Mitogenomic Phylogeny, Diversification, and Biogeography of
SouthAmericanSpinyRats
Pierre-Henri Fabre,*
,1,2
Nathan S. Upham,
3,4
Louise H. Emmons,
2
Fabienne Justy,
1
Yuri L.R. Leite,
5
Ana
Carolina Loss,
5
Ludovic Orlando,
6,7
Marie-Ka Tilak,
1
Bruce D. Patterson,
4
and Emmanuel J.P. Douzery
1
1
Institut des Sciences de l’Evolution (ISEM, UMR 5554 CNRS-IRD-UM), Universite´ de Montpellier, Montpellier, France
2
National Museum of Natural History, Smithsonian Institution, Washington, DC
3
Ecology and Evolutionary Biology, Yale University, New Haven, CT
4
Integrative Research Center, Field Museum of Natura l History, Chicago, I L
5
Departamento de Ci
^
encias Biol
ogicas, Universidade Federal do Esp
ırito Santo, Vit
oria, Esp
ırito Santo, Brazil
6
Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark
7
Laboratoire d’Anthropobiologie Mole´culaire et d’Imagerie de Synthe`se, Universite´ de Toulouse, University Paul Sabatier, Toulouse,
France
*Corresponding author: E-mail: phfmourade@gmail.com.
Associate editor: Emma Teeling
Abstract
Echimyidae is one of the most speciose and ecologically diverse rodent families in the world, occupying a wide range of
habitats in the Neotropics. However, a resolved phylogeny at the genus-level is still lacking for these 22 genera of South
American spiny rats, including the coypu (Myocastorinae), and 5 genera of West Indian hutias (Capromyidae) relatives.
Here, we used Illumina shotgun sequencing to assemble 38 new complete mitogenomes, establishing Echimyidae, and
Capromyidae as the first major rodent families to be completely sequenced at the genus-level for their mitochondrial
DNA. Combining mitogenomes and nuclear exons, we inferred a robust phylogenetic framework that reveals several
newly supported nodes as well as the tempo of the higher level diversification of these rodents. Incorporating the full
generic diversity of extant echimyids leads us to propose a new higher level classification of two subfamilies:
Euryzygomatomyinae and Echimyinae. Of note, the enigmatic Carterodon displays fast-evolving mitochondrial and
nuclear sequences, with a long branch that destabilizes the deepest divergences of the echimyid tree, thereby challenging
the sister-group relationship between Capromyidae and Euryzygomatomyinae. Biogeographical analyses involving higher
level taxa show that several vicariant and dispersal events impacted the evolutionary history of echimyids. The diver-
sification history of Echimyidae seems to have been influenced by two major historical factors, namely (1) recurrent
connections between Atlantic and Amazonian Forests and (2) the Northern uplift of the Andes.
Key words: biogeography, diversification, Echimyidae, mitogenomics, Neotropics, nuclear DNA, fast-evolving gene,
Carterodon.
Introduction
Thanks to a unique geological history and ecology, the
Neotropical biota together composes the richest realm of
biodiversity in the world. The formation of complex riverine
systems and the uplift of the Andean Cordillera has, together
with climatic changes, driven several spectacular biological
radiations (Hoorn et al. 2010; Patterson and Costa 2012).
