; thus, tooth durability is an important factor controlling longevity in ungulate taxa (e.g., Kurte´n 1953; Van Valen 1964; Gaillard et al. 2000a). Second, different food materials and substrates (sandy vs. less sandy) result in different tooth wear rates (e.g., Stirton 1947; Kay and Covert 1983; Skogland 1988). Third, a significant correlation exists in extant ungulates between hypsodonty and proxies for exogenous grit (feeding in open habitats, feeding close to the ground), even when controlling for phylogenetic effects (Janis 1988; Williams and Kay 2001). Diet is also correlated with hypsodonty, but the relationship is somewhat more complex (e.g., Janis 1995; Solounias and Moellecken 1993; Solounias et al. 1995). Level of aridity, which promotes the presence of both grasses and exogenous grit, and potentially negatively affects the nutritive value of graze and browse, is less clearly linked (Williams and Kay 2001, but see Damuth and Fortelius 2001; Fortelius et al. 2002). Although hypsodonty likely acts to prolong the period of effective chewing, it does not appear to contribute to higher effectiveness in the comminution of tough or gritty plant material. Consequently, it does not solve problems of decreased food intake at high population density or lowered availability of high-nutrition, easily chewed food (contra Williams and Kay 2001). Rate of food ingestion should instead relate more closely to the morphology of the occlusal surface and chewing behavior (Pe´rezBarberı´a and Gordon 1998a,b). Hypsodonty is often associated with complex ridging of the occlusal surface (such as lophodonty), promoting higher chewing effectiveness at moderate tooth wear (Rensberger 1973; Lanyon

and Sanson 1986). However, these two dental properties seem often to have been evolutionarily decoupled, including in horses (e.g., Rensberger et al. 1984; Janis and Fortelius 1988). Nevertheless, acquisition of hypsodonty in equids co-occurred with several changes in cheek tooth morphology that may also have increased chewing effectiveness (increased complexity of enamel folding, development of cementum covering the tooth crowns, and altered direction of enamel edges and jaw movement; e.g., Simpson 1951; Rensberger et al. 1984; MacFadden 1998). How these modifications relate to the evolution of hypsodonty will be discussed further below. Fitness. The proof that different dental morphologies influence fitness is largely circumstantial, relying on the apparent ‘‘fit’’ of tooth shapes to diet in modern mammals (Butler 1983; see above). Possible cases of selection on horizontal molar dimensions have been recognized in mass death assemblages of extinct horses (‘‘paleopopulations’’; MacFadden 1989, 1992) as a decrease in variance of measurements among older members of the population (e.g., ‘‘Merychippus’’ primus; Kurte´n 1953; Van Valen 1963, 1964, 1965; although note that the use of such cross-sectional data for calculating lifetime fitness is dubious [Arnold and Wade 1984b]). However, the effect of tooth crown height on fitness has not been measured in extant or fossil mammals in this way. Instead, Kurte´n (1953) and Van Valen (1964) argued the selective value of hypsodonty from the fact that many extant/fossil ungulates that (presumably) died from starvation due to worn-out molars seem in other respects to have been physically (i.e., reproductively) fit. Recent reviews of ecological research, revealing fundamental similarities in population dynamics among large herbivorous mammals, substantiate their claims (e.g., Gaillard et al. 2000a). Neoecological data suggest that adult life span commonly is a more important component of overall individual fitness than are so-called recruitment parameters (fecundity, juvenile survival) because of its relatively low phenotypic plasticity (Pfister 1998; Gaillard et al. 2000a,b). Moreover, although old females show a decline in survival, caused pri-

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marily by worn-out teeth (starvation), as well as in fecundity, the reproductive senescence has a later onset and is slower than the survival senescence (Clutton-Brock et al. 1988; Garrott et al. 1991; Be´rube´ et al. 1999; Gaillard et al. 2000a). Consequently, many females reproduce at moderate rates until death (e.g., Gaillard et al. 2000a). A trait such as hypsodonty, acting to extend the life of the cheek teeth and thereby slow the survival senescence, could significantly enhance lifetime reproductive output, and therefore potentially enhance fitness. Population Genetics. Hypotheses about microevolutionary processes require detailed information about population genetics (e.g., to understand gene flow; Arnold and Wade 1984a; Brandon 1990; Lauder et al. 1993). Fossil equids are unusual in the sense that quite a bit is known about their population dynamics (mortality, reproductive rates, demographic and social structure) and phenotypic variance—including for ‘‘Parahippus’’ leonensis, the closest sister taxon of Equinae (Fig. 1) (see MacFadden 1992 for review). This may allow reconstruction of some aspects of intra-demic genetic architecture, provided that the genetics of the trait are known. To my knowledge, no attempts have been made to present an explicit model for evolution of hypsodonty based on such information (but see Van Valen 1964). Selective Factor. Identification of the correct selective factor is vital in diagnosing natural selection and adaptation (Lauder et al. 1993; Leroi et al. 1994; Grandcolas and D’Haese 2003). The traditional explanation is ingestion of abrasives (grass or grit), but several alternatives have been discussed (see reviews in Fortelius 1985; Janis 1988). Most importantly, it has been suggested that hypsodonty was fixed in certain mammalian lineages as a result of positive allometric scaling to accommodate the metabolic requirements of mammals with larger body size (Simpson 1944; Van Valen 1960; Radinsky 1984) or to permit extended tooth use in mammals with longer life spans (generally correlated with body size [Huxley 1953]). However, studies of both extant and fossil ungulates have rejected these hypotheses (Simpson 1944; Fortelius 1985;

