Congruent Phylogenetic and Fossils Signa

ORIGINAL ARTICLE

doi101111evo12787

Congruent phylogenetic and fossilsignatures of mammalian diversificationdynamics driven by Tertiary abiotic changeJuan L Cantalapiedra123 Manuel Hernandez Fernandez45 Beatriz Azanza6 and Jorge Morales2

1Museum fur Naturkunde Leibniz Institute for Evolution and Biodiversity Science Invalidenstraszlige 43 Berlin 10115

Germany2Departamento de Paleobiologıa Museo Nacional de Ciencias Naturales Consejo Superior de Investigaciones Cientıficas

Pinar 25 28006 Madrid Spain3E-mail jlopezcantgmailcom

4Departamento de Paleontologıa Facultad de Ciencias Geologicas Universidad Complutense de Madrid Jose Antonio

Novais 2 28040 Madrid Spain5Departamento de Cambio Medioambiental Instituto de Geociencias (UCM CSIC) Jose Antonio Novais 2 28040 Madrid

Spain6Departamento 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 recordmdashover 1200

species spanning 50 myrmdashand their living-species phylogeny Significantly our results revealed that the ruminantrsquos 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 im-

portance for understanding macroevolutionary and macroecologi-

cal processes (Benton and Emerson 2007 Morlon 2014) Mostly

diversification through time has been estimated from fossilsmdash

using taxa occurrences (Foote 2000 Alroy 2008) or placing

fossil ranges on evolutionary trees (Smith 1988 Wagner 1995

Mannion et al 2010)mdashor 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

2 9 4 1Ccopy 2015 The Author(s) Evolution Ccopy 2015 The Society for the Study of EvolutionEvolution 69-11 2941ndash2953

JUAN L CANTALAPIEDRA ET AL

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) Be-

sides depicting evolutionary relationships among extant species

dated extant-taxa trees contain valuable information on the pro-

cesses 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) Interest-

ingly 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 com-

paring 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

approachesmdashfossils or extant-taxa trees For instance reason-

able 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 impov-

erished groupsmdashfor example rhinoceros with a 40 myr history

and only six surviving speciesmdashmust 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 con-

trasting 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 be-

hind tree shape beyond the pure fitting of evolutionary models

For instance a given turnover pulsemdashfaunal replacementmdashwith

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 informa-

tion 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 (Quen-

tal 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 extensivemdashover 1200 species

spanning the last 50 myrmdashand reasonably well known (see the

50 40 30 20 10 0

Time before present (Ma)

EOCENE OLIGOCENE MIOCENE PLI PL

Hypertragulidae

Leptomerycidae

Blastomerycidae

Dremotheriidae

Moschidae

Gelocidae

Climacoceratidae

Archaeomerycidae

Andegamerycidae

Lophiomerycidae

Hoplitomerycidae

Bachitheriidae

daggerdaggerdaggerdagger

dagger

daggerdaggerdaggerdaggerdagger

dagger

Sp

ecie

s D

ive

rsity

30

20

10

0

s

s

s

Sp

ecie

s D

ive

rsity

0

100

200

300

400 Bovidae

Cervidae

Giraffidae

Antilocapridae

Tragulidae

Palaeomerycidae

Dromomerycidaeothers (below)

daggerdagger

A

B

Figure 1 Ruminants diversity through time Raw species diver-

sity of the 19 ruminant families through time plotted in 1 myr

time bins Families are ordered by species richness (A) Small fami-

lies are plotted in detail in plate (B) dagger extinct clade ϒ 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 phy-

logeny 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 phyloge-

netic hypotheses for the group have been published recently (Bibi

2013 2014) In this study we estimated diversification from two

large distributions of ruminant treesmdashwhich cover a wide array

of node-age configurationsmdashas well as from fossil species oc-

currence data using two different approaches We then tested for

a common signal in the rate-through-time curves from paleonto-

logical and neontological data while assessing which node-age

arrangements improved the fit against the fossil-derived rates

2 9 4 2 EVOLUTION NOVEMBER 2015

CONGRUENT PHYLOGENETIC AND FOSSIL SIGNATURES OF MAMMALIAN DIVERSIFICATION

Molecular estimates suggest that crown ruminants probably ap-

peared in the Eocene 45ndash40 Ma (Meredith et al 2011 Bibi

2013) but the radiation of the living groups mainly took place

in the last 30ndash20 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 datamdashboth at the species

