Journal of Biogeography (J. Biogeogr.) (2010) 37, 305–324
ORIGINAL
ARTICLE
Molecular clocks keep dispersal
hypotheses afloat: evidence for
trans-Atlantic rafting by rodents
Diane L. Rowe1,2*, Katherine A. Dunn3, Ronald M. Adkins4 and
Rodney L. Honeycutt5,2
1
Pengana Place, Blackmans Bay, TAS,
Australia, 2Department of Wildlife & Fisheries
Sciences, Texas A&M University, College
Station, TX, USA, 3Department of Biology,
Dalhousie University, Halifax, NS, Canada,
4
Department of Pediatrics, University of
Tennessee Health Sciences Center, Memphis,
TN and 5Natural Sciences Division,
Pepperdine University, Malibu, CA, USA
ABSTRACT
Aim In order to resolve disputed biogeographical histories of biota with
Gondwanan continental distributions, and to assess the null hypothesis of
vicariance, it is imperative that a robust geological time-frame be established. As
an example, the sudden and coincident appearance of hystricognath rodents
(Rodentia: Hystricognathi) on both the African and South American continents
has been an irreconcilable controversy for evolutionary biologists, presenting
enigmas for both Gondwanan vicariance and Late Eocene dispersal hypotheses. In
an attempt to resolve this discordance, we aim to provide a more robust
phylogenetic hypothesis and improve divergence-date estimates, which are
essential to assessing the null hypothesis of vicariance biogeography.
Location The primary centres of distribution are in Africa and South America.
Methods We implemented parsimony, maximum-likelihood and Bayesian
methods to generate a phylogeny of 37 hystricognath taxa, the most comprehensive taxonomic sampling of this group to date, on the basis of two nuclear
gene regions. To increase phylogenetic resolution at the basal nodes, these data
were combined with previously published data for six additional nuclear gene
regions. Divergence dates were estimated using two relaxed-molecular-clock
methods, Bayesian multidivtime and nonparametric rate smoothing.
Results Our data do not support reciprocal monophyly of African and South
American lineages. Indeed, Old World porcupines (i.e. Hystricomorpha) appear
to be more closely related to New World lineages (i.e. Caviomorpha) than to
other Old World families (i.e. Bathyergidae, Petromuridae and Thryonomyidae).
The divergence between the monophyletic assemblage of South American lineages
and its Old World ancestor was estimated to have occurred c. 50 Ma.
Main conclusions Our phylogenetic hypothesis and divergence-date estimates
are strongly at odds with Gondwanan-vicariance isolating mechanisms. In
contrast, our data suggest that transoceanic dispersal has played a significant role
in governing the contemporary distribution of hystricognath rodents. Molecularclock analyses imply a trans-Tethys dispersal event, broadly confined to the Late
Cretaceous, and trans-Atlantic dispersal within the Early Eocene. Our analyses
also imply that the use of the oldest known South American rodent fossil as a
calibration point has biased molecular-clock inferences.
*Correspondence: Diane L. Rowe, 16 Pengana
Place, Blackmans Bay, TAS 7052, Australia.
E-mail: [email protected]
ª 2009 Blackwell Publishing Ltd
Keywords
Dispersal, fossil, historical biogeography, Hystricognathi, molecular clocks,
phylogenetics, rodents, vicariance.
www.blackwellpublishing.com/jbi
doi:10.1111/j.1365-2699.2009.02190.x
305
D. L. Rowe et al.
INTRODUCTION
Whether vicariance or dispersal mechanisms should be
invoked to account for biogeographically disjunct distributions
of terrestrial biota that are widely separated by oceanic barriers
remains a point of contention (Hunn & Upchurch, 2001; de
Queiroz, 2005). Inferences about the biogeographical history
of the Southern Hemisphere, in particular, continue to
generate intense debate (e.g. Cook & Crisp, 2005; McGlone,
2005; Sparks & Smith, 2005; Gamble et al., 2008). Since the
advancement of plate-tectonic theory in the 1960s, Gondwanan distributions of flora and fauna have been routinely
ascribed to the geological fragmentation (i.e. vicariance) of the
southern continents, supported by concordance of pattern (i.e.
similar area-cladograms) across numerous unrelated taxonomic groups (Nelson & Platnik, 1981; Patterson, 1981; Craw,
1982; Morrone & Crisci, 1995; Sparks & Smith, 2004).
Unfortunately, such pattern-based conclusions, for which
cladogenesis coincides with the geological sequence of continental fragmentation, neglect to address the problem of
diminishing statistical power in inferring concordance as the
number of clades and occupied continents declines. For
instance, the pattern of species cladogenesis has a high
probability of matching the geological sequence of fragmentation by chance alone when only three continents are
occupied. Intuitively, when this is reduced to only two
continents, pattern becomes irrelevant, and an independent
inference of the geological time-frame is essential to assessing
the null hypothesis of vicariance (Lavin et al., 2004). However,
even for groups with such a restricted distribution, vicariance
conclusions are persistently given precedence by a priori
discounting the possibility of shared dispersal avenues, and
lent credence irrespective of the establishment of an independent temporal framework (e.g. Craw et al., 1999; Sparks &
Smith, 2004).
Such presumptions are being challenged with the widespread application of molecular-clock methods for estimating
divergence dates, resulting in a paradigm shift to transoceanic
dispersal as the leading contributor to contemporary biogeographical disjunctions (de Queiroz, 2005; Cowie & Holland,
2006). Problematically, however, molecular-clock estimates
are often dramatically inconsistent, reinforcing scepticism
about the utility and reliability of such methods (Benton,
1999; Smith & Peterson, 2002). Furthermore, because inferences of time may be prone to circularity and bias owing to
an incomplete and/or fragmented fossil record, controversy
persists. Nowhere is this disparity more prominently played
out than across the southern Atlantic, where a number of
unrelated taxonomic groups share a disjunct distribution, on
the continents of Africa and South America (e.g. Vences
et al., 2001; Schrago & Russo, 2003; Danforth et al., 2004).
Discerning whether these distributions are the product of
vicariance or dispersal mechanisms is fraught with difficulties,
as exemplified by the monophyletic rodent suborder Hystricognathi (Hartenberger, 1998; Adkins et al., 2001; Marivaux
et al., 2004).
306
Although rodents are extraordinarily taxonomically diverse
and geographically widespread, representing more than onethird of all extant mammalian lineages and distributed widely
across nearly all continents (Wilson & Reeder, 1993), the oldest
undisputed fossil representative is only 55 Myr old (Hartenberger, 1998). However, a Gondwanan vicariance explanation
requires that lineage divergences must pre-date the geological
opening of the Atlantic Ocean, c. 100 Ma (Parrish, 1993).
Thus, for many, attributing the distribution of a derived
suborder of rodents (i.e. Hystricognathi) to Gondwanan
geological events seems a remote and unrealistic extrapolation,
particularly given that the oldest fossils attributable to any
modern Eutherian mammalian order are only around 65 Myr
old (McKenna & Bell, 1997). However, early molecular-clock
estimates upheld this notion, suggesting that the order
Rodentia, and more specifically the suborder Hystricognathi,
may have been derived over 100 Ma (Kumar & Hedges, 1998).
Not surprisingly, inferences about the process by which
reciprocally monophyletic groups of hystricognath rodents
came to occupy Africa and South America became the subject
of intense debate, presenting enigmas to both Gondwanan
vicariance and dispersal hypotheses (Lavocat, 1969; Patterson
& Wood, 1982; George, 1993a,b; Craw et al., 1999; Huchon &
Douzery, 2001; Marivaux et al., 2002; Martin, 2005).
It is widely accepted that the contemporary distributions of
a few Hystricognathi species in Southeast Asia and North
America are attributable to overland dispersal following
continental re-connections during the Miocene and Pliocene,
respectively (Jaeger, 1988; Janis, 1993; Flynn & Wyss, 1998).
However, prior to the Miocene, identifiable hystricognath
lineages are known only from the African and South American
continents, being notably absent from fossiliferous beds
elsewhere in the world (George, 1993a; McKenna & Bell,
1997; Hartenberger, 1998; Marivaux et al., 2004). Interestingly,
the first unambiguous lineages assigned to the group are not
observed in the fossil record until the Late Eocene, emerging
nearly simultaneously on both continents (c. 35 Ma; Wyss
et al., 1993; McKenna & Bell, 1997). If, by default, a vicariance
explanation is invoked then we are forced to contend with a
conspicuous absence of lineages in the fossil record during the
60-Myr interim between the opening of the Atlantic Ocean and
the Eocene debut of hystricognath lineages. Alternatively, given
that the null hypothesis of vicariance cannot be rejected on the
basis of pattern alone, owing to a restricted two-continent
distribution, a temporal inference would intuitively take
precedence. In this instance, a strict interpretation of the fossil
record indicates a Late Eocene time-frame, requiring oceanic
dispersal of more than 1700 km (Janis, 1993; Holroyd & Maas,
1994) by a terrestrial organism (Lavocat, 1969). However,
fossils themselves generally serve only as indicators of the
minimum ages of lineages (Smith & Peterson, 2002; Renner,
2005), with uncertainty in the case of hystricognath rodents
compounded by known gaps of 10–15 Myr in the terrestrial
fossil record immediately preceding the appearance of rodents
in both Africa and South America (Flynn & Wyss, 1998; Flynn
et al., 2002; Jaeger, 2003).
