Download Evolution of hypsodonty in equids: testing a hypothesis of adaptation

Paleobiology, 32(2), 2006, pp. 236–258
Evolution of hypsodonty in equids:
testing a hypothesis of adaptation
Caroline A. E. Strömberg
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. Strömberg. 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
EVOLUTION OF HYPSODONTY IN EQUIDS
237
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; Strömberg 2002).
However, an alternative record of vegetation
change has recently become available through
fossilized plant opal (phytoliths; Strömberg
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CAROLINE A. E. STRÖMBERG
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 (Strömberg
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 (Strömberg 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
EVOLUTION OF HYPSODONTY IN EQUIDS
239
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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CAROLINE A. E. STRÖMBERG
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 (Strömberg 2005). Biogeographical regions are from Janis et al. (1998). See text for
further explanation.
vegetation change based on phytoliths (Figs.
4, 5) (Strömberg 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
EVOLUTION OF HYPSODONTY IN EQUIDS
241
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 Strömberg (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
242
CAROLINE A. E. STRÖMBERG
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; Pérez-Barberı́a 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.,
Kurtén 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 (PérezBarberı́a 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; Kurtén 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, Kurtén (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-
EVOLUTION OF HYPSODONTY IN EQUIDS
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; Bérubé 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;
243
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]) (Kurtén 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; Strömberg 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-
244
CAROLINE A. E. STRÖMBERG
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
EVOLUTION OF HYPSODONTY IN EQUIDS
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-
245
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
246
CAROLINE A. E. STRÖMBERG
EVOLUTION OF HYPSODONTY IN EQUIDS
FIGURE 6.
247
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.
248
CAROLINE A. E. STRÖMBERG
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 (Strömberg
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
(Strömberg 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 (Strömberg 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 Strömberg 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 Strömberg (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
249
EVOLUTION OF HYPSODONTY IN EQUIDS
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
(Strömberg 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 (Strömberg 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; Strömberg 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
Strömberg 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)
(Strömberg 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-
250
CAROLINE A. E. STRÖMBERG
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-
EVOLUTION OF HYPSODONTY IN EQUIDS
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
(Strömberg 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-
251
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 (Strömberg 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 (Strömberg 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
252
CAROLINE A. E. STRÖMBERG
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 (Strömberg
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 Strömberg 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]: Forstén 1970b; ‘‘Parahippus’’ leonensis: Bader 1956; ‘‘Merychippus’’ primus: Van Valen 1963; other ‘‘Merychippus’’ species: Downs 1961; Forstén 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-
EVOLUTION OF HYPSODONTY IN EQUIDS
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’’
253
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.
254
CAROLINE A. E. STRÖMBERG
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.
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