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Janis 1988; Solounias et al. 1994; Hansen 1997). Feeding on grass or grit, both associated with open habitats, therefore remains most viable as hypothesized selective factors for hypsodonty (see below for further discussion). It is questionable whether the selection criteria can be satisfied at this point. Instead, the pattern of roughly coincidental, independent origins of hypsodonty during the early Miocene constitutes the strongest evidence that selection acting across lineages with different genetic backgrounds was responsible for the fixation of this trait (e.g., Baum and Larson 1991; Lauder et al. 1993; Martins 2000). The progressive, albeit irregular increase in relative tooth crown height in various Equinae lineages over the past 18 Myr also supports an adaptive scenario for hypsodonty (as opposed to genetic drift, pleiotropy, or sorting [see Stirton 1947]) (Kurte´n 1953; Hansen 1997). Phylogenetic Criteria Apomorphy. Phylogenetic analyses (Prothero et al. 1986; Hulbert 1989; Hulbert and MacFadden 1991) have confirmed that hypsodonty is a derived character state in rhinoceroses and equids. Also, the proposed character state polarity is consistent with the temporal distribution of taxa in the fossil record (e.g., Janis et al. 1998). Correlation between Trait and Demand for Trait. As mentioned, the major obstacle to examining whether the earliest hypsodont horses lived in open habitats and/or fed on grass has been that the paleobotanical record previously did not allow detailed reconstruction of Eocene to Miocene vegetation changes in the Great Plains (Jacobs et al. 1999; Stro¨mberg 2002, 2004). Hence, workers have classically used the correlation between hypsodonty and diet/habitat in modern ungulates to make inferences about the ecology of related fossil taxa (e.g., Janis 1988, 1995). Even authors seeking expressly to test adaptive explanations for the evolution of hypsodonty have relied on the circular assumption that grassdominated habitats emerged coincidentally with high-crowned ungulates (or rodents; Hansen 1997; Mess et al. 2001; Williams and Kay 2001). In recent years, study of tooth wear has pro-

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vided more direct information about the diet of fossil ungulates (e.g., Walker et al. 1978; Teaford 1988; Janis 1990; Hayek et al. 1992; Fortelius and Solounias 2000; Solounias and Semprebon 2002). These data point to increased tooth wear in hypsodont equids and ‘‘Parahippus’’ taxa relative to more basal equids (Hulbert 1982, 1984; Hayek et al. 1992; Fortelius and Solounias 2000; Solounias and Semprebon 2002), perhaps consistent with a diet that incorporated some grass or other abrasive material. However, because only a few fossil horse taxa have been examined for tooth wear so far, it is not yet clear when, and in what taxa, significant amounts of abrasives became incorporated in the diet (i.e., when the demand for the function occurred). Moreover, microwear studies, which have provided vital diet information for extinct equids (e.g., Hayek et al. 1992; Solounias and Semprebon 2002), are not always reliable. This is because microwear only reflects the last few days or even hours of food processing (Solounias et al. 1994). Mesowear data that do not suffer from this ‘‘Last Supper Syndrome’’ (Solounias et al. 1994) have, to my knowledge, not yet been collected for the relevant taxa. Given the potential for behavioral flexibility (discussed below), a shift in diet may also not be a good proxy for the environmental change that is assumed to have ultimately stimulated the evolution of hypsodonty. Instead, habitat reconstruction must depend on direct paleobotanical data, providing information about openness as well as the presence and abundance of grasses. To summarize this assessment, it seems that hypsodonty fulfills enough of the adaptation criteria to qualify as a trait with high adaptedness (an aptation [Gould and Vrba 1982]), that is, as a trait of current utility to ungulates inhabiting open, grass-dominated habitats. There is also some suggestion that selection, rather than random, unique factors, was responsible for shaping this trait in a variety of ungulate lineages. In contrast, it is virtually unknown what the temporal and spatial correlation was between the earliest open, grassdominated habitats and the first appearance of equids with high-crowned cheek teeth (Fig. 3). Therefore, whether hypsodonty was a re-

sult of adaptive evolution in direct response to vegetation changes remains to be tested. Materials and Methods Despite the benefits of testing multiple, independent examples of evolution of hypsodonty, I am herein restricted to equids as a case study. The reason for this is the limited phylogenetic resolution in most non-equid ungulate clades (see Janis et al. 1998). There is also less agreement on what constitutes ‘‘hypsodont’’ and what functional significance should be placed on a relative increase in crown height; compare for example descriptions of crown height of ticholeptine oreodonts in Lander (1998) and Janis et al. (2004a). As a consequence, hypotheses of adaptation are currently not as well formulated for nonequid ungulates, even though the changes in these groups are often cited as examples of adaptive response to the spread of grasslands (Webb 1977; MacFadden 1997, 2000; see discussion in Janis 1988). Rhinocerotoids, which have a robust phylogeny (Prothero et al. 1986; Prothero 1998a,b), initially evolved hypsodonty in Eurasia (Prothero et al. 1989; Prothero 1998b); thus, the phylogenetic criteria cannot be evaluated using North American data. Equid Phylogeny Cladogram. The cladogram of equid relationships used in this study (see Fig. 6) is derived primarily from the overall cladogram presented by MacFadden (1992). This reconstruction is based on manual cladistic treatments of various groups of equids (e.g., MacFadden 1977, 1984, 1985, 1988; Prothero and Shubin 1989; see also Evander 1989), as well as maximum parsimony analyses (Hooker 1989; Hulbert 1989). More detailed resolution of the basalmost members of the clade Equinae is given by Hulbert (1989) and Hulbert and MacFadden (1991). Hulbert and MacFadden (1991) provide additional information about taxa within the paraphyletic genus ‘‘Parahippus.’’ Thus, ‘‘P.’’ cognatus and ‘‘P.’’ coloradensis were tentatively placed as sister taxa (in an unresolved polytomy) to the clade consisting of ‘‘P.’’ leonensis 1 Equinae as they share some of the derived characters that unite ‘‘P.’’ leonensis and Equinae (Hulbert and

