O R I G I NA L A RT I C L E

doi:10.1111/evo.12787

Congruent phylogenetic and fossil

signatures of mammalian diversification
dynamics driven by Tertiary abiotic change
4,5

Juan L. Cantalapiedra,1,2,3 Manuel Hernandez

Fernandez,
Beatriz Azanza,6 and Jorge Morales2
1

Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstrae 43, Berlin 10115,
Museum fur

Germany
2

Departamento de Paleobiologa, Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Cientficas,

Pinar 25, 28006 Madrid, Spain

3
4

E-mail: jlopezcant@gmail.com

Departamento de Paleontologa, Facultad de Ciencias Geologicas,

Universidad Complutense de Madrid, Jose Antonio

Novais 2, 28040 Madrid, Spain

5

Departamento de Cambio Medioambiental, Instituto de Geociencias (UCM, CSIC), Jose Antonio Novais 2, 28040 Madrid,

Spain
6

Departamento de Ciencias de la Tierra, Facultad de Ciencias, Universidad de Zaragoza, Pedro Cerbuna 12, 50009

Zaragoza, Spain

Received February 11, 2015

Accepted September 22, 2015
Computational methods for estimating diversification rates from extant species phylogenetic trees have become abundant in
evolutionary research. However, little evidence exists about how their outcome compares to a complementary and direct source
of information: the fossil record. Furthermore, there is virtually no direct test for the congruence of evolutionary rates based on
these two sources. This task is only achievable in clades with both a well-known fossil record and a complete phylogenetic tree.
Here, we compare the evolutionary rates of ruminant mammals as estimated from their vast paleontological recordover 1200
species spanning 50 myrand their living-species phylogeny. Significantly, our results revealed that the ruminants fossil record
and phylogeny reflect congruent evolutionary processes. The concordance is especially strong for the last 25 myr, when living
groups became a dominant part of ruminant diversity. We found empirical support for previous hypotheses based on simulations
and neontological data: The pattern captured by the tree depends on how clade specific the processes are and which clades are
involved. Also, we report fossil evidence for a postradiation speciation slowdown coupled with constant, moderate extinction in
the Miocene. The recent deceleration in phylogenetic rates is connected to rapid extinction triggered by recent climatic fluctuations.
KEY WORDS:

Diversification, evolutionary rates, fossil record, mammals, phylogeny, turnover.

The study of diversification patterns through time is of major importance for understanding macroevolutionary and macroecological processes (Benton and Emerson 2007; Morlon 2014). Mostly,
diversification through time has been estimated from fossils
using taxa occurrences (Foote 2000; Alroy 2008) or placing
fossil ranges on evolutionary trees (Smith 1988; Wagner 1995;


C

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Mannion et al. 2010)or from calibrated phylogenies of living

taxa (Mooers and Heard 1997; Stadler 2011a). Usually, fossils
have been recognized as evidence of the antiquity of life as well
as the succession and evolution of organisms on planet Earth.
Patterns of fossil preservation are usually employed as a reliable
source of information on past diversity patterns and processes

C 2015 The Society for the Study of Evolution.

2015 The Author(s). Evolution 
Evolution 69-11: 29412953

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EVOLUTION NOVEMBER 2015

A
Bovidae
Cervidae
Giraffidae
Antilocapridae
Tragulidae
Palaeomerycidae
Dromomerycidae
others (below)

Species Diversity

400

300

200

100

0
Hypertragulidae
Leptomerycidae
Blastomerycidae
Dremotheriidae
Moschidae
Gelocidae

B
30

Species Diversity

such as origination, extinction, dispersal, and turnover (Alroy

2009; Ezard et al. 2011; Domingo et al. 2014). On the other hand,
living species phylogenies also provide valuable information on
such evolutionary processes (Ricklefs 2007; Jetz et al. 2012). Besides depicting evolutionary relationships among extant species,
dated extant-taxa trees contain valuable information on the processes that have shaped the evolutionary history of a group and
have given rise to its extant species. These evolutionary processes
are responsible for phylogenetic trees being far from balanced
and presenting odd distributions of splitting times (Nee et al.
1992; Harvey et al. 1994a; Mooers and Heard 1997). Interestingly, these footprints on the topology of trees are quantifiable
(Mooers and Heard 2002; Stadler 2011a) and recent methods
allow for statistical analyses of such patterns by fitting and comparing different macroevolutionary models of diversification in
highly resolved phylogenies (Rabosky 2006; Rabosky and Lovette
2008; Alfaro et al. 2009; Paradis 2011; Stadler 2011b).
In most cases, scholars are limited to one of the two
approachesfossils or extant-taxa trees. For instance, reasonable phylogenetic information may be available for extant groups
lacking an adequate fossil record. In those circumstances, the
study of evolutionary patterns through phylogenetic approaches
might be especially helpful (Fordyce 2010). On the other hand,
the study of evolutionary patterns of extinct or severely impoverished groupsfor example, rhinoceros, with a 40 myr history
and only six surviving speciesmust rely on the fossil record
(Lloyd et al. 2008; Silvestro et al. 2014b). In a few cases, both
comprehensive fossil and phylogenetic information are available
for a group, and the comparison of the two proxies is desirable
(Simpson et al. 2011; Etienne et al. 2012). Exploring and contrasting the outcome of both methods may help us to overcome
their particular limitations (Fritz et al. 2013). Additionally, such
comparison might shed some light on the particular processes behind tree shape, beyond the pure fitting of evolutionary models.
For instance, a given turnover pulsefaunal replacementwith
both elevated origination and extinction rates may have resulted in
high origination of lineages leading to extant species, thus being
recovered as a diversification pulse if only phylogenetic information is used. However, studies comparing evolutionary rates from
trees of living taxa with the fossil record are few. Furthermore,
these typically focus solely on fossil taxonomic diversity (Quental and Marshall 2010; Morlon et al. 2011; Springer et al. 2012),
rather than assessing fossil-based rates (but see Simpson et al.
2011). Directly testing the similarity between evolutionary rates
estimated from fossil occurrences and living species trees is the
goal of this contribution.
To this aim, we focus on ruminants because they provide
an ideal study group for testing the congruence between these
two sources. Their fossil record is extensiveover 1200 species
spanning the last 50 myrand reasonably well known (see the

