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ORIGINAL ARTICLE
doi:10.1111/evo.14187
Why aren’t rabbits and hares larger?
Susumu Tomiya1,2,3, 4,5 and Lauren K. Miller4
1Center for International Collaboration and Advanced Studies in Primatology, Kyoto University Primate Research
Institute, Inuyama, Aichi 484–8506, Japan
2Negaunee Integrative Research and Gantz Family Collections Centers, Field Museum of Natural History, Chicago, IL
60605, USA
3Museums of Paleontology and Vertebrate Zoology, University of California, Berkeley, CA 94720, USA
4Department of Integrative Biology, University of California, Berkeley, CA 94720, USA
5E-mail: tomiya.susumu.8r@kyoto-u.ac.jp
Received June 17, 2020
Accepted February 3, 2021
Macroevolutionary consequences of competition among large clades have long been sought in patterns of lineage diversication.
However, mechanistically clear examples of such effects remain elusive. Here, we postulated that the limited phenotypic diversity
and insular gigantism in lagomorphs could be explained at least in part by an evolutionary constraint placed on them by potentially
competing ungulate-type herbivores (UTHs). Our analyses yielded three independent lines of evidence supporting this hypothesis:
(1) the minimum UTH body mass is the most inuential predictor of the maximum lagomorph body mass in modern ecoregions;
(2) the scaling patterns of local-population energy use suggest universal competitive disadvantage of lagomorphs weighing over
approximately 6.3 kg against artiodactyls, closely matching their observed upper size limit in continental settings; and (3) the
trajectory of maximum lagomorph body mass in North America from the late Eocene to the Pleistocene (37.5–1.5 million years ago)
was best modeled by the body mass ceiling placed by the smallest contemporary perissodactyl or artiodactyl. Body size evolution
in lagomorphs has likely been regulated by the forces of competition within the clade, increased predation in open habitats, and
importantly, competition from other ungulate-type herbivores. Our ndings suggest conditionally-coupled dynamics of phenotypic
boundaries among multiple clades within an adaptive zone, and highlight the synergy of biotic and abiotic drivers of diversity.
KEY WORDS: Body size, competition, macroecology, macroevolution, Lagomorpha.
Efforts to unravel the biotic and abiotic drivers of biological di-
versity can be traced back at least to Lyell’s (1832) Principles
of Geology, which highlighted the deep temporal dimension of
the problem and paved the way for the Darwinian revolution in
evolutionary biology (cf. Egerton 1968). Almost two centuries
later, our constantly expanding knowledge of Earth’s past con-
tinues to provide fresh insights into the dynamics of biodiver-
sity. In this field of inquiry, there has been a longstanding debate
on the relative importance of biotic versus abiotic processes for
shaping diversity (e.g., Van Valen 1973; Vrba 1985, 1992; Ben-
ton 1987), generating dichotomous views that have come to be
called the Red Queen and Court Jester models (Barnosky 2001;
Benton 2009; but see Liow et al. 2011 on the less restrictive orig-
inal Red Queen hypothesis of Van Valen [1973]). Recent stud-
ies, however, point to the critical need to better understand the
linkage of those processes (Ezard et al. 2011; Liow et al. 2011;
Condamine et al. 2019). The present study helps fill that knowl-
edge gap by clarifying the complementary roles of climate, pre-
dation, and inter-clade competition in shaping the evolutionary
trajectory of the mammalian order Lagomorpha (pikas, rabbits,
and hares). While processes that regulate diversity are typically
investigated in clades with strikingly high taxic and phenotypic
diversities, it is difficult to disentangle multitudes of forces act-
ing on disparate constituents of such clades. Less speciose and
more homogeneous groups such as lagomorphs offer uniquely-
valuable study systems because they bring into focus the factors
that limit diversity.
Lagomorphs are, if anything, remarkably successful mam-
mals. The approximately 92 extant species are distributed across
all continents except Antarctica, collectively inhabiting a wide
1
© 2021 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original
work is properly cited.
Evolution
S. TOMIYA AND L. K. MILLER
range of environments from tropical forests to arctic deserts. In
many regions, they are locally abundant and represent a major
element of the small-mammalian herbivore guild (Chapman and
Flux 2008; Lacher et al. 2016). Considering such ecological suc-
cess, the diversity of lagomorphs is strikingly limited both taxi-
cally and phenotypically compared to those of rodents (extant
sister clade of lagomorphs with ∼2400 living species; Lacher
et al. 2016) and terrestrial artiodactyls (another widespread group
of herbivorous mammals with ∼380 living species; Wilson and
Mittermeier 2011). Importantly, the narrow phenotypic range of
wild lagomorphs is not a mere reflection of their limited taxic di-
versity: their per-lineage rates of body size evolution have been
low compared to those of rodents and artiodactyls (Venditti et al.
2011), and contrary to the evolutionary lability of domestic rab-
bits under artificial selection (cf. Darwin 1868).
A peculiar aspect of today’s low lagomorph diversity is the
negative skew of their body size distribution (Fig. 1A; sample-
size adjusted Fisher-Pearson coefficient of skewness G1=−1.1
for body mass data from Jones et al. 2009; see also Gardezi and
da Silva [1999]). It is in contrast to the positive skews of rodents
(G1=0.90), terrestrial artiodactyls (G1=0.11), and indeed,
late Quaternary terrestrial mammals in general (Smith and Lyons
2011), which has been attributed to diffusive body size evolu-
tion under the combination of a lower boundary and gradually
increasing extinction risk above the modal body mass (Clauset
and Erwin 2008). The opposite skew of extant lagomorph body
mass distribution therefore suggests the existence of an upper
boundary at ∼5 kg in the wild in continental settings. This ap-
parent barrier has been crossed by some domesticated rabbits
such as the Flemish Giant rabbit—a breed of Oryctolagus cu-
niculus weighing ∼7−8 kg (Roth and Cornman 1916)—and an
extinct leporid from the island of Menorca, Nuralagus rex, with
the estimated mean body mass of ∼8 kg (Quintana et al. 2011;
Moncunill-Solé et al. 2015). We therefore inferred that the upper
body mass boundary in wild continental lagomorphs is set not in-
trinsically but ecologically by ubiquitous processes (cf. Lomolino
et al. 2012).
In modern ecoregions, terrestrial artiodactyls or ungulate-
like caviomorph rodents frequently occupy the herbivore size
class immediately above those of lagomorphs, and play sim-
ilar ecological roles (Dubost 1968). In fact, lagomorphs have
been described as miniature analogs of ungulates (here loosely
defined as hoofed mammalian herbivores) with regard to their
dietary and locomotor behaviors (Vaughan 1978; Rose 2006).
We, therefore, hypothesized that the evolution of maximum aver-
age body size in lagomorphs has been competitively constrained
by small ungulates and other small ungulate-like herbivores
because lagomorphs lose their competitive advantage above cer-
tain body size (or sizes, depending on the environment). Previ-
ously, Vaughan (1978), Rose (2006), and Yamada (2017) sur-
mised that competitive pressures from other mammalian groups
such as ungulates and rodents may have somehow limited the
diversity of lagomorphs. We distilled this idea into quantitative
models that focused on body size because it defines a major bio-
logical axis along which many physiological, ecological, and life-
history traits strongly covary (Eisenberg 1981; Demment and Van
Soest 1985). Competition between species in the same ecologi-
cal guild is thus expected to intensify with increasing similarity in
body size, unless attenuated by niche differentiation (MacArthur
and Levins 1967; Gotelli and Graves 1996); conversely, to the
extent that body size constraints feeding ecology, size separation
tends to enable coexistence of mammalian herbivores that use
overlapping resources (Laca et al. 2010).
In this study, we first examined the biogeographic patterns
of maximum lagomorph body masses in modern ecoregions and
evaluated their potential biotic- and abiotic-environmental pre-
dictors including the minimum body masses of co-occurring
ungulate-type herbivores. We then examined the scaling of local-
population energy use with body mass (Damuth 1981) in extant
lagomorphs and ungulates to seek a mechanistic explanation for
the observed macrogeographic patterns of body size relationships
from an evolutionary-ecological perspective. Finally, focusing on
North America, which long served as the center stage for the evo-
lution of leporids (Dawson 2008; Lopez-Martinez 2008; Ge et al.
2013), we estimated body masses of fossil lagomorphs within a
phylogenetic framework, and evaluated ecological models of the
maximum lagomorph body mass since the late Eocene, 37.5 mil-
lion years ago. These spatial and temporal analyses compensate
for the shortcomings of each other: on one hand, the modern ge-
ographic distributions and co-occurrence patterns of species may
be heavily affected by human activities (Verde Arregoitia et al.
2015; Lyons et al. 2016); on the other hand, our knowledge of
fossil taxa and their paleoenvironment is much more limited.
Methods
Unless noted otherwise, computations were performed in the R
programming environment ver. 3.6.0 (R Development Core Team
2018). Data sets are archived in the Dryad Digital Repository as
Electronic Supplementary Materials (ESMs; Tomiya and Miller
2021).