levelmdashmay sum to the debate on ecological limits and their im-

pact on postradiation evolutionary rates (Rabosky and Lovette

2008 Moen and Morlon 2014 Harmon and Harrison 2015)

Ruminants have played a paramount role in terrestrial ecosys-

tems 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 paleoecologi-

cal proxies (Bobe and Eck 2001 Hernandez Fernandez and Vrba

2006 Kaiser and Rossner 2007) However their macroevolution-

ary 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 diver-

sification 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 im-

portant implications for unveiling past environmental shifts within

mammalian communities during the Cenozoic

MethodsTIME 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 pre-

sented 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

papermdashavailable for 80 of the nodesmdashin a Bayesian frame-

work (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 Bibirsquos recent study (2013) Twelve percent of

the nodes were calibrated using priors based on a conservative in-

terpretation of the fossil record Thus the node ages in Bibirsquos tree

are significantly younger than those obtained by Cantalapiedra

et al (2014b) We used two tree distributions with different node-

age arrangements to identify how disparate node-age configura-

tions may impact the fit with the fossil record For simplicity we

will refer to these two datasets as ldquoBibirdquo and ldquoCantalapiedrardquo

To estimate time series of phylogenetic diversification dy-

namics 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 Devel-

opment 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 ex-

tinction parameter Nevertheless the waiting times contained in

evolutionary trees that yuleWindow measures should reflect net

diversification (speciation minus extinction λ minus μ 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 myrmdashwith two 5 myr

time slicesmdashor the last 6 myrmdashwith 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 pro-

vided 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)

EVOLUTION NOVEMBER 2015 2 9 4 3


FOSSILS-BASED EVOLUTIONARY RATES

We assessed relevant evolutionary rates (speciation and extinc-

tion) from the ruminant fossil record using two methods First

we used the most recent version of Alroyrsquos ldquothree-timersrdquo-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 andor poor sampling The method incorporates

the interval-to-interval variation of preservation rate (see Sup-

porting Information) Alroyrsquos 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 replace-

ment 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 es-

timated speciation extinction and net diversification from the

fossil record using a birthndashdeath MCMC analyses in a Bayesian

framework (BDMCMC as implemented in PyRate Silvestro et al

2014ab) The BDMCMC algorithm uses fossil occurrences data

to simultaneously estimate speciation and extinction times for

each species while finding the birthndashdeath model that better fits

the fossil record (Silvestro et al 2014ab) The model also incorpo-

rates sampling and the BDMCMC algorithm explores alternative

diversification models with different number of rate shifts (Silve-

stro et al 2014b) Importantly the method is robust toward data

incompleteness and is capable to recover a wide array of rates-

shift scenarios We randomly resampled the age of fossil occur-

rences from the occurrence intervals (from uniform distributions)

10 times using the R function extractages included in the PyRate

files Each replicate was analyzed independently for 10000000

generations using Python 26 in the Computational Cluster Trueno

at the CSIC We set the extant number of species to 197 the num-

ber 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 Alroyrsquos 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 Archaeomeryci-

dae (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

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 pecoransmdashthe ldquomodern ruminantsrdquo

which usually have horns and include five of the six living fam-

ilies (Bibi 2014)mdashand 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 occur-

rences 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 ex-

tinction When the term ldquonet diversificationrdquo is used we refer to

this balance The term ldquodiversificationrdquo 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 oc-

currence 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 Kendallrsquos 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

Kendallrsquos correlations between each of the 1000 rate curves ob-

tained 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 Alroyrsquos method and PyRate The correlation tests

were repeated using the fossil-derived curves (speciation and net

diversification from Alroyrsquos method and the BDMCMC analysis)

obtained from the fossil record of the six surviving ruminant fam-

ilies 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



where the extant families hold much of the fossil record A total

of 8000 Kendallrsquos correlations were estimated

To visualize the results we plotted the density distributions of

the P-values (for significance) and Kendallrsquos taus (τ for the sense

of the correlation) To explore whether different node-age arrange-

ments 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)

ResultsPHYLOGENETIC 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 radi-

ation 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 agesmdashmainly Bibirsquos distributionmdash

place these events in the early Miocene (20 Ma) and middle

Miocene (15 Ma) respectively In both tree distributions a slow-

down follows the second big burst followed by a recoverymdashwith

a synchronic peak in both datasets around 7 Mamdashand a final

slowdown toward the present (Bibirsquos dataset shows a recovery in

the Plio-Pleistocene Fig 2A)