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
Trans-Atlantic dispersal of rodents
In an attempt to resolve this discordance, molecular-clock
methods (Welch & Bromham, 2005) have been applied as a
means of ascertaining a more robust temporal framework.
However, age estimates for lineage separation between the two
continents have varied widely, from 37 to 85 Ma (see Table 1).
Such inconsistencies have persisted despite the development of
numerous and increasingly sophisticated methods of dealing
with the inherent complexities of molecular-clock dating
(Rodrı́guez-Trelles et al., 2002; Bromham & Penny, 2003;
Bromham & Woolfit, 2004; Near & Sanderson, 2004; Rutschmann, 2006). In addition, alternative phylogenetic hypotheses,
based on molecular data, have brought into question the
validity of reciprocal monophyly of the clades occupying the
two continents, Africa and South America, and are further
suggestive of the possibility of an ancestral presence in Asia
(e.g. Adkins et al., 2001; Huchon & Douzery, 2001). Such
alternative phylogenetic hypotheses can modify area-cladograms to a three-continent distribution, and, consequently,
impact on the plausibility of vicariance based on pattern.
Therefore, at present, phylogenetic and temporal uncertainty
prohibit sound inference of the biogeographical history of
hystricognath rodents.
To better understand the mechanism by which hystricognath rodents first came to occupy South America, we enhance
both the resolution of phylogenetic relationships and the
Table 1 Estimates for the timing of separation of African and South American hystricognath rodent lineages derived from
molecular-clock methods (NPRS indicates
nonparametric rate-smoothing methods) and
utilizing various gene regions (‘nuc’ indicates
nuclear gene regions and ‘mt’ refers to
mitochondrial gene regions).
Age (Ma)
Data
reliability of molecular-clock estimates for lineages within the
suborder Hystricognathi. In particular, we focus on minimizing the impact of two implicated sources of error: insufficient
taxonomic sampling and fossil calibration-point limitations
(Bromham et al., 2000; Conroy & van Tuinen, 2003; Graur &
Martin, 2004; Near & Sanderson, 2004; Linder et al., 2005). In
addition, we address potential problems associated with the
seemingly routine incorporation of the geological age of the
oldest known South American rodent fossil as a calibrating
point for inferring the timing of their initial occupation of the
South American continent.
MATERIALS AND METHODS
Phylogenetic framework
Taxon sampling and DNA sequences
Throughout this manuscript, we make reference to three
reciprocally monophyletic crown-clades, as recognized by
Wood (1965; see George, 1993a). These include the New
World Caviomorpha, the Old World porcupines (i.e.
Hystricomorpha), and a strictly African clade composed of
Bathyergomorpha and Phiomorpha (herein designated
Bathy–Phiomorpha). Taxonomic sampling was inclusive of
Method
African and South American lineage split
37 (34–40)
1 nuc, 1 mt
Bayesian
38 (16–54)
2 nuc
NPRS
38 (34–42)
19 nuc, 3 mt
Bayesian
(Murphy et al., 2001b)
43–54
1 nuc
Local clocks
45 (41–49)
3 nuc
Bayesian
(Huchon et al., 2002)
55 (42–69)
2 nuc
Bayesian
58–66
1 nuc (TTR)
NPRS
85 (71–85)
12 mt
Rate correct
South American (Caviomorpha) radiation
31.5–37
Oldest fossil
Radiometric
22–57
3 nuc
Local clocks
(Huchon et al., 2002)
28–51
1 nuc
Linearized
32 (29–35)
1 nuc
Bayesian
34 (32–36)
1 nuc, 1 mt
Bayesian
34.5 (33–36) 12 nuc, 1 mt
Bayesian
(Murphy et al., 2001a)
37
2 mt
Local clocks
37 (33–41)
3 nuc
Bayesian
(Huchon et al., 2002)
40–46
1 nuc
(TTR) NPRS
45 (35–53)
2 nuc
Bayesian
SA-cavy
Reference
Yes; 37 Ma
No
No
Opazo, 2005
Adkins et al., 2003
Springer et al., 2003;
Yes; 31 Ma
No
Huchon & Douzery, 2001
Poux et al., 2006;
No
No
No
This study
This study
Mouchaty et al., 2001
32 Ma
Yes; 31 Ma
Wyss et al., 1993
Douzery et al., 2003;
Yes;
Yes;
Yes;
Yes;
Huchon et al., 2000
Galewski et al., 2005
Opazo, 2005
Hasegawa et al., 2003;
31
32
37
37
Ma
Ma
Ma
Ma
No
No
Montgelard et al., 2002
Poux et al., 2006;
No
No
This study
This study
The age of the oldest known rodent fossil in South America is provided for comparison, and
molecular studies utilizing this fossil as a calibration point (and its estimated geological age) are
indicated in the column ‘SA-cavy’.
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
307
D. L. Rowe et al.
all 16 extant families of Hystricognathi (Wilson & Reeder,
1993; Honeycutt et al., 2007). All seven genera of Bathy–
Phiomorpha and one of the three extant genera of the family
Hystricidae (Hystricomorpha) represented the Old World
lineages. Twenty-nine of the 47 extant New World genera were
included, representative of the four Caviomorpha superfamilies. Within the species-rich group Caviomorpha, taxon
sampling was designed to include lineages encompassing the
diversity and breadth of body sizes and life-history traits, as
these attributes appear to be correlated with rates of molecular
evolution (Rowe & Honeycutt, 2002), and ultimately influence
the utility of molecular-clock methods. Two outgroup taxa,
Ctenodactylus and Pedetes, were incorporated for all phylogenetic analyses, with the former being the probable sister-group
to Hystricognathi (Bugge, 1985; Adkins et al., 2001; Huchon
et al., 2002; Marivaux et al., 2002; Veniaminova et al., 2007).
Two nuclear gene regions, intron 1 of the transthyretin gene
(TTR, 1264 bp) and exon 10 of the growth hormone receptor
gene (GHR, 831 bp) were sequenced for use in phylogenetic
analyses of the 39 sampled taxa. In addition, our data from
TTR and GHR were combined with previously published
nuclear sequence data of taxonomic subsets held in common,
and combined phylogenetic analyses were performed. These
subsets included: (1) an analysis of 25 taxa for TTR, GHR and
von Willebrand factor (vWF, 1263 bp; Huchon & Douzery,
2001); and (2) an analysis of eight taxa for TTR, GHR and
vWF, plus five nuclear genes (PNOC, RAG1, TYR, CREM,
PLCB4) reported by Murphy et al. (2001a). GenBank accession
numbers for sequences are listed in Table 2.
Phylogenetic inference
Sequences were aligned using ClustalX (Thompson et al.,
1997) and modified to conform to amino acid sequence in the
case of GHR, vWF, PNOC, RAG1 and TYR. Genes were
analysed separately and in combination, following partitionhomogeneity tests for combinability (PHT; Farris et al., 1995)
using paup* (version 4.0b10; Swofford, 2002). Maximum
parsimony (MP) and maximum likelihood (ML) analyses were
also performed using paup*. MP analyses employed equal
weighting and heuristic searches with 10 random additions of
tree bisection–reconnection (TBR) branch-swapping. Prior to
ML analyses, the program Modeltest (version 3.0, Posada &
Crandall, 1998) and hierarchical Akaike information criteria
(AIC) were used to select the most appropriate model of
molecular evolution. All ML analyses employed heuristic
searches with 10 random additions of TBR branch-swapping.
Support for nodes in resultant phylogenies derived from both
MP and ML analyses were determined using bootstrap analyses
and the same heuristic search options.
Phylogenetic analyses of the two-gene (i.e. TTR and GHR)
and eight-gene (i.e. TTR, GHR, vWF, PNOC, RAG1, TYR,
CREM and PLCB4) combinations were conducted using a
partitioned mixed-model Bayesian analysis with posterior
probabilities estimated using a Markov chain Monte Carlo
(MCMC) procedure. The optimal model of sequence evolution
308
for each partition was determined using Modeltest (version
3.0, Posada & Crandall, 1998) and the model substitution
parameters estimated using the program MrBayes (version
3.1; Ronquist & Huelsenbeck, 2003). Starting from random
trees, four chains were run simultaneously in each analysis,
over 5 · 106 generations. To check for consistency, the runs
were repeated with 1 · 106 generations. A consensus of postburn-in trees, determined empirically from likelihood values,
sampled every 100 generations was created for each dataset.
One-tailed Kishino–Hasegawa tests (KH-tests; Kishino &
Hasegawa, 1989) were implemented to assess a priori taxonomic hypotheses, reflecting the uncertain relationships of Old
World and New World porcupines (Hystricidae and Erethizontidae, respectively; Wood, 1965; Bugge, 1985; Lavocat &
Parent, 1985; Woods & Hermanson, 1985).