Climacoceratidae
Archaeomerycidae
Andegamerycidae
Lophiomerycidae
Hoplitomerycidae
Bachitheriidae

20

10

0
EOCENE

50

40

OLIGOCENE

30

MIOCENE

20

PLI PL

10

Time before present (Ma)

Ruminants diversity through time. Raw species diversity of the 19 ruminant families through time plotted in 1 myr

Figure 1.

time bins. Families are ordered by species richness (A). Small families are plotted in detail in plate (B). , extinct clade; , clade with

horned forms; s, stem group according to Metais

and Vislovokowa
(2007); Pli, Pliocene; Pl, Pleistocene; Ma, million years ago. Note the
change of scale between plates A and B.

Methods section, Figs. 1 and S1). Also, their most complete phylogeny to date comprises all known species and is relatively well
resolved (12% of the nodes are polytomies; Hernandez Fernandez
and Vrba 2005; Cantalapiedra et al. 2014b) and newer phylogenetic hypotheses for the group have been published recently (Bibi
2013, 2014). In this study, we estimated diversification from two
large distributions of ruminant treeswhich cover a wide array
of node-age configurationsas well as from fossil species occurrence data using two different approaches. We then tested for
a common signal in the rate-through-time curves from paleontological and neontological data while assessing which node-age
arrangements improved the fit against the fossil-derived rates.

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Molecular estimates suggest that crown ruminants probably appeared in the Eocene, 4540 Ma (Meredith et al. 2011; Bibi
2013), but the radiation of the living groups mainly took place
in the last 3020 myr (DeMiguel et al. 2014). Thus, we expect
higher concordance between rates from the two sources during the
last half of the study interval. Furthermore, the characterization
of the speciation-extinction interplay across such radiation using
living-taxa trees and extensive fossil databoth at the species
levelmay sum to the debate on ecological limits and their impact on postradiation evolutionary rates (Rabosky and Lovette
2008; Moen and Morlon 2014; Harmon and Harrison 2015).
Ruminants have played a paramount role in terrestrial ecosystems and their evolutionary history is relatively well known (for
recent reviews, see Cantalapiedra et al. 2014a; Clauss and Rossner
2014; DeMiguel et al. 2014). Due to their sensitivity to habitat
change, ruminants have being commonly used as paleoecological proxies (Bobe and Eck 2001; Hernandez Fernandez and Vrba
2006; Kaiser and Rossner 2007). However, their macroevolutionary patterns are only known from raw diversity curves that are
temporal and spatially fragmentary (Vrba 1995; Blondel 2001;
Costeur and Legendre 2008; Maridet and Costeur 2010; Clauss
and Rossner 2014). We here present the first estimate of diversification trends of this large clade of terrestrial mammals at the
global scale. Because ruminants are a habitat-informative clade, a
detailed study of their diversification patterns may also have important implications for unveiling past environmental shifts within
mammalian communities during the Cenozoic.

Methods
TIME SERIES OF DIVERSIFICATION FROM THE TREE
OF LIVING RUMINANTS

For comparison, we estimated phylogenetic speciation rates

through time from two different tree distributions. First, we drew
on a recently published distribution of resolved and recalibrated
trees (Cantalapiedra et al. 2014b) based on the topology presented by Hernandez Fernandez and Vrba (2005), which includes
all living ruminant species. This tree distribution was obtained
by randomly resolving polytomies and recalibrating the nodes
using the extensive fossil and molecular dates of the original
paperavailable for 80% of the nodesin a Bayesian framework (see supplementary methods in Cantalapiedra et al. 2014b).
Interestingly, by using this tree distribution, we incorporate broad
topological and temporal uncertainties into our phylogenetic-rates
analyses. Second, we estimated speciation rates from the Bayesian
tree distribution in Bibis recent study (2013). Twelve percent of
the nodes were calibrated using priors based on a conservative interpretation of the fossil record. Thus, the node ages in Bibis tree
are significantly younger than those obtained by Cantalapiedra

et al. (2014b). We used two tree distributions with different nodeage arrangements to identify how disparate node-age configurations may impact the fit with the fossil record. For simplicity, we
will refer to these two datasets as Bibi and Cantalapiedra.
To estimate time series of phylogenetic diversification dynamics, we carried out a time windows analysis (Simpson et al.
2011). We estimated speciation every 1 myr window. For each
window, speciation rate was calculated using the yuleWindow
function in the LASER (Rabosky 2006) package in R (R Development Core team 2015), in which yuleWindow fits a pure birth
Yule model based on the distribution of nodes and branch lengths
(Simpson et al. 2011). This means it does not estimate an extinction parameter. Nevertheless, the waiting times contained in
evolutionary trees that yuleWindow measures should reflect net
diversification (speciation minus extinction, ; Harvey et al.
1994a). Other available maximum likelihood methods (Stadler
2011b) allow estimating extinction directly. However, to estimate
accurate rates such methods require at least 30 branching events
per time slice (Jetz et al. 2012). In our dataset, this would imply
limiting our analyses interval to the last 10 myrwith two 5 myr
time slicesor the last 6 myrwith three 2 myr times slices. A
speciation time series was calculated for 500 trees of each tree
distributions. Each of the 1000 curves was retained for plotting
and for individual correlation test with fossil-derived rates.