MODELING OF MAXIMUM LAGOMORPH BODY
MASS IN MODERN ECOREGIONS
Based on present range maps (IUCN 2013) and species mean
body mass data (Jones et al. 2009), the largest leporid lagomorph
and the smallest ungulate-type herbivore species (excluding lago-
morphs) were identified in 574 non-island ecoregions (Olson
et al. 2001; ESM Dataset 1). We considered the following taxa to
be ungulate-type herbivores (UTHs): artiodactyls, perissodactyls,
2EVOLUTION 2021
BODY SIZE EVOLUTION IN LAGOMORPHS
Figure 1. Modern macrogeography of maximum lagomorph body size. (A) Global body mass distributions (data from Jones et al. 2009)
in extant lagomorphs (orange), rodents (gray), and artiodactyls (blue); extinct insular leporid Nuralagus rex (black) for comparison. (B)
Bivariate plot of maximum lagomorph body mass (Mmaxlag) and minimum ungulate-type herbivore body mass (Mminuth ; predominantly
EVOLUTION 2021 3
S. TOMIYA AND L. K. MILLER
and ungulate-like or leporid-like caviomorphs (cf. Dubost 1968;
Seckel and Janis 2008) consisting of Cuniculus,Dasyprocta,My-
oprocta,Dolichotis,Chinchilla,Lagidium,andLagostomus.Om-
nivorous or semiaquatic taxa (suids, tayassuids, hippopotamids,
and Hydrochoerus) were excluded.
We conducted boosted regression-tree analysis (Elith et al.
2008) of the maximum lagomorph body mass (log10Mmaxlag )
with the following predictors: (1) minimum UTH body mass
(log10Mminuth ); (2) mean annual temperature (Hijmans et al.
2005); (3) mean annual precipitation (Hijmans et al. 2005); (4)
precipitation variance (as a measure of seasonality) (Hijmans
et al. 2005); (5) soil nutrient availability (Fischer et al. 2008); (6)
mean tree cover (Hansen et al. 2013; downsampled by averaging
to a 30-minute resolution); (7) elevation (Hijmans et al. 2005); (8)
introduction status of the largest lagomorph; and (9) mean resid-
ual of neighboring ecoregions as a spatial autocovariate (Crase
et al. 2012). Mean predictor values for individual ecoregions
were calculated from digital spatial data using the program QGIS
(QGIS Development Team 2018) and the R packages ‘rgdal’ ver-
sion 1.4-3 (Bivand et al. 2018) and ‘rgeos’ version 0.4-3 (Bivand
and Rundel 2019). The model of Mmaxlag was developed using the
cross-validation method (Elith et al. 2008) and the tree complex-
ity, learning rate, and bag fraction values of 3, 0.005, and 0.75,
as recommended by Elith et al. (2008). This analysis was per-
formed using the package ‘gbm’ version 2.1.5 (Greenwell et al.
2019) and the script ‘brt.functions.R’ (Elith et al. 2008).
LOCAL-POPULATION ENERGY USE
The theoretical scaling of energy use Eby a local population of
individuals with body mass Mwas calculated from empirically-
derived allometric scaling patterns of basal metabolic rate (i.e.,
individual energy use) R=aMband local population density
D=cMdas follows (cf. Damuth 1981):
E=RD =acM(b+d),or
log10E=log10 R+log10D=log10 a+log10c
+(b+d)log10M.(1)
To this end, we performed GLS regression analyses of D
and Ragainst body mass (Paradis and Schliep 2019; Smaers
and Mongle 2020) using published data for extant leporids,
herbivorous terrestrial artiodactyls, and perissodactyls (Jones
et al. 2009), and a time-calibrated species-level mammalian
supertree (Bininda-Emonds et al. 2007, Bininda-Emonds et al.
2008); Pagel’s (1999) λwas constrained to be between 0 and
1 (cf. Revell 2010). Confidence bands for parameter estimates
were obtained using the R package ‘evomap’ (Smaers and Mon-
gle 2020). Data on the basal metabolic rates of perissodactyls
were not available for the taxa with population density data; we,
therefore, assumed that perissodactyls fit the tightly-constrained
scaling of Rcommon to leporids and artiodactyls (Fig. 2B).
‘Energy-equivalent’ lagomorph body masses for observed mini-
mum perissodactyl body masses in the fossil record (see below)
were determined by solving Equation (1).
MODELING OF MAXIMUM LAGOMORPH BODY
MASS IN NORTH AMERICAN FOSSIL RECORD
Fossil occurrence data
Occurrence data for North American fossil lagomorphs, un-
gulates (perissodactyls and artiodactyls excluding helohyids,
entelodontids, anthracotheriids, and tayassuids), and rodents
(to estiamte glires fossil recovery potential; note there are no
ungulate-like terrestrial rodents within the scope of this analysis)
were obtained from the Paleobiology Database (Alroy and Uhen
2020, ESM Dataset S5) for the period of 46.2−30.5 million years
ago (Ma), and from MIOMAP (Carrasco et al. 2005) and FAUN-
MAP (Graham and Lundelius 2010) databases for the period of
30.5−0 Ma. Localities (or “collections” [Alroy and Uhen 2020])
and associated taxon occurrence data whose geologic ages had
uncertainties exceeding 4.2 million years (equivalent to the dura-
tion of Ar2—the longest North American Land Mammal ‘Age’
[NALMA] subage) were excluded. Taxonomic names in the oc-
currence data set were checked for synonymy and internal con-
sistency (Janis et al. 1998; Prothero and Foss 2007).
The occurrence data were grouped into 1.5 million-year time
bins starting at 43.5 Ma; this temporal resolution was selected
in view of the median locality-age uncertainty of 1.1 million
years for the Neogene occurrence data and the median species
duration of 2−3 million years for North American fossil mam-
mals (Alroy 2009). We used time bins of equal lengths instead of
geochronologic units of uneven durations to simplify the time se-
ries analysis. Species were assumed to be present in North Amer-
ica between their first and last appearances. The species- and
genus-level taxonomy of fossil lagomorphs follows Dawson
artiodactyls) in 547 ecoregions in Indo-Malay (gold), Afrotropical (green), Palearctic (light blue), Nearctic (pink), and Neotropical (brown)
realms, against line of equality (gray). (C–E) Log10Mmaxlag (C), log10 Mminuth (D), and residuals of boosted regression-tree model predicting
log10Mmaxlag (E) across ecoregions. (F) Partial dependence plots from boosted regression-tree analysis of log10Mmaxlag in modern ecore-
gions. Percent values represent relative inuences of predictors. Silhouettes from PhyloPic (http://phylopic.org): N. rex by Steven Traver,
Cuniculus paca by Margot Michaud, and Moschus chrysogaster by Andrew Farke (https://creativecommons.org/publicdomain/zero/1.0/);
Leporidae by Sarah Werning (http://creativecommons.org/licenses/by/3.0/).
4EVOLUTION 2021
BODY SIZE EVOLUTION IN LAGOMORPHS
Figure 2. Model of local-population energy use by extant leporids (orange) and ungulates (blue; herbivorous terrestrial artiodactyls and
perissodactyls). Empirical scaling patterns of local-population density D(A) and ‘basal’ metabolic rate R(B) against body mass M;data
for ungulate-like caviomorphs (gray) are overlaid in (A), with Cuniculus paca labeled. (C) Theoretical scaling of local-population energy
use Eagainst M, illustrating our conceptual model of lagomorph body size evolution: lagomorphs in open habitats experience increased
predation pressure and undergo selection for greater cursoriality, resulting in body size increase (right-pointing arrow); large lagomorphs
are kept out of more closed habitats by competitively superior smaller lagomorphs, while further body-size increase is opposed by the
competitive pressure from larger ungulate-type herbivores (left-pointing arrow). Polygons represent 95% condence bands. See Figure 1
caption for PhyloPic credit.
(2008). Extant species were assigned body masses from the Pan-
THERIA database (Jones et al. 2009).
Body mass estimation for fossil taxa
Body masses of fossil lagomorphs and ungulates were esti-
mated from published and original measurements of mandibular
and dental dimensions (Supplementary Information [SI]; ESM
Datasets S2–S4). For lagomorphs, we newly developed allo-
metric models from our measurements of 164 specimens of 34
extant species, for which associated individual body-mass data
were available. Phylogenetic covariance and intraspecific vari-
ations were incorporated into the lagomorph models (Garland
and Ives 2000; Hansen and Bartoszek 2012; Bartoszek 2019;
Paradis and Schliep 2019) using a time-calibrated molecular
tree (Ge et al. 2013). The parameters of the allometric mod-
els for fossil ungulates were estimated from a published data
set (Mendoza et al. 2006) combined with a time-calibrated su-
pertree (Bininda-Emonds et al. 2007, Bininda-Emonds et al.
2008).
Predictor variables
As potential predictors of Mmaxlag in North America since
the late Eocene, we considered: (1) competitive ceiling body
mass, log10Mceiling , consisting of the energy-equivalent lago-
morph body mass for the contemporary minimum perissodactyl
body mass (see Local-Population Energy Use, above) for the
periods of 37.5−24.0 and 15.0−1.5 Ma and the minimum ar-
tiodactyl body mass for the period of 24.0−15.0 Ma; (2) min-
imum perissodactyl body mass, log10Mminper ; (3) global ben-
thic δ18O (1.5 million-year means) as a temperature proxy (Za-
chos et al. 2001); (4) mean North American fossil ungulate
hypsodonty index (Hung) as a precipitation proxy (cf. Fortelius
et al. 2002; Eronen et al. 2010); and (5) logit-transformed
range-through sampling probability for glires genera (i.e., ro-
dents and lagomorphs), Rglires, as a measure of fossil recovery
potential for lagomorphs (cf. Tomiya 2013). The mean ungu-
late hypsodonty index was first calculated for NALMA sub-
ages using published data for artiodactyls and perissodactyls
(Jardine et al. 2012), and interpolated to the midpoints of the
1.5 million-year time bins.