RATES FROM FOSSIL OCCURRENCES

Rates estimated from fossil occurrences (net diversification spe-

ciation and extinction) obtained from the ldquothree-timersrdquo method

and the BDMCMC are depicted in Fig 2B and C respectively

Patterns of net diversification are congruent between both ap-

proaches although the speciation and extinction processes differ

in some aspects

According to the ldquothree-timersrdquo method important speci-

ation 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 turnovermdash

low extinction and very slow speciationmdash(Fig 2B) At the

end of the Oligocene net-diversification rates peaked again re-

maining high across the Oligocene-Miocene boundary (around

24 Ma) Speciation decelerated afterwards From about 20 Ma

onwards several speciation and extinction peaks render a rela-

tively constant turnover A negative net-diversification peak is

recovered around 15 Ma followed by a recovery between 12 and

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

replacement rate stemming from an episode of elevated specia-

tion 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 ldquothree-timersrdquo methodology net di-

versification cannot be recovered from the last three bins of the

analysis interval

The BDMCMC analyses reveal high and maintained specia-

tion rates of crown ruminant lineages throughout the Eocene the

Oligocene and the earliest Miocene (Fig 2D) This high specia-

tion 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 bound-

ary 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 Ex-

tinction 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 in-

terval Gamma distributions best fitted the time of origin of crown

ruminants (offset = 4263 shape = 176 rate = 046 mean =4647 95 highest posterior density (HPD) = 4285ndash5224) pec-

orans (offset = 2696 shape = 168 rate = 057 mean = 2990

95 HPD = 2704ndash3330) and groups with horned forms (offset

= 2649 shape = 202 rate = 196 mean = 2751 95 HPD =2656ndash2906 Fig 2C)

CURVE CORRELATIONS

The results of the 8000 Kendallrsquos correlations are shown in

Figure 3 When the ldquothree-timersrdquo were used to estimate fossil-

based evolutionary rates the speciation rates based on the deepest

treesmdashfrom Cantalapiedrarsquos tree distributionmdashshowed high con-

gruence with the speciation in fossil crown Ruminantia and with

speciation and net diversification in the fossil lineages of the liv-

ing 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 correlationmdashand high positive

tausmdashwith the net-diversification curve of the crown fossil ru-

minants Speciation rates estimated from Bibirsquos trees correlated

positively with speciation in the fossil lineages of the living ru-

minant families This correlation is weaker for the trees whose

deeper nodes are younger

Rates calculated from tree distribution in Cantalapiedra cor-

related positively with speciation and net diversification in the

fossil record of the six living families as estimated by the BDM-

CMC algorithm (Fig 3GndashL) Only rates in Bibirsquos deepest trees



groups withhorned forms

crown pecoranscrown ruminantsfirst fossil horns

times of origin(density)

05

0

A

B

C

D

00

01

02

03

04

05

50 40 30 20 10 0

tree-

base

d sp

ecia

tion


50 40 30 20 10 0

50 40 30 20 10 0


BibiCantalapiedra et al

-025

000

025

050

075

lsquothre

e-tim

ersrsquo

rate

s net-diversificationnet-div living familiesspeciationextinction

-03

00

03

06

Time (Ma)

PyR

ate

rate

s

inception offirst C3 grasslands


permanentEAIS

onset ofmodern glaciations

Bering Strait

ArabianConnection

net-diversificationnet-div living familiesspeciationextinction

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 ldquothree-timersrdquo

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 PyRatersquos 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 rumi-

nants for the younger trees in Bibirsquos dataset

DiscussionPast evolutionary processes left a congruent signal in the fossil

record and the phylogeny of the living ruminants The concor-

dance was stronger when fossil-based rates were estimated from

paleontological data of the living groups only (Figs 2 and 3) We



Figure 3 Congruence of tree-based and fossils-based rates from the ldquothree-timersrdquo method (AndashF) and PyRate (GndashL) Density plots of

P-values (A) P-values from Kendallrsquos correlation tests plotted against the mean age of the 25 older nodes (B) and younger nodes (C)

of each tree Density plots of ldquotausrdquo (τ) (D) ldquotausrdquo Kendallrsquos 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 (GndashL)

In each plot continuous LOESS lines represent results for trees in Cantalapiedra et al (2014b) and dashed lines results for Bibirsquos 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 dif-

ferent phylogenetic datasets and fossil-based methodsmdashldquothree-

timersrdquo and PyRatemdashperformed disparately (Fig 3) This is not

surprising given the nature of the evolutionary processes them-

selves and the particularities and limitations of each of the meth-

ods used in this study to recover the past Despite the many com-

parisons among rate profiles conducted here (ie 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 ru-

minant 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 (ie a

discrete-bin-based approach and a birthndashdeath Bayesian algo-

rithm) portrait disparate evolutionary scenarios for this period

(especially regarding speciation rates green curves in Fig 2B and

D) The ldquothree-timersrdquo approach reconstructed overall low specia-

tion and moderate-to-negative net diversification in the 50ndash24 Ma

temporal span Only one relevant speciation event was estimated

around 40 Ma (Fig 2B) This is a more literal read of the fossil



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 ldquothree-timersrdquo method was used the correlation between tree-

based rates and fossil speciation of the crown ruminants was

strong for most of the trees in the Cantalapiedra dataset and some

of Bibirsquos trees

PyRatersquos 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 phy-

logenetic rates (Fig 3GndashL) The BDMCMC approach places the

highest speciation rates in the Eocene Oligocene and earliest

Miocene (45ndash22 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 low-

est values in this temporal span (Fig 2A) This striking differ-

ence with respect to the ldquothree-timersrdquo 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 esti-

mate of high extinction rates is probably robust toward sampling

Although Alroyrsquos method yielded negative Eocene and

Oligocene diversification rate and subsequent diversity lossmdash

also visible in the raw diversity plot (Fig 1)mdashPyRate 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 ldquoGrand Coupurerdquo

