Journal of Mammalogy, 96(4):690–702, 2015
DOI:10.1093/jmammal/gyv077
Genetic diversity in Xenarthra and its relevance to patterns of neotropical
biodiversity
Nadia Moraes-Barros and Maria Clara Arteaga*
Cibo-InBio Laboratório Associado, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, R.
Padre Armando Quintas, 4485–661 Vairão, Portugal (NM-B)
Laboratório de Biologia Evolutiva e Conservação de Vertebrados (LABEC), Departamento de Genética e Biologia Evolutiva,
Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 277, Cidade Universitária, São Paulo, São Paulo 05508-090,
Brazil (NM-B)
Departamento de Biología de la Conservación, Centro de Investigación Científica y de Educación Superior de Ensenada
(CICESE), Carretera Ensenada-Tijuana 3918, C.P. 22860, Baja California, México (MCA)
* Correspondent: [email protected]
Here, we review population genetic, phylogeographic, and phylogenetic studies on xenarthrans and show how
this information fits in current discussions about patterns of diversification within the Neotropics. Specifically,
we focus on how the genetic diversity of xenarthrans has been shaped by important historical processes such as
Andean uplift, the Great American Biotic Interchange, and fluctuating linkages between the Amazon and Atlantic
forests. We also describe latitudinal patterns of differentiation within the Atlantic forest and discuss how these
might have been generated. Even with the modest amount of information currently available, our comparative
analyses indicate 3 things: the Andes may have promoted events of intraspecific divergence for at least 2 xenarthran
species; the biogeographic history of the Neotropical rain forests influenced the divergence of clades in sloths; and
inter- and intra-specific genetic patterns reveal a very high diversity in xenarthrans, probably higher than currently
recognized from morphological data. Finally, we highlight Xenarthra as an appropriate model for investigating
biogeographic patterns in the Neotropics and also point to additional directions to be taken in future studies of this
unique mammal group.
Revisamos los estudios realizados sobre genética de poblaciones, filogeografía y filogenia de los Xenarthra y
mostramos como la información generada se ajusta a la discusión actual acerca de los patrones de diversificación
en el Neotrópico. Enfocamos nuestro análisis en la influencia de 4 eventos pasados importantes relacionados con la
dinámica del paisaje Neotropical y la diversificación de la fauna, sobre la diversidad genética de los Xenarthra; estos
son el levantamiento de los Andes, el gran intercambio de fauna del Pleistoceno, la relación entre el bosque Amazónico
y el bosque Atlántico y los patrones latitudinales de diferenciación en el bosque Atlántico. Aunque la información
disponible aún es escasa, nuestro análisis comparativo indica que los Andes pudieron haber promovido eventos
de diversificación intraespecífica, al menos en 2 especies de Xenarthra; que la historia biogeográfica del bosque
húmedo Neotropical tuvo influencia sobre la divergencia de linajes de perezosos; y que los patrones genéticos intra
e interespecíficos revelan una gran diversidad en Xenarthra, probablemente mayor que la actualmente reconocida
con datos morfológicos. Finalmente, resaltamos a los Xenarthra como un modelo apropiado para investigar patrones
biogeográficos en el Neotrópico y sugerimos líneas adicionales a considerarse en futuros estudios sobre este grupo
único de mamíferos.
Key words: Andes, Cingulata, evolutionary lineages, Neotropical rain forests, Pilosa
© 2015 American Society of Mammalogists, www.mammalogy.org
Members of Xenarthra are classified in the orders Cingulata
(armadillos, Dasypodidae) and Pilosa (anteaters, Vermilingua;
sloths, Folivora), and consist of 31 extant species (Gardner
2005). The monophyly of Xenarthra, as well as its contained
orders, is well supported by both molecular and morphological
data (Engelmann 1985; de Jong 1998; Delsuc et al. 2001, 2002,
2004). Considered one of the older placental lineages (Morgan
et al. 2013; O’Leary et al. 2013; Romiguier et al. 2013),
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SPECIAL FEATURE—XENARTHRAN GENETIC DIVERSITY AND PATTERNS691
xenarthrans emerged about 100 million years ago (mya—
Delsuc et al. 2004; Murphy et al. 2007) and were once hugely
diverse, with approximately 218 genera recognized (McKenna
and Bell 1997). However, as occurred with many other mammalian groups, the majority of xenarthrans became extinct by
the end of the Pleistocene.