Model evaluation
After exploratory analyses, we compared the fit of 11 linear re-
gression models with autocovariates to the observed time series
of log10Mmaxlag from37.5to1.5Mabasedonthesample-size
adjusted Akaike information criterion (AICc; Burnham and An-
derson 2002). Five of them (Models 1−5) each included one of
the five predictor variables, and the remaining six models each
included two predictors as follows: Mceiling and Rglires (Model 6),
Mminper and Rglires (Model 7), Mceiling and Hung (Model 8), Mminper
and Hung (Model 9), Mceiling,andδ18O (Model 10), Mminper and
δ18O (Model 11); given the result, we did not consider models
with more than two predictors. The autocovariate for each model
was defined as the initial model residual for the preceding time
bin, obtained from a preliminary regression analysis that ignored
the potential autocorrelation of residuals. For our data set, this ap-
proach was more effective at removing autocorrelation than the
EVOLUTION 2021 5
S. TOMIYA AND L. K. MILLER
use of first-order autoregressive models, based on inspection of
autocorrelograms and comparison of AICcvalues.
We excluded the most recent 1.5 million-year interval from
our analysis so as to avoid influences of human activities on
species associations and body mass distributions (Lyons et al.
2016; Smith et al. 2018). To take into account the uncertainties
in the ages of fossil localities and body mass estimates, this anal-
ysis was repeated 1,000 times, each time stochastically generat-
ing a set of locality ages (from uniform distributions bounded by
the maximum and minimum ages of individual localities) and a
set of lagomorph and ungulate body mass estimates (from nor-
mal distributions with the means equal to the point estimates and
variances informed by the models; Garland and Ives 2000;
Hansen and Bartoszek 2012). The regression analyses were per-
formed with the R package ‘nlme’ (Pinheiro et al. 2012).
Results
In all 574 modern continental terrestrial ecoregions analyzed,
the smallest ungulate is an artiodactyl, and in 133 of them
(131 of 143 Neotropical and 2 of 107 Nearctic ecoregions), the
smallest ungulate-type herbivore excluding leporids (UTH) is a
caviomorph rodent. At the ecoregional level, the largest lago-
morph and the smallest UTH tend to have similar body masses in
parts of the Indo-Malay and Afrotropical realms, where some of
the smallest extant artiodactyls weighing less than 10 kg occur, as
well as in Neotropical ecoregions with ungulate-like caviomorphs
(Fig. 1B–D). In Palearctic ecoregions, the two groups are typi-
cally separated by a moderately large body mass gap, and in many
Nearctic ecoregions, the body mass gap is especially pronounced
because small ungulates weighing less than ∼50 kg are gener-
ally absent. Overall, the body mass gap widens with increasing
minimum UTH body mass (Fig. 1B).
Boosted regression-tree analysis of the modern pheno-
geographic data generated a model of log10Mmaxlag with 5,350
regression trees that explained an average of 76% of the de-
viance in cross-validation trials. Of the nine predictors considered
here, log10Mminuth was the most influential, accounting for 43% of
the contributions of all environmental predictors (excluding the
spatial autocovariate; Fig. 1F). Nevertheless, all predictors con-
tributed sufficiently to warrant their inclusion in the final model.
Partial dependence plots (Fig. 1F) show an increase in
Mmaxlag with increasing Mminuth and decreasing mean annual tem-
perature, and to lesser degrees, with decreasing tree cover (but
onlydownto∼50%), decreasing mean annual precipitation (but
only below ∼1,500 mm/year), decreasing elevation, and highest
levels of nutrient limitation. In addition, the largest lagomorph
in an ecoregion tended to be larger when it was an introduced
species. The relationship between each predictor and the pre-
dicted maximum lagomorph body mass is generally better de-
scribed as polygonal than simply linear (SI Fig. S1), as is often
the case in macroecological patterns (Brown 1995; Gaston and
Blackburn 2008). Prediction residuals from the global model do
not show any major geographic bias at the level of realms, imply-
ing that similar rules govern Mmaxlag in ecoregions across biogeo-
graphic realms (Fig. 1E; SI Fig. S2).
Next, we compared the expected local-population energy
use in extant leporids and ungulates (predominantly herbivo-
rous terrestrial artiodactyls but also including perissodactyls).
Our analysis suggests that, while the scaling of metabolic rate
with body mass in leporids and ungulates can be adequately de-
scribed by the same regression line (Fig. 2B), the two groups
exhibit markedly different patterns of population density scaling
with body mass (Fig. 2A; SI Table S3). Among leporids, the local
population density can be very high for small-sized species, but
declines sharply with increasing body mass, and much more so
than in ungulates. As a result, the equilibrial body mass in lep-
orids and ungulates with respect to the local-population energy
use occurs at ∼6.3 kg (Fig. 2C), near the observed maximum
mean body mass of continental lagomorphs at ∼5 kg. Below this
energetically-equilibrial body mass, leporids are expected to be
competitively dominant over similar-sized ungulates if they share
resources. Above it, ungulates of any size should have an advan-
tage over similar-sized leporids where they co-occur, unless lep-
orids are somehow able to ‘bend’ the allometric curve upwards by
a substantial degree—an evolutionary adjustment that they have
apparently been unable to make.
The estimated mean adult body masses for 74 fossil species
of North American lagomorphs from the past 43.5 million years
ranged from 0.1 to 2.6 kg (SI Fig. S3; ESM Dataset S3),
falling within the range of mean body masses for extant species
(0.07−4.80 kg; Fig. 1A). During the entire existence of lago-
morphs in that continent, the smallest ungulate has always been
an artiodactyl and not a perissodactyl (Fig. 3A; SI Fig. S3).
The oldest lagomorphs in North America (Mytonolagus spp.)
are estimated to have weighed 0.8 kg, comparable to small- to
medium-sized extant species of North American cottontail rab-
bits (Sylvilagus spp.). After first appearing at ∼44−43 Ma (Daw-
son 2008), the maximum body size of lagomorphs increased to
2.6 kg (Megalagus brachydon) by 37 Ma (Fig. 3A), that is, within
the first one-sixth of the group’s history in that continent. The
maximum lagomorph body size remained stable for the subse-
quent ∼12 million years until the late Oligocene. This same pe-
riod saw abundance of small artiodactyls with estimated body
masses on the order of 0.1−1 kg, including some of the smallest
known artiodactyls of all time. As a result, the body mass ranges
of lagomorphs and artiodactyls overlapped from the late Eocene
to the Oligocene (Fig. 3A; SI Fig. S4A).
The transition from the Oligocene to the Miocene Epoch
was marked by extinctions of very small artiodactyls and
6EVOLUTION 2021
BODY SIZE EVOLUTION IN LAGOMORPHS
Figure 3. Macroevolution of maximum lagomorph body size in North America. (A) Trajectories of maximum lagomorph body mass
(Mmaxlag; orange), minimum perissodactyl body mass (Mminper ; dark blue), minimum artiodactyl body mass (Mminart; blue), and energy-
equivalent lagomorph body mass for contemporary minimum perissodactyl body mass (red), showing uncertainties in locality ages and
body mass estimates across 1,000 pseudo-replicates; gray area corresponds to body mass range in which near-complete reliance on
rumen fermentation is energetically sustainable (Demment and Van Soest 1985). Lagomorphs in body size region above red line would
be competitively inferior to smallest contemporary perissodactyl according to scaling patterns of local-population energy use (Fig. 2C). (B)
Competitive ceiling body mass (Mceiling; purple), which combines energy-equivalent lagomorph body mass for contemporary minimum
perissodactyl body mass (37.5−24.0, 15.0−1.5 Ma) and minimum artiodactyl body mass (24.0−15.0 Ma) as seen in (A). (C) Additional
potential predictors of Mmaxlag, including global benthic δ18 O (green), mean ungulate hypsodonty (Hung; beige), and range-through
sampling probability for glires genera (Rglires; 1,000 pseudo-replicates in aquamarine). (D, E) Top eight models (out of 11 compared) of
maximum lagomorph body mass for 37.5−1.5 Ma, showing number of times each model received most support (D) and distributions
of AICcfor 1000 pseudo-replicates (E). Pliohippus silhouette by Zimices (http://creativecommons.org/licenses/by/3.0/) from PhyloPic
(http://phylopic.org); see Figure 1 caption for additional credits.
hare-sized (>2 kg) lagomorphs. Consequently, the body size
ranges of lagomorphs and artiodactyls rapidly segregated, and
their opposing body mass boundaries gradually increased there-
after, closely tracking each other from the late Oligocene until
the middle Miocene, ca. 24−15 Ma (Fig. 3A). Beginning in the
latter half of the Miocene, the rise in the maximum lagomorph
body mass appears to have slowed down or hit a ceiling, increas-
ingly lagging behind the minimum artiodactyl body mass and
EVOLUTION 2021 7
S. TOMIYA AND L. K. MILLER
widening the size gap between the two groups (SI Fig. S4A). This
trend parallels the tropical-to-Holarctic realm-level transition in
modern ecoregions (SI Fig. S5). Still, for most of the past 43.5
million years, the smallest artiodactyls remained smaller than:
(1) the energetically equilibrial body mass of ∼6.3kg(Figs.2C
and 3A), which would have put them at a competitive disadvan-
tage against similar-sized lagomorphs if their resource uses had
largely overlapped; and (2) the ∼9.4 kg threshold for transition to
a digestive system that is heavily reliant on foregut fermentation
(Demment and Van Soest 1985; gray areas in Fig. 3A and B).
Unlike the artiodactyls, the smallest perissodactyls—the
likes of which are absent in modern faunas—maintained sub-
stantially larger body sizes (generally by an order of magnitude
or more) than contemporary lagomorphs throughout their history
in North America (Fig. 3A; SI Fig. S4B). However, from the late
Eocene to the late Oligocene and again from the middle Miocene
onwards, the maximum lagomorph body mass closely tracked
the theoretical energy-equivalent lagomorph body mass for the
smallest perissodactyl in the same time bin (red lines in Fig. 3A;
derived from the scaling patterns of local-population energy use
in Fig. 2C). The latter remained relatively stable over the entire
history of coexistence of lagomorphs and perissodactyls in the
continent despite an approximately eightfold increase in the
minimum perissodactyl body mass between 43.5 and 1.5 Ma—a
consequence of the much shallower slope of local-population en-
ergy use against body mass in ungulates compared to lagomorphs
(Fig. 2C).