ANALYSIS OF THE RUMINANT FOSSIL RECORD

Information of ruminant species occurrences in the fossil record

was compiled from the New and Old Worlds (NOW) database
(Fortelius 2015) and the Paleobiology Database (Alroy 2015),
both accessed in July 2014. Taxa not identified at the species level
were excluded (1763 occurrences; see Supporting Information for
their temporal distribution). Subsequently, the combined database
was completed and refined with information from the literature
(see Supporting Information) and information on synonyms provided by the NOW collaborators. Finally, we gathered a database
containing 9234 occurrences of 1246 ruminant species, whose
record spans the last 50 myr (Fig. 1; see also Dataset S1 in Dryad
repository). Species belonging to the six extant families (8558
occurrences of 1100 species) represent around 88% of ruminant
fossil diversity, being recorded continuously since around 24 Ma
and making most of the ruminant fossil record since around 20
Ma (Fig. 1). Significant gaps in the fossil record were identified
for Tragulidae, Leptomerycidae, Gelocidae, Blastomerycidae,
and Moschidae (noncontinuous colors in Fig. 1). We performed
an estimation of the quality of the ruminant fossil record by
exploring the temporal distribution of fossil occurrences, their
assigned temporal range and the preservation rate through time
(Alroy 2008; Simpson et al. 2011; Supporting Information;
Fig. S1).

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FOSSILS-BASED EVOLUTIONARY RATES

We assessed relevant evolutionary rates (speciation and extinction) from the ruminant fossil record using two methods. First,
we used the most recent version of Alroys three-timers-based
equations (Alroy 2014). This method uses a four-interval moving
window that has been proved to be robust toward noise produced
by high turnover and/or poor sampling. The method incorporates
the interval-to-interval variation of preservation rate (see Supporting Information). Alroys rates were estimated after dividing
the analysis interval in 1 myr bins. To test the significance of
the evolutionary rates, our dataset was bootstrapped with replacement 5000 times, using species occurrences as sampling units.
Because occurrence data are usually assigned to temporal ranges
broader than 1 myr, for each bootstrap occurrences were randomly
assigned to one of the 1 myr bins falling within their temporal
ranges. We did this to include all the temporal uncertainty in our
analyses. For each time bin, we estimated the mean rate (Finarelli
and Badgley 2010).
Additionally, to the bin-based method (three-timers), we estimated speciation, extinction, and net diversification from the
fossil record using a birthdeath MCMC analyses in a Bayesian
framework (BDMCMC as implemented in PyRate; Silvestro et al.
2014a,b). The BDMCMC algorithm uses fossil occurrences data
to simultaneously estimate speciation and extinction times for
each species while finding the birthdeath model that better fits
the fossil record (Silvestro et al. 2014a,b). The model also incorporates sampling and the BDMCMC algorithm explores alternative
diversification models with different number of rate shifts (Silvestro et al. 2014b). Importantly, the method is robust toward data
incompleteness and is capable to recover a wide array of ratesshift scenarios. We randomly resampled the age of fossil occurrences from the occurrence intervals (from uniform distributions)
10 times using the R function extract.ages included in the PyRate
files. Each replicate was analyzed independently for 10,000,000
generations using Python 2.6 in the Computational Cluster Trueno
at the CSIC. We set the extant number of species to 197, the number of species of our bigger tree, and allowed the preservation
rates to change across lineages following a gamma distribution.
Mean rates through time were estimated after discarding the 20%
of the logged rate estimates as burn-in and combining the results
from the 10 independent runs.
Both Alroys method and the BDMCMC algorithm were used
to analyze the complete fossil record of crown ruminants (9186
occurrences; see Fig. 1) and the fossil record of the six living
ruminant families (8558 occurrences). We followed Metais and
Vislovokowa (2007) and considered crown ruminants all families
except Hypertragulidae, Lophiomerycidae, and Archaeomerycidae (Fig. 1). Some authors have considered the Eocene forms
Archaeotragulus and Krabitherium to belong to the extant family
Tragulidae (but see Sanchez et al. 2010), thus implying a 10 myr

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gap in the fossil record (from around 33 to 24 Ma; see Fig. 1) that
would certainly yield misleading rate estimates from this time
interval. Thus, we exclude these two genera from the six living
families fossil occurrences subset.
We used PyRate to estimate fossil-based origination times
of the crown ruminants, the pecoransthe modern ruminants,
which usually have horns and include five of the six living families (Bibi 2014)and the groups with horned forms (Fig. 1).
This was done by extracting the posterior samples of the ages
of origin of the fossil species of interest derived from all occurrences replicates after modeling the fossil sampling process, and
accounting for the uncertainties around the estimated ages of first
occurrences (Silvestro et al. 2015). Thus, these estimates predate
the oldest fossil occurrence of each group. Then, we fitted normal,
lognormal, and gamma distributions to these dates and choose the
best fit based on the Akaike Information Criterion (Burnham and
Anderson 2002). In this way, we obtain origin age estimates that
may ease the discussion on evolutionary patterns, and distribution
parameters that may be used in future phylogenetic analyses as
node-age priors (Silvestro et al. 2015).
Net diversification was estimated as speciation minus extinction. When the term net diversification is used, we refer to
this balance. The term diversification may be sometimes used
regarding evolutionary rates in a broader sense.
CORRELATION OF THE TREE-BASED AND
FOSSILS-BASED CURVES