Xenarthrans present several characteristics that together
make them a good model for studying the historical processes associated with spatial patterns of phylogenetic lineages in the Neotropics. First, they are the only group of
mammals to evolve exclusively in the New World. Coupled
with the fact that Xenarthra is presumed to have emerged
approximately 100 mya (Delsuc et al. 2004; Murphy et al.
2007), one might assume that patterns of genetic diversity
in xenarthrans will be intimately linked with the biogeographic events that shaped the Neotropics. Some current
evidence supports this view. For example, molecular dating
of divergence times among the main clades of xenarthrans,
extant genera, and even species matches well with periods
of climatic variation and tectonic phases, such as uplift of
the Andes, since Paleocene to early Pliocene (66 to 5 mya—
Delsuc et al. 2004; Hoorn et al. 2010).
Xenarthrans also show great diversity in habitat preferences,
ranging from strictly arboreal species to fossorial ones. In addition, these species occur along a gradient from dry and open
environments to moist forests. Within Cingulata are species
whose habitats are among the most specialized, as reflected by
their small range size (Table 1). Among Pilosa, all sloth species
and the pygmy anteater (Cyclopes didactylus) are restricted to
forested habitats (Table 1). Sloths and pygmy anteaters, along
with the cingulate Dasypus kappleri, are good models for
investigating phylogeographic patterns within Neotropical forest biomes (Moraes-Barros et al. 2006, 2007; Lara-Ruiz et al.
2008), in part because they are sympatric throughout large
portions of these biomes. Thus, the finding of consistent patterns across species may indicate the influence of widespread
biogeographical events, with potentially important insights
into controversial topics such as mammalian speciation within
Amazonia, and historical fragmentation within the Atlantic forest (Patterson and Costa 2012).
One of the more conspicuous events that shaped the fauna of
the Neotropics over the last several million years was the Great
American Biotic Interchange, a wave of migration of fauna and
flora between North American and South American continents
that occurred after the uprise of the volcanic Isthmus of Panama
(Marshall et al. 1982). Although the Isthmus of Panama fully
separated the Caribbean Sea and Pacific Ocean about 3 mya,
its formation began earlier and seems to be associated to the
northern Andean uplift, around 24 mya (Farris et al. 2011).
Throughout most of the Tertiary, Xenarthra, together with
marsupials and “archaic” ungulates, inhabited South America.
They radiated in an enormous diversity of forms during a long
period of “splendid isolation” (Simpson 1980) when the continent was an island, separated from North America by an open
seaway. Subsequently, the complete emergence of the Isthmus
of Panama during the Pliocene allowed for amazing dispersal
events in which mammals from North America moved south
and mammals from South America moved north (Marshall
et al. 1982; Coates et al. 2004—for a complete review and
deeper discussion on inferred times and implications on biodiversity, see Coates and Stallard 2013; Bagley and Johnson
2014). During this time, Xenarthra was one of the most important groups that spread north into Central and North America
(Webb 1976). Thus, we can expect that studies of genetic diversity within these northward-moving species will allow reconstruction of the history of colonization, i.e., a phylogeographic
analysis.
In general, phylogeographic studies can provide important information about the linkages between demography and
split events (at multiple taxonomic levels), thus furthering
our understanding of the evolution of certain lineages (Avise
2000). Unfortunately, there are a limited number of phylogeographic studies on Xenarthra. For instance, only 2 of the 21
cingulate species have been examined in sufficient detail to
provide representative sampling of significant parts of their
distribution: the nine-banded armadillo, Dasypus novemcinctus (Arteaga et al. 2012), and the large hairy armadillo,
Chaetophractus villosus (Poljak et al. 2010). However, other
studies that focus on molecular phylogenies (Barros et al.