From these historical patterns, we visually identified a
set of apparent body mass ceilings placed on lagomorphs by
perissodactyls (37.5−24.0 and 15.0−1.5 Ma) and artiodactyls
(24.0−15.0 Ma), here termed the ‘competitive ceiling body
mass’ (Mceiling), as a potentially powerful predictor of the maxi-
mum lagomorph body mass in the North American fossil record
(purple lines in Fig. 3B). In essence, it represents a series of the
smaller of (A) the energy-equivalent lagomorph body mass for
the minimum perissodactyl body mass (red lines in Fig. 3A) and
(B) the minimum artiodactyl body mass (blue lines in Fig. 3A),
which must also be larger than the maximum lagomorph body
mass (hence the “ceiling”). Information-theoretic comparison of
regression models (Fig. 3D, E) showed that taking into consider-
ation the uncertainties in locality ages and body mass estimates,
the maximum lagomorph body mass between 37.5 Ma and
1.5 Ma was indeed best predicted by (and positively correlated
with) the ‘competitive ceiling body mass’ rather than by the
minimum perissodactyl body mass, global benthic δ18Ovalue(a
global temperature proxy; Zachos et al. 2001), mean hypsodonty
index for North American ungulates (Hung, a precipitation proxy;
Eronen et al. 2010), or range-through sampling probability for
glires genera (Rglires, a measure of fossil recovery potential).
Moreover, the next three best models (generally with evidence
ratios of <10) all included Mceiling as one of the predictors, in
combination with δ18O, Rglires,orHung.
Discussion
Macroevolutionary consequences of competition have long been
investigated in divergent patterns of lineage diversification
among speciose clades (e.g., Van Valen and Sloan 1966; Gould
and Calloway 1980; Stanley and Newman 1980; Cifelli 1981;
Krause 1986; Maas et al. 1988; Janis 1989; Benton 1996; Sep-
koski Jr 1996; Van Valkenburgh 1999; Rabosky 2013; Pedersen
et al. 2014; Liow et al. 2015; Silvestro et al. 2015; Condamine
et al. 2019). However, even when inverse diversity dynamics are
observed among higher taxa (i.e., the rise of one group is accom-
panied by the fall of another), the underlying mechanism is rarely
clear from analysis of taxon counts alone (Jablonski 2008; Liow
et al. 2015). Moreover, there is growing evidence that speciation
and phenotypic evolution in mammals are not as tightly coupled
as traditionally assumed (Venditti et al. 2011; Slater 2015), such
that exclusive focus on taxic diversity may miss important pro-
cesses that shape biological diversity. Additional insights have
come from studies tracking phenotypic ranges of potentially-
competing lineages in the fossil record (e.g., Janis et al. 1994;
Hopkins 2007; Brusatte et al. 2008; Friscia and Van Valkenburgh
2010; Kimura et al. 2013; Benson et al. 2014; Slater 2015). Lago-
morphs and other ungulate-type herbivores together present a rel-
atively simple—and thus ideal—study system for interpreting the
dynamics of phenotypic boundaries because: (1) they are extant
clades with extensive fossil records; (2) their basic ecological
adaptations have remained relatively stable through much of their
evolutionary histories (Wood 1940; Dawson 2008); (3) as pri-
mary consumers, their occurrences are tied directly to vegetation
and closely to climate (Leach et al. 2015a; Vrba 1992; Eronen
et al. 2010); and (4) the potential for inter-clade competition is
high given their broadly similar dietary and locomotor specializa-
tions (cf. Cope 1884; Gidley 1912; Wood 1957; Vaughan 1978;
Rose 2006).
The limited body size range of North American fossil lago-
morphs reinforces the long-held perception of evolutionary sta-
bility in lagomorphs (Wood 1940; Dawson 2008). Over the past
43.5 million years, their maximum average body mass never ex-
ceeded the presently observed upper limit of ∼5kginNorth
America (Fig. 3A), and while the history of the crown-group
Lagomorpha likely goes back by an additional 10 million years to
∼53 million years ago (Rose et al. 2008), we are not aware of any
fossil lagomorph from any continent that would have weighed
much more than 5 kg. At the same time, the trajectory of maxi-
mum lagomorph body mass during the Eocene (Fig. 2A, B) illus-
trates the possibility of rapid body size evolution in lagomorphs
as is also suggested by the gigantism of certain domestic breeds
8EVOLUTION 2021
BODY SIZE EVOLUTION IN LAGOMORPHS
and extinct insular species (Roth and Cornman 1916; Quintana
et al. 2011; Lomolino et al. 2013; Moncunill-Solé et al. 2015).
Our analyses of the geographic and historical distributions
of lagomorph body masses consistently show that the maximum
lagomorph body mass is strongly linked to the minimum body
mass of ungulates at relatively large spatiotemporal scales, and
suggest that the evolution of lagomorph body size has been con-
strained by ungulates. This view comes into sharper focus when
the local-population energy use Eis considered. First, the dis-
tinct scaling patterns of Ein extant leporids and ungulates gen-
erate the following basic expectations where they compete for
limited resources (Fig. 2C; see also Van Valen 1973; Damuth
1981, 1987, 2007): (1) lagomorphs weighing more than ∼6.3 kg
are at a competitive disadvantage to, and unlikely to stably co-
exist with, ungulates of all sizes (left-pointing arrow in Fig. 2C);
(2) large, hare-type lagomorphs are at a competitive disadvan-
tage to, and unlikely to stably coexist with, smaller, rabbit-type
lagomorphs. Competitive pressure could be mitigated by dietary
differentiation, but the combination of morphological, digestive,
and behavioral specializations in lagomorphs (Hirakawa 2001;
Hume 2002) is apparently not amenable to major departures from
a primarily folivorous diet (e.g., frugivory as seen in modern trag-
ulids), making it difficult for lagomorphs to escape intra- and
inter-clade competition (Leach et al. 2015b; Hulbert and Ander-
sen 2001).
Expectation 1 is supported by the universal absence of con-
tinental lagomorphs weighing much more than ∼6.3kgwhere
ungulates co-occur. The close correspondence of the observed
continental maximum lagomorph body mass (∼5 kg) with the
intersection of the regression lines representing the scaling of
Ein lagomorphs and ungulates (Fig. 2C) is not a mathemati-
cal necessity, and cannot be easily explained without invoking
evolutionary-ecological stability (cf. Damuth 1981, 2007). It is
noteworthy that ungulate-like caviomorph rodents, despite be-
longing to the extant sister clade of lagomorphs, are not con-
fined within the same upper size limit as lagomorphs, and that
they may have achieved large body sizes by maintaining rela-
tively high population densities, as in the case of the lowland paca
(Cuniculus paca; Fig. 2A).
Expectation 2 is supported by the habitat-level segrega-
tion of sympatric small and large leporids into closed and open
habitats, respectively (MacCracken 1982; Flux 2008). This phe-
nomenon may be traced back to the late Eocene (Webb 1977),
when the largest lagomorphs attained the body masses compara-
ble to those of extant hares (Fig. 3A). Because maximum running
speed is correlated with body size (Garland 1983), we interpret
the association of large lagomorphs with open grassland habi-
tats as primarily a consequence of elevated predation risks (Flux
2008) and selection for increased cursoriality (right-pointing
arrow in Fig. 2C). At the same time, the steep decline of the
local-population energy use with increasing body mass and the
resulting competitively-induced restriction on the range of en-
vironments where large lagomorphs can thrive may have con-
tributed to the generally slow per-lineage rates of body size evo-
lution in lagomorphs (Venditti et al. 2011).
The scaling relationship of local-population energy uses in
lagomorphs and ungulates allows for estimation of energetically-
equivalent (at the population level) body masses in the two
groups. When the minimum perissodactyl body masses in the
North American fossil record were converted into energetically-
equivalent lagomorph body masses, much of the apparent body
size gap between contemporary lagomorphs and perissodactyls
disappeared (dark blue vs. red lines in Fig. 3A). Because lago-
morphs exceeding these ecological threshold body masses (red
lines in Fig. 3A) are expected to be competitively inferior to
the smallest perissodactyls (Fig. 2C), the tight body mass ceiling
placed above the lagomorphs by the perissodactyls (purple lines
in Fig. 3B) is interpreted to be an evolutionary constraint for the
lagomorphs. As pointed out by one of the reviewers of this paper
(see also Illius and Gordon 1992), the fact that lagomorphs and
perissodactyls are both hindgut fermenters may have intensified
the resource competition between the two groups.
Small artiodactyls also played a key role in constraining the
body size evolution of lagomorphs, as demonstrated by the model
with the competitive ceiling body mass, and especially during the
period from the late Oligocene to the middle Miocene (Fig. 3A,
B). However, unlike in the case of perissodactyls, the smallest ar-
tiodactyls during this time were within the body size range where
they are expected to have been at a competitive disadvantage
against similar-sized lagomorphs (i.e., below ∼6.3kginFig.2C).
In that context, the tightly coupled upward shifts of the minimum
artiodactyl and maximum lagomorph body masses between ca.
24 and 15 Ma can be interpreted as gradual displacement of artio-
dactyls by lagomorphs, and the competitive pressure appears to
have only slowed down, rather than prevented, the size increase
in lagomorphs.