So far, comparisons between evolutionary rates from fossil occurrence data and living species phylogenies have mostly relied
on pure visual and descriptive inspections (Simpson et al. 2011).
Here, to test whether curves are in phase with one another, we
used Kendalls correlation tests (Hammer and Harper 2006). This
method has been extensively applied to temporal series (Hammer
and Harper 2006; Mannion et al. 2010), and assesses whether
the peaks and troughs correspond between two curves. That is,
it will here measure the concordance in shifts in evolutionary
rates.
Because we aim to explore the impact of different node-age
configurations on the fit with fossil-derived curves, we estimated
Kendalls correlations between each of the 1000 rate curves obtained from living-species phylogenies (500 from the trees in
Cantalapiedra and 500 from Bibi) and the mean fossil-derived
speciation and net-diversification curves estimated for the crown
ruminants using Alroys method and PyRate. The correlation tests
were repeated using the fossil-derived curves (speciation and net
diversification from Alroys method and the BDMCMC analysis)
obtained from the fossil record of the six surviving ruminant families. This was done to empirically assess whether the congruence
between fossil-based and tree-based rates is independent of the
inclusion of clades without phylogenetic representation in cases

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where the extant families hold much of the fossil record. A total
of 8000 Kendalls correlations were estimated.
To visualize the results, we plotted the density distributions of
the P-values (for significance) and Kendalls taus (, for the sense
of the correlation). To explore whether different node-age arrangements influence the correlation with the fossil record, we plotted
P-values and taus obtained from each correlation test against the
mean node age of the 25% older and 25% younger nodes of the tree
involved. To help data interpretation, we fitted loess curves with
smoothing parameters estimated by generalized cross-validation
to avoid over-fitting to the data (Kohn et al. 2000).

Results
PHYLOGENETIC RATES

The two tree distributions encompass a wide array of node-age

configurations (Fig. 2A). Nevertheless, both datasets show a very
similar profile. The speciation curves obtained from the two tree
distributions show a first pulse related to pecoran and tragulid
basal splits and a second part corresponding with the large radiation within the six living families. The deepest trees place the
first pulse in the early Oligocene (32 Ma) and the beginning
of within-family radiations in the Oligocene-Miocene (24 Ma).
The trees with younger node agesmainly Bibis distribution
place these events in the early Miocene (20 Ma) and middle
Miocene (15 Ma), respectively. In both tree distributions, a slowdown follows the second big burst, followed by a recoverywith
a synchronic peak in both datasets, around 7 Maand a final
slowdown toward the present (Bibis dataset shows a recovery in
the Plio-Pleistocene; Fig. 2A).

10 Ma. The Miocene to Pliocene transition marks a peak of the

replacement rate stemming from an episode of elevated speciation and extinction rates (Fig. 2B). Afterwards, net diversification
increased again, in part due to low extinction at the beginning
of the Pliocene. Due to the three-timers methodology, net diversification cannot be recovered from the last three bins of the
analysis interval.
The BDMCMC analyses reveal high and maintained speciation rates of crown ruminant lineages throughout the Eocene, the
Oligocene and the earliest Miocene (Fig. 2D). This high speciation was coupled with elevated extinction rates, particularly severe
in the late Eocene, and much of the Oligocene (between 47 and
26 Ma). The confidence intervals are broad until around 26 Ma,
probably due to the large occurrence temporal ranges (Fig. S1).
The diversification maximum at the Oligocene-Miocene boundary is here a result of decelerating extinction and sustained
high speciation. The end of the net-diversification pulse, around
20 Ma, was rendered by a slowdown in speciation rates. Moderate
speciation and extinction characterized much of the Miocene. Extinction and speciation recovered around 8 and 6 Ma, respectively.
Whereas speciation stayed constant until the present, extinction
intensely peaked during the last two million years resulting in the
most severe negative net-diversification pulse of the analysis interval. Gamma distributions best fitted the time of origin of crown
ruminants (offset = 42.63; shape = 1.76; rate = 0.46; mean =
46.47; 95% highest posterior density (HPD) = 42.8552.24), pecorans (offset = 26.96; shape = 1.68; rate = 0.57; mean = 29.90;
95% HPD = 27.0433.30), and groups with horned forms (offset
= 26.49; shape = 2.02; rate = 1.96; mean = 27.51; 95% HPD =
26.5629.06; Fig. 2C).

RATES FROM FOSSIL OCCURRENCES

CURVE CORRELATIONS

Rates estimated from fossil occurrences (net diversification, speciation, and extinction) obtained from the three-timers method
and the BDMCMC are depicted in Fig. 2B and C, respectively.
Patterns of net diversification are congruent between both approaches, although the speciation and extinction processes differ
in some aspects.
According to the three-timers method, important speciation pulses are recovered during the middle and late Eocene
(45 Ma; Fig. 2B), and the Eocene-Oligocene boundary (34 Ma)
featured high extinction and speciation. The early Oligocene is
characterized by overall neutral net diversification and turnover
low extinction and very slow speciation(Fig. 2B). At the
end of the Oligocene net-diversification rates peaked again, remaining high across the Oligocene-Miocene boundary (around
24 Ma). Speciation decelerated afterwards. From about 20 Ma
onwards, several speciation and extinction peaks render a relatively constant turnover. A negative net-diversification peak is
recovered around 15 Ma followed by a recovery between 12 and