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

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 (27ndash22 Ma Fig 2) Al-

though the two fossil-based approaches show an increase in net-

diversification rates paired with low extinction they differ in

the macroevolutionary context of such major net-diversification

peaks Alroyrsquos method depicts accelerating speciation rates as ru-

minant 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 ldquoadvancedrdquomdash

mostly hornedmdashruminants the pecorans (see Fig 1 and further

discussion below) The major radiation encompassed the appear-

ance 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 phylo-

genetic rates in the last 25 myr of the study interval Correla-

tions showed significant concordance among curves from differ-

ent fossil-based methods and tree distributions when the fossil

record of the living groups was used (Fig 3) Only the youngest

trees from Bibirsquos 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 specia-

tion 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 out-

come First the middle Miocene (17ndash12 Ma) was indeed a period

of relatively low macroevolutionary rates and the younger trees

within Bibirsquos dataset are simply too young to reflect the true trend

Second Bibirsquos 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 combinedmdash

our fossil data include stem forms If true this second scenario



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 lineagesmdashas it

may be the case heremdashthe selection of true crown fossil calibra-

tion points is crucial (Bibi 2013) In this regard new total-evidence

methods (ldquotip-datingrdquo 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 total-

evidence 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 paleocli-

matic evidences the Paleogene-Neogene transition was a period

of profound change in terrestrial ecosystems New available adap-

tive 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 tectonicsmdashfor example ru-

minants 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 evolu-

tionary 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 pro-

cesses in the last 10 million years (Fig 2) The fossil data sug-

gest an increase of extinction from that time onwards and a later

rebound of speciation rates Estimates from the ldquothree-timersrdquo

method and PyRate fit showing neutral-to-negative net diversi-

fication that translated into a late Miocene diversity loss Phylo-

genetic rates remained steady or slightly decreased Overall we

do not recognize a direct resemblance among curves in this tem-

poral point Nevertheless it may be the case that late Miocene

depletion also contributed to the low branching rates recovered

earlier in the trees (15ndash10 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 pre-

vented 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 075

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 25 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 esti-

mates 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 recov-

ered 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 myrmdashonly provided by PyRate see Methodsmdash

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 estab-

lishment of continental northern-hemisphere glaciations Miller

et al 2005) and human activity reshaping mammalian faunas have

been proposed for several mammalian clades (Delson 1985 Kim-

bel 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 neg-

ative net diversificationmdashextinction above speciationmdashas being

behind the slowdowns in living species trees toward the tips often

reported in the literature (Moen and Morlon 2014) This empir-

ical 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 phy-

logenetic trees of extant taxa Most researchers have focused on

estimate evolutionary ratesmdashthat is speciation and extinctionmdash

from phylogenies of living species (Rabosky and Lovette 2008

Alfaro et al 2009 Stadler 2011a) Other studies have pursued



the identification of past episodes in evolutionary trees by com-

parison 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 be-

tween 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 rep-

resentation 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 fossil-

informed 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 (ldquothe lull

before the stormrdquo 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 ldquoMiocene ru-

minant radiationrdquo begun in Oligocene times and prolonged until

22 Ma (Fig 2) This pulse concomitant with the origin of ldquomod-

ernrdquo ruminants (Fig 2BndashD) has been linked to the acquisition

of larger body sizes (Morales et al 1993) new dietary strate-

gies (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 (275 Ma) largely

predates the first fossil evidence of horns in ruminants (19ndash17

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 paleobio-

logical studies (Blondel 2001) This may be also the case for other

groups of land vertebrates with only a reasonable post-Paleogene

ldquophylogenetic coveragerdquo 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 commu-

nitiesrsquo dynamics will largely benefit from fossil data And basal

ruminants probably have a lot to teach us about it

ACKNOWLEDGMENTSWe want to thank A Oslash Mooers F Bibi and J Muller for their insightfulcomments on different versions of the manuscript We also thank P Wag-ner and an anonymous reviewer for their many helpful comments andideas which substantially helped to improve this study I M Sanchezmade valuable observations on basal ruminants We acknowledge tech-nical assistance for using the Cluster Trueno (Spanish Research Coun-cil) from D Basabe A de Castro and H Gascon D Silvestro helpedwith the PyRate workflow This is a contribution by the Palaeoclima-tology Macroecology and Macroevolution of Vertebrates research team(wwwpmmvcomes) of the Complutense University of Madrid as a partof the Research Group UCM 910607 on Evolution of Cenozoic Mammalsand Continental Palaeoenvironments This research was made possible byprojects from the Spanish Ministry of Science and Innovation (CGL2006-01773BTE CGL2010-19116BOS and CGL2011-25754) and from theComplutense University of Madrid (PR106-14470-B) This is Paleobi-ology Database official publication number 240 JLC is currently fundedby the Humboldt Foundation and thus belongs to the ldquoLeyendas Urbanasrdquogroup of the Spanish Ministry of Education