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MacFadden 1991: p. 20). Other, more basal taxa within the ‘‘Parahippus’’ grade (following information in MacFadden 1998) were placed at a polytomous node outside this. This topology represents an untested hypothesis of relationships; an alternative arrangement would have been to leave the ‘‘parahippines,’’ save ‘‘P.’’ leonensis, as an unresolved node. Note that the two different topologies do not affect the timing of the origin of the clade consisting of Equinae 1 ‘‘Parahippus.’’ The remaining outgroups comprise genera of fossil equids; the systematics of these taxa are often problematic (see MacFadden 1998 for discussion). This hypothesis of relationships for equids was constructed using a range of morphological characters, but with an emphasis on dental morphology, including unworn/little worn M1 (or M2) mesostyle crown heights (M1MSTHT; or m1/m2 metaconid crown heights, if the upper molars are not available) (MacFadden 1992, 1998; Hulbert and MacFadden 1991). Hypsodont cheek teeth are by this definition unworn M1 and M2 with crown heights of greater than about 23–28 mm (MacFadden 1992, 1998). The latter character is closely related to degree of hypsodonty (which is a relative measurement). The use of characters that are the focus of comparative studies in tree-building is an issue only in cases where the exclusion or inclusion of the characters influences the topology of the cladogram (de Queiroz 2000). Several presumably independent characters support each node in the equid phylogeny used herein (see MacFadden 1992, 1998), so that the hypothesis of relationships does not hinge on crown height. In this study, hypsodont horses (Equinae) are referred to as the ingroup and the rest of the equid taxa are treated as outgroups. Only taxa that have their first appearance in the period for which vegetation data are available (middle Eocene to middle Miocene) are considered in the analysis. Character State Mapping. The present study is chiefly concerned with the initial acquisition of hypsodonty and treats it as a semiqualitative character, but note that relative tooth crown height in general is better de-

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scribed as a quantitative, continuously evolving feature (Fig. 2C) (Hansen 1997). The states for the character ‘‘degree of hypsodonty’’ are principally from MacFadden (1998) and include (1) brachydont, or lowcrowned teeth (Fig. 2A,C), (2) mesodont (comprising submesodont to incipient hypsodont), or middle-crowned teeth, (Fig. 2C), and (3) moderately hypsodont to hypsodont, or highcrowned, teeth (Fig. 2B,C). Degree of hypsodonty (hypsodonty index, HI) is defined as the unworn/little worn M1MSTHT divided by the greatest anteroposterior length of M1 (M1APL; or M2, m1/m2 if M1 is not available; MacFadden 1992, 1998). ‘‘Brachydont’’ refers to the situation when HI , 1; ‘‘hypsodont’’ is when HI . 1. Mesodonty is not rigorously defined, but it is transitional between brachydont and hypsodont; that is, HI is somewhat less than 1 (Fig. 2C) (B. MacFadden personal communication 2004). Note that authors have measured hypsodonty in different ways (compare Janis 1988, MacFadden 1998, and Fortelius et al. 2002; see Janis and Fortelius 1988 for review). For example, Janis et al. (2000, 2002, 2004a) and Williams and Kay (2001) recently used an HI (herein HIm3) defined as the unworn m3 height divided by m3 width (Janis 1988), and classified ‘‘brachydont’’ as HIm3 , 1.5, ‘‘hypsodont’’ as a HIm3 . 2.5, and ‘‘mesodont’’ as 1.5 , HIm3 , 2.5 (Janis 1988; Janis et al. 2000). Although it is not entirely clear how this scheme compares with MacFadden’s (1998), it is generally more conservative in what taxa qualify as hypsodont. Thus, the various merychippines that MacFadden (1998) labels ‘‘hypsodont’’ are ‘‘mesodont’’ by Janis et al.’s (2000, 2004a) standards. Despite these differences in terminology, vertebrate paleontologists agree on the pattern of a marked increase in relative crown height at the base of Equinae, and also subscribe to a hypothesis of adaptation to a changing environment indicated by these evolutionary changes (e.g., Simpson 1951; Webb 1977; MacFadden 1992, 2000; Janis 1993). MacFadden’s (1998) data are used herein because they are the most comprehensive for the Equidae and because they represent the most traditional treatment of hypsodonty. However, the difference in results when applying the

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FIGURE 6.

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Continued.

classification devised by Janis et al. (2000) will also be discussed. Temporal Ranges of Equids. The temporal ranges of equid taxa are from MacFadden (1998) and Hulbert and MacFadden (1991). The branching points on the phylogeny in Figure 6 represent the minimum age of divergence. Note that MacFadden et al. (1991) calculated a somewhat younger maximum age for the divergence of the Equinae lineage and ‘‘Parahippus’’ leonensis under the assumption that ‘‘Parahippus’’ leonensis contained the ancestral stock for Equinae. According to this interpretation, the divergence of the Equinae

lineage and ‘‘P.’’ leonensis can be dated to between the last occurrence of ‘‘P.’’ leonensis (17.7 6 1.4 Ma) and the first dated co-occurrence of ‘‘Merychippus’’ gunteri, ‘‘M.’’ primus, and ‘‘M.’’ cf. isonesus (16.2 6 1.4 Ma). Fossil Data, Geographic and Temporal Scope The Great Plains region is classically cited as the center for grassland evolution in North America (e.g., Wing 1998; Jacobs et al. 1999) and some of the first occurrences of Equinae and its closest sister taxa are recorded here (Janis et al. 1998). This study concentrated on the temporally relatively complete sedimen-