Based on geology and zoogeography (
Morrone 2014), the
tropical Americas can be subdivided into six major biomes
(fig. 1): Amazon Basin, Central Andes and Guyana Shield
(AM), the trans-Andean region plus Choc
o(CH),the
Northern Andes and northern coastal dry forests in
Venezuela and Colombia (NA), Caatinga, Chaco, Cerrado
and the Pantanal (CC), Atlantic Forest (AF), and the insular
West Indies (WI). These biomes are characterized by several
large forested regions (Amazon Basin, Atlantic Forest, Choc
o,
Orinoco watersheds and West Indies), open habitats (CC:
Cerrado þ Caatinga, and Ch aco; NA: Pan tanal þ Llanos),
and the Andean mountain range (Central þ Northern
Andes). The major barriers currently separating the forested
biomes were formed following climate aridification and/or
mountain uplift during the Miocene (
Hoorn et al. 2010),
and have substantially contributed to biotic divergence and
endemism in the Neotropics. The Amazon Basin forms the
largest Neotropical biome and is surrounded to the west by
the Choc
o wet forest (across the Northern Andes), both the
Orinoco watershed and the northern coastal dry forests in
Venezuela and Colombia, and the coastal Atlantic Forest of
Brazil and Paraguay. Disjunct distributions of terrestrial ver-
tebrate species among the Amazon Basin and the Atlantic
Forests reflect a common geoclimatic divergence structuring
in South American biotas (
da Silva and Patton 1993; Patton
et al. 2000
; Batalha-Filho et al. 2013). Biotas of those two
rainforests are among the most diverse globally, and are sep-
arated by a diagonal region of xeric habitats comprising the
Article
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Cerrado and Caatinga biomes (Ab’S
aber 1977). Geological
and paleontological data (
Hoorn et al. 2010)suggestthat
areas of the Amazon Basin and Atlantic Forest have under-
gone successive separations and connections since the
Miocene, including: (1) expansion of foreland hydrologic
basins of the West Amazon basin (23–7 Ma; see
Lundberg
et al. 1998
; Wesselingh and Salo 2006; Wesselingh et al. 2006);
(2) potential watershed shifts between the Paran
a Sea and the
Amazon River (12–7 Ma;
Hoorn 1996; R
€
as
€
anen and Linna
1996
; Lundberg et al. 1998; Roddaz et al. 2006); and, (3)
more recent Plio-Pleistocene climatic events (Costa 2003).
Xeric habitats appear to have represented more labile barriers
to gene flow than previously hypothesized (
Patton et al. 2000)
as demonstrated by the relatively young phylogeographic
structure in birds and mammals of the northern
Neotropics (
Batalha-Filho et al. 2013; Nascimento et al.
2013
).NorthoftheAmazonBasin,theupliftofthe
Northern Andes and emergence of the Orinoco watershed
has also shaped patterns of biodiversity, both as a vicariant
barrier between Mesoamerica and coastal areas north of the
Amazon Basin, and as a heterogeneous region within which
species can be isolated, diverge, and later disperse to other
regions (i.e. , a “species pump”) (
Cracraft and Prum 1988; Ron
2000
; Patterson and Costa 2012).
In this paleo-geographical context, South American spiny
rats (Mammalia: Rodentia: Echimyidae) have radiated across
multiple biomes, and encompass today a vast array of life
histories and ecomorphological adap tations, including
capacities for semi-fossorial, arboreal, and s emi-aquatic
lifestyles (see review by
Emmons et al. 2015).
Understanding the process of higher level diversification of
Echimyidae is at the core of several major biogeographical
questions. Historical biogeography has been posited (
Leite
and Patton 2002
; Galewski et al. 2005) as a main driver of
echimyid rodent divergence, with two major regions involved
in alternating vicariance and dispersal through time: (1) east-
ern South America, including the Atlantic Forest, and the
open formations of the Cerrado and Caatinga; and, (2) the
Amazon Basin, including the cis-Andean highland regions
and the forests of the Southern Orinoco Basin and Guiana
Shield. The lowland rainforest of the Amazon Basin supports
most of the extant echimyid diversity, with eight arboreal
genera (Dactylomys, Echimys, Isothrix, Makalata, Mesomys,
Lonchothrix, Toromys, Pattonomys) and the speciose terres-
trial genus Proechimys (at least 22 species;
Emmons et al.
2015
). The Atlantic Forest biome also harbors a diverse as-
semblage of echimyid species grouped into three arboreal
genera (Kannabateomys, Phyllomys, Callistomys), one terres-
trial genus (Trinomys), and one semi-fossorial genus
(Euryzygomatomys). In between the Amazon Basin and
Atlantic Forest, echimyids also diversified in: (1) grasslands,
as semi-fossorial specialists in the Cerrado and Caatinga bio-
mes (Carterodon,andCl yomys) and, (2) within open vegeta-
tion of the Caatinga, Cerrado, Chaco and Pantanal with the
ground-dwelling terrestrial genus Thrichomys (
Borodin et al.