DATA ARCHIVINGThe fossil occurrence dataset is available in the Dryad Digital Repository(httpdxdoiorg105061dryadkp153)

LITERATURE CITEDAlfaro M E F Santini C Brock H Alamillo A Dornburg D L Rabosky

G Carnevale and L J Harmon 2009 Nine exceptional radiations plushigh turnover explain species diversity in jawed vertebrates Proc NatlAcad Sci USA 10613410ndash13414

Alroy J 2008 Dynamics of origination and extinction in the marine fossilrecord Proc Natl Acad Sci USA 10511536ndash11542

mdashmdashmdash 2009 Speciation and extinction in the fossil record of North Americanmammals Pp 301ndash323 in R Butlin J Bridle and D Schluter edsEcology and speciation Cambridge Univ Press Cambridge

mdashmdashmdash 2014 Accurate and precise estimates of origination and extinctionrates Paleobiology 40374ndash397

mdashmdashmdash 2015 Paleobiology database Macquarie University SydneyAvailable at httppaleodborg Accessed July 2014



Benton M J and B C Emerson 2007 How did life become so diverse Thedynamics of diversification according to the fossil record and molecularphylogenetics Palaeontology 5023ndash40

Bibi F 2013 A multi-calibrated mitochondrial phylogeny of extant Bovidae(Artiodactyla Ruminantia) and the importance of the fossil record tosystematics BMC Evol Biol 131ndash15

mdashmdashmdash 2014 Assembling the ruminant tree combining morphologymolecules fossils and extant taxa Zitteliana B 321ndash15

Bibi F M Bukhsianidze A Gentry D Geraads D Kostopoulos and EVrba 2009 The fossil record and evolution of Bovidae state of thefield Palaeontol Electronica 121ndash11

Blondel C 2001 The eocenendasholigocene ungulates from Western Europe andtheir environment Palaeogeogr Palaeoclimatol Palaeoecol 168125ndash139

Bobe R and G G Eck 2001 Responses of African bovids to Plioceneclimatic change Paleobiology 271ndash48

Brashares J T Garland and P Arcese 2000 Phylogenetic analyses of coad-aptation in behavior diet and body size in the African antelope BehavEcol 11452ndash463

Bruch A D Uhl and V Mosbrugger 2007 Miocene climate in Europemdashpatterns and evolution a first synthesis of NECLIME PalaeogeogrPalaeoclimatol Palaeoecol 2531ndash7

Burnham K P and G C Anderson 2002 Model selection and multimodelinference a practical information-theoretic approach Springer-VerlagNew York

Cantalapiedra J L G M Alcalde and M Hernandez Fernandez 2014aThe contribution of phylogenetics to the study of ruminant evolutionaryecology Zitteliana 321ndash6

Cantalapiedra J L R G FitzJohn T S Kuhn M Hernandez Fernandez DDeMiguel B Azanza J Morales and A Oslash Mooers 2014b Dietary in-novations spurred the diversification of ruminants during the CaenozoicProc R Soc B 281

Cantalapiedra J L M Hernandez Fernandez and J Morales 2014c Thebiogeographic history of ruminant faunas determines the phylogeneticstructure of their assemblages at different scales Ecography 371ndash9

Cerling T E J M Harris B J MacFadden M G Leakey J QuadeV Eisenmann and J R Ehleringer 1997 Global vegetation changethrough the MiocenePliocene boundary Nature 389153ndash158

Clauss M and G E Rossner 2014 Old world ruminant morphophysiologylife history and fossil record exploring key innovations of a diversifi-cation sequence Ann Zool Fenn 5180ndash94

Costeur L and S Legendre 2008 Spatial and temporal variation in Euro-pean Neogene large mammals diversity Palaeogeogr PalaeoclimatolPalaeoecol 261127ndash144

Crisp M D and L G Cook 2009 Explosive radiation or cryptic massextinction Interpreting signatures in molecular phylogenies Evolution632257ndash2265

Delson E 1985 Neogene African catarrhine primates climatic influence onevolutionary patterns S Afr J Sci 81273ndash274