← FIGURE 6. Comparison between occurrences of equid taxa and grass-dominated habitats in the Great Plains of North America. Hypsodont taxa appear after the spread of grass-dominated habitats in all regions; see text for further explanation. A, Nebraska/eastern Wyoming. B, Northeastern Colorado. C, Southwestern Montana/Idaho. For key to cheek tooth crown height (color of box representing fossil taxon), see Figure 2C; for NALMA abbreviations, see Figure 1. Gray area indicates occurrence of grass-dominated habitats; area with oblique dotted lines indicate uncertainty in occurrence of grass-dominated habitats (see Fig. 5 and text for explanation); ovals and circles with stippled dots denote occurrence of taxon in region of interest; height of oval indicates degree of uncertainty in age of fossil (often the extent of the NALMA); black ovals (in A) denote occurrence of taxon in South Dakota (area adjacent to Nebraska/Wyoming). Taxa: ‘‘P. ’’ 5 ‘‘Parahippus;’’ ‘‘M.’’ 5 ‘‘Merychippus.’’ Note that MacFadden et al. (1991) would place the divergence of the Equinae lineage and ‘‘P. ’’ leonensis at a point in time after 17.7 6 1.4 Ma, based on the assumption that ‘‘P. ’’ leonensis represented the ancestral stock for Equinae.

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tological and fossil mammal records from the Central Great Plains (Nebraska/eastern Wyoming, northeastern Colorado) and Northern Great Plains (southwestern Montana/Idaho) (Fig. 4; biogeographical regions from Janis et al. 1998). This enabled a comparison of faunal and floral changes across latitudes and for a comprehensive span of time, from the Middle or late Eocene through the middle Miocene. As explained below, the sampling protocol was designed so that paleobotanical data could be closely correlated with the fossil record of mammals. Equid Occurrence Data. Occurrence data for ingroup and outgroup equids in Nebraska/ eastern Wyoming, northeastern Colorado, and southwestern Montana/Idaho were taken from MacFadden (1998), Hulbert and MacFadden (1991), Janis et al. (2004a), Nichols et al. (2001), Bailey (2004), D. Lofgren (unpublished data), and MIOMAP (http://www. ucmp.berkeley.edu/miomap/). These occurrence points were plotted onto the equid phylogeny to evaluate when each taxon appeared in the surveyed regions. Because the goal of the study is to come as close as possible to assessing the habitat in which the ingroup and sister taxa evolved, the emphasis was on early occurrences of each taxon. The age of each faunal locality is commonly given as a biostratigraphic subdivision of the North American Land Mammal Ages (NALMAs) following Janis et al. (1998). This relative timescale has been refined and more closely linked to global chronostratigraphy through recent magnetostratigraphy and absolute dating (e.g., Woodburne 1987, 2004; Alroy 1992, 1998; MacFadden and Hunt 1998; Prothero and Whittlesey 1998; see Prothero 1998c for review). Paleobotanical Data and Analysis. The phytolith study that forms the basis for this test is described in detail elsewhere (Stro¨mberg 2004, 2005). However, a brief account of the sampling strategy, methods, and inferred vegetation patterns is nevertheless needed. To fit the faunal and floral data into a common stratigraphic framework, sampling focused on (1) actual and proposed lithostratigraphical type and reference sections and (2) well-known mammal quarries. Whenever

possible, several facies were collected to test for spatial variation in vegetation, which might otherwise obscure the signal. The resulting data set consists of 99 phytolith assemblages (52 from Nebraska/eastern Wyoming, 22 from Colorado, and 25 from southwestern Montana/Idaho) (Fig. 4) extracted from sediment using modified standard methods (Stro¨mberg 2004, 2005). For each phytolith assemblage, vegetation was inferred by comparing the relative abundance of so-called forest indicator phytoliths (phytoliths typically produced by herbaceous and woody dicotyledons, conifers, and ferns, as well as palms and gingers), with the relative abundance of grass phytoliths (grass silica short cells) (Fig. 5A,B). The grass silica short cells were further differentiated into short cells produced by grasses that thrive in more closed habitats (e.g., bamboos and basal grasses) and short cells from open-habitat grasses. Within open-habitat grasses, C3 pooids can be distinguished from C4 panicoids and chloridoids (Stro¨mberg 2004, 2005). The analysis of vegetation change concerned relative changes through time, but generally, phytolith assemblages with abundant (.50%) forest indicator phytoliths and grass short cells inferred to derive mainly from bamboos and other closedhabitat grasses were interpreted as reflecting forest (Fig. 5A) (see Stro¨mberg 2004, 2005 for details). Assemblages dominated by grass short cells from open-habitat grasses were interpreted as representing grass-dominated habitats, such as woodland, savanna, or more open grassland—depending on the relative amounts of forest indicators and grass short cells (Fig. 5B). Pattern. As outlined by Stro¨mberg (2005), habitats such as woodlands or savannas, dominated by mainly C3 pooid open-habitat grasses, existed in Nebraska/eastern Wyoming by (at least) the early late Arikareean (earliest Miocene; $21.9 Ma), in northeastern Colorado by the early Hemingfordian ($19 Ma), and in southwestern Montana/Idaho by the late Hemingfordian ($17 Ma) (Fig. 5C). Prior to this, the Central Great Plains (Nebraska/Wyoming and Colorado) appear to have been covered by closed forests with an understory of bambusoid/basal grasses. Closed forests