2003; Moraes-Barros et al. 2011) or the population genetics of xenarthrans have been accumulating over the past few
years (Huchon et al. 1999; Frutos and Van Den Bussche 2002;
Collevatti et al. 2007; Moss et al. 2012). Together, the results
from such analyses can provide useful information on how historical processes have shaped current patterns of genetic diversity within Xenarthra.
Here, we present a review of phylogeographic, phylogenetic,
and population genetic studies that have been published on
xenarthrans (Supporting Information S1). We relate the findings to biogeographic patterns well known for other mammals (Patterson and Costa 2012). We include studies of both
intra- and inter-specific genetic variation and focus specifically
on the following 4 issues: the link between Andean uplift and
xenarthran diversification events; patterns of genetic variation
resulting from colonization of Central America after closing of
the Isthmus of Panama; the way patterns of genetic variation in
species that exclusively use forest habitats reflect the historical
bridge between the Amazon and the Atlantic forests; and patterns of latitudinal divergence in the genetic makeup of species occupying the Brazilian Atlantic forest. To more precisely
understand the timing of xenarthran diversification relative to
these various events, we also present new data and analyses
related to the molecular phylogeny and timing of divergence
for 3 species of Xenarthra (see Supporting Informations S1 and
S2 for details).
Andean Uplift
Xenarthrans began to diversify 65 mya, before the 1st major
Andean uplift (around 45 mya—Delsuc and Douzery 2008;
Hoorn et al. 2010). The synchronous nature of subsequent
diversification among independent xenarthran lineages is well
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Table 1.—Overview of xenarthrans with description of their geographical distribution and habitats. All species except B. pygmaeus occur in
South America. Some also are found in Central America (CA), and a few reach northern Central America (NCA) and North America (NA), in
the southern United States. Five species occur on both sides of the northern Andes (cross-Andean species); 6 species are limited to either the
west or east side of the northern Andean mountain range. For species found exclusively in forests, AF = Atlantic forest, AMZ = Amazon forest,
CAF = Central American forests, M = mangroves of the island Escudo de Veraguas, and PY = Peruvian Yungas; for species occupying nonforested environments, D = dry or xeric environment, HG = high-altitude grasslands, and OS = open or shrubland habitats. Endemic species and
those restricted to very narrow ranges (<100,000 km2) are indicated by superscripts. Data compiled from Abba and Superina (2010) and Superina
et al. (2010a, 2010b).
Distribution
Cross- Andes
One side of Andes
West
East
species
Order, suborder
Part of range not in
South America
Bradypus variegatus
Choloepus hoffmanni
Cyclopes didactylus
Myrmecophaga tridactyla
Dasypus novemcinctus
Pilosa, Folivora
Pilosa, Folivora
Pilosa, Vermilingua
Pilosa, Vermilingua
Cingulata
CA
CA
NCA
CA
NA
Tamandua mexicana
Cabassous centralis
Choloepus didactylus
Tamandua tetradactyla
Cabassous unicinctus
Priodontes maximus
Bradypus pygmaeusa,b
Bradypus torquatusa,b
Bradypus tridactylus
Cabassous chacoensis
Cabassous tatouay
Calyptophractus retusus
Chaetophractus nationic
Chaetophractus vellerosus
Chaetophractus villosusc
Chlamyphorus truncatusa
Dasypus hybridus
Dasypus kappleri
Dasypus pilosusa,b
Dasypus sabanicola
Dasypus septemcinctus
Dasypus yepesia,b
Euphractus sexcinctus
Tolypeutes matacus
Tolypeutes tricinctus
Zaedyus pichiyc
Pilosa, Vermilingua
Cingulata
Pilosa, Folivora
Pilosa, Vermilingua
Cingulata
Cingulata
Pilosa, Folivora
Pilosa, Folivora
Pilosa, Folivora
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
Cingulata
NCA
NCA
Habitat
Exclusively in forests
CAF
AMZ
×
×
×
×
×
×
Not in forests
Generalists
AF
×
×
×
×
×
×
×
×
×
×
CA
M
×
×
D
×
D
HG
D
×
D
×
×
PY
OS
×
×
×
D
D
D
Endemic species.