Divergence-date estimates
Detecting among-lineage rate heterogeneity
Prior to estimating divergence times from relaxed-molecularclock methodologies, two approaches were used to assess rate
homogeneity among taxa. First, adherence to a strict molecular
clock was investigated by comparing ML-derived log-likelihood values, using a GTR+C (general time-reversible nucleotide substitutions with a gamma distribution for rate
heterogeneity across sites) model of evolution, for a given tree
topology with and without enforcement of a molecular clock.
A likelihood ratio test was used to verify the validity of the
molecular-clock hypothesis (Tajima, 1993; P < 0.05). In the
event of significant rate heterogeneity, two different relaxedmolecular-clock methods were implemented to infer divergence dates.
The pattern of rate heterogeneity was subsequently examined by implementing the Lintre program (Takezaki et al.,
1995). Use of both the branch-length test and the two-cluster
test allowed identification of both lineages and clades undergoing rates of evolution significantly different from the
average. Tamura–Nei distances were used, as the GTR model
was unavailable for this analysis. Assessment of rate patterns
allowed us to optimize the implementation of fossil calibration
points across lineages experiencing a variety of rates of
evolution.
Calibration point designation
Ideally, fossil calibration points should be applied broadly
across the phylogeny to reduce the magnification of error
associated with extrapolating to nodes increasingly distant
from the calibration points (Nei et al., 2001; Linder et al.,
2005). As such, fossils were targeted to span the phylogenetic
breadth and depth of hystricognath rodents (see Tables 2
and 3). To minimise unforeseen errors associated with amonglineage rate heterogeneity, calibration points were chosen to
incorporate the potential range of evolutionary-rate classes
through inclusion of fossil representatives from five different
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
Trans-Atlantic dispersal of rodents
Table 2 GenBank accession numbers of the hystricognath rodent taxa and nuclear gene regions (GHR, TTR, vWF, PNOC, RAG1, TYR,
CREM and PLCB4) included in this study.
Species
Outgroups
Pedetidae
Pedetes capensis
Ctenodactylidae
Ctenodactylus gundi (vali*)
Bathy–Phiomorpha
Bathyergidae
Bathyergus suillus
Cryptomys hottentottus
Georychus capensis
Heliophobius argenteocinereus
Heterocephalus glaber
Petromuridae
Petromus typicus
Thryonomyidae
Thryonomys swinderianus
Hystricomorpha
Hystricidae
Hystrix africaeaustralis
Atherurus macroura*
Caviomorpha
Cavioidea
Agoutidae
Agouti taczanowski (paca*)
Caviidae
Cavia tschudii (porcellus*)
Dolichotis patagonum
Galea musteloides
Kerodon rupestris
Microcavia australis
Dasyproctidae
Dasyprocta aguti
Myoprocta acouchi
Hydrochaeridae
Hydrochaeris hydrochaeris
Chinchilloidea
Chinchillidae
Chinchilla laniger
Lagidium viscacia
Lagostomus maximus
Dinomyidae
Dinomys branickii
Erethizontoidea
Erethizontidae
Coendou bicolour
Erethizon dorsatum
Sphiggurus mexicanus (melanurus*)
Octodontoidea
Abrocomidae
Abrocoma bennetti
Capromyidae
Capromys piliroides
Ctenomyidae
Ctenomys boliviensis (maulinus*)
Echimyidae
Echimys chrysurus
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
GHR
TTR
vWF
AF332025/H551
FJ865447/H551
AJ238389
AF332042/H2202
FJ865448/H2202
AJ238387*
FJ855201/BS
FJ855202/H688
FJ855203/GPPH3
FJ855204/H066
AF332034/unk
AF159321/BS
AF159314/CHH1
AF159319/GPPH3
AF159323/H066
AF159324/H004
AJ238384
AJ251132
AJ251133
AJ251134
FJ855205/H550
AF159313/H550
AJ251144
AF332035/unk
AF159312/H571
AJ224674
AF332033/unk
AF159311/SP7702
AJ251131*
AF433929/H6192
AF433882/H6192
AJ251136*
FJ855206/H5601
AF433939/H6193
AF433933/AK13818
AF433938/H5835
AF433937/AK13309
FJ865449/H5601
AF433893/H6193
AF433886/AK13818
AF433892/H5835
AF433889/AK13309
AJ224664*
FJ855207/NZG6227
AF433945/H5837
FJ865450/NZG6227
AF433899/H5837
U31607
FJ855208/NK13155
FJ865451/NK13155
AJ251137
AF520660/NK13161
FJ855209/NK14538
FJ855210/UF571
FJ865452/HZG
FJ865453/NK14538
FJ865454/UF569
AJ238385
AF520659/K8
FJ865455/K8
AJ251145
AF520663/K5
FJ855211/H5828
FJ855212/H5830
FJ865456/K5
FJ865457/H5828
FJ865458/H5830
AJ251135
AJ224664*
FJ855213/H5613
FJ865459/H5613
AJ251143
AF433949/H575
AF433903/H575
AJ251142
FJ855214/NK15277
FJ865460/NK15277
AJ251138*
FJ855215/LMP27
FJ865461/LMP27
AJ251141
309
D. L. Rowe et al.
Table 2 Continued
Species
GHR
TTR
vWF
Isothrix bistriata
Proechimys longicaudatus (oris*)
Myocastoridae
Myocastor coypus
Octodontidae
Aconaemys fuscus
Octodon lunatus
Octodontomys gliroides
Octomys mimax
Spalacopus cyanus
Tympanoctomys barrerae
Data from Murphy et al. (2001a)
Species
Pedetes capensis
Heterocephalus glaber
Hystrix (brachyura*)
Cavia tschudii
Hydrochaeris hydrochaeris
Dinomys branickii
Erethizon dorsatum
Myocastor coypus
FJ855216/M1273
FJ855217/NK15758
FJ865462/M1273
FJ865463/NK15758
AJ849308
AJ251139*
AF520662/H584
AF520669/H584
AJ251140
AF520657/K38
AF520650/H4463
AF520649/AK15686
AF520665/AK13474
AF520653/H5626
AF520655/AK13811
FJ865464/H4468
FJ865465/H4463
FJ865466/AK15686
FJ865467/AK13474
FJ865468/H5626
FJ865469/AK13811
PNOC
AY011824
AY011830
AY011827*
AY011831
AY011832
AY011834
AY011828
AY011833
RAG1
AY011882
AY011889
AY011886*
AY011890
AY011891
AY011893
AY011887
AY011892
TYR
AY012000
AY012005
AY012003*
AY012006
AY012007
AY012009
AY012004
AY012008
AJ238386
CREM
AY011642
AY011649
AY011646*
AY011650
AY011651
AY011653
AY011647
AY011652
PLCB4
AY011765
AY011772
AY011769*
AY011773
AY011774
AY011776
AY011770
AY011775
Numbers in bold identify the GHR and TTR sequences generated in this study, with accession numbers followed by specimen identification numbers
(GenBank accession number/species identification number). Unknown specimens are labelled ‘unk’. An asterisk (*) is indicative of the concatenation of sequence information from congeneric species, when identical species were not available. Specimens are listed in accordance with taxonomy, with the outgroup taxa and members of Hystricomorpha ranging from Africa to Southeast Asia, the Bathy–Phiomorpha being restricted to
Africa, and Caviomorpha occurring primarily within South and Central America.
families that encompass various life-history attributes (Wilson
& Reeder, 1993; Rambaut & Bromham, 1998; Rowe &
Honeycutt, 2002; Dobson & Oli, 2007). In effect, we employed
only calibration points that collectively fitted the criteria of
falling within the group of interest (i.e. Hystricognathi),
spanning the range from recent to more basal nodes, and
representing both slow and rapid rate classes (i.e. the range of
observed rates of molecular evolution).
Bayesian
MULTIDIVTIME
estimations
multidivtime (Thorne & Kishino, 2002), a Bayesian methodology that incorporates a probabilistic model to describe
changes in rates of molecular evolution through time, was
selected because it allows for the simultaneous use of multiple
calibration points, can accommodate multiple genes or data
partitions with different evolutionary characteristics, and
provides credibility intervals for estimated divergence times
(Rodrı́guez-Trelles et al., 2002; Thorne & Kishino, 2002).
Because fossils are not considered to be precise representations
of a true lineage and their ages are not known without error,
the use of lower and upper bounds to constrain node ages,
rather than the definition of fixed ages, provides a more
realistic approach. When employed as lower bounds, fossils
were used to establish a minimum age for the node immedi310
ately prior to the clade within which they exhibit synapomorphies (Smith & Peterson, 2002; Renner, 2005).
An upper bound (i.e. maximum age) for multidivtime
analyses was most reliably designated at the node associated
with the diversification of caviomorph lineages (i.e. Caviomorpha), given the more widespread geographical distribution
and comparative abundance of fossil information (i.e. both
presence and absence of fossils) available from South America.