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also seem to have predominated in the Northern Great Plains (Montana/Idaho) during the Eocene and Oligocene. In many Northern Great Plains floras, grasses of unclear affinity (but potentially related to open-habitat grasses) were abundant. However, their autecology is not interpreted as typical open-habitat (Stro¨mberg unpublished data). The record in Nebraska/eastern Wyoming implies a subtle trend toward increasingly open savanna/ woodland landscapes during the early Miocene. The interpretation of the date in million years for the vegetation change reflects the estimated absolute age of the localities (Stro¨mberg 2005). The large uncertainty in timing (marked in Fig. 5C by the areas with oblique dotted lines) relates to (a) the lack of late Oligocene–early Miocene sediments in the regions (primarily in Colorado), and (b) problems with dating localities independently of lithostratigraphy, biostratigraphy, or both. The latter is particularly a problem in Nebraska/eastern Wyoming, where phytolith assemblages that would be assigned, on the basis of lithostratigraphy and faunal association, to the late Oligocene (Monroe Creek Formation) may be as young as 21.9 Ma (MacFadden and Hunt 1998; Stro¨mberg unpublished data). Comparison of Paleobotanical and Equid Data. The data on first appearances of equid taxa with mesodont and hypsodont cheek teeth were contrasted with the timing of the spread of grasslands in each region separately: Nebraska/eastern Wyoming (Fig. 6A), northeastern Colorado (Fig. 6B), and southwestern Montana/Idaho (Fig. 6C). The comparisons were made on a regional scale, not on a locality-by-locality basis. Although there is ample faunal material collected from these areas in various museums (e.g., American Museum of Natural History, University of California Museum of Paleontology, University of Nebraska State Museum, University of Montana; see Stro¨mberg 2005), much of it is still not described and it is likely that the occurrence data will change as more faunal assemblages are treated in detail. Also, the geographic spread of phytolith data points is evidence for a regional occurrence of grass-dominated habitats (Figs. 4, 5). It seems therefore that a regional-

scale study is appropriate at this point. The chronostratigraphy of the Great Plains deposits is still in progress and the detailed correlation among regions and localities may change (Janis et al. 1998). These changes are likely to be most important on an interregional scale and have less effect on the intraregional comparisons between flora and fauna that form the focus of this study. To make phytolith data and faunal data comparable, I binned the phytolith assemblages in North American Land Mammal Ages (NALMAs), rather than using their absolute ages (when available). For example, all phytolith assemblages from the early late Arikareean (and possibly one from the late early Arikareean) indicate plant communities with a large proportion of open-habitat grasses, and it is assumed that this vegetation type prevailed throughout this NALMA (early late Arikareean). Results From the character states mapped on the horse cladogram (Fig. 6), it is inferred that a marked increase in cheek tooth crown height—to full hypsodonty—occurred by the time the members of Equinae had diverged (by ;18 Ma). An increase in relative crown height (to mesodont) occurred already by the early late Arikareean (23–19.2 Ma), at the base of the paraphyletic genus ‘‘Parahippus,’’ constituting the sister taxa to Equinae. The plots show that, in this limited data set, most of the earliest occurrences of ingroup and immediate outgroup taxa were in Nebraska/eastern Wyoming (Fig. 6A) (Janis et al. 1998). These data are thus most appropriate for testing the hypothesis of adaptation and will be described first. Fortuitously, the timing for the spread of grass-dominated habitats is also best constrained for this region (Fig. 5C) (Stro¨mberg 2005). The comparison of faunal and floral information for Nebraska/eastern Wyoming demonstrates that although the emergence of mesodont members of ‘‘Parahippus’’ during the early late Arikareean coincided on a very rough scale with the earliest open, grass-dominated habitats, basal members of Equinae appeared in the area at least 4 Myr after this veg-

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etation change. Using Janis et al.’s (2000, 2004a) classification of tooth crown height increases the offset in timing between grassy vegetation and ‘‘truly’’ hypsodont horses (HIm3 . 2.5) in the Central Great Plains. The first hypsodont horse, according to this scheme, were members of the genus Protohippus (Fig. 1), which appeared in New Mexico in the late Hemingfordian (17.5–16 Ma). However, the earliest member of Equinae to occur in the Central Great Plains was Calippus, known from the early Barstovian (15–14 Ma)—at least 10 Myr after the spread of grassdominated habitats. As mentioned earlier, the merychippines are classified as mesodont and ‘‘Parahippus’’ species as submesodont (Janis et al. 2004a). The records from Colorado and Montana/ Idaho point to a similar pattern, with mesodont and hypsodont (sensu MacFadden 1998) equids appearing only after the regional spread of open, grass-dominated habitats in (or before) the Hemingfordian ($18–16 Ma; Fig. 6B,C). Note that, in the case of Colorado, the interpretation is obscured by the scarcity of floral and faunal data from the Arikareean. Discussion Pattern The $4 Myr lag between the spread of open-habitat grasses and manifestation of full hypsodonty in equids implies that the presumed functional demand for markedly increased cheek tooth crown height significantly preceded the evolution of this trait. If variation in tooth crown height existed in equid populations (see discussion below), the same can be said for the performance advantage of possessing relatively higher tooth crowns. Given this substantial offset in timing between task and trait, can hypsodonty be considered a direct evolutionary response to grassland habitats (Fig. 3B)? The coincidence, at a currently coarse scale, of mesodont ‘‘Parahippus’’ taxa and grassdominated habitats in the Central Great Plains sheds some light on this question. Although more data from the early late Arikareean are needed to verify the pattern, it implies that (small) changes in tooth crown height in this

lineage started roughly at a time when grasses were becoming important parts of ecosystems. This study, therefore, cannot reject the hypothesis that increased cheek tooth crown height in equids was an evolutionary response to open, grass-dominated habitats, but suggests that it was substantially slower than has been previously assumed (e.g., MacFadden and Cerling 1994; Wang et al. 1994; Hansen 1997; Jacobs et al. 1999; MacFadden 1998, 2000; Janis et al. 2000; but see Stirton 1947; Janis 1982). In this context, what can be said about the diet of ‘‘Parahippus’’? Tooth wear data indicate that early to middle Miocene equids were mixed feeders (or unusual [C3] grazers), but that progressively more grass was included in the diet in later taxa (Hayek et al. 1992; Fortelius and Solounias 2000; Solounias and Semprebon 2002). This implies that equids such as ‘‘Parahippus’’ taxa did not fully utilize the new food resource (grasses), or that they fed mainly on less abrasive (and grit-free), fresh grass, and consequently would not ‘‘need’’ fully hypsodont teeth. On the other hand, there is evidence from study of enamel microstructure in fossil equids that at least ‘‘Parahippus’’ leonensis had acquired cheek teeth with alternative modifications for increased resistance to dietary wear that may have compensated in part for lower crown heights in this taxon (Pfretzschner 1993). ‘‘P.’’ leonensis possessed teeth with a significantly thickened layer of radial enamel relative to other equid taxa (Pfretzschner 1992, 1993; note that this feature may also have implications for the interpretation of this species as the direct ancestor of Equinae). This equid also showed the modest beginnings of the modified radial enamel layer that characterize the hypsodont horses in Equinae. This material is modeled to better withstand shear stresses associated with the chewing movements in grazers as opposed to browsers (Rensberger et al. 1984; Pfretzschner 1992, 1993). However, in ‘‘P.’’ leonensis it was apparently too thin and in the wrong location to affect enamel strength (Pfretzschner 1992, 1993). Comments on Process Why did no early Miocene equids quickly adapt to take advantage of the earliest grass-