2006
; D’El
ıa and Myers 2014). This pattern suggests the influ-
ence of vicariant processes between the Amazonian and
Atlantic forests (
Galewski et al. 2005; Fabre, Galewski et al.
FIG.1.Distribution map for all genera of Echimyidae and correspondence between their ranges and the biogeographical provinces of the
Neotropics.
Fabre et al.
.
doi:10.1093/molbev/msw261 MBE
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2013), as well as the influence of past Andean uplift
(
Patterson and Velazco 2008; Upham et al. 2013), offering
two important drivers for the genus-level diversification of
echimyid species.
Previous phylogenetic results suggest the initial diversifica-
tion of Echimyidae during the Early Miocene (
Galewski et al.
2005
; Upham and Patterson 2012; Fabre, Galewski, et al.
2013
), including independent originations of arboreality in
the Amazon and presumably again in the Atlantic Forest
on the lineage leading to Callistomys (
Loss et al. 2014). The
main arboreal clade of echimyids, which includes taxa in both
Amazonian and Atlantic rainforest areas, indicates that mul-
tiple transitions have been made among these regions
(
Upham and Patterson 2012; Fabre et al. 2013). If these obli-
gate arboreal taxa could not have crossed the dry biomes of
Caatinga and Cerrado without a forest corridor, then
Miocene introgressions of freshwater (e.g., Pebas, or Acre
Systems) could have played a role in the arboreal diversificat-
ion of mammals, as has been suggested for Chaetomys (
Vilela
et al. 2009
)andothervertebrates(Martini et al. 2007;
Pellegrino et al. 2011; Fouquet et al. 2012). As this pattern is
not well documented in mammalian lineages (but see
Costa
2003
and Costa and Leite 2012), additional comparisons with
phylogenetic, biogeographical and geological results will offer
a better understanding of isolation processes in this area
through the Miocene.
TheroleoftheNorthernAndesasabarrierbetweenthe
lowland rainforests of the Choc
o and Orinoco watersheds,
and those of the Amazon Basin are overlooked in all current
biogeographical models. Since the late Miocene, Andean or-
ogeny has been an active force in major faunal separation
between these areas (
Cracraft and Prum 1988; Ron 2000;
Delsuc et al. 2004; Hoorn et al. 2010; Patterson and Costa
2012
; Patterson et al. 2012). This mountain uplift has led to:
(1) cis- (eastern slope) and trans-Andean (eastern-to-western
slope) vicariant separations of several mammalian groups
(
Ron 2000; Patterson and Costa 2012); and, (2) south-to-
north divergences between the Amazon Basin and Orinoco
watershed. At least five echimyid genera are now endemic to
the Northern Andes, including Olallamys, Hoplomys and
Diplomys in trans-Andean Choc
o rainforest and Central
America, and Pattonomys and Santamartamys in cis-
Andean north of the Cassiquiare canals (we exclude
Amazonian Pattonomys occasius, a species pending revision;
Emmons LH and Fabre P-H, personal communication). The
trans-Andean regions include the basins between the separ-
ate branches of the northern Andes, the lowland Pacific
coastal region, the very wet Choc
o forest, and the extension
of that biome into southern Central America—the barriers
between which may have encouraged alternating events of
vicariance and dispersal for echimyids.
The picture of phylogenetic, ecomorphological and bio-
geographical evolution of echimyids is complicated by
Capromyidae, the family comprising several extinct and ex-
tant genera of hutias endemically distributed in the West
Indies (
D
avalos and Turvey 2012). Capromyids also display
various life history traits and adaptations, including terrestrial,
scansorial and arboreal taxa. Because capromyids have been
considered as a distinct family closely related to echimyids
(
Woods and Kilpatrick, 2005; Upham and Patterson 2012), or
even nested within a paraphyletic echimyid assemblage
(
Galewski et al. 2005; Upham and Patterson 2012, 2015;
Fabre, Galewski et al. 2013, Fabre et al. 2014), taxa from
both families should be sampled to understand the evolution
of these taxa.