Designation of an upper bound for the root node (Hystricognathi–Ctenodactylidae) would have been ideal, but was
prohibitive in terms of the potential for misleading conclusions. Given the current limitations of the palaeontological
record, particularly the rarity of Late Cretaceous–Palaeocene
fossil records outside Laurasia (Savage & Russell, 1983;
Novacek, 1992; Lucas, 2001; Smith et al., 2001; Jaeger, 2003;
Marivaux et al., 2004), a reliable age estimate for this node
could not be established. In particular, there is a lack of
substantial information from the Late Cretaceous–Palaeocene
of Southeast Asia and Africa, the probable areas of origin for
ancestral ctenodactyloid and hystricognath lineages, respectively (Hartenberger, 1998; Marivaux et al., 2002; Jaeger, 2003;
Seiffert, 2006).
The combined dataset, with independently modelled gene
partitions (TTR-all + GHR-all), was used to estimate divergence times. For comparison, the GHR gene region was further
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
Trans-Atlantic dispersal of rodents
partitioned into individual codons (GHR-123), and TTR was
reanalysed after removing gaps from the dataset (TTR-gap). In
all instances, model parameters were estimated using an F84+C
model of evolution (the most complex model available in the
program) on a defined tree topology that was derived from
the combined ML analysis of the TTR and GHR data
(TTR + GHR). Model parameters were estimated using the
program baseml (paml v.3.14; Yang, 1997). These parameters
were then used to estimate the branch lengths in the rooted
evolutionary tree, in conjunction with a variance–covariance
matrix of the branch lengths estimated using the program
estbranches (Thorne et al., 1998). After pruning the outgroup (Pedetes), the program multidivtime (Thorne &
Kishino, 2002) was used to approximate the posterior distribution of substitution rates and divergence times. An MCMC
analysis was run for 100 million generations and sampled
every 100 generations after the initial burn-in period of 50,000
cycles. To ensure convergence, multiple chains of the MCMC
analyses were performed. Priors specified included an upper
bound for the origination of Caviomorpha (55 or 90 Ma) and
lower bounds as indicated in Table 3. Other prior distribution
settings included: 0.70 (70 Ma) for rttn (mean of the distribution for the time separating the in-group root from the
present), 0.35 (35 Ma) for rttnsd (the standard deviation), 0.15
for rtrate (mean distribution for the rate of molecular
evolution at the in-group root node), 0.075 for rtratesd (the
standard deviation), 0.75 for Brownmean (Brownian motion
parameter v, determining the permitted rate change between
ancestral and descendant nodes), and 1.5 (150 Ma) for bigtime
(the largest value of time between the root and the tips).
Nonparametric rate-smoothing estimations
The nonparametric rate-smoothing (NPRS) method was
utilized primarily to allow direct comparison with previously
published studies. This approach, like Bayesian methods, does
not assume globally or locally constant rates of molecular
evolution, but uses a stochastic method to optimize rate
changes across all lineages (Sanderson, 1997). It is based on the
assumption that rates are auto-correlated and attempts to
maximize covariance of rates over the entire tree according to
an optimal least-squares smoothing criterion.
Analyses based on the NPRS method used fixed fossilcalibration points, independently assigned to particular nodes,
in order to estimate absolute ages for all other nodes on the
phylogeny. Given the greater uncertainty in placing the most
primitive hystricognath lineages in the context of a molecular
phylogeny of extant taxa, we applied the more derived
Hydrochaeridae and Octodontidae as fixed calibration points
(F1 and F2, respectively, in Table 3). In addition, the oldest
South American rodent fossil (‘dasyproctid indet.’; F3 in
Table 3) was assigned to a more derived node, in contrast to
previous molecular studies, but in accordance with palaeontological identification as a dasyproctid (Wyss et al., 1993, 1994).
No constraints were directly placed on the node associated with
the colonization of South America. However, in all instances,
Table 3 Relevant palaeontological information and life-history traits of African and South American hystricognath rodents are summarized
for the calibration points implemented in the molecular-clock analyses.
Calibration point designations
Family
Hydrochaeridae
Octodontidae
Capromyidae
Chinchillidae
Thryonomyidae
Designations
F1, L1
F2, L2
L3
L4
L5
Chasicomys/
Palaeoctodon
11
Zazamys
Gaudeamus
19
Eoviscaccia/
chinchillid
30
34
‘dasyproctid
indet.’
31
60–300
2–10
77–109
1.5–6
7
4, 5, 8, 13
500–8500
1–6
110–140
10
11
11, 13
500–4500
1–6
111–166
5–12
20
2–5, 7, 8, 13
4000–9000
1–2
137–172
12
4
1, 4, 10, 12, 13
600–4000
1–2
99–120
8–12
17
2, 3, 8, 9, 13
Palaeontological information
Genera
Prodolichotis/
Procardiatherium
Fossil age (Ma)
16
Life-history traits
Body size (g)
40,000–70,000
Litter size
2–8
Gestation (d)
149–156
Maturity (mo)
15
Longevity (yr)
12
References
3, 4, 5, 11, 13
Dasyproctidae
F3
References: 1, Lavocat (1973); 2, Wyss et al. (1993); 3, Flynn & Swisher (1995); 4, McKenna & Bell (1997); 5, Walton (1997); 6, Hartenberger (1998);
7, Kay et al. (1999); 8, Vucetich et al. (1999); 9, Flynn et al. (2002); 10, Antoñanzas et al. (2004); 11, MacPhee (2005); 12, Seiffert (2006); 13, Wilson
& Reeder (1993)
Calibration points are referred to by familial alignment and are additionally designated numbers (F1–F3, L1–L5) for assignment to specific
phylogenetic nodes. A calibration point designation beginning with the letter F signifies use as a fixed point, whereas an L signifies use as a lower
bound (minimum age). The oldest named genera representing the families are listed, along with geological age estimates of the fossil beds
from which they were derived. For the life-history traits, age at maturity reflects documented ages for first reproduction by females, and longevity is
the maximum number of years documented in captivity.
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311
D. L. Rowe et al.
the date of the basal Hystricognathi divergence was constrained
to lie between 34 Ma (i.e. the oldest hystricognath rodent fossil)
and 110 Ma (i.e. accounting for hiatuses in the fossil records of
both Africa and South America, and in accordance with previous
molecular studies of mammalian diversification; Kumar &
Hedges, 1998; Penny et al., 1999). These ages were broadly
defined in order to increase the likelihood of including the true
age of that node. Independent divergence-date estimates were
obtained for the TTR and GHR datasets.
Using the designated calibration points in conjunction with
estimates of branch lengths, absolute ages for nodes could be
inferred. To estimate branch lengths, the tree topology was first
constrained to match that of the ML analysis of the concatenated TTR + GHR dataset. The appropriate model of
molecular evolution previously designated for each independent dataset (i.e. TTR and GHR) was then used to obtain ML
branch-length estimates, as implemented in paup* (Swofford,
2002). Branch lengths were scaled by a factor of 1000 to convert
fractional numbers to whole numbers, as done by Adkins et al.
(2003). To determine branch lengths near the base of the tree
more accurately, an additional non-hystricognath rodent
(Pedetes) was used to root the tree. For the estimation of
divergence dates, Pedetes was pruned from the rooted tree. This
allowed determination of the length of branches on each side of
the root (i.e. Hystricognathi and the Ctenodactylidae outgroup) of the phylogeny. Divergence times were then estimated
using the NPRS methodology, as implemented in the program
r8s (version 1.60 for Unix; Sanderson, 1997, 2003).
RESULTS
Phylogenetic relationships
There were minor topological differences observed between the
independent TTR and GHR phylogenetic estimations, particularly concerning the placement of Abrocoma, Capromys and
Figure 1 Summary of the phylogenetic relationships among African and South American hystricognath rodent lineages, with taxonomic
designations and general distributions as outlined in Table 2. (a) Phylogenetic topology derived from the two-gene (TTR + GHR) dataset,
consistent with maximum parsimony (MP), maximum-likelihood (ML) and Bayesian reconstruction methods. Bootstrap values are indicated above the branches subtending nodes, with ML preceded by MP values (i.e. MP/ML). Posterior probabilities are given below the
branches. In all instances, an asterisk (*) indicates a bootstrap or posterior value of 100% or 1.00, respectively. An ‘X’ signifies bootstrap
support of less than 50%. (b) Maximum-likelihood phylogram derived from the eight-gene dataset, inclusive of a reduced number of
representative taxa. The MP and Bayesian phylogenies are identical to this topology. MP and ML (i.e. MP/ML) bootstrap support values are
given above the nodes, and the Bayesian posterior probabilities are displayed below the branches.
312
Journal of Biogeography 37, 305–324
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Trans-Atlantic dispersal of rodents
Agouti, and genera within the family Batheyergidae (data not
shown). However, when the two datasets were combined (i.e.