The transition from the perissodactyl-dominated to
artiodactyl-dominated constraint on lagomorphs approximately
coincided with rapid expansion of grassland biomes in mid-
continental North America (cf. Strömberg 2005). The resulting
restructuring of the competitive regimes for mammalian herbi-
vores evidently reset the course of evolution for lagomorphs,
and may have been part of a threshold-induced critical transition
in the large-scale ecosystem (Scheffer et al. 2012). The second
transition back to the perissodactyl-dominated constraint was
roughly contemporaneous with the end of the middle Miocene
Climatic Optimum at ∼15 million years ago (Holbourn et al.
2014) and the onset of a trend toward widespread aridification
(Eronen et al. 2012). Thus, climate change has likely played
major roles in lagomorph evolution, but more as a catalyst of
EVOLUTION 2021 9
S. TOMIYA AND L. K. MILLER
state shifts than a constant driver of phenotypic evolution (see
also Barnosky 2005; Figueirido et al. 2012; Orcutt and Hopkins
2013). Although evolutionary response to climate change has
been a subject of intense study (see Blois and Hadly [2009] for a
review), the modulating role of climate in inter-clade competition
may be a more prevalent feature of evolution than is generally
realized (cf. Barnosky 2001; Liow et al. 2011).
More broadly, the persistence of dynamic upper body-size
limits in North American fossil lagomorphs is also consistent
with the competitive suppression hypothesis given the ∼12 mil-
lion years of evolutionary ‘head starts’ that artiodactyls and peris-
sodactyls had over lagomorphs in North America (Rose 2006;
Theodor et al. 2007; Dawson 2008). In fact, lagomorphs co-
existed with artiodactyls for their entire evolutionary histories
in all continents, and in most continents, artiodactyls were al-
ready well established when lagomorphs first appeared there
(Lopez-Martinez 2008; Winkler and Avery 2010; Flynn et al.
2014). Moreover, the same sequence applies to lagomorphs
and caviomorph rodents in South America (Woodburne 2010;
Vucetich et al. 2015). These temporal patterns conform to the
phenomenon of incumbent advantage, or priority effect, at a
macroevolutionary scale, which has been observed in a wide ar-
ray of vertebrate and invertebrate groups (Van Valkenburgh 1999;
Valentine et al. 2008; Schueth et al. 2015; Roopnarine et al.
2019). From this historical viewpoint, the positive association
between the introduction status and body mass of the largest
lagomorphs in modern ecoregions (Fig. 1F), which is mainly ob-
served in the Neotropical realm, may be interpreted as a sign of
major anthropogenic defaunation of native ungulates—and thus
reduction in competitive pressures—where leporids have been in-
troduced (cf. Dirzo et al. 2014).
It is interesting that the smallest living ungulates such as
chevrotains (Tragulidae) and miniature antelopes (Bovidae) are
able to coexist with similar-sized and sometimes even larger lep-
orids at the ecoregional scale (Fig. 1B) in spite of their appar-
ent competitive disadvantage (Fig. 2C). A similar phenomenon
of overlapping body size ranges is observed between artiodactyls
and lagomorphs in the late Eocene to the late Oligocene of North
America (Fig. 3A). These instances of coexistence are likely en-
abled by dietary separation, with the small ungulates tending
more toward frugivory or browsing (Dubost 1984; Gagnon and
Chew 2000; Meijaard 2011) and the leporids having the capac-
ity to be more graminivorous (Ge et al. 2013). The importance
of such dietary separation is also suggested by the biogeographic
history of lagomorphs: in Africa, where tragulids with primar-
ily folivorous rather than frugivorous diet appeared by the early
Miocene (Ungar et al. 2012), the establishment of large, leporid-
type lagomorphs was much delayed until the Quaternary Pe-
riod despite: (1) the presence of the order there since the early
Miocene (Winkler and Avery 2010) and (2) the rapid spread of
leporids across the neighboring continent of Eurasia after ∼8Ma
(Flynn et al. 2014).
Among ruminants, heavy utilization of high-quality foods
such as fruits is most feasible in small-bodied taxa in tropical
to subtropical forests (Demment and Van Soest 1985; Fleming
et al. 1987). Such environments are rare in the Palearctic and
Nearctic ecoregions, resulting in the frequent absence of very
small ungulates and contributing to the generally greater body-
size separation of the two groups (Fig. 1B; SI Fig. S5). The same
explanation fits the upward shift in the minimum body mass of
ungulate-type herbivores in the late Miocene of North America
(Fig. 3A; SI Fig. S4), which coincided with the spread of arid
biomes across the continent (Eronen et al. 2012). Nevertheless,
we caution against inferring local paleoenvironments from the
body-size relationship of the two groups alone: as a case in point,
the lagomorph and artiodactyl body-mass ranges overlapped sub-
stantially in the late Eocene to the late Oligocene of North Amer-
ica (Fig. 3A), when the most fossiliferous midcontinental regions
were probably cooler and drier than today’s tropics (Retallack
2007; Zanazzi et al. 2007; Boardman and Secord 2013; Eronen
et al. 2015; Pound and Salzmann 2017). Additional research into
the ecology of herbivorous mammals during this peculiar chapter
of mammalian evolution is warranted.
Conclusion
We found remarkably broad concordance between the patterns
of the modern pheno-geography and the paleontological time se-
ries, both pointing to prevalent evolutionary constraints placed
on lagomorphs by ungulate-type herbivores. From the mechanis-
tic standpoint, lagomorphs offer perhaps the clearest evidence yet
for the significant role of competition in dynamic subdivision of
an adaptive zone (cf. Van Valen 1973; Liow et al. 2011), bridging
tiers of evolutionary time (cf. Gould 1985). Our findings also pro-
vide empirical support for Damuth’s (1981, 1987, 2007) energy-
equivalence rule as a powerful guiding principle for interpreting
the history of biological diversity.
AUTHOR CONTRIBUTIONS
S.T. conceived of the study, collected data, carried out analyses, drafted
the manuscript, and coordinated the study. L.K.M. collected data and
improved data collecting procedure. Both authors gave final approval for
publication.
ACKNOWLEDGMENTS
We thank Maureen E. Flannery (California Academy of Sciences),
Christopher J. Conroy, Eileen A. Lacey, and James L. Patton (Mu-
seum of Vertebrate Zoology, Berkeley), Patricia A. Holroyd (University
of California Museum of Paleontology [UCMP]), William T. Stanley
(Field Museum of Natural History [FMNH]), and Darrin P. Lunde (U. S.
National Museum of Natural History) for access to specimens under their
care; Brian P. Kraatz (Western University of Health Sciences), Lawrence
10 EVOLUTION 2021
BODY SIZE EVOLUTION IN LAGOMORPHS
R. Heaney and Bruce D. Patterson (FMNH), David M. Grossnickle, Dal-
las Krentzel, and Jonathan S. Mitchell (University of Chicago), María E.
Pérez (FMNH and Museo Paleontológico Egidio Feruglio), and mem-
bers of the Sections of Evolutionary Morphology and Systematics and
Phylogeny of the Kyoto University Primate Research Institute for illu-
minating discussions; Anthony D. Barnosky and Kaitlin Clare Maguire
(University of California, Berkeley) for inspirational teaching of evolu-
tionary paleoecology and biogeography; John D. Orcutt (Cornell Col-
lege) for encouragement; and B. P. Kraatz, the editors David Hall and
Anjali Goswami, and two anonymous reviewers for insightful comments
on earlier manuscripts of this paper. The Future Development Funding
Program of Kyoto University Research Coordination Alliance funded
the open-access publication of this paper. This is UCMP publication no.
3012 and Paleobiology Database publication no. 392.
DATA ARCHIVING
The Electronic Supplementary Materials, including lists of museum
specimens and their repositories, are archived in the Dryad Digital
Repository (https://doi.org/10.5061/dryad.ns1rn8ps3).
LITERATURE CITED
Alroy, J. 2009. Speciation and extinction in the fossil record of North Amer-
ican mammals. Pp. 301–323 in R. K. Butlin, J. R. Bridle, and D.
Schluter, eds. Speciation and Patterns of Diversity. Cambridge Univ.
Press, Cambridge.
Alroy, J., and M. D. Uhen. 2020. Taxonomic occurrences of Artiodactyla
Perissodactyla from North America recorded in, Fossilworks, the
Evolution of Terrestrial Ecosystems database, and the Paleobiology
Database. http://fossilworks.org.
Barnosky, A. D. 2001. Distinguishing the effects of the Red Queen and Court
Jester on Miocene mammal evolution in the northern Rocky Mountains.
J. Vertebr. Paleontol 21:172–185.
Barnosky, A. D. 2005. Effects of Quaternary climatic change on speciation in
mammals. J. Mammal. Evol 12:247–264.
Bartoszek, K. 2019. R package “GLSME”, ver. 1.0.5. https://CRAN.R-
project.org/package=GLSME.
Benson, R. B., R. A. Frigot, A. Goswami, B. Andres, and R. J. Butler. 2014.
Competition and constraint drove Cope’s rule in the evolution of giant
flying reptiles. Nat. Commun 5:3567.
Benton, M. J. 1996. On the nonprevalence of competitive replacement in the
evolution of tetrapods. Pp. 185–210 in D. Jablonski, D. H. Erwin, and J.
H. Lipps, eds. Evolutionary Paleobiology. University of Chicago Press,
Chicago.
Benton, M. J. 1987. Progress and competition in macroevolution. Biol. Rev
62:305–338.
Benton, M. J. 2009. The Red Queen and the Court Jester: species diversity and
the role of biotic and abiotic factors through time. Science 323:728–732.
Bininda-Emonds, O. R., M. Cardillo, K. E. Jones, R. D. MacPhee, R. M.
Beck, R. Grenyer, S. A. Price, R. A. Vos, J. L. Gittleman, and A. Purvis.
2007. The delayed rise of present-day mammals. Nature 446:507–512.
Bininda-Emonds, O. R. P., M. Cardillo, K. E. Jones, R. D. E. MacPhee, R.