Beyond biogeographical patterns, the Echimyidae have
been the focus of recent taxonomic debates (see
Carvalho
and Salles 2004
; Emmons 2005; Patton et al. 2015 for an
overview). Pioneering taxonomies were primarily based on
external characters and teeth occlusal patterns that are
now considered homoplasic (
Candela and Rasia 2012; Fabre
et al. 2013
). Recent molecular studies (Lara et al. 1996; Leite
and Patton 2002
; Galewski et al. 2005; Fabre et al. 2013;
Upham et al. 2013) have indicated that the terrestrial spiny
rats Proechimys and Trinomys, long considered congeneric,
belong to different e chimyid clades and are not closely
related, despite overall morphological similarities. Within
the main arboreal clade, there is a lack of phylogenetic signal
at deeper nodes so that many basal relationships remain
unresolved (
Galewski et al. 2005; Fabre, Galewski, et al.
2013
; Upham et al. 2013). The sampling of new molecular
markers, as well as hitherto unsequenced genera (Carterodon,
Callistomys, Diplomys, Pattonomys, Santamartamys)there-
fore promises to enhance our understanding of echimyid
systematics and biogeographic history (
Upham and
Patterson 2015
).
Theriseofnext-generationDNAsequencing(NGS)meth-
ods (e.g., Illumina;
Meyer et al. 2008) has made access to
mitochondrial (mito) genomes and nuclear genes from fresh
tissues readily available, and in an increasingly time- and cost-
effective manner for museum skins (
Rowe et al. 2011;
Guschanski et al. 2013). High-throughput sequencing meth-
odologies have for example increased the number of available
complete mitogenomes of mammals (
Horner et al. 2007;
Horn et al. 2011; Fabre, Jønsson, et al. 2013), including two
recent studies on Caviomorpha, the lineage of South
American rodents to which echimyids belong (
Tomasco
et al. 2011
; Vilela et al. 2013). Moreover, the availability of
probabilistic mixture models of sequence evolution (
Lartillot
2004
; Lartillot et al. 2007) allow us to maximally extract phylo-
genetic information from mitochondrial sequences, nuclear
genes, and a combination thereof.
Here, we used an Illumina shotgun sequencing approach
(
Tilak et al. 2015) to obtain 38 new mitogenomes of
Echimyidae (including members of the Capromyidae and
Myocastorinae) and up to five slower-evolving nuclear exons
from key taxa. Our approach has, for example, generated the
first complete mitogenomes from rare museum specimens of
endemic species in the genera Santamartamys, Olallamys,
and Mesocapromys. After combining these newly sequenced
mitogenomes and nuclear markers with publically available
sequences, we used model-based approaches (maximum like-
lihood, Bayesian inference ) to infer the ph ylogeny of
Echimyidae þ Capromyidae and to estimate a timeframe
for their diversification. Then we explored their Neogene evo-
lutionary history addressing the following questions:
Mitogenomic Phylogeny, Diversification, and Biogeography of South American Spiny Rats
.
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(1) Does the addition of new mitogenomic and nuclear
gene data, plus enhanced sampling of arboreal taxa, help to
improve the node support of the higher level echimyid and
capromyid phylogeny? (2) What has been the timeframe of
the Echimyidae þ Ca promyidae diversification? (3) To what
extent are geo-climatic historical events reflected in the high-
er level composition of echimyid communities within
Neotropical biomes?