The results of the 8000 Kendalls correlations are shown in

Figure 3. When the three-timers were used to estimate fossilbased evolutionary rates, the speciation rates based on the deepest
treesfrom Cantalapiedras tree distributionshowed high congruence with the speciation in fossil crown Ruminantia and with
speciation and net diversification in the fossil lineages of the living groups. These correlations seemed unaffected by the different
node ages of the tree set. Only the rate curves obtained from
the oldest trees showed significant correlationand high positive
tauswith the net-diversification curve of the crown fossil ruminants. Speciation rates estimated from Bibis trees correlated
positively with speciation in the fossil lineages of the living ruminant families. This correlation is weaker for the trees whose
deeper nodes are younger.
Rates calculated from tree distribution in Cantalapiedra correlated positively with speciation and net diversification in the
fossil record of the six living families as estimated by the BDMCMC algorithm (Fig. 3GL). Only rates in Bibis deepest trees

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tree-based speciation

Bibi
Cantalapiedra et al.

0.5
0.4
0.3
0.2
0.1
0.0

EOCENE
50

three-timers rates

OLIGOCENE

40

30

MIOCENE
20

inception of
first C3 grasslands

permanent
EAIS

PLI PL
10

inception of
first C4 grasslands

0
onset of
modern glaciations

0.75

Arabian
Connection
Bering Strait

net-diversification
net-div. living families
speciation
extinction

0.50

0.25

0.00

crown ruminants

PyRate rates

0.5
first fossil horns

50

groups with
horned forms

crown pecorans

40

30

20

10

times of origin
(density)

-0.25

0.6

0.3

0.0
net-diversification
net-div. living families
speciation
extinction

-0.3

EOCENE
50

40

OLIGOCENE
30

MIOCENE
20

PLI PL
10

Time (Ma)
Figure 2.

Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants. (A) Tree-based speciation

rates estimated from 1000 living species phylogenies from Bibi (2013) and Cantalapiedra et al. (2014b). The shadowed area represents the
95% confidence intervals. (B) Net diversification, speciation, and extinction in fossil crown ruminants estimated using the three-timers
method (Alroy 2014). (C) Estimated times of origins of crown ruminants, pecorans (advanced ruminants) and groups with horned forms
according to PyRate. (D) Net diversification, speciation, and extinction in fossil crown ruminants estimated using PyRate (Silvestro et al.
2014a). In (B) and (D), net diversification in fossil lineages of the living groups is shown in light blue. Shadowed areas in (B) and (D)
represent the 95% confidence interval for the net diversification. The first record of horned ruminants (gray) is based on DeMiguel et al.

(2014). Mayor tectonic, climatic, and ecological episodes (Cerling et al. 1997; Zachos et al. 2008; Stromberg
2011) are shown in colors.
EAIS, East Antarctic Ice Sheet; Pli, Pliocene; Pl, Pleistocene. Ma, million years ago.

showed a significant positive correlation with PyRates speciation

and net diversification in the fossil record of the living groups.
Phylogenetic rates from this tree set correlated negatively with
speciation in fossil crown ruminants. A negative correlation was
found also with the net diversification of the fossil crown ruminants for the younger trees in Bibis dataset.

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Discussion
Past evolutionary processes left a congruent signal in the fossil
record and the phylogeny of the living ruminants. The concordance was stronger when fossil-based rates were estimated from
paleontological data of the living groups only (Figs. 2 and 3). We

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Figure 3. Congruence of tree-based and fossils-based rates from the three-timers method (AF) and PyRate (GL). Density plots of
P-values (A), P-values from Kendalls correlation tests plotted against the mean age of the 25% older nodes (B) and younger nodes (C)

of each tree. Density plots of taus () (D), taus Kendalls correlation tests plotted against the mean age of the 25% older nodes (E)
and younger nodes (F) of each tree. Same plots for P-values and taus when phylogenetic rates were compared with PyRate results (GL).
In each plot, continuous LOESS lines represent results for trees in Cantalapiedra et al. (2014b) and dashed lines results for Bibis trees
(Bibi 2013). Dark blue and light blue, fits of phylogenetic rates with net diversification in fossil lineages of crown ruminants and living
groups, respectively. Dark green and light green, fits of phylogenetic rates with speciation in fossil lineages of crown ruminants and
living groups, respectively. Circles and triangles in plates A, D, G, and J represent the medians of the parameter values of correlations for
trees in Cantalapiedra et al. (2014b) and Bibi (2013), respectively.

found less agreement in comparisons that used the entire fossil

record of crown ruminants, where correspondences among different phylogenetic datasets and fossil-based methodsthreetimers and PyRateperformed disparately (Fig. 3). This is not
surprising given the nature of the evolutionary processes themselves and the particularities and limitations of each of the methods used in this study to recover the past. Despite the many comparisons among rate profiles conducted here (i.e., two different
tree distributions, two fossil-based methods, two different fossil
subsets), we obtained unambiguous results about their fit through
a large array of different phylogenetic trees (Fig. 3).
The capacity of living ruminant phylogenies to reconstruct
the most basal events of ruminant evolution (the Eocene and

Oligocene, from around 50 to 24 Ma) critically determines the

extent to which they match evolutionary rates estimated from
the fossil record. Reconstructed branching events in living ruminant trees are scarce during this early stage of the analysis
interval, yielding very low speciation rates (Fig. 2A). On top
of this, different interpretations of our large fossil data (i.e., a
discrete-bin-based approach and a birthdeath Bayesian algorithm) portrait disparate evolutionary scenarios for this period
(especially regarding speciation rates, green curves in Fig. 2B and
D). The three-timers approach reconstructed overall low speciation and moderate-to-negative net diversification in the 5024 Ma
temporal span. Only one relevant speciation event was estimated
around 40 Ma (Fig. 2B). This is a more literal read of the fossil