M. D. Beck, R. Grenyer, S. A. Price, R. A. Vos, J. L. Gittleman, and A.
Purvis. 2008. Corrigendum: The delayed rise of present-day mammals.
Nature 456:1038.
Bivand, R., T. Keitt, and B. Rowlingson. 2018. R package “rgdal”: Bindings
for the “Geospatial” Data Abstract Library, ver. 1.4-3. https://CRAN.R-
project.org/package=rgdal.
Bivand, R., and C. Rundel. 2019. R package “rgeos”: interface to Geometry
Engine Open Source (‘GEOS’), ver. 0.4-3. https://CRAN.R-project.org/
package=rgeos.
Blois, J. L., and E. A. Hadly. 2009. Mammalian response to Cenozoic climatic
change. Annu. Rev. Earth Planet. Sci 37:181–208.
Boardman, G. S., and R. Secord. 2013. Stable isotope paleoecology of
White River ungulates during the Eocene–Oligocene climate transi-
tion in northwestern Nebraska. Palaeogeogr. Palaeoclimatol. Palaeoecol
375:38–49.
Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago.
Brusatte, S. L., M. J. Benton, M. Ruta, and G. T. Lloyd. 2008. Superior-
ity, competition, and opportunism in the evolutionary radiation of di-
nosaurs. Science 321:1485–1488.
Burnham, K., and D. Anderson. 2002. Model Selection and Multimodel In-
ference: a practical information-theoretic approach. 2nd ed. Springer-
Verlag, New York.
Carrasco, M. A., B. P. Kraatz, E. B. Davis, and A. D. Barnosky. 2005.
Miocene Mammal Mapping Project (MIOMAP), University of Califor-
nia Museum of Paleontology. https://www.ucmp.berkeley.edu/miomap/.
Chapman, J. A., and J. E. Flux. 2008. Introduction to the Lagomorpha. Pp.
1–9 in P. Alves and K. Hackländer, eds. Lagomorph Biology: evolution,
ecology, and conservation. Springer, Berlin.
Cifelli, R. L. 1981. Patterns of evolution among the Artiodacyla and Perisso-
dactyla (Mammalia). Evolution 35:433–440.
Clauset, A., and D. H. Erwin. 2008. The evolution and distribution of species
body size. Science 321:399–401.
Condamine, F. L., J. Romieu, and G. Guinot. 2019. Climate cooling and clade
competition likely drove the decline of lamniform sharks. Proc. Natl.
Acad. Sci 116:20584–20590.
Cope, E. D. 1884. The Vertebrata of the Tertiary formations of the West.
Repo. United States Geol. Surv. Territories 3:1–1009.
Crase, B., A. C. Liedloff, and B. A. Wintle. 2012. A new method for deal-
ing with residual spatial autocorrelation in species distribution models.
Ecography 35:879–888.
Damuth, J. 1981. Population density and body size in mammals. Nature
290:699–700.
Damuth, J. 1987. Interspecific allometry of population density in mammals
and other animals: the independence of body mass and population
energy-use. Biol. J. Linn. Soc 31:193–246.
Damuth, J. 2007. A macroevolutionary explanation for energy equivalence
in the scaling of body size and population density. Am. Nat 169:621–
631.
Darwin, C. 1868. The variation of animals and plants under domestication.
John Murray, London.
Dawson, M. R. 2008. Lagomorpha. Pp. 293–310 in C. M. Janis, G. F. Gunnell,
and M. D. Uhen, eds. Evolution of Tertiary Mammals of North America.
Cambridge University Press, Cambridge.
Demment, M. W., and P. J. Van Soest. 1985. A nutritional explanation for
body-size patterns of ruminant and nonruminant herbivores. Am. Nat
125:641–672.
Dirzo, R., H. S. Young, M. Galetti, G. Ceballos, N. J. Isaac, and B. Collen.
2014. Defaunation in the Anthropocene. Science 345:401–406.
Dubost, G. 1984. Comparison of the diets of frugivorous forest ruminants of
Gabon. J. Mammal 65:298–316.
Dubost, G. 1968. Les niches écologiques des forêts tropicales sud-
américaines et africaines, sources de convergences remarquables entre
Rongeurs et Artiodactyles. La terre et la vie 22:3–28.
Egerton, F. N. 1968. Studies of animal populations from Lamarck to Darwin.
J. Hist. Biol 1:225–259.
Eisenberg, J. F. 1981. The Mammalian Radiations: an analysis of trends
in evolution, adaptation, and behaviour. University of Chicago Press,
Chicago.
Elith, J., J. R. Leathwick, and T. Hastie. 2008. A working guide to boosted
regression trees. J. Anim. Ecology 77:802–813.
EVOLUTION 2021 11
S. TOMIYA AND L. K. MILLER
Eronen, J. T., M. Fortelius, A. Micheels, F. T. Portmann, K. Puolamäki, and
C. M. Janis. 2012. Neogene aridification of the Northern Hemisphere.
Geology 40:823–826.
Eronen, J. T., C. M. Janis, C. P. Chamberlain, and A. Mulch. 2015. Mountain
uplift explains differences in Palaeogene patterns of mammalian evolu-
tion and extinction between North America and Europe. Proc. R. Soc.
B: Biol. Sci 282:20150136.
Eronen, J. T., K. Puolamäki, L. Liu, K. Lintulaakso, J. Damuth, C. Janis,
and M. Fortelius. 2010. Precipitation and large herbivorous mammals I:
estimates from present-day communities. Evol. Ecol. Res 12:217–233.
Ezard, T. H., T. Aze, P. N. Pearson, and A. Purvis. 2011. Interplay between
changing climate and species’ ecology drives macroevolutionary dy-
namics. Science 332:349–351.
Figueirido, B., C. M. Janis, J. A. Pérez-Claros, M. De Renzi, and P. Palmqvist.
2012. Cenozoic climate change influences mammalian evolutionary dy-
namics. Proc. Natl. Acad. Sci 109:722–727.
Fischer, G., F. Nachtergaele, S. Prieler, H. T. van Velthuizen, L. Verelst, and
D. Wiberg. 2008. Global Agro-ecological Zones Assessment for Agri-
culture (GAEZ 2008). IIASA and FAO, Laxenburg, Austria, and Rome,
Italy.
Fleming, T. H., R. Breitwisch, and G. H. Whitesides. 1987. Patterns of tropi-
cal vertebrate frugivore diversity. Annu. Revie. Ecol. Syst 18:91–109.
Flux, J. E. 2008. A review of competition between rabbits (Oryctolagus cu-
niculus) and hares (Lepus europaeus). Pp. 241–249 in P. Alves and K.
Hackländer, eds. Lagomorph Biology: evolution, ecology, and conser-
vation. Springer, Berlin.
Flynn, L. J., A. J. Winkler, M. Erbaeva, N. Alexeeva, U. Anders, C. Angelone,
S. ˇ
Cermák, F. A. Fladerer, B. Kraatz, and L. A. Ruedas. 2014. The Lep-
orid Datum: a late Miocene biotic marker. Mamm. Rev 44:164–176.
Fortelius, M., J. Eronen, J. Jernvall, L. Liu, D. Pushkina, J. Rinne, A. Tesakov,
I. Vislobokova, Z. Zhang, and L. Zhou. 2002. Fossil mammals resolve
regional patterns of Eurasian climate change over 20 million years.
Evol. Eco. Res 4:1005–1016.
Friscia, A. R., and B. Van Valkenburgh. 2010. Ecomorphology of North
American Eocene carnivores: evidence for competition between car-
nivorans and creodonts. Pp. 311–341 in A. Goswami and A. R. Friscia,
eds. Carnivoran evolution: new views on phylogeny, form, and function.
Cambridge University Press, Cambridge.
Gagnon, M., and A. E. Chew. 2000. Dietary preferences in extant African
Bovidae. J. Mammal 81:490–511.
Gardezi, T., and J. da Silva. 1999. Diversity in relation to body size in mam-
mals: a comparative study. Am. Nat 153:110–123.
Garland, T. 1983. The relation between maximal running speed and body
mass in terrestrial mammals. J. Zool 199:157–170.
Garland, T., and A. R. Ives. 2000. Using the past to predict the present: con-
fidence intervals for regression equations in phylogenetic comparative
methods. Am. Nat 155:346–364.
Gaston, K., and T. Blackburn. 2008. Pattern and Process in Macroecology.
Blackwell Science, Oxford.
Ge, D., Z. Wen, L. Xia, Z. Zhang, M. Erbajeva, C. Huang, and Q. Yang. 2013.
Evolutionary history of lagomorphs in response to global environmental
change. PLoS One 8:e59668.
Gidley, J. W. 1912. The lagomorphs an independent order. Science 36:285–
286.
Gotelli, N. J., and G. R. Graves. 1996. Null Models in Ecology. Smithsonian
Institution Press, Washington, DC.
Gould, S. J. 1985. The paradox of the first tier: an agenda for paleobiology.
Paleobiology 11:2–12.
Gould, S. J., and C. B. Calloway. 1980. Clams and brachiopods—ships that
pass in the night. Paleobiology 6:383–396.
Graham, R. W., and E. Lundelius. 2010. FAUNMAP II: New data for North
America with a temporal extension for the Blancan, Irvingtonian and
early Rancholabrean. https://ucmp.berkeley.edu/faunmap/index.html.
Greenwell, B., B. Boehmke, and J. Cunningham. 2019. and GBM Developers.
R package “gbm”: Generalized Boosted Regression Models, ver. 2.1.5.
https://CRAN.R-project.org/package=gbm.