TTR + GHR), the inconsistencies were resolved, and all
associated nodes received strong bootstrap support and
posterior probabilities (see Fig. 1). There was strong support
for the placement of two taxonomically problematic genera,
with Dinomys aligning with the superfamily Chinchilloidea and
Abrocoma within Octodontoidea (Woods & Hermanson, 1985;
Martin, 1994; McKenna & Bell, 1997; Köhler et al., 2000). All
data unequivocally supported monophyly of the South American Caviomorpha and its component superfamilial groupings
(Cavioidea, Chinchilloidea, Erethizontoidea and Octodontoidea), consistent with previous studies (e.g. Vucetich et al.,
1999; Huchon & Douzery, 2001). However, the placement of
New World porcupines (Erethizontoidea) within the Caviomorpha remained problematic (Bugge, 1985; Woods &
Hermanson, 1985; Huchon & Douzery, 2001). Placement
varied with both taxonomic and character sampling and the
method of phylogenetic reconstruction (data not shown).
Although most analyses suggested a sister-group relationship
between the superfamilies Cavioidea and Erethizontoidea, the
node was considered unresolved in all subsequent analyses.
This study provides the strongest support to date for the
relationship among the three reciprocally monophyletic
crown-group clades of hystricognath rodents, Bathy–Phiomorpha (Wood, 1965; see George, 1993a), Hystricomorpha
(sensu Wood, 1965) and Caviomorpha (sensu Wood, 1955;
Lavocat, 1973). Overwhelmingly, the data are consistent with a
basal placement for the strictly African lineages of Bathy–
Phiomorpha, outside the sister-group association between the
South American Caviomorpha and the Old World Hystricomorpha (Asian and African porcupines). In contrast to
previous studies, we rejected both a monophyletic assemblage
of all Old World lineages (Bathy–Phiomorpha + Hystricomorpha; e.g. Lavocat, 1973; Jaeger, 1988; Murphy et al.,
2001b) and a basal placement for Hystricomorpha (e.g. Adkins
et al., 2001, 2003; Eizirik et al., 2001; Huchon & Douzery,
2001; Douzery et al., 2003; Huchon et al., 2007). Monophyly
of the Old World hystricognath lineages was rejected using
both the three-gene (TTR + GHR + vWF) and the eight-gene
dataset (KH-tests, P < 0.05). Likewise, a basal placement for
the Hystricomorpha, with a sister-group relationship between
the African (Bathy–Phiomorpha) and South American (Caviomorpha) clades, was rejected using the eight-gene dataset
(P < 0.05).
Rate heterogeneity
Relative-rate tests (RRT; Tamura-Nei+C model, a = 3.2),
including branch-length and two-cluster tests (Lintre; Takezaki et al., 1995), indicated a substantial amount of rate
heterogeneity among lineages and clades for both the TTR and
the GHR datasets. Over one-third of all terminal taxa for TTR
and more than three-quarters of taxa for GHR were evolving at
rates significantly different from the average rate (P < 0.05;
data not shown). Nearly half of all nodes had descendant
Journal of Biogeography 37, 305–324
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lineages identified as deviating from rate homogeneity
(P < 0.05), for both the TTR and the GHR dataset.
Divergence-date estimates
Representative node ages, estimated using the multidivtime
and r8s programs, are summarized in Table 4. Dates derived
from the two different methodologies are generally consistent.
Divergence times estimated using multidivtime and their 95%
confidence intervals, derived from five lower-bound calibration
points and an upper bound of 55 Ma, are depicted by the
phylogram in Fig. 2. The Bayesian prior date assumption, when
increased from 55 to 90 Ma for the initial diversification
of Caviomorpha (node 70), resulted in a roughly 2–7 Myr
increase (c. 15%) in node ages across the phylogeny (Table 4).
Our phylogenetic and temporal framework implicates a
trans-Tethyan dispersal event of the Hystricognathi ancestor
from Asia to Africa, occurring in the interim between the
ancestral hystricognath splitting from the ctenodactyloid
ancestor and the onset of hystricognath lineage diversification
within Africa (i.e. between nodes 73 and 72, Fig. 2 and Table 4),
between c. 92 and 59 Ma. Our estimated Palaeocene divergence
of the ancestral Hystricomorpha from the Bathy–Phiomorpha
(c. 59 Ma; node 72 in Fig. 2 and Table 4), within Africa, is
closely followed by the derivation of the ancestor to Caviomorpha near the Palaeocene–Eocene boundary (c. 55 Ma; node 71).
Diversification of Caviomorpha lineages within South America
appears to have commenced by c. 45 Ma (node 70). This places
their African ancestor well before the Late Eocene–Early
Oligocene appearance in the fossil record (c. 34 Ma; McKenna
& Bell, 1997), but long after the rifting of Africa from South
America (c. 100 Ma; Parrish, 1993). The interim between the
divergence from an African ancestor and the descendant
radiation of the South American crown-group implies an Early
Eocene trans-Atlantic dispersal event (c. 45–55 Ma). The
subsequent diversification of Caviomorpha lineages on the
South American continent is estimated to have commenced
roughly 10–20 Myr prior to their first appearance in the fossil
record, preceding estimates derived from the majority of
molecular studies by c. 20 Myr (see Table 1). Extension of the
Bayesian age prior (e.g. upper bound) at this node (i.e. node 70)
to 90 Ma, allowing for the possibility of Gondwanan isolating
mechanisms, resulted in a Palaeocene–Early Eocene posterior
age estimate (c. 62–51 Ma) for the African–South American
divergence. Placing no constraints directly at this node, utilizing
the NPRS dating method for the TTR gene region, gave similar
estimates of c. 66–46 Ma for the divergence of African and
South American lineages (see Tables 1 and 4).
Although our estimates are overwhelmingly consistent across
our chosen fossil calibration points, between the two methods
(multidivtime and NPRS) and, in general, among gene
partitions, dates derived from the GHR gene region for the
NPRS method did give some highly stochastic and anomalous
results (Table 4). In one instance, for the Hydrochaeridae
calibration point (F1, Table 3), derived dates tended to be
much younger than other inferences, with the GHR estimates
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D. L. Rowe et al.
Table 4 Representative divergence-date estimates for given nodes (‘Node no.’) of African and South American hystricognath rodents, as
derived from both Bayesian multidivtime and nonparametric rate-smoothing (NPRS) molecular-clock methods using the growth hormone receptor (GHR) and transthyretin (TTR) datasets.
Bayesian multidivtime age estimates (Ma)
Gene partitions, U = 55 Ma
Calibration
points
GHR
U = 90 Ma
TTR
GHR/TTR
GHR/TTR
Node no.
Cal.
Age
All
123
All
Gap
123/all
All/gap
All/gap
42
43
44
45
46
51
53
58
59
63
68
69
70
71
72
73
–
L5
–
–
L1
–
–
–
L2
L3
–
L4
U
–
–
–
–
30
–
–
16
–
–
–
11
19
–
30
55
–
–
–
24
41
12
18
21
32
09
07
23
17
28
40
42
47
51
87
23
46
13
20
23
38
12
07
21
14
34
45
47
53
55
82
43
68
07
17
21
37
19
12
24
19
28
42
46
65
71
94
39
62
09
18
23
38
19
10
24
18
26
40
44
58
64
89
32
54
07
17
20
33
13
09
22
16
26
39
42
55
58
94
34
55
09
19
23
37
15
08
22
15
29
43
45
55
59
92
38
61
11
22
26
42
17
09
25
17
33
48
51
62
66
101
(22–49)
(41–70)
(05–16)
(13–27)
(17–32)
(28–47)
(08–23)
(05–12)
(17–30)
(11–21)
(20–38)
(33–52)
(35–54)
(42–69)
(44–74)
(68–121)
Nonparametric rate-smoothing (NPRS) age estimates (Ma)
F1
F2
F3
Calibration points
Hydrochaeridae
Octodontidae
Dasyproctidae
Node no.
Cal.
Age
GHR
TTR
GHR
TTR
GHR
TTR
42
43
44
45
46
51
53
58
59
63
68
69
70
71
72
73
–
–
–
F1
–
F3
–
F2
–
–
–
–
–
–
–
–
–
–
–
16
–
31
–
11
–
–
–
–
–
–
–
–
18
30
08
16
18
25
09
05
14
09
24
32
33
36
39
55
38
61
07
16
19
36
17
11
25
19
29
42
46
65
68
93
44
74
20
40
43
61
22
11
35
24
60
79
80
89
97
138
38
62
07
16
20
36
17
11
25
19
29
43
46
66
69
94
23
39
11
21
23
32
11
06
18
12
31
41
42
46
51
72
34
54
06
14
17
32
15
10
22
17
26
38
40
58
61
83
For multidivtime analyses, gene regions were analysed unpartitioned (‘all’) as well as partitioned by codon positions (‘123’) for GHR and
without gaps (‘gap’) for TTR. Node ages with 95% posterior probability estimates, shown in parentheses, are provided for the GHR/TTR-all/gap
analysis. This combined dataset (GHR/TTR, all/gap) was reanalysed with the upper bound (‘U’) for Caviomorpha extended from 55 to 90 Ma, as
displayed in the far right column. Nodes with calibrating lineages are identified in bold, where the node number refers to those designated in Fig. 2.