Materials and Methods
Taxonomic Sampling
We sampled all 26 extant genera (Emmons 2005; Woods and
Kilpatrick 2005
) in the clade composed of Echimyidae (23/23;
including Myocastorinae) and Capromyidae (5/5). Biological
samples were obtained of both museum and fresh tissue
collections from the American Museum of Natural History
(AMNH: New York, NY), the Field Museum of Natural History
(FMNH: Chicago, IL), the Museum of Comparative Zoology
(MCZ: Cambridge, MA), the Museum of Vertebrate Zoology,
University of California (MVZ: Berkeley, CA), the U.S. National
Museum of Natural History (USNM-S mithsonia n:
Washington DC), the Nationaal Natuurhistorisch Museum
(Naturalis: Leiden, The Netherlands), the Royal Ontario
Museum (ROM: Toronto, Canada), the Universidade
Federal do Espirito Santo—Animal Tissue Collection (UFES-
CTA: Vit
oria, Brazil) and the University of Montpellier (UM-
ISEM: Montpellier, FR) (see
supplementary table S1,
Supplementary Material online). In total, we obtained com-
plete mitogenomes for 38 taxa spanning all extant members
of Echimyidae and Capromyidae. In addition, we searched
NCBI (see also
supplementary table S1, Supplementary
Material
online) for mitogenomic and nuclear sequences
documented by voucher specimens. We incorporated repre-
sentatives of the octodontoid families Ctenomyidae and
Octodontidae, their closest Caviomorpha relatives (Upham
and Patterson, 2015
), to serve as outgroups. We also included
one member of the families Caviidae, Erethizontidae, and
Chinchillidae, to represent the other three superfamilies of
caviomorphs, as more distant outgroups to stabilize the
Octodontoidea relationships.
Sequencing and Assembly of Complete Mitochondrial
Genomes
Eleven museum skin samples were stored in Eppendorf tubes,
a subset of which was processed in the “Degraded DNA”
facility of the University of Montpellier, France (dedicated
to processing low quality/quantity DNA tissue samples).
Alcohol-preserved samples of fresh tissues were available for
27 other taxa (
table 1 and supplementary table S1,
Supplementary Material online); the DNA from these sam-
ples was extracted in a dedicated room of the laboratory to
reduce contamination risks. An additional DNA extract of
Santamartamys rufodorsalis was included in the preparation
of genomic libraries, derived using methods described in
Upham et al. (2013). DNA was extracted using the DNeasy
Blood and Tissue Kit (Qiagen) following the manufacturer’s
instructions, with a final elution in water. The 11 oldest
samples were extracted in small batches (of 3 samples max-
imum),andanegativecontrolwasincludedineachbatchto
monitor possible contamination. The DNA was fragmented
by sonication using an ultrasonic cleaning unit (Elmasonic).
The 3
0
-ends of the obtained fragments were then repaired
anddouble-strandfilledbeforebeingligatedwithadaptors
and tagged according to a cost-effective protocol for Illumina
library preparation (
MeyerandKircher2010; Tilak et al. 2015).
Tagged DNA libraries were pooled and sequenced as single
end reads on Illumina HiSeq 2000 lanes at the GATC–Biotech
company (Konstanz, Germany).
Raw 101-nt reads were imported in Geneious R6 (
Kearse
et al. 2012
) and adaptor fragments were removed by the “trim
ends” utility. Then, a mapping of the reads on the phylogen-
etically closest available mitochondrial genome was per-
formed for each species. The following mapping parameters
were used in the Geneious read mapper: a minimum of 24
consecutive nucleotides (nt) perfectly matching the refer-
ence, a maximum 5% of single nt mismatch over the read
length, a minimum of 95%-nt similarity in overlap region, and
a maximum of 3 % of gaps with a maximum gap size of 3-nt.
Iterative mapping cycles were performed in order to elongate
the sequence until recovery of the complete mitogenome. A
high-quality consensus was generated and the circularity of
the mitogenome was verified by the exact 100-nt sequence
superimposition at the assembly extremities. The number of
satellite repeats in the control region remained underesti-
mated, as there were Illumina reads consisting entirely of
repeats, making it difficult to determine the exact copy num-
ber. New mitochondrial genomes are available under acces-
sion numbers KU762015, and KU892752 to KU892788.