DeMiguel D B Azanza and J Morales 2014 Key innovations in ruminantevolution a paleontological perspective Integr Zool 9412ndash433

Domingo M S C Badgley B Azanza D DeMiguel and M Alberdi 2014Diversification of mammals from the Miocene of Spain Paleobiology40196ndash220

Eronen J K Puolamaki L Liu K Lintulaakso J Damuth C Janis andM Fortelius 2010 Precipitation and large herbivorous mammals IIapplication to fossil data Evol Ecol Res 12235ndash248

Etienne R S B Haegeman T Stadler T Aze P N Pearson A Purvis andA B Phillimore 2012 Diversity-dependence brings molecular phy-logenies closer to agreement with the fossil record Proc Biol Sci2791300ndash1309

Ezard T H G T Aze P N Pearson and A Purvis 2011 Interplay be-tween changing climate and speciesrsquo ecology drives macroevolutionarydynamics Science 332349ndash351

Finarelli J A and C Badgley 2010 Diversity dynamics of Miocene mam-mals in relation to the history of tectonism and climate Proc R Soc B2772721ndash2726

Foote M 2000 Origination and extinction components of taxonomic diver-sity general problems Paleobiology 2672ndash102

Fordyce J A 2010 Host shifts and evolutionary radiations of butterfliesProc R Soc B 2773735ndash3743

Fortelius M 2015 Neogene of the Old World database of fossil mammals(NOW) University of Helsinki Finland

Fritz S A J Schnitzler J T Eronen C Hof K Bohning-Gaese and CH Graham 2013 Diversity in time and space wanted dead and aliveTrends Ecol Evol 28509ndash516

Gomez Cano A R J L Cantalapiedra A Mesa A Moreno Bofarull andM Hernandez Fernandez 2013 Global climate changes drive ecologicalspecialization of mammal faunas trends in the Iberian Plio-Pleistocenerodent assemblages BMC Evol Biol 131ndash9

Grimm G W P Kapli B Bomfleur S McLoughlin and S S Renner2015 Using more than the oldest fossils dating Osmundaceae withthree Bayesian clock approaches Syst Biol 64396ndash405

Hammer Oslash and D A T Harper 2006 Paleontological data analysis Black-well Publishing Oxford UK

Harmon L J and S Harrison 2015 Species diversity is dynamic andunbounded at local and continental scales Am Nat 185584ndash593

Harvey P H E C Holmes A Oslash Mooers and S Nee 1994a Inferringevolutionary processes from molecular phylogenies Pp 313ndash333 in

R W Scotland D J Siebert and D M Williams eds Models inphylogeny reconstruction Clarendon Press Oxford UK

Harvey P H R M May and S Nee 1994b Phylogenies without fossilsEvolution 48523ndash529

Hernandez Fernandez M and E S Vrba 2005 A complete estimate of thephylogenetic relationships in Ruminantia a dated species-level supertreeof the extant ruminants Biol Rev 80269ndash302

mdashmdashmdash 2006 Plio-Pleistocene climatic change in the Turkana Basin (EastAfrica) evidence from large mammal faunas J Hum Evol 50595ndash626

Hipsley C A D B Miles and J Muller 2014 Morphological disparityopposes latitudinal diversity gradient in lacertid lizards Biol Lett 101ndash5

Janis C 1982 Evolution of horns in ungulates ecology and paleoecologyBiol Rev Camb Philos Soc 57261ndash317

mdashmdashmdash 1989 A climatic explanation for patterns of evolutionary diversity inungulate mammals Palaeontology 32463ndash481

mdashmdashmdash 2008 An evolutionary history of browsing and grazing ungulates Pp21ndash45 in I J Gordon and H H T Prins eds The ecology of browsingand grazing Springer Berlin

Janis C M J Damuth and J M Theodor 2000 Miocene ungulates andterrestrial primary productivity where have all the browsers gone ProcNatl Acad Sci USA 977899ndash7904

Jetz W G H Thomas J B Joy K Hartmann and A Oslash Mooers 2012 Theglobal diversity of birds in space and time Nature 491444ndash448

Kaiser T M and G E Rossner 2007 Dietary resource partitioning in rumi-nant communities of Miocene wetland and karst palaeoenvironments inSouthern Germany Palaeogeogr Palaeoclimatol Palaeoecol 252424ndash439

Kimbel W H 1995 Hominid speciation and Pliocene climatic change Pp425ndash437 in E S Vrba G H Denton T C Partridge and L H Burckeeds Paleoclimate and evolution with an emphasis on human originsYale Univ Press New Haven



Kohn R M G Schimek and M Smith 2000 Spline and Kernel regressionfor dependent data Pp 135ndash158 in M G Schimekk ed Smoothingand Regression approaches computation and application John Wileyamp Sons Inc New York