The calibration points (‘Cal.’) and assigned ages (‘Age’) are concordant with those listed in Table 3.
sometimes less than half that of the TTR age estimates. Perhaps
coincidentally, this combination yielded an estimated Africa–
South America divergence of c. 36–33 Ma, similar to results in
314
the majority of previously published molecular studies (see
Table 1). In much the same manner, but at the other extreme,
the GHR data with the Octodontidae calibration point (F2,
Journal of Biogeography 37, 305–324
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Trans-Atlantic dispersal of rodents
Figure 2 Chronogram of divergences in African and South American hystricognath rodents, as estimated from the two-gene dataset
(GHR/TTR-all/gap) using five internal calibration points set as minimal ages (designated in bold as L1–L5) and a maximum age of 55 Ma
(U = 55 Ma) for the diversification of Caviomorpha (node 70). The nodes at which fixed calibrations were applied for nonparametric
rate-smoothing analyses are included for reference purposes, identified here as F1, F2 and F3. Grey horizontal bars indicate the 95%
posterior probabilities for key nodes (labelled with numbers between 42 and 73, as presented in Table 4), as derived from the Bayesian
multidivtime analysis. Approximate positions of continents at 105 and 45 Ma are given below the figure, and vertical bars (black, white,
grey) at the right of the figure indicate contemporary geographical distributions of taxa. Node 71, marked with a star, identifies a
transoceanic disjunction that post-dates the associated continental break-up of Africa and South America, inferring a long-distance dispersal
event. Key to epochs on the timeline: L-CR, Late Cretaceous; PAL, Palaeocene; OLIG, Oligocene; Pl, Pliocene; and P, Pleistocene, with K-T
identifying the Cretaceous–Tertiary boundary.
Table 3) yielded exceptionally old date estimates of c. 89–80 Ma
for the same event, similar to ages reported by Mouchaty et al.
(2001). These extreme estimates are reminiscent of the original
controversy over inferences derived from a strict interpretation
of the fossil record and presumptions of Gondwanan vicariance.
DISCUSSION
employing the same molecular-clock dating methods (i.e.
Bayesian multidivtime and NPRS), our relaxation of temporal constraints otherwise imposed at the node defining
South American origins (i.e. node 70, Fig. 2) appears to have
allowed for older divergence-date estimates to be obtained.
Nonetheless, age estimates never coincided with or preceded
the geological fragmentation of relevant continents and, thus,
vicariance isolating mechanisms can be rejected.
Evidence for dispersal
Both phylogenetic and temporal inferences rejected the notion
of Gondwanan vicariance as a driving force in hystricognath
rodent diversification. In comparison to previous studies
Journal of Biogeography 37, 305–324
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Phylogenetic pattern
Our data strongly supported a monophyletic New World clade
(i.e. Caviomorpha) nested within a paraphyletic group of Old
315
D. L. Rowe et al.
World taxa, rejecting the traditionally held reciprocal monophyly of Old World and New World lineages. It has generally
been assumed that the suborder Hystricognathi descended
from an Asian ctenodactyloid ancestor (George, 1993a; Flynn &
Swisher, 1995; Marivaux et al., 2002) and that the widespread
distribution of contemporary Hystricomorpha lineages (i.e.
Asia and Africa) is attributable to overland dispersal following
the Miocene collision of the African and Asian continental
plates (Janis, 1993). As such, reciprocal monophyly of the Old
World and New World hystricognath clades generates an areacladogram not inconsistent with vicariance biogeography (i.e.
[Asia (Africa–South America)]; Nelson & Platnik, 1981; Craw
et al., 1999). However, our non-traditional placement of the
Old World porcupines (i.e. Hystricomorpha) allows for the
possibility of an ancient Hystricomorpha lineage originating in
Asia. This leaves the sequential pattern of continental occupation open to speculation and various area-cladogram
interpretations plausible, some of which would be inconsistent
with vicariance biogeography. Nevertheless, the testing of
vicariance and dispersal mechanisms based on these areacladograms alone is subject to untenable assumptions concerning the complicated myriad of plausible lineage duplication and continental extinction events, each incurring a predetermined cost that is inversely related to some preconceived
likelihood of occurring (e.g. Ronquist, 1997). Owing to such
uncertainty in pattern, reliable age estimates remain an
essential component of a full understanding of the evolutionary history of hystricognath rodents.
In support of our proposed age estimates, Palaeogene faunal
exchanges between south Asia and the Arabo-African continent, occurring well after Pangean fragmentation and long
before the well-known Miocene collision of Africa with Eurasia
(Janis, 1993), have been proposed for numerous other
mammalian groups, such as anthracotheres, proboscideans,
primates and anomalurid rodents (Ducrocq, 1997, 2001; Jaeger
et al., 1999; Marivaux et al., 2002, 2004). Although there is
growing support for concerted transoceanic dispersal events
(e.g. Givnish & Renner, 2004; Pennington & Dick, 2004;
Sanmartı́n & Ronquist, 2004; de Queiroz, 2005), without a
need to invoke stepping-stone modes of dispersal, the range of
proposed dates of divergence presented here does, nonetheless,
encompass a major marine regression (c. 63–68 Ma; Haq et al.,
1987). Although such marine low-stands have been hypothesized to facilitate island-hopping dispersal via emergent island
chains, the temporal coincidence of favourable palaeocurrents
and palaeowinds could conceivably have aided either steppingstone or chance (i.e. long-distance) dispersal in a westerly
direction during the Late Cretaceous–Palaeocene time period
(Holroyd & Maas, 1994). Likewise, a major marine regression
with exceptionally low sea levels also occurred c. 88 Ma,
potentially facilitating dispersal between the continents at this
time. Such a scenario is consistent with our molecular data,
but more strongly at odds with the current status of
palaeontological information, with the oldest known fossil of
relevance dating only to the Late Eocene.
Narrowing the gap in trans-Atlantic dispersal
Inference of trans-Tethys dispersal
The proposed Late Cretaceous–Palaeogene split (c. 92–59 Ma)
between an Asian ctenodactyloid ancestor and the origin of
Hystricognathi clearly post-dates the continental fragmentation
of Pangea (e.g. > 165 Ma; Scotese et al., 1988), leading to the
rejection of vicariance in association with the divergence of
Asian and African clades. A more precise biogeographical
interpretation, however, of transoceanic dispersal and Hystricognathi origins, is untenable at present owing to the exceptionally large standard error observed at the root node of the
phylogeny (node 73, Fig. 2 and Table 4). Both simulated and
empirical evidence has indicated that the estimation of ancient
divergence times using recent calibration points is prone to
increasing error with increasing distance from the calibration
points (Nei et al., 2001; Linder et al., 2005), and our observations are consistent with this finding. Unfortunately, given the
biogeographical and temporal biases in the rodent fossil record,
the nearest calibration point that could reliably be applied to
infer the age of the Hystricognathi–Ctenodactylidae split (i.e.
node 73) was a much more recent divergence (the African
Thryonomyidae, c. 34 Ma; McKenna & Bell, 1997). Furthermore, we cannot dismiss the possibility of limited taxonomic
sampling of the outgroup (i.e. ctenodactylids) confounding our
ability to infer accurate patterns of rate change near the root
node, potentially leading to some degree of error in age estimates
at the base of the phylogeny (Yoder & Yang, 2000).
316
Our age estimate for divergence between African and South
American lineages (c. 45–55 Ma) falls between the traditionally
inferred extremes of Gondwanan geological events (c. 100 Ma)
and Late Eocene fossil records (c. 30–35 Ma), requiring a less
substantial c. 25-Myr absence of detection in the fossil record
and favouring transoceanic dispersal across a somewhat
narrower Atlantic Ocean (Holroyd & Maas, 1994). Likewise,
our estimates contradict previously published molecular-clock
studies that support a Late Eocene–Early Oligocene dispersal
event (see Table 1 and references therein), even when the same
molecular-clock methodologies were employed (e.g. Bayesian
multidivtime and NPRS). Our more comprehensive taxonomic sampling is likely to have improved the effectiveness of
correcting for among-lineage rate heterogeneity (Sanderson,
1998; Welch & Bromham, 2005) and expanded the number
and breadth of calibrating nodes, providing for more robust
divergence-date estimates from relaxed-clock methods (Near &
Sanderson, 2004; Linder et al., 2005).
Perhaps most importantly, and in contrast to our own
approach, previous studies attempting to infer divergence
times of hystricognath rodents from molecular data have
routinely incorporated the oldest known South American
rodent fossil (c. 32 Ma, ‘dasyproctid indet.’; Wyss et al., 1993,
1994) as a fixed calibration point or as an upper bound (e.g.
Huchon et al., 2000; Huchon & Douzery, 2001; Hasegawa
et al., 2003; Galewski et al., 2005; Opazo, 2005). In some cases,
Journal of Biogeography 37, 305–324
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Trans-Atlantic dispersal of rodents
the age of this fossil has been directly applied or used to
enforce a limit on the age of the node (i.e. node 70, Fig. 2) for
which the inferred posterior age estimates are subsequently
taken as evidence for the timing of the arrival of rodents to
South America. Constraining a node in a phylogenetic tree
in this way runs the risk of circularity in biogeographical
interpretation. In this instance, by limiting the window of
opportunity and precluding vicariance, it enforces the assumption that a Late Eocene dispersal event accounts for the arrival
of ancestral lineages to South America, rather than independently assessing the temporal coincidence of this fossil with
molecular age estimates. Not surprisingly, in cases where this
fossil has been used to represent the age of Caviomorpha, the
posterior age estimates for the node tend to converge on the
imposed limit (e.g. Hasegawa et al., 2003; Galewski et al., 2005;
Opazo, 2005), further indicating that it may be an unrealistic,
hard upper bound (Yang & Rannala, 2006). Additional
problems with this particular fossil calibration point will be
discussed in more detail in the following section.