Hansen, M. C., P. V. Potapov, R. Moore, M. Hancher, S. A. Turubanova,
A. Tyukavina, D. Thau, S. V. Stehman, S. J. Goetz, T. R. Loveland,
et al. 2013. High-Resolution Global Maps of 21st-Century Forest Cover
Change. Science 342:850–853.
Hansen, T. F., and K. Bartoszek. 2012. Interpreting the evolutionary regres-
sion: the interplay between observational and biological errors in phy-
logenetic comparative studies. Syst. Biol 61:413–425.
Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis. 2005.
Very high resolution interpolated climate surfaces for global land areas.
Int. J. Climatol 25:1965–1978.
Hirakawa, H. 2001. Coprophagy in leporids and other mammalian herbivores.
Mamm. Rev 31:61–80.
Holbourn, A., W. Kuhnt, M. Lyle, L. Schneider, O. Romero, and N. Andersen.
2014. Middle Miocene climate cooling linked to intensification of east-
ern equatorial Pacific upwelling. Geology 42:19–22.
Hopkins, S. S. B. 2007. Causes of lineage decline in the Aplodontidae: test-
ing for the influence of physical and biological change. Palaeogeogr.
Palaeoclimatol. Palaeoecol 246:331–353.
Hulbert, I. A., and R. Andersen. 2001. Food competition between a large
ruminant and a small hindgut fermentor: the case of the roe deer and
mountain hare. Oecologia 128:499–508.
Hume, I. D. 2002. Digestive strategies of mammals. Acta Zoologica Sinica
48:1–19.
Illius, A. W., and I. J. Gordon. 1992. Modelling the nutritional ecology of un-
gulate herbivores: evolution of body size and competitive interactions.
Oecologia 89:428–434.
IUCN. 2013. The IUCN Red List of Threatened Species.
Jablonski, D. 2008. Biotic interactions and macroevolution: extensions and
mismatches across scales and levels. Evolution 62:715–739.
Janis, C. M. 1989. A climatic explanation for patterns of evolutionary diver-
sity in ungulate mammals. Palaeontology 32:463–481.
Janis, C. M., I. J. Gordon, and A. W. Illius. 1994. Modelling equid/ruminant
competition in the fossil record. Hist. Biol 8:15–29.
Janis, C. M., K. M. Scott, L. L. Jacobs, G. F. Gunnell, and M. D. Uhen. 1998.
Evolution of tertiary mammals of North America: Volume 1, terrestrial
carnivores, ungulates, and ungulate like mammals. Cambridge Univer-
sity Press, Cambridge.
Jardine, P. E., C. M. Janis, S. Sahney, and M. J. Benton. 2012. Grit not grass:
concordant patterns of early origin of hypsodonty in Great Plains ungu-
lates and Glires. Palaeogeogr. Palaeoclimatol. Palaeoecol 365:1–10.
Jones, K. E., J. Bielby, M. Cardillo, S. A. Fritz, J. O’Dell, C. D. L. Orme, K.
Safi, W. Sechrest, E. H. Boakes, and C. Carbone. 2009. PanTHERIA: a
species-level database of life history, ecology, and geography of extant
and recently extinct mammals: Ecological Archives E090-184. Ecology
90:2648–2648.
Kimura, Y., L. L. Jacobs, and L. J. Flynn. 2013. Lineage-specific re-
sponses of tooth shape in murine rodents (Murinae, Rodentia) to late
Miocene dietary change in the Siwaliks of Pakistan. PLoS One 8:
e76070.
Krause, D. W. 1986. Competitive exclusion and taxonomic displacement in
the fossil record; the case of rodents and multituberculates in North
America. Pp. 95–117 in K. M. Flanagan and J. A. Lillegraven, eds. Ver-
tebrates, Phylogeny, and Philosophy. University of Wyoming, Laramie,
Wyoming.
12 EVOLUTION 2021
BODY SIZE EVOLUTION IN LAGOMORPHS
Laca, E. A., S. Sokolow, J. R. Galli, and C. A. Cangiano. 2010. Allometry and
spatial scales of foraging in mammalian herbivores. Ecol. Lett 13:311–
320.
Lacher, T. E., W. J. Murphy, J. Rogan, A. T. Smith, and N. S. Upham. 2016.
Evolution, phylogeny, ecology, and conservation of the Clade Glires:
Lagomorpha and Rodentia. Pp. 15–26 in D. E. Wilson, T. E. Lacher,
and R. A. Mittermeier, eds. Handbook of the Mammals of the World,
vol. 6, lagomorphs and rodents I. Lynx Edicions, Barcelona.
Leach, K., R. Kelly, A. Cameron, W. I. Montgomery, and N. Reid. 2015a. Ex-
pertly validated models and phylogenetically-controlled analysis sug-
gests responses to climate change are related to species traits in the order
Lagomorpha. PLoS One 10:e0122267. Public Library of Science.
Leach, K., W. I. Montgomery, and N. Reid. 2015b. Biogeography, macroe-
cology and species’ traits mediate competitive interactions in the order
Lagomorpha. Mamm. Rev 45:88–102.
Liow, L. H., T. Reitan, and P. G. Harnik. 2015. Ecological interactions on
macroevolutionary time scales: clams and brachiopods are more than
ships that pass in the night. Ecol. Lett 18:1030–1039.
Liow, L. H., L. Van Valen, and N. C. Stenseth. 2011. Red Queen: from popu-
lations to taxa and communities. Trends Ecol. Evol 26:349–358.
Lomolino, M. V., D. F. Sax, M. R. Palombo, and A. A. van der Geer. 2012. Of
mice and mammoths: evaluations of causal explanations for body size
evolution in insular mammals. J. Biogeogr 39:842–854.
Lomolino,M.V.,A.A.vanderGeer,G.A.Lyras,M.R.Palombo,D.F.Sax,
and R. Rozzi. 2013. Of mice and mammoths: generality and antiquity
of the island rule. J. Biogeogr 40:1427–1439.
Lopez-Martinez, N. 2008. The lagomorph fossil record and the origin of the
European rabbit. Pp. 27–46 in Lagomorph biology. Berlin, Heidelberg:
Springer.
Lyell, C. 1832. Principles of Geology, being an Attempt to Explain the For-
mer Changes of the Earth’s Surface, by Reference to Causes now in
Operation. John Murray, London.
Lyons, S. K., K. L. Amatangelo, A. K. Behrensmeyer, A. Bercovici, J. L.
Blois, M. Davis, W. A. DiMichele, A. Du, J. T. Eronen, and J. T. Faith.
2016. Holocene shifts in the assembly of plant and animal communities
implicate human impacts. Nature 529:80–83.
Maas, M. C., D. W. Krause, and S. G. Strait. 1988. The decline and extinc-
tion of Plesiadapiformes (Mammalia: ?Primates) in North America: dis-
placement or replacement? Paleobiology 14:410–431.
MacArthur, R., and R. Levins. 1967. The limiting similarity, convergence,
and divergence of coexisting species. Am. Nat 101:377–385.
MacCracken, J. G. 1982. Herbaceous vegetation of habitat used by blacktail
jackrabbits and Nuttall cottontails in southeastern Idaho. Amer. Midl.
Nat 107:180–184.
Meijaard, E. 2011. Family Tragulidae (chevrotains). Pp. 320–334 in D. E.
Wilson and R. A. Mittermeier, eds. Handbook of the Mammals of the
World, vol. 2, hoofed mammals. Lynx Edicions, Barcelona.
Mendoza, M., C. M. Janis, and P. Palmqvist. 2006. Estimating the body mass
of extinct ungulates: a study on the use of multiple regression. J. Zool
270:90–101.
Moncunill-Solé, B., J. Quintana, X. Jordana, P. Engelbrektsson, and M.
Köhler. 2015. The weight of fossil leporids and ochotonids: body
mass estimation models for the order Lagomorpha. J. Zool 295:269–
278.
Olson, D. M., E. Dinerstein, E. D. Wikramanayake, N. D. Burgess, G. V.
Powell, E. C. Underwood, J. A. D’amico, I. Itoua, H. E. Strand, and J.
C. Morrison. 2001. Terrestrial Ecoregions of the World: A New Map of
Life on Earth. Bioscience 51:933–938.
Orcutt, J. D., and S. S. Hopkins. 2013. Oligo-Miocene climate change and
mammal body-size evolution in the northwest United States: a test of
Bergmann’s Rule. Paleobiology 39:648–661.
Pagel, M. 1999. Inferring the historical patterns of biological evolution.
Nature 401:877–884.
Paradis, E., and K. Schliep. 2019. ape 5.0: an environment for modern phylo-
genetics and evolutionary analyses in R. Bioinformatics 35:526–528.
Pedersen, R. Ø., B. Sandel, and J.-C. Svenning. 2014. Macroecological evi-
dence for competitive regional-scale interactions between the two major
clades of mammal carnivores (Feliformia and Caniformia). PLoS One
9:e100553.
Pinheiro, J., D. Bates, S. DebRoy, and D. Sarkar. 2012. and R Development
Core Team. R package “nlme”: Linear and nonlinear mixed effects mod-
els, ver. 3.1. https://CRAN.R-project.org/package=nlme.
Pound, M. J., and U. Salzmann. 2017. Heterogeneity in global vegetation
and terrestrial climate change during the late Eocene to early Oligocene
transition. Sci. Rep 7:43386.
Prothero, D. R., and S. E. Foss (eds). 2007. The Evolution of Artiodactyls.
Johns Hopkins University Press, Baltimore.
QGIS Development Team. 2018. QGIS Geographic Information System.
Open Source Geospatial Foundation Project.
Quintana, J., M. Köhler, and S. Moyà-Solà. 2011. Nuralagus rex,gen.et
sp. nov., an endemic insular giant rabbit from the Neogene of Minorca
(Balearic Islands, Spain). J. Vertebr. Paleontol 31:231–240.