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record than that offered by PyRate (see below). The interpretation

of an early evolutionary calm before the big Miocene radiation
fits better the classic paleontological view (based on fossil ranges
and raw diversity curves; Janis et al. 2000; Costeur and Legendre
2008; Maridet and Costeur 2010) and the phylogenetic inferences
(Fig. 2A and B). The two tree distributions yielded confidence
intervals that overlap with zero in this temporal span. Thus, when
the three-timers method was used, the correlation between treebased rates and fossil speciation of the crown ruminants was
strong for most of the trees in the Cantalapiedra dataset and some
of Bibis trees.
PyRates BDMCMC algorithm estimates a different scenario
for the first 25 myr of ruminant evolution, especially with respect
to speciation rates (compare green curves in Fig. 2B and D).
Unsurprisingly, this notably influenced the congruence with phylogenetic rates (Fig. 3GL). The BDMCMC approach places the
highest speciation rates in the Eocene, Oligocene, and earliest
Miocene (4522 Ma, Fig. 2D). As a result, PyRate speciation and
diversification estimates for the fossil crown ruminants yielded
a poor fit with our phylogenetic rates, which show their lowest values in this temporal span (Fig. 2A). This striking difference with respect to the three-timers rates could be explained
by a deficient sampling rate (especially low for the Oligocene;
Fig. S1). Surprisingly, although the BDMCMC algorithm (after
modeling the sampling to estimate the corrected life span of each
lineage; Silvestro et al. 2014a) showed high speciation rates, it
still estimated accelerated extinction rates between 37 and 26 Ma
(Fig. 2C). In this regard, both methods agree, suggesting that we
are recovering a true macroevolutionary signal and that the estimate of high extinction rates is probably robust toward sampling.
Although Alroys method yielded negative Eocene and
Oligocene diversification rate and subsequent diversity loss
also visible in the raw diversity plot (Fig. 1)PyRate revealed
a scenario where net diversification slowed down but remained
positive. Nonetheless, PyRate yielded broad confidence intervals
for this temporal span, suggesting other scenarios should not be
discarded. The high Eocene-Oligocene speciation and extinction
rates should have rendered a profound replacement in ruminant
faunas. This result is consistent with the high turnover previously
reported in Eurasian faunas (the so-called Grand Coupure;
Janis 2008; Springer et al. 2012), which has been associated with
cooler and more arid conditions in early Oligocene terrestrial
habitats (Mosbrugger et al. 2005; Zachos et al. 2008). However,
understanding the impact of the Oligocene new environmental
context in mammalian communities demands further exploration.
A comprehensive characterization of dietary shifts in Oligocene
ruminant lineages will be very insightful in this regard (Blondel
2001). Interestingly, the Oligocene extinction peak is clearly
reflected by the trees as a prolonged period of low branching
rate (Fig. 2A). We suggest that this lineage depletion marked the

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shape of the living ruminants tree to a great extent, restricting

the number of lineages that it recovers from the Eocene and
Oligocene (Fig. 2). This provides an empirical proof of the
footprint that prolonged and high extinction rates leave in living
species phylogenies (Harvey et al. 1994b; Morlon et al. 2011).
A major net-diversification pulse is robustly recovered from
both the fossil record and the phylogenetic trees during the
late Oligocene and early Miocene (2722 Ma, Fig. 2). Although the two fossil-based approaches show an increase in netdiversification rates paired with low extinction, they differ in
the macroevolutionary context of such major net-diversification
peaks. Alroys method depicts accelerating speciation rates as ruminant lineages approached the Oligocene-Miocene limit. PyRate
suggests that the high speciation rates represent continuity with
regard to Eocene and Oligocene times, and that extinction would
have dropped as modern groups evolved around 27 Ma (Fig. 2C
and D). This moment marked the shift toward a second major
stage of ruminant evolution: the dominion of the advanced
mostly hornedruminants, the pecorans (see Fig. 1 and further
discussion below). The major radiation encompassed the appearance of several living and extinct groups and a rapid accumulation
of species diversity (Fig. 1). Extant groups may have exhibited
early Miocene rates above those estimated for the crown group
as a whole (Fig. 2D). As a result, ruminant diversity was rapidly
dominated by living groups since the early Miocene until today
(Fig. 1; Costeur and Legendre 2008; Maridet and Costeur 2010).
Indeed, diversification rates in fossil lineages of the crown and the
living families are very similar for the rest of the analysis interval
(Figs. 2 and S2). This preponderance is also congruent with the
high agreement found between fossil-derived rates and phylogenetic rates in the last 25 myr of the study interval. Correlations showed significant concordance among curves from different fossil-based methods and tree distributions when the fossil
record of the living groups was used (Fig. 3). Only the youngest
trees from Bibis dataset show nonsignificant fits. Overall, as early
Miocene net diversification recovered after a prolonged period of
high extinction, the concordance between the macroevolutionary
signal in the fossil record and our phylogenetic data significantly
increased.
After the Oligocene-Miocene diversification burst, speciation and net diversification significantly declined. However, only
trees from the dataset in Cantalapiedra et al. show a comparable
pattern (Fig. 2). There are two potential explanations for this outcome. First, the middle Miocene (1712 Ma) was indeed a period
of relatively low macroevolutionary rates and the younger trees
within Bibis dataset are simply too young to reflect the true trend.
Second, Bibis trees correctly reflect the timing of speciation of
crown living lineages, whereas the other sources are recovering
the speciation of stem and crown living families combined
our fossil data include stem forms. If true, this second scenario