Concordance with palaeontological information
It is conceivable that colonization of South America by rodents
could have commenced up to c. 55 Ma, as our data suggest,
without being detected in the fossil record for some time,
particularly if caviomorph lineages originally occupied areas of
northern South America where palaeontological deposits of
an appropriate age are presently unknown. The theoretical
counter-clockwise rotation of Africa from South America,
during the Late Cretaceous, resulted in tropical western Africa
being the last part of Africa in proximity to north-eastern
South America, and fossil beds are exceptionally rare or absent
in both of these biogeographical regions (Parrish, 1993; Flynn
et al., 2002; Jaeger, 2003; MacFadden, 2006). If dispersal did
indeed occur from western Africa to north-eastern South
America, then we might expect a significant gap in time to
exist from the earliest stages of colonization and diversification
in these lowland tropical areas to presence being detectable (i.e.
numerous and geographically dispersed enough to increase the
likelihood of being preserved) in the Late Eocene of central
Chile, where the oldest South American rodent fossils are
presently recorded (c. 31–37 Ma; Flynn et al., 2002). An earlier
colonization, prior to the Eocene–Oligocene debut in the fossil
record, is also consistent with intercontinental habitat similarity facilitating the survival of new immigrants. From the
Late Cretaceous through to the Early Eocene (c. 50 Ma), global
climatic belts were more tropical than they are today, with
warm and humid tropical-temperate forests existing throughout South America and Africa from c. 50 to 80 Ma (Janis,
1993; Flynn & Wyss, 1998; MacFadden, 2006).
The fossil record is not necessarily inconsistent with a
significantly earlier colonization of the continent than the
oldest known rodent fossil might suggest. Many palaeontologists accept an older date of origin for Caviomorpha (Wyss
et al., 1994; Hartenberger, 1998; Flynn et al., 2002; Vucetich
et al., 2004; MacPhee, 2005). In fact, Marivaux et al. (2002)
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
concluded that ‘the fossil record of hystricognathous rodents
(virtually unknown before the Late Eocene) is still inadequate
for proposing a realistic palaeobiogeographical model to
explain the subsequent arrival in South America’. However,
most biogeographical interpretations based on molecular
clocks have relied on the most ambiguous of fossils (e.g. the
oldest known South American rodent) that contradict this
statement. This example reinforces the importance of a
thorough investigation of palaeontological knowledge prior
to the designation of calibration points for molecular clocks
(e.g. Conroy & van Tuinen, 2003; Sanderson et al., 2004).
Use of the ‘oldest known’ fossil in this way is also
inappropriate on other grounds. The primitive morphological
characteristics and fragmentary nature of this particular fossil
specimen render its phylogenetic placement uncertain (Wyss
et al., 1993, 1994; Flynn et al., 2002). The default, however, has
been placement at the base of the crown-group, Caviomorpha,
as a means of calibrating molecular clocks. This has been done
repeatedly, despite the original descriptions of the fossil
inferring alignment with the caviomorph superfamily Cavioidea (Wyss et al., 1993, 1994), and subsequent identification of
an additional rodent from the same fossil bed, probably
belonging to the caviomorph superfamily Chinchilloidea
(Flynn et al., 2002). Two such divergent lineages at the same
locale suggest that rodents must have originated and diversified in South America well before the Eocene–Oligocene
boundary. Thus, imposing a date of c. 32 Ma as a calibration
point or as an upper bound at this node is unsubstantiated and
likely to bias molecular-clock estimates. Concordant with this
suggestion, our derived placement of this fossil (i.e. placed at
the node immediately preceding the diversification of the
family Dasyproctidae; node 51 in Fig. 2) as a fixed calibration
point, in accordance with its palaeontological identification
(‘dasyproctid indet.’; Wyss et al., 1993, 1994), yields divergence dates (e.g. NPRS method, TTR gene region) consistent
with our independent multidivtime and NPRS (e.g. TTR
gene) estimates based on other calibration points.
Considering a southern dispersal route
The plausibility of a southern dispersal route should not be
precluded, in the light of evidence of trans-Antarctic dispersal
playing a predominant role in southern faunal and floral
exchange (Sanmartı́n & Ronquist, 2004). Furthermore, the
distribution of fossil and extant Caviomorpha lineages is
concordant with the observation of South America being
clearly divisible into two biotic provinces with different
biogeographical affinities: a Southern Biome and a northern
Amazon Basin Biome (Vucetich et al., 1999; Sanmartı́n &
Ronquist, 2004). Following from these observations, the first
appearance of rodents in the Southern Biome of South
America (i.e. central Chile; Wyss et al., 1993) might seem to
lend credibility to a southern route of colonization.
Although the common ancestors of ctenodactylid and
hystricognath rodents appear to be Asian in origin, inferring
the geographical origin of the suborder Hystricognathi itself
317
D. L. Rowe et al.
has been controversial. Both Asian (e.g. Marivaux et al., 2002)
and African (e.g. Lavocat, 1969) origins have been supported,
as have multiple hypotheses for the subsequent origin and
dispersal of Caviomorpha lineages to South America. Although
North America is viewed as an unlikely source for the South
American radiation (Martin, 1994; Marivaux et al., 2002), a
southern route via Antarctica was not ruled out in a previous
study (Huchon & Douzery, 2001). As such, we consider the
compatibility of our temporal data with a proposed Asian
origin for Hystricognathi and a southern route of dispersal to
South America.
If an Asian ancestor gave rise to the suborder Hystricognathi
on the same continent, then multiple dispersal events must be
invoked to account for their contemporary distribution in
Asia, Africa and South America. Under this scenario, the subSaharan-restricted Bathy–Phiomorpha clade would have arisen
as a consequence of an ancestral hystricognath lineage
dispersing from Asia to Africa – some time between the origin
of the crown-group Hystricognathi (node 72) and the
subsequent radiation of Bathy–Phiomorpha lineages within
Africa (node 43). According to our molecular-clock estimates,
this would have occurred in the interim of roughly 59–55 Ma.
Regardless of the precise timing of this proposed dispersal
event across the Tethys Sea, a minimum of one additional
transoceanic dispersal event from an Asian ancestor would also
need to be inferred to account for the presence of rodents in
South America if they arrived via Antarctica.
A transoceanic dispersal event from Southeast Asia to
Australia would be required in the interim of c. 45–55 Ma
(i.e. between nodes 70 and 71; Fig. 2 and Table 4), according
to our molecular-clock estimates, a time when Australia
remained geographically isolated from Southeast Asia
(Scotese et al., 1988). Subsequent to arriving in Australia, a
terrestrial dispersal route could have been facilitated, albeit
requiring coverage of a vast terrestrial expanse within a
relatively narrow time-frame, as well as widespread extinction
(or lack of detection) from the Australian continent. To
accommodate a terrestrial expansion, dispersal across the
Australian continent would have been required within a
10-Myr time-frame, as some degree of separation of Antarctica from Australia was attained by 40 to 50 Ma (Lee &
Lawver, 1995). Likewise, dispersal across the Antarctic
continent in a similar time-frame would have been required
to allow for the colonization of South America before the
geological interruption of the Antarctic corridor connection
(with South America) at c. 35 Ma (Lawver et al., 1992). This
timing is surprisingly concordant with the initial Late Eocene
emergence of rodents in the South American fossil record,
which first appeared in the Southern Biome (c. 31–37 Ma;
Wyss et al., 1993).
However, because this southern route requires either one
additional transoceanic dispersal event or a rapid and extensive
geo-dispersal across Australia and Antarctica, as well as
continental extinctions or lack of detection in the fossil record,
it is deemed the less parsimonious explanation for the presence
of lineages in South America. Therefore, at present, we favour
318
an African origin for Hystricognathi and a trans-Atlantic
dispersal of lineages to South America during the Late Eocene.
Reliability of age estimates
Factors influencing estimates of divergence time
Although rejecting Gondwanan vicariance biogeography by a
wide margin, the time-frame inferred for dispersal is likely to
be refined as methodological approaches improve. At present,
it appears that the younger estimates derived from molecularclock studies may be largely attributable to two important
factors: taxon sampling and calibration point designation. Our
minimization of the potential errors associated with limited
taxonomic sampling, erroneous fossil calibration points, and
distant extrapolations is likely to provide a more robust
interpretation of the evolutionary history of hystricognath
rodents. Nonetheless, much remains to be elucidated about the
utility of relaxed-molecular-clock methods.