R Development Core Team. 2018. R: a language and environment for statis-
tical computing. R Foundation for Statistical Computing, Vienna.
Rabosky, D. L. 2013. Diversity-dependence, ecological speciation, and the
role of competition in macroevolution. Annu. Rev. Ecol. Evol. Syst
44:481–502.
Retallack, G. J. 2007. Cenozoic paleoclimate on land in North America. J.
Geol 115:271–294.
Revell, L. J. 2010. Phylogenetic signal and linear regression on species data.
Methods Ecol. Evol 1:319–329.
Roopnarine, P. D., K. D. Angielczyk, A. Weik, and A. Dineen. 2019. Eco-
logical persistence, incumbency and reorganization in the Karoo Basin
during the Permian-Triassic transition. Earth Sci. Rev 189:244–263.
Rose, K. D. 2006. The Beginning of the Age of Mammals. Johns Hopkins
University Press, Baltimore.
Rose, K. D., V. B. DeLeon, P. Missiaen, R. S. Rana, A. Sahni, L. Singh, and T.
Smith. 2008. Early Eocene lagomorph (Mammalia) from Western India
and the early diversification of Lagomorpha. Proc. R. Soc. B: Biol. Sci
275:1203–1208.
Roth, W. F., and C. T. Cornman. 1916. Rabbit and Cavy Culture: A Complete
and Official Standard of All the Rabbits and Cavies. Poultry Item Press,
Sellersville, Pennsylvania.
Scheffer, M., S. R. Carpenter, T. M. Lenton, J. Bascompte, W. Brock, V.
Dakos, J. Van de Koppel, I. A. Van de Leemput, S. A. Levin, and E. H.
Van Nes. 2012. Anticipating critical transitions. Science 338:344–348.
Schueth, J. D., T. J. Bralower, S. Jiang, and M. E. Patzkowsky. 2015. The
role of regional survivor incumbency in the evolutionary recovery of
calcareous nannoplankton from the Cretaceous/Paleogene (K/Pg) mass
extinction. Paleobiology 41:661–679.
Seckel, L., and C. Janis. 2008. Convergences in scapula morphology among
small cursorial mammals: an osteological correlate for locomotory spe-
cialization. J. Mamm. Evol 15:261–279.
Sepkoski, Jr, J. J. 1996. Competition in macroevolution: the double wedge
revisited. Pp. 211–255 in D. Jablonski, D. H. Erwin, and J. H. Lipps,
eds. Evolutionary Paleobiology. University of Chicago Press, Chicago.
Silvestro, D., A. Antonelli, N. Salamin, and T. B. Quental. 2015. The role of
clade competition in the diversification of North American canids. Proc.
Natl. Acad. Sci 112:8684–8689.
Slater, G. J. 2015. Iterative adaptive radiations of fossil canids show no ev-
idence for diversity-dependent trait evolution. Proc. Natl. Acad. Sci
112:4897–4902.
EVOLUTION 2021 13
S. TOMIYA AND L. K. MILLER
Smaers, J., and C. Mongle. 2020. R package “evomap.”, ver. 0.0.0.9000.
https://github.com/JeroenSmaers/evomap.
Smith, F. A., and S. K. Lyons. 2011. How big should a mammal be? A
macroecological look at mammalian body size over space and time.
Philos. Trans. the R. Soc. B: Biol. Sci 366:2364–2378.
Smith, F. A., R. E. E. Smith, S. K. Lyons, and J. L. Payne. 2018. Body
size downgrading of mammals over the late Quaternary. Science 360:
310–313.
Stanley, S. M., and W. A. Newman. 1980. Competitive exclusion in evolu-
tionary time: the case of the acorn barnacles. Paleobiology 6:173–183.
Strömberg, C. A. 2005. Decoupled taxonomic radiation and ecological expan-
sion of open-habitat grasses in the Cenozoic of North America. Proc.
Natl. Acad. Sci 102:11980–11984.
Theodor, J. M., J. Erfurt, and G. Métais. 2007. The earliest artiodactyls. Pp.
32–58 in D. R. Prothero and S. E. Foss, eds. The evolution of artio-
dactyls. Johns Hopkins University Press, Baltimore.
Tomiya, S. 2013. Body size and extinction risk in terrestrial mammals above
the species level. Am. Nat 182:E196–E214.
Tomiya, S., and L. K. Miller. 2021. Data from: Why aren’t rabbits and
hares larger? Dryad Digital Repository https://doi.org/10.5061/dryad.
ns1rn8ps3.
Ungar, P. S., J. R. Scott, S. C. Curran, H. M. Dunsworth, W. E. H. Harcourt-
Smith, T. Lehmann, F. K. Manthi, and K. P. McNulty. 2012. Early Neo-
gene environments in East Africa: Evidence from dental microwear of
tragulids. Palaeogeogr. Palaeoclimatol. Palaeoecol 342:84–96.
Valentine, J. W., D. Jablonski, A. Z. Krug, and K. Roy. 2008. Incumbency,
diversity, and latitudinal gradients. Paleobiology 34:169–178.
Van Valen, L. 1973. A new evolutionary law. Evol. Theory 1:1–30.
Van Valen, L., and R. E. Sloan. 1966. The extinction of the multituberculates.
Syst. Zool 15:261–278.
Van Valkenburgh, B. 1999. Major patterns in the history of carnivorous mam-
mals. Annu. Rev. Earth Planet. Sci 27:463–493.
Vaughan, T. A. 1978. Mammalogy. 2nd ed. Saunders, Philadelphia, Pennsyl-
vania.
Venditti, C., A. Meade, and M. Pagel. 2011. Multiple routes to mammalian
diversity. Nature 479:393–396.
Verde Arregoitia, L. D., K. Leach, N. Reid, and D. O. Fisher. 2015. Diversity,
extinction, and threat status in Lagomorphs. Ecography 38:1155–1165.
Vrba, E. S. 1985. Environment and evolution: alternative causes of the tem-
poral distribution of evolutionary events. S. Afr. J. Sci 81:229–236.
Vrba, E. S. 1992. Mammals as a key to evolutionary theory. J. Mammal 73:1–
28.
Vucetich, M. G., M. Arnal, C. M. Deschamps, M. E. Pérez, and E. C.
Vieytes. 2015. A brief history of caviomorph rodents as told by the fos-
sil record. Pp. 11–62 in A. I. Vassallo and D. Antenucci, eds. Biology of
caviomorph rodents: diversity and evolution. Sociedad Argentina para
el Estudio de los Mamíferos, Buenos Aires.
Webb, S. D. 1977. A history of savanna vertebrates in the New World. Part I:
North America. Annu. Rev. Ecol. Syst 8:355–380.
Wilson, D., and R. A. Mittermeier (eds). 2011. Handbook of the mammals of
the world, vol. 2. Hoofed mammals. Lynx Edicions, Barcelona, Spain.
Winkler, A. J., and D. Avery. 2010. Lagomorpha. Pp. 305–317 in L. Werdelin
and W. J. Sanders, eds. Cenozoic mammals of Africa. University of
California Press, Berkeley.
Wood, A. E. 1940. The mammalian fauna of the White River Oligocene. Part
III. Lagomorpha. Trans. Amer. Philos. Soc 28:271–362.
Wood, A. E. 1957. What, if anything, is a rabbit? Evolution 11:417–425.
Woodburne, M. O. 2010. The Great American Biotic Interchange: dispersals,
tectonics, climate, sea level and holding pens. J. Mamm. Evol 17:245–
264.
Yamada, F. 2017. Lagomorphology: biology of evasion and escaping strategy.
University of Tokyo Press, Tokyo.
Zachos, J., M. Pagani, L. Sloan, E. Thomas, and K. Billups. 2001. Trends,
rhythms, and aberrations in global climate 65 Ma to present. Science
292:686–693.
Zanazzi, A., M. J. Kohn, B. J. MacFadden, and D. O. Terry. 2007. Large tem-
perature drop across the Eocene–Oligocene transition in central North
America. Nature 445:639–642.
Associate editor: A. Goswami
Handling Editor: D. W. Hall
Supporting Information
Additional supporting information may be found online in the Supporting Information section at the end of the article.
Fig. S1. Maximum lagomorph body masses in modern ecoregions predicted by boosted-regression tree model, plotted against individual predictors.
Fig. S2. Residuals from boosted regression-tree analysis of maximum lagomorph body mass (log10Mmaxlag) in modern ecoregions, compared across
biogeographic realms.
Fig. S3. Observed species temporal ranges (horizontal lines and dots [for single occurrences] based on locality midpoint ages) of leporid-like stem
lagomorphs and leporids (orange), ochotonids (pink), artiodactyls (blue), and perissodactyls (dark blue) in North America from 43.5 to 1.5 Ma plotted
against body masses (point estimates).
Fig. S4. Trajectories of body mass difference between minimum artiodactyl (A) or perissodactyl (B) and maximum lagomorph in North America from
43.5to1.5Ma.
Fig. S5. Bivariate plot of maximum lagomorph and minimum artiodactyl body masses in 547 modern ecoregions.
Fig. S6. Illustration of dental predictor variables used in lagomorph body-mass estimation (Lepus townsendii [MVZ 105670] as an example).
Tab l e S1 . Parameter estimates for lagomorph body-mass prediction models (in order of decreasing predictive accuracy as measured by |D|).
Tab l e S2 . Parameter estimates for ungulate body-mass prediction models (in order of decreasing predictive accuracy).
Tab l e S3 . GLS model parameters for population density Dand ‘basal’ metabolic rate Ragainst body mass in extant leporids and ungulates (non-‘suoid’
artiodactyls and perissodactyls).
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