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dominated habitats? Previous research offers several explanations for such offsets in timing. Evolutionary lags can be a function of weak selection for a trait relating to extrinsic factors and/or behavioral compensation (see Blomberg and Garland 2002). For example, if the vegetation became incrementally more open during the early Miocene, there may have been a change in selection pressure toward more full grazing in certain equid populations (Stro¨mberg 2002). Behavioral plasticity, for example seeking out browse or less abrasive, fresh grass would initially act to dampen selection in this case (Wake et al. 1983; Edwards and Naeem 1993). Phytolith data are partly consistent with this hypothesis (Fig. 5). As mentioned above, habitats of the earliest Miocene (early late Arikareean) appear to have contained a greater non-grass (tree) component than later vegetation, and would potentially have been able to sustain a higher number of browsers. Information about habitat patchiness, which might be of relevance to test this hypothesis, is inconclusive because of limited temporal control on the phytolith assemblages analyzed to date. Nevertheless, it is important to note that even early Miocene habitats were grass-dominated, and by at least the late late Arikareean (about 1 Myr, or one mammal zone [biochron], before the radiation of hypsodont horses), open-habitat grasses dominated all parts of the landscape in Nebraska/eastern Wyoming. A change in selection intensity during the late early Miocene could similarly be hypothesized to be a consequence of a heightened influx of grit (Stirton 1947; Janis 1988). Stirton (1947) cited the increasing prevalence of coarser sediment types—sand instead of silt—with a (continued) high component of volcanic ash in the Central Great Plains during the late Oligocene to early Miocene (late Arikareean: Harrison Formation, Anderson Ranch Formation) as evidence for this idea. This shift in sedimentation is roughly coincident with the spread of grass-dominated environments as indicated by phytoliths and cannot itself explain the discrepancy between ecosystem change and equid morphology (e.g., Swinehart et al. 1985). It has recently been suggested that hypso-

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donty is/was favored by changes in vegetation indicative of ‘‘generalized water stress’’ leading to intensified tooth wear (Fortelius et al. 2002; but see Williams and Kay 2001 for a different view). Apart from increased representation of phytoliths and dust, such changes would include lowered nutritive value and higher fiber content of plants. According to this view, more pronounced (seasonal) aridity in Great Plains savanna habitats during the early Miocene would have diminished the digestibility of grasses and other plants. This would have provided added selective pressure by necessitating increased intake of food to maintain nutritional status. A marked increase in seasonal aridity in the late early Miocene is not supported by phytolith data, which show the prevalence of palms and other moisture-dependent plants in the Northern and Central Great Plains through the middle Miocene (Stro¨mberg unpublished data). Moreover, the explanation for the empirical relationship between water-stress and hypsodonty (Fortelius et al. 2002) may need adjustments. Modern ecological studies have shown that while temperature is positively related to shear strength and a decline in digestibility in plants, aridity appears to have the opposite effect (Wilson and Hacker 1987; Wilson et al. 1991; Wilson and Kennedy 1996; Henry et al. 2000; Barreto et al. 2001; Groot et al. 2003). It is also not clear to what extent fiber content and/or toughness of food material affects tooth wear (which depends mainly on differences in hardness [Lucas et al. 2000]). Finally, it has been proposed that selection for tooth durability increased during the early Miocene as a direct result of a coevolutionary ‘‘arms race’’ between horses and grasses (Stirton 1947; Stebbins 1981; McNaughton and Tarrants 1983). Phytolith production in several lineages of open-habitat grasses would have accelerated in the late early Miocene as a response to higher levels of grazing, which in its turn stimulated the evolution of hypsodonty. For several reasons, this appears to be a less likely explanation (Stro¨mberg 2002). First, phytolith formation is plesiomorphic within the grass clade and abundant silica production characterizes grasses of both closed-habitat and open-habitat ecology (e.g., Piperno