Lloyd G T K E Davis D Pisani J E Tarver M Ruta M Sakamoto DW E Hone R Jennings and M J Benton 2008 Dinosaurs and thecretaceous terrestrial revolution Proc Biol Sci 2752483ndash2490

Lyons S K F A Smith and J H Brown 2004 Of mice mastodons andmen human-mediated extinctions on four continents Evol Ecol Res6339ndash358

Maglio V J 1978 Patterns of faunal evolution Pp 603ndash619 in V J Maglioand H B S Cooke eds Evolution of African mammals Harvard UnivPress Cambridge MA

Mannion P D P Upchurch M T Carrano and P M Barrett 2010 Testingthe effect of the rock record on diversity a multidisciplinary approach toelucidating the generic richness of sauropodomorph dinosaurs throughtime Biol Rev 86157ndash181

Maridet O and L Costeur 2010 Diversity trends in Neogene Europeanungulates and rodents large-scale comparisons and perspectives DieNaturwissenschaften 97161ndash172

McGuire J A C C Witt J J V Remsen A Corl D L Rabosky DL Altshuler and R Dudley 2014 Molecular phylogenetics and thediversification of hummingbirds Curr Biol1ndash7

Meredith R W J E Janecka J Gatesy O A Ryder C A Fisher E CTeeling A Goodbla E Eizirik T L L Simao T Stadler et al 2011Impacts of the cretaceous terrestrial revolution and KPg extinction onmammal diversification Science 334521ndash524

Metais G and I Vislobokova 2007 Basal ruminants Pp 189ndash212 in D RProthero and S E Foss eds The evolution of artiodactyls The JohnHopkins Univ Press Baltimore

Miller K G M A Kominz J V Browning J D Wright G S MountainM E Katz P J Sugarman B S Cramer N Christie-Blick and S FPekar 2005 The Phanerozoic record of global sea-level change Science3101293ndash1298

Moen D and H Morlon 2014 Why does diversification slow down TrendsEcol Evol 29190ndash197

Mooers A Oslash and S B Heard 1997 Inferring evolutionary process fromphylogenetic tree shape Quart Rev Biol 7231ndash54

mdashmdashmdash 2002 Using tree shape Syst Biol 51833ndash834Morales J M Pickford and D Soria 1993 Pachyostosis in a Lower Miocene

giraffoid from Spain Lorancameryx pachyostoticus nov gen nov spand its bearing on the evolution of bony appendages in artiodactylsGeobios 26207ndash230

Morlon H 2014 Phylogenetic approaches for studying diversification EcolLett 17508ndash525

Morlon H T L Parsons and J B Plotkin 2011 Reconciling molecular phy-logenies with the fossil record Proc Natl Acad Sci USA 10816327ndash16332

Mosbrugger V T Utescher and D L Dilcher 2005 Cenozoic continen-tal climatic evolution of Central Europe Proc Natl Acad Sci USA10214964ndash14969

Nee S A Oslash Mooers and P H Harvey 1992 Tempo and mode of evolu-tion revealed from molecular phylogenies Proc Natl Acad Sci USA898322ndash8326

Paradis E 2011 Time-dependent speciation and extinction from phylogeniesa least squares approach Evolution 65661ndash672

Quental T B and C R Marshall 2010 Diversity dynamics molecularphylogenies need the fossil record Trends Ecol Evol 25434ndash441

R Development Core team 2015 R a language and environment for statisticalcomputing R Foundation for Statistical Computing Viena Austria

ISBN 3-900051-07-0 Available at httpwwwR-projectorg AccessedJuly 2014

Rabosky D L 2006 LASER a maximum likelihood toolkit for detectingtemporal shifts in diversification rates from molecular phylogenies EvolBioinform 2273ndash260

Rabosky D L and I J Lovette 2008 Explosive evolutionary radiationsdecreasing speciation or increasing extinction through time Evolution621866ndash1875

Ricklefs R E 2007 Estimating diversification rates from phylogenetic in-formation Trends Ecol Evol 22601ndash610

Ronquist F S Klopfstein L Vilhelmsen S Schulmeister D L Murrayand A P Rasnitsyn 2012 A total-evidence approach to dating withfossils applied to the early radiation of the Hymenoptera Syst Biol61973ndash999

Sanchez I V Quiralte J Morales and M Pickford 2010 A new genus oftragulid ruminant from the early Miocene of Kenya Acta PalaeontolPol 55177ndash187

Sanchez I M D DeMiguel V Quiralte and J Morales 2011 The firstknown Asian Hispanomeryx (Mammalia Ruminantia Moschidae) JVertebr Paleontol 311397ndash1403

Silvestro D N Salamin and J Schnitzler 2014a PyRate a new programto estimate speciation and extinction rates from incomplete fossil dataMeth Ecol Evol 51126ndash1131