C O N G RU E N T P H Y L O G E N E T I C A N D F O S S I L S I G NAT U R E S O F M A M M A L I A N D I V E R S I F I C AT I O N

implies that high branching rates in living species trees may not
fit the rates estimated from the fossil record, where a distinction
of crown and stem forms is very problematic even in a group with
a well-known fossil record as the ruminants (Sanchez et al. 2011;
Bibi 2014). Thus, in cases where there is a significant temporal
lag between the diversification of stem and crown lineagesas it
may be the case herethe selection of true crown fossil calibration points is crucial (Bibi 2013). In this regard, new total-evidence
methods (tip-dating; Ronquist et al. 2012; Grimm et al. 2015)
are contributing to overcome this issue by placing fossils within
the phylogenetic trees based on morphology while using them
to estimate divergence times (Ronquist et al. 2012). Future totalevidence analyses based on molecular data and morphology of
living and fossil ruminants will clarify this disagreement.
The great diversification pulse of the Oligocene-Miocene
and the following deceleration of speciation rates may contribute
a first-hand empirical proof of the impact of ecological limits on
postradiation evolutionary rates (Moen and Morlon 2014; Harmon
and Harrison 2015). According to paleontological and paleoclimatic evidences, the Paleogene-Neogene transition was a period
of profound change in terrestrial ecosystems. New available adaptive space was probably created by important shifts in Oligocene
and early Miocene climate (Bruch et al. 2007; Eronen et al. 2010),
environments (Stromberg 2011), and tectonicsfor example, ruminants entered Africa for the first time (Maglio 1978). Under this
view, speciation rates would have slowed down as the adaptive
space filled. Importantly, extinction rates remained at basal levels,
showing that the Miocene slowdown in the living ruminant tree is
rendered at the end of an expansion phase of the modern forms and
not by extinction increasing above speciation (Moen and Morlon
2014). Distinguishing between these alternatives is challenging
if just living species trees are used (Rabosky and Lovette 2008).
Ecological saturation occurs at the species level, and only evolutionary rates estimated from species-level fossil occurrence data
should be used to address such questions precisely (Harmon and
Harrison 2015). In this regard, our fossil-based analyses provide
valuable support to previous conclusions built on neontological
information and simulations (Rabosky and Lovette 2008).
Ruminant faunas underwent critical macroevolutionary processes in the last 10 million years (Fig. 2). The fossil data suggest an increase of extinction from that time onwards and a later
rebound of speciation rates. Estimates from the three-timers
method and PyRate fit, showing neutral-to-negative net diversification that translated into a late Miocene diversity loss. Phylogenetic rates remained steady or slightly decreased. Overall, we
do not recognize a direct resemblance among curves in this temporal point. Nevertheless, it may be the case that late Miocene
depletion also contributed to the low branching rates recovered
earlier in the trees (1510 Ma; see Rabosky and Lovette 2008). If
the Oligocene prolonged extinction erased most of the branches

before 30 Ma, the late Miocene diversity loss may also have prevented part of the evolutionary signal from the middle Miocene
to be recorded in the living species trees (Harvey et al. 1994a).
We rule out the possibility that this extinction pulse is an artifact
derived from poor sampling. Preservation rates of the ruminant
fossil record are relatively high for the late Miocene (around 0.75;
Fig. S1). Furthermore, the two methods used to analyze the fossil
data account for heterogeneous sampling in very different ways
and yet yield very similar results with tight confidence intervals
(Fig. 2). Our results show a recovery in speciation during the latest
Miocene and the Pliocene, from around 7 to 2.5 Ma. Late Pliocene
speciation rebound to levels comparable to the early Miocene. As
argued above, this recovery probably is reflected by the trees with
nodes slightly deeper in time due to the deeper molecular estimates, toward the Miocene-Pliocene. Very likely, mainly bovids
and deer lineages led that speciation pulse including the radiation
of American deer and that of African bovid tribes (Bibi et al.
2009; Cantalapiedra et al. 2014c).
The Plio-Pleistocene was one of the most dramatic episodes
in ruminant evolution. A critical net diversification drop recovered from the fossil record couples a slowdown in the phylogenetic
rates toward the end of our analysis interval (Fig. 2). Fossil-based
rates for the last 2 myronly provided by PyRate, see Methods
exhibited a severe extinction event. Speciation rate still remained
close to early Miocene levels during this period, but extinction
significantly surpassed it (Fig. 2D). The resulting replacement
process would have reshaped ruminant faunas faster than ever.
The idea of a major Plio-Pleistocene climatic shift (the establishment of continental northern-hemisphere glaciations; Miller
et al. 2005) and human activity reshaping mammalian faunas have
been proposed for several mammalian clades (Delson 1985; Kimbel 1995; Lyons et al. 2004; Gomez Cano et al. 2013). These
suggestions are supported by our results.
To our knowledge, this is the first direct evidence for negative net diversificationextinction above speciationas being
behind the slowdowns in living species trees toward the tips often
reported in the literature (Moen and Morlon 2014). This empirical case opens the possibility that, indeed, progressive decrease
in phylogenetic rates toward recent times may, in some cases,
be the result of recent and drastic climatic fluctuations triggering
extinction.
Concluding remarks