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and Pearsall 1998; Kellogg 2001). Although it has not been explicitly tested, extant relatives of open-habitat grasses that were likely foraged upon in early Miocene savannas do not seem to deposit more silica than, for example, bamboos, which were present in the Great Plains from at least the late Eocene (Stro¨mberg 2004; but note that it cannot be ruled out that bamboos were also fed upon and put under selective pressure to produce more opal). Second, phenotypic plasticity in silica production is not related to grazing pressure (Vicari and Bazely 1993), but potentially to environmental moisture levels (see Stro¨mberg 2004 for discussion). Third, despite voluminous research on the subject (e.g., McNaughton and Tarrants 1983; McNaughton et al. 1985; Cid et al. 1989), there is no convincing evidence for a deterring effect of phytoliths on modern vertebrate grazers (see review in Vicari and Bazely 1993). Phylogenetic inertia (sensu Wilson 1975; see Blomberg and Garland 2002 for discussion), caused by various genetic, developmental, physical, and behavioral factors and conditions (‘‘constraints’’; e.g., Hansen 1997) can also retard the evolution of a trait. For instance, there may simply not have been enough genotypic/phenotypic variation in equid populations to allow for selection (Wilson 1975; Edwards and Naeem 1993). There is little evidence that this was the case. A 4–10% phenotypic variation in tooth measurements, including unworn tooth crown height of various cheek teeth, seems to have been standard in fossil equid populations (Hyracotherium species [horizontal measurements only]: Gingerich 1981; ‘‘Mesohippus bairdii’’ [horizontal measurements only]: Forste´n 1970b; ‘‘Parahippus’’ leonensis: Bader 1956; ‘‘Merychippus’’ primus: Van Valen 1963; other ‘‘Merychippus’’ species: Downs 1961; Forste´n 1970a; see MacFadden 1989, 1992 for review). Of particular interest is ‘‘Parahippus’’ leonensis, which exhibited an unusual variance both in tooth measurements and in non-dimensional traits such as amount of cementum, complexity of enamel patterns, and manifestation of the crochet (Bader 1956). Unfortunately, the phenotypic variability of earlier species of ‘‘Parahippus’’ is unknown. Developmental or functional constraints

may occur if the evolution of a particular trait is dependent on that of another (Hansen 1997). To this effect, Radinsky (1983, 1984) argued that evolution of fully hypsodont cheek teeth would not have been possible in ‘‘Parahippus’’ and earlier taxa given the limited space beneath the eye. A fundamental reorganization of the cranium, which included a forward shift of the entire tooth row relative to the eye socket, occurred parallel to the initial changes in relative tooth crown height in the ‘‘parahippines’’ (Radinsky 1984). These modifications were therefore exaptive with respect to full hypsodonty, and it has been proposed that they may be linked to the evolution of larger and more efficient jaw musculature (Radinsky 1983, 1984). It can be noted that the evolution of hypsodonty in camels was not accompanied by the same degree of posterior shift of the eye socket; as a result, the roots of their cheek teeth protrude into the orbit (C. M. Janis personal communication 2004). Other authors have put forward that the acquisition of crown cementum or a certain enamel microstructure that would act to strengthen the teeth may have been vital to enable the evolution of full hypsodonty; such changes were initiated within the ‘‘Parahippus’’ grade (Stirton 1947; Simpson 1951; Pfretzschner 1993). Several other morphological and behavioral changes that may have been crucial to enable full grazing include alteration of the digestive system and predator evasion (Simpson 1951; Mayr 1963; Hansen 1997). Thus, it can be concluded that if hypsodonty was an adaptation to feeding in open habitats, then a combination of weak (and changing) selection pressure and phylogenetic inertia may explain the lag between the spread of grassdominated vegetation and the evolution of the tools necessary to take advantage of it. Hansen (1997) expressed a similar idea. He modeled the evolution of hypsodonty as a progressive, but irregular, shift in the realized or ‘‘local’’ adaptive optimum toward a primary adaptive optimum of full grazing in modern horses. The rate of this change was determined by phylogenetic inertia due to phylogenetic correlation and past ‘‘selective regimes’’ (sensu Hansen 1997). Implicit in this model was that the hypothetical primary op-

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timum originated at the base of the Equinae; in contrast, the current study suggests that there was a more gradual shift in the primary optimum (selective factor) throughout the early Miocene. Hansen’s (1997) theoretical framework is a modern take on Simpson’s (1944) model of long-term evolution of horses, in focusing on the movement of adaptive peaks rather than movement of populations between adaptive peaks. This causes organisms to be ‘‘locally’’ adapted to their environment at every point in time, against a background of constraints (Hansen 1997). Accordingly, the tooth crown height of ‘‘Parahippus’’ taxa would be locally adapted to a diet of mixed browse and graze or on less abrasive, fresh grass. It is important in this context to emphasize the modern view of equid evolution as something far from a progressive march toward grazing, but more like a branching bush (MacFadden 1992, 2005) (see Fig. 6). Various taxa within the ‘‘Parahippus’’ grade, although classically regarded as morphologically and ecologically ‘‘transitional,’’ persisted until ca. 11 Ma, and equids with browser morphology coexisted with hypsodont horses in Miocene savanna habitats (MacFadden 1992). The rough correlation in time and space between hypsodont taxa and grassland vegetation in Montana/Idaho in the late Hemingfordian (17.5–16 Ma) (Fig. 6C) is also interesting from the viewpoint of the models of evolution described above. The association indicates that early hypsodont (and perhaps mesodont) horses tracked open, grass-dominated habitats as they spread from the Central Great Plains northward. This suggests that the earliest high-crowned horses relied on grasses as a source of food, or on grasslands as habitats, and were therefore clearly removed from their ancestral selective regimes (Hansen 1997). Assuming that hypsodonty was, broadly speaking, an adaptation to open, grass-dominated habitats, was the change in diet to grasses or increased consumption of grit ultimately responsible for this trait? Phytolith information cannot resolve this question, because vegetation dominated by open-habitat grasses is almost by definition open, and thereby exposed to wind-transported dust. However, the microwear patterns found in ‘‘Parahippus’’