Certainly, Bayesian methods are known to be sensitive to the
designation of priors (Bell & Donoghue, 2005; Ho et al., 2005;
Renner, 2005; Welch & Bromham, 2005; Welch et al., 2005;
Smith et al., 2006). In particular, a prior assumption of a
lognormal distribution of rates has been shown to lead to an
underestimation bias for nodes, particularly for those older
than the calibration points (Ho et al., 2005). Alternatively,
NPRS has been shown to over-fit the data, leading to rapid
fluctuations in rates where there are short internodes, and
hence to overestimated ages near the root (Bell & Donoghue,
2005; Rutschmann, 2006). In this regard, it is encouraging to
see a general agreement between our Bayesian and NPRS
estimates, particularly at the root nodes.
The stochastic nature of dates derived from our GHR
dataset using the NPRS method may be attributable to known
inadequacies of this method in terms of over-fitting of the data
(Bell & Donoghue, 2005). Overestimation with NPRS has been
shown to be particularly severe when only a shallow, recent,
node is used as a calibration point. In such cases, estimates for
the root age are ‘equally likely to move off to infinity or to
retain more realistic values’ (Sanderson et al., 2004). Qualitatively, in our dataset, the degree to which GHR age estimates
do not conform is magnified as more shallow calibrating nodes
are implemented. For example, extreme ‘overestimation’ is
observed for the Octodontidae calibration point (F2 in
Table 3), designated at 11 Ma. Intermediate ‘underestimation’
is observed for the Hydrochaeridae calibration point (F1) at
16 Ma, and no ‘deviant age estimates’ are obtained from the
dasyproctid calibration point (F3) at 32 Ma. However, this
pattern was observed only for the GHR gene region, and not
for TTR. Nonetheless, we might have expected greater
stochasticity in age estimates to be observed with the GHR
dataset given that there were fewer variable characters and,
thus, a greater likelihood of inaccurate branch-length estimates
(Sanderson et al., 2004). In particular, exceptionally short
internodes were observed near the base of the tree, and some
branches were assigned a length of zero (data not shown).
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
Trans-Atlantic dispersal of rodents
Consequently, this combination of parameters may have
contributed to the anomalous nature of estimates derived
from the GHR dataset using the NPRS method. In addition,
more severe rate shifts are observed among clades within the
GHR dataset (data not shown), potentially violating the
underlying assumption of autocorrelation of rates.
Taxonomic sampling pitfalls
The detection of variable rates of evolution is known to be
sensitive to taxonomic sampling (Sanderson, 1998; Bromham
et al., 2000), and, more importantly, a recent empirical study
suggests that poor taxonomic sampling leads to erroneous
estimations of divergence dates even when relaxed-clock
methods are employed (Linder et al., 2005). There appears
to be a logarithmic relationship between the proportion of
under-sampling and the degree of age underestimation,
particularly for the NPRS methodology (Linder et al., 2005).
In this instance, sampling less than 10% of extant species
resulted in estimates that were half the ages of those obtained
under full taxonomic sampling. In this respect, our inferences
are unlikely to be vastly underestimated (e.g. to the degree of
half of their true age), as we have incorporated about 18% of
extant Hystricognathi lineages. In addition, Bayesian methods
have been shown to be more resilient to under-sampling
effects, and we obtain similar age estimates using this method.
Sparse taxonomic sampling might, however, account for
some of the younger age estimates reported in previous
molecular studies, particularly in cases where the NPRS
relaxed-clock method has been implemented. However, this
is unlikely to be a universal explanation, given that equally
young age estimates have been reported using the Bayesian
multidivtime method (see Table 1).
Compounding effects of under-sampling and calibration
distance
Both simulated and empirical evidence has indicated that the
estimation of ancient divergence times by using recent calibration points is prone to increasing error with increasing distance
from calibration points (Nei et al., 2001; Linder et al., 2005).
Linder et al. (2005) further reported a positive linear relationship between degree of age underestimation and distance from
the calibration point, for both NPRS and Bayesian methods. In
other words, the greater the distance from the calibrating node,
the more sensitive the age estimates become to under-sampling
(i.e. leading to the underestimation of true ages). This is an
important relationship, and fits with the observation of young
age estimates being obtained when sparse taxonomic sampling
has accompanied the use of distant calibration points in previous
molecular studies employing Bayesian methods (e.g. Adkins
et al., 2003; Hasegawa et al., 2003; Springer et al., 2003). Our
divergence-date estimates are likely to be more resilient to these
effects, given our greater taxonomic sampling and the use of
multiple calibration points within the study group, in close
proximity to the node ages being estimated.
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd
FUTURE STUDIES
Terrestrial and freshwater animals, as well as plants traditionally considered to be poor dispersers, appear to have crossed
the Atlantic Ocean more regularly than previously appreciated,
with an ever-growing number of studies proposing transoceanic dispersal of biota (e.g. Danforth et al., 2004; Givnish &
Renner, 2004; Pennington & Dick, 2004; de Queiroz, 2005;
Renner, 2005). Among them, molecular-clock studies indicate
that primates (e.g. Schrago & Russo, 2003) and freshwater
cichlid fishes (e.g. Vences et al., 2001) may have shared a
dispersal avenue with hystricognath rodents, from Africa to
South America, during the Middle to Late Eocene (c. 35–
58 Ma). In addition to transoceanic voyagers to the New
World, it appears that wind-dependent dispersalists, such as
insects, could have been contemporary colonists as well (e.g.
Danforth et al., 2004). Whether such long-distance transoceanic dispersal events exhibit regularity, as an identifiable and
predominant biogeographical pattern, or whether they are
simply a random and coincident sampling of trans-Atlantic
dispersalists certainly warrants further investigation. For
instance, could these concomitant events be a product of
biogeographically and temporally biased fossil records and/or
uncertainties in the processes of molecular evolution underlying molecular clocks, errors of which are compounded when
biased fossil records are used to calibrate irregularly ticking
molecular clocks?
Combining geological, oceanographic and climatic data with
temporal inferences has the potential to provide important
clues to unravelling evolutionary history. It is certainly evident
that wind and water circulation systems are not randomly
distributed in space and time and, it seems, may have persisted
for geologically significant and relevant time periods (Morley
& Dick, 2003; Sanmartı́n & Ronquist, 2004; Renner, 2005).
Given that wind and ocean currents are known to influence
contemporary dispersal, we might predict that the observation
of biased patterns in the timing and direction of historical
transoceanic dispersal is inevitable. While a biogeographical
bias in pattern might be detectable, although potentially
confounded by lineage-specific differences in dispersal and
establishment capabilities, discernment of the predominant
pattern may require the examination of a large number of
taxonomic groups (Pennington & Dick, 2004; Sanmartı́n &
Ronquist, 2004; Renner, 2005). Most critically, reliable temporal time-frames (i.e. divergence-date estimates) must be
established. To achieve this goal, both palaeontological and
molecular-clock estimates of time must be scrutinized, as both
types of analyses can be biased or mislead interpretations of
evolutionary history. Studies of this nature should include a
comprehensive evaluation of the fossil record and identify
potential errors associated with molecular analyses in order to
establish the reliability of the temporal component and
facilitate combination of data into large meta-analyses (Conroy & van Tuinen, 2003; Sanderson et al., 2004). Only then
may we begin to elucidate the mechanisms by which contemporary distribution patterns of biota have been assembled.
319
D. L. Rowe et al.
ACKNOWLEDGEMENTS
The authors thank the many individuals and institutions that
generously provided tissue samples for this study: R. J. Baker,
Texas Tech University Museum; Cincinnatti Zoo, Ohio; L. P.
Costa, Museum of Vertebrate Zoology, University of California,
Berkeley; R. C. Dowler; L. Emmons; M. Gallardo; A. Harlin; C.
W. Kilpatrick, University of Vermont; E. Louis, Henry Doorley
Zoo, Nebraska; J. Patton; Smithsonian National Zoological
Park; and T. L. Yates, Museum of Southwest Biology, University
of New Mexico. P. G. Wolf, C. P. Burridge and anonymous
referees provided comments that improved the manuscript.
Support for this research was provided by a grant from the
National Science Foundation to R.L.H. (DEB 9615163).
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BIOSKETCHES
Diane L. Rowe has a wide range of systematic research
interests, including molecular evolution, historical biogeography and patterns of species diversification. Current projects
are focused on the geological and palaeontological calibration
of molecular clocks, life-history correlates of rates of molecular
evolution, and ecological correlates of adaptive radiations.
Katherine A. Dunn is a postdoctoral research fellow in the
Department of Biology at Dalhousie University. Her research
currently focuses on comparative prokaryote genomics and
statistical models of molecular evolution.
Ronald M. Adkins is Assistant Professor in the Department
of Pediatrics at the University of Tennessee Health Sciences
Center. His primary research interests are in the genetics of
foetal growth regulation, the genomics of the growth hormone
locus, and mammalian systematics.
Rodney L. Honeycutt is Professor of Biology at Pepperdine
University. His focal areas of research are in mammalian
evolution and population genetics.
Editor: Robert McDowall
Journal of Biogeography 37, 305–324
ª 2009 Blackwell Publishing Ltd