Sequencing and Assembly of Nuclear Markers
To complement the mitochondrial information with nuclear
DNA markers, we used the protocol of Fabre et al. (2014:cf.,
Supplementary Methods intheDataSupplement,
Supplementary Material online) to capture five partial nuclear
exons for Carterodon and Callistomys (apoB, GHR, IRBP, RAG1,
vWF). In brief, nine primer sets from the literature were used
to amplify nuclear DNA baits from modern genomic extracts
of Caprom ys pilorides. Bait amplicons were sheared into
300–500 bp fragments. All purified amplicons were built
into blunt-end libraries. Captured libraries were amplified be-
fore being pooled equimolarly and sequenced on one lane of
a Illumina MiSeq (50 bp) single-read run. Another capture
using just the nuclear DNA baits was also sequenced on one
lane of a HiSeq2000 run. Newly acquired nuclear exons were
combined with previously published ones (
Fabre et al. 2014).
With the exception of two taxa (Lonchothrix emiliae and
Santamartamys rufodorsalis), we obtained nuclear gene se-
quences for all examined species. New nuclear exons are
available under accessions KY303652 to KY303660.
DNA and Protein Supermatrices
We compared our newly obtained mitogenomes and nu-
clear data with sequences available from public databases
(
Lara et al. 1996; Lara and Patton 2000; Leite and Patton
2002; Galewski et al. 2005; Patterson and Velazco 2008;
Fabre et al.
.
doi:10.1093/molbev/msw261 MBE
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Meredith et al. 2011; Fabre, Galewski, et al. 2013; Upham
et al. 2013
). Complete mitogenomes and nuclear exons
were aligned with MUSCLE (
Edgar 2004), as implemented
in S
EAVIEW v4.5.2 (
Gouy et al. 2010),andwithMACSE version
1.01b (
Ranwez et al. 2011). Ambiguous regions of the align-
ments were cleaned with trimAl version 1.4 (
Capella-
Gutie´rrez et al. 2009
).
We combined the mitochondrial and nuclear sequences
into three DNA supermatrices: (1) the complete mitoge-
nomes (47 taxa and 15,896 sites; 0.7% of missing character
states, i.e., calculated on the taxon x site basis), (2) the con-
catenated nuclear exons (45 taxa and 5,415 sites, 32% of
missing character states), and (3) the complete mitogenomes
combined with nuclear exons that maximize our character
sampling (47 taxa and 21,311 sites; 11% of missing character
states). We also concatenated the 13 mitochondrial and 5
nuclear protein-coding genes translated into amino acid (AA)
sequences in a super-protein dataset (47 taxa and 5,614 sites,
partition “AA”; 15% of missing character states).
Phylogenetic Analyses
Individual gene trees for the 13 mitochondrial protein-coding
genes and the 5 nuclear exons were built using maximum
likelihood (ML) with parameters and topologies estimated
Table 1. List of the Species Treated in This Study and GenBank Accession Numbers of Sequences.
Taxa Collection Tissue_number Publication Accession mitogenome Tissues
Ctenomys rionegrensis ——
Tomasco et al. (2011) HM544130.1 Fresh tissue
Octodon degus ——
Tomasco et al. (2011) HM544134.1 Fresh tissue
Spalacopus cyanus ——
Tomasco et al. (2011) HM544133.1 Fresh tissue
Tympanoctomys barrerae ——
Tomasco et al. (2011) HM544132.1 Fresh tissue
Proechimys longicaudatus ——
Tomasco et al. (2011) HM544128.1 Fresh tissue
Trinomys dimidiatus ——
Voloch et al. (2013) JX312694.1 Fresh tissue
Callistomys pictus UFES-CTA RM-233 This paper KU892754 Fresh tissue
Capromys pilorides MVZ Mammals MVZ-191417 This paper KU892766 Fresh tissue
Carterodon sulcidens UFES-CTA LGA-735 This paper KU892752 Fresh tissue
Clyomys laticeps UFES-CTA MCNM-2009 This paper KU892753 Fresh tissue