Since the first studies on tree shape (Nee et al. 1992; Harvey
et al. 1994b), an extensive body of research has been devoted to
understand how evolutionary processes leave their signal in phylogenetic trees of extant taxa. Most researchers have focused on
estimate evolutionary ratesthat is, speciation and extinction
from phylogenies of living species (Rabosky and Lovette 2008;
Alfaro et al. 2009; Stadler 2011a). Other studies have pursued

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the identification of past episodes in evolutionary trees by comparison with simulations (Crisp and Cook 2009). Surprisingly,
little research has been carried out to compare the evolutionary
rates derived from living species trees and paleontological data
(using raw diversity data; Quental and Marshall 2010; Morlon
et al. 2011; Etienne et al. 2012). Simpson et al. (2011) compared
phylogenetic rates with fossil-based rates, but the correlation between curves was not tested statistically. Here, we have shown
how the combination of speciation and extinction, as recovered
from the fossil record, left a signal in the living species phylogeny
of ruminants through 50 myr of evolution. Our findings suggest
that the ability of a living species phylogeny to capture past events
depends on how clade specific the processes are and which clades
are involved. Also, the high correlations reported here between
tree-based and fossils-based rates very likely stems from the fact
that nearly 90% of the species richness in the fossil record of the
group belongs to the six surviving ruminant families (Fig. 1). We
acknowledge that this might not be the case scenario for many
study groups.
The evidence presented here suggests that phylogenetic trees
probably hold reliable information about evolutionary processes
if the most species-rich subclades still have a comprehensive representation among extant species and extinct subclades do not
constitute an important part of the past evolutionary history of
the group in terms of species richness (here around 12%). Also,
calibrating phylogenies using highly tight and conservative fossilinformed priors may not yield rate profiles that fit rates through
time from the fossil record, because the major pulses in lineage
speciation may have taken place in stem lineages.
Our results also provide new views on ruminant evolution
that should be contrasted in the future. The classic perception of
ruminant evolution portraits the Eocene and Oligocene as a long
period featuring small, hornless, and browser forms that were
not involved in any extraordinary diversification pulse (the lull
before the storm Janis 2008). This historical notion derives from
the direct interpretation of raw diversity plots through time as that
in Figure 1. These basal ruminants have a poorer fossil record
and have received less attention than the Neogene explosion of
extant groups (Metais and Vislobokova 2007). In contrast, our
PyRate analyses suggest that basal crown ruminants may have
experienced the most intense and prolonged lineage origination
and replacement in the history of the group (Fig. 2C).
Our analyses strongly suggest that the classic Miocene ruminant radiation begun in Oligocene times and prolonged until
22 Ma (Fig. 2). This pulse, concomitant with the origin of modern ruminants (Fig. 2BD), has been linked to the acquisition
of larger body sizes (Morales et al. 1993), new dietary strategies (Cantalapiedra et al. 2014b), and behavior (Janis 1982, 1989;
Brashares et al. 2000). However, this event and the estimated
origin of ruminant groups with horned forms (27.5 Ma) largely

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EVOLUTION NOVEMBER 2015

predates the first fossil evidence of horns in ruminants (1917

Ma, see DeMiguel et al. 2014; Fig. 2C). This implies that either
most of the diversification event occurred prior to the independent
evolution of horns in several lineages (DeMiguel et al. 2014), or
those horned ruminants are to be found in the Oligocene.
Finally, since little can be recovered from living species trees
about the first 25 myr of ruminant evolution, improving the poor
Eocene and Oligocene fossil record is crucial for future paleobiological studies (Blondel 2001). This may be also the case for other
groups of land vertebrates with only a reasonable post-Paleogene
phylogenetic coverage due to a high faunal replacement and
lineage depletion in Eocene and Oligocene times (Springer et al.
2012; Hipsley et al. 2014; McGuire et al. 2014). In summary,
unveiling Paleogene environmental trends and mammal communities dynamics will largely benefit from fossil data. And basal
ruminants probably have a lot to teach us about it.
ACKNOWLEDGMENTS
We want to thank A. . Mooers, F. Bibi, and J. Muller for their insightful
comments on different versions of the manuscript. We also thank P. Wagner and an anonymous reviewer for their many helpful comments and
ideas, which substantially helped to improve this study. I. M. Sanchez
made valuable observations on basal ruminants. We acknowledge technical assistance for using the Cluster Trueno (Spanish Research Council) from D. Basabe, A. de Castro, and H. Gascon. D. Silvestro helped
with the PyRate workflow. This is a contribution by the Palaeoclimatology, Macroecology and Macroevolution of Vertebrates research team
(www.pmmv.com.es) of the Complutense University of Madrid as a part
of the Research Group UCM 910607 on Evolution of Cenozoic Mammals
and Continental Palaeoenvironments. This research was made possible by
projects from the Spanish Ministry of Science and Innovation (CGL200601773/BTE, CGL2010-19116/BOS, and CGL2011-25754) and from the
Complutense University of Madrid (PR1/06-14470-B). This is Paleobiology Database official publication number 240. JLC is currently funded
by the Humboldt Foundation and thus belongs to the Leyendas Urbanas
group of the Spanish Ministry of Education.

DATA ARCHIVING
The fossil occurrence dataset is available in the Dryad Digital Repository
(http://dx.doi.org/10.5061/dryad.kp153).

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Associate Editor: M. Friedman

Handling Editor: J. Conner

C O N G RU E N T P H Y L O G E N E T I C A N D F O S S I L S I G NAT U R E S O F M A M M A L I A N D I V E R S I F I C AT I O N

Supporting Information
Additional Supporting Information may be found in the online version of this article at the publishers website:
Figure S1. Quality of the ruminant fossil record.
Figure S2. Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants.

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