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spp. and hipparionine horses consist of numerous fine scratches and nearly no large pits or gouges. This implies that abrasive plant material, not grit, was primarily responsible for wear in these animals (Solounias and Semprebon 2002). MacFadden and Cerling (1994) also pointed out that there is no correlation between hypsodont horses and particular sedimentary environments where high levels of windblown dust might be inferred. These patterns tentatively corroborate the classical scenario for the evolution of hypsodonty in equids as an evolutionary response to grasses (e.g., Kowalevsky 1873; Osborn 1910; Webb 1977, 1983). On the other hand, a very close temporal co-evolutionary link between the expansion of open-habitat grasses and grazing animals (suggested by, for example, Stebbins 1981; Webb 1983; McNaughton and Tarrants 1983; Retallack 2001) is not supported in this case, although it cannot be excluded that grazers influenced the evolution of grasses on a smaller scale, and vice versa (McNaughton et al. 1985). This study also substantiates previous suggestions that hypsodonty in certain Eocene ungulates (e.g., leptauchiniine oreodonts and stenomyline camels) was not a response to the spread of modern, open-habitat grasses (Janis 1995; Janis et al. 1998). Conclusion This study represents one of the first to use direct paleobotanical data temporally and spatially correlated with fossil mammals in a phylogenetic context to test a hypothesis of adaptation. It showed that grass-dominated vegetation significantly pre-dated the evolution of full hypsodonty in horses. This weakens the argument for coevolution in lockstep between grasses and horses, but cannot reject that hypsodonty was an adaptation to feeding in open, grass-dominated habitats. Proof that natural selection was responsible for shaping this feature is beyond the scope of this study and likely intractable. Nevertheless, the demonstrated pattern of evolutionary lag in presumed adaptations is an important lesson for neontologists, and should be kept in mind by paleontologists who are restricted to using functional morphology to infer environmental changes.

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From existing data it is difficult to tease apart the potential roles of selection intensity and constraints in the observed 4 Myr delay between the spread of open, grass-dominated habitats and the evolution of high-crowned equids. Future work on the adaptive role of hypsodonty must attempt to integrate information on changes in tooth morphology and in other associated traits (relating to locomotion, mastication, etc.; see Rensberger et al. 1984; Janis et al. 2004b) for all clades of ungulates (and rodents) that evolved highcrowned teeth at the time when grass-dominated habitats spread—and those that evolved them much earlier. A comparative study of the order and timing of character evolution should be possible once appropriate phylogenetic hypotheses become available. In combination with knowledge of genetic and functional correlation among traits in groups with extant members (Blomberg and Garland 2002), such an examination may provide some insight into the factors that influenced the timing of the evolution of high-crowned teeth in ungulates. Additional studies should also include refinement and broadening of the pattern of vegetational and faunal correlation presented herein. The geographic areas and exact times of cladogenesis and morphological evolution in horses and other ungulates are not fully understood. A further complication is the degree of faunal endemism during the early Miocene (Webb 1977; Hulbert and MacFadden 1991). It is also apparent from the number of ghost lineages in the phylogeny (Figs. 1, 6) that many equid taxa are under-sampled and that first appearance events in the fossil record may be crude approximations of actual first appearances (see discussion in Alroy 1998). Despite the many uncertainties, this type of analysis currently represents the only way to test the hypothesis that hypsodonty evolved in the context of open grasslands. As such, it can serve as a starting point for future, more refined paleoecological investigations. Acknowledgments This work is part of dissertation research conducted in the Department of Integrative Biology and Museum of Paleontology

(UCMP), University of California at Berkeley. I thank W. A. Clemens, H. W. Greene, T. F. Hansen, B. J. MacFadden, and K. Padian for discussions around adaptation and horse evolution, and the UCMP students, faculty, and staff for input and discussion. I am grateful to N. C. Arens, C. M. D’Antonio, M. Fortelius, P. D. Gingerich, P. A. Holroyd, D. R. Kaplan, D. R. Lindberg, K. Padian, L. Werdelin, G. P. Wilson, and two anonymous reviewers for constructive criticism and useful comments on earlier versions of this manuscript. This work was funded by research grants from the Department of Integrative Biology (Summer Fellowships), UCMP, von Beskow’s Fund, Royal Academy of Science (Sweden), Geological Society of America, Paleontological Society of America, Sigma Xi, and National Science Foundation (Dissertation Improvement Grant DEB-1-0104975) as well as a Swedish Research Council grant to E. M. Friis and L. Werdelin. This is UCMP contribution no. 1896. Literature Cited Alroy, J. 1992. Conjunction among taxonomic distributions and the Miocene mammalian biochronology of the Great Plains. Paleobiology 18:326–343. ———. 1998. Diachrony of mammalian appearance events: implications for biochronology. Geology 26:23–26. Arnold, S. J. 1983. Morphology, performance and fitness. American Zoologist 23:347–361. ———. 1994. Investigating the origins of perfomance advantage: adaptation, exaptation and lineage effects. Pp. 123–168 in P. Eggleton and R. Vane-Wright, eds. Phylogenetics and ecology. Academic Press, London. Arnold, S. J., and M. J. Wade. 1984a. On the measurement of selection in natural and laboratory populations: theory. Evolution 38:709–719. ———. 1984b. On the measurement of selection in natural and laboratory populations: application. Evolution 38:720–733. Bader, R. S. 1956. A quantitative study of the Equidae of the Thomas Farm Miocene. Bulletin of the Museum of Comparative Zoology 115:47–78. Bailey, B. E. 2004. Biostratigraphy and biochronology of early Arikareean through late Hemingfordian small mammal faunas from the Nebraska panhandle and adjacent areas. Paludicola 4:81–113. Baker, G., L. H. P. Jones, and I. D. Wardrop. 1959. Cause of wear in sheeps’ teeth. Nature 184:1583–1584. Barreto, G. P., M. d. A. Lira, M. V. F. d. Santos, and J. C. B. Dubeux Ju´nior. 2001. Evaluation of elephant grass clones (Pennisetum purpureum Schum.) and an elephant grass 3 pearl millet (Pennisetum glaucum (L.) R. Br.) hybrid submitted to water stress. 2. Nutritive value. Revista Brasileira de Zootecnia 30:7–11. Baum, D. A., and A. Larson. 1991. Adaptation reviewed: a phylogenetic methodology for studying character macroevolution. Systematic Biology 40:1–18. Be´ rube´, C., M. Festa-Bianchet, and J. T. Jorgenson. 1999. Indi-

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