Dactylomys dactylinus UFES-CTA UFROM-339 This paper KU762015 Fresh tissue
Diplomys labilis USNM-Smithsonian USNM-335742 This paper KU892776 Dry study skin
Echimys chrysurus UM-ISEM T-3835 This paper KU892781 Fresh tissue
Euryzygomatomys spinosus UFES-CTA CTA-1028 (YL-53) This paper KU892755 Fresh tissue
Geocapromys browni Naturalis-Leiden ZMA.MAM.23884 This paper KU892767 Dry study skin
Geocapromys ingrahami USNM-Smithsonian USNM-395696 This paper KU892768 Dry study skin
Hoplomys gymnurus MVZ Mammals MVZ-225082 This paper KU892779 Fresh tissue
Isothrix sinnamariensis UM-ISEM T-4377 This paper KU892785 Fresh tissue
Kannabateomys amblyonyx UFES-CTA MBML-3001 This paper KU892775 Fresh tissue
Lonchothrix emiliae FMNH FMNH 140821 This paper KU892786 Dry study skin
Makalata didelphoides UM-ISEM T-5023 This paper KU892782 Fresh tissue
Mesocapromys melanurus MCZ-Harvard MCZ-34406 This paper KU892769 Dry study skin
Mesomys hispidus UM-ISEM T-6523 This paper KU892787 Fresh tissue
Mesomys stimulax Naturalis-Leiden RMNH.MAM.21728 This paper KU892788 Dry study skin
Myocastor coypu UM-ISEM T-0245 This paper KU892780 Fresh tissue
Mysateles prehensilis gundlachi MCZ-Harvard MCZ-17090 This paper KU892770 Dry study skin
Olallamys albicauda USNM-Smithsonian USNM-241343 This paper KU892774 Dry study skin
Pattonomys carrikeri ROM ROM-107955 This paper KU892783 Fresh tissue
Phyllomys blainvillii UFES-CTA CTA-1205 This paper KU892756 Fresh tissue
Phyllomys dasythrix UFES-CTA AC-628 This paper KU892757 Fresh tissue
Phyllomys lundi UFES-CTA CTA-881 This paper KU892758 Fresh tissue
Phyllomys mantiqueirensis UFES-CTA CTA-912 This paper KU892759 Fresh tissue
Phyllomys pattoni UFES-CTA CTA-984 This paper KU892760 Fresh tissue
Plagiodontia aedium Naturalis-Leiden RMNH.MAM.3865 This paper KU892771 Dry study skin
Proechimys cuvieri UM-ISEM T-5765 This paper KU892778 Fresh tissue
Proechimys roberti UFES-CTA CTA-1524 This paper KU892772 Fresh tissue
Santamartamys rufodorsalis AMNH AMNH-34392 This paper KU892777 Dry study skin
Thrichomys apereoides MVZ Mammals MVZ-197573 This paper KU892773 Fresh tissue
Toromys grandis FMNH FMNH 92198 This paper KU892784 Dry study skin
Trinomys albispinus UFES-CTA AL-3054 This paper KU892761 Fresh tissue
Trinomys iheringi UFES-CTA ROD-156 This paper KU892762 Fresh tissue
Trinomys paratus UFES-CTA CTA-588 This paper KU892763 Fresh tissue
Trinomys setosus UFES-CTA YL-710 This paper KU892764 Fresh tissue
Trinomys yonenagae UFES-CTA PEU-880027 This paper KU892765 Fresh tissue
NOTE.—Voucher numbers of the newly sequenced taxa used in this study are given in gray shades. AMNH, American Museum of Natural History, New York, NY; FMNH, Field
Museum of Natural History, Chicago, IL; MCZ, Museum of Comparative Zoology, Harvard University, Cambridge, MA; MVZ, Museum of Vertebrate Zoology, Berkeley, CA;
Naturalis, Nationaal Natuurhistorisch Museum, Leiden, The Netherlands; ROM, Royal Ontario Museum, Toronto, Ontario, Canada; UFES-CTA, Animal Tissue Collec tion,
Universidade Federal do Esp
ırito Santo, Brazil; UM, University of Montpe llier collections, Montpellier, France; USNM, National Museum of Natural History, Smithsonian
Institution, Washington, DC. Most of these samples are vouchered and archived in accessible collections. Additional information could be retrieved via the following database
webpages: http://vertnet.org/.
Mitogenomic Phylogeny, Diversification, and Biogeography of South American Spiny Rats
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doi:10.1093/molbev/msw261 MBE
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