Silvestro D J Schnitzler L H Liow A Antonelli and N Salamin 2014bBayesian estimation of speciation and extinction from incomplete fossiloccurrence data 63349ndash367

Silvestro D B Cascales-Minana C D Bacon and A Antonelli 2015Revisiting the origin and diversification of vascular plants through acomprehensive Bayesian analysis of the fossil record New Phytol207425ndash436

Simpson C W Kiessling H Mewis R C Baron-Szabo and J Muller2011 Evolutionary diversification of reef corals a comparison of themolecular and fossil records Evolution 653274ndash3284

Smith A B 1988 Patterns of diversification and extinction in early Palaeozoicechinoderms Palaeontology 31799ndash828

Springer M S R W Meredith J Gatesy C A Emerling J Park DL Rabosky T Stadler C Steiner O A Ryder J E Janecka et al2012 Macroevolutionary dynamics and historical biogeography of pri-mate diversification inferred from a species supermatrix PLoS ONE 7e49521

Stadler T 2011a Inferring speciation and extinction processes from extantspecies data Proc Natl Acad Sci USA 10816145ndash16146

mdashmdashmdash 2011b Mammalian phylogeny reveals recent diversification rateshifts Proc Natl Acad Sci USA 1086187ndash6192

Stromberg C A E 2011 Evolution of grasses and grassland ecosystemsAnnu Rev Earth Pl Sc 39517ndash544

Vrba E S 1995 The fossil record of African Antelopes (Mammalia Bovidae)in relation to human evolution and paleoclimate Pp 385ndash324 in E SVrba G H Denton T C Patridge and L H Burcke eds Paleoclimateand evolution with emphasis on human origins Yale Univ Press NewHaven

Wagner P J 1995 Diversification among early Paleozoic gastropodsmdashcontrasting taxonomic and phylogenetic description Paleobiology21410ndash439

Zachos J C G R Dickens and R E Zeebe 2008 An early Cenozoicperspective on greenhouse warming and carbon-cycle dynamics Nature451279ndash283

Associate Editor M FriedmanHandling Editor J Conner



Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisherrsquos website

Figure S1 Quality of the ruminant fossil recordFigure S2 Evolutionary rates from living species phylogenetic trees and the fossil record of the ruminants



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) Be-

sides depicting evolutionary relationships among extant species

dated extant-taxa trees contain valuable information on the pro-

cesses 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) Interest-

ingly 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 com-

paring 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

approachesmdashfossils or extant-taxa trees For instance reason-

able 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 impov-

erished groupsmdashfor example rhinoceros with a 40 myr history

and only six surviving speciesmdashmust 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 con-

trasting 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 be-

hind tree shape beyond the pure fitting of evolutionary models

For instance a given turnover pulsemdashfaunal replacementmdashwith

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 informa-

tion 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 (Quen-

tal 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 extensivemdashover 1200 species

spanning the last 50 myrmdashand reasonably well known (see the

50 40 30 20 10 0

Time before present (Ma)


Hypertragulidae

Leptomerycidae

Blastomerycidae

Dremotheriidae

Moschidae

Gelocidae

Climacoceratidae

Archaeomerycidae

Andegamerycidae

Lophiomerycidae

Hoplitomerycidae

Bachitheriidae

daggerdaggerdaggerdagger

dagger

daggerdaggerdaggerdaggerdagger

dagger

Sp

ecie

s D

ive

rsity

30

20

10

0

s

s

s

Sp

ecie

s D

ive

rsity

0

100

200

300

400 Bovidae

Cervidae

Giraffidae

Antilocapridae

Tragulidae

Palaeomerycidae

Dromomerycidaeothers (below)

daggerdagger

A

B

Figure 1 Ruminants diversity through time Raw species diver-

sity of the 19 ruminant families through time plotted in 1 myr

time bins Families are ordered by species richness (A) Small fami-

lies are plotted in detail in plate (B) dagger extinct clade ϒ 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 phy-

logeny 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 phyloge-

netic hypotheses for the group have been published recently (Bibi

2013 2014) In this study we estimated diversification from two

large distributions of ruminant treesmdashwhich cover a wide array

of node-age configurationsmdashas well as from fossil species oc-

currence data using two different approaches We then tested for

a common signal in the rate-through-time curves from paleonto-

logical and neontological data while assessing which node-age

arrangements improved the fit against the fossil-derived rates































OF LIVING RUMINANTS

































































Fig S1)




















and Badgley 2010)




































































rates

















































in some aspects



















analysis interval






















CURVE CORRELATIONS
























05

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00

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analysis interval






















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of Bibirsquos trees














































































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extinction

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study groups






































































































































































































































































































Documents

Congruent Phylogenetic and Fossils Signa