Area of occurrence narrow (<100,000 km2).
c
Occurs on both sides of the Andes, but restricted to the southern region.
a
b
established and assumed to reflect common responses to major
tectonic and climatic events. According to Delsuc et al. (2004),
the Andean tectonic crisis can be linked to 3 distinct evolutionary events within Xenarthra: the diversification of anteaters and
armadillos in the Eocene; the radiation of modern sloth lineages and Tolypeutinae in the early Miocene; and the diversification of living Euphractine armadillos and the split between
long-nosed armadillos (Dasypus) in the late Miocene (around
7 mya), when a significant increase in the height of the Andes
occurred.
Andean uplift and associated changes in climate and landscape had a very profound impact not only on xenarthran diversity but also on much of the biodiversity of South America.
Episodes of tectonic uplift during the Cenozoic led to an
increase in elevation of the Andes and subsequent modifications
in atmospheric circulation, which in turn led to major changes
in habitats and climatic conditions, thus shaping faunal and floral assemblages (Pascual and Ortiz Jaureguizar 1990; Marshall
and Sempere 1993; Hoorn et al. 2010). In addition, the Andean
mountain range itself may have become a significant physical and climatic barrier to species that were once evenly distributed throughout northwestern South America (Lessa et al.
2003; Miller et al. 2008; Hoorn et al. 2010; Rull 2011). Such a
scenario may apply to 2 pairs of congeneric species, the anteaters Tamandua mexicana and T. tetradactyla and the armadillos
Cabassous centralis and C. unicinctus; both pairs of species
have their distributions limited by the Andes. These species
may be good models for testing the hypothesis of the Andes
SPECIAL FEATURE—XENARTHRAN GENETIC DIVERSITY AND PATTERNS693
as promoting isolation and speciation. However, at present, the
phylogenetic relationships between the 2 Tamandua species
and between the 2 Cabassous species have not been investigated, and there are no data available on the molecular diversity
of these species. Still, in each instance, 1 species is restricted to
the west side of the Andes and the other to the east (Table 1—
see also Abba and Superina 2010; Superina et al. 2010a). The
2 anteaters have distinct morphological characteristics and are
believed to have speciated after isolation on the 2 sides of the
Andes (Wetzel 1975). Likewise, although C. centralis is closely
related to C. unicinctus, the Andes appear to form a partial, but
probably not absolute, barrier between the 2 (Wetzel 1985).
Data from 5 other xenarthrans that occur on both sides of the
northern Andes (Bradypus variegatus, Choloepus hoffmanni,
C. didactylus, D. novemcinctus, and Myrmecophaga tridactyla;
Table 1) provide further support for the view of Andean uplift
as a major influence on intraspecific diversification. All 5 species contain subspecies restricted to 1 side of the Andes or the
other (Supporting Information S3). Thus, these subspecies may
represent differentiation events, triggered by isolation due to
Andean uplift. However, such an assertion must remain tentative until conclusive genetic and morphological studies are
completed.
What data are available do provide some support for the
hypothesis that Andean uplift has led to diversification of xenarthrans. D. novemcinctus is the only armadillo distributed on
both sides of the northern Andes. Gardner (2008) recognizes 4
subspecies for Central and South America, with 2 confined to
the west side of the Andes. A molecular phylogenetic analysis
encompassing previously published and new data also identified
4 lineages for D. novemcinctus in Central and South America,
but they were not quite the same as previous subspecies designations. One lineage was distributed on the east side of the
Andes and a 2nd well to the east in French Guiana (Loughry and
McDonough 2013:166–167, figure 7.2); the remaining 2 were
west of the Andean range in Colombia and in Central and North
America, respectively (Arteaga et al. 2012). Finally, a study of
diversity and genetic structure of D. novemcinctus populations
from the grassy plains (llanos) of Colombia, east of the Andes,
found that the haplotypes present there represent a divergent
clade from a previously studied population in the western
Andes of Colombia (Caballero et al. 2013). Collectively then,
molecular data suggest that the Andes are a boundary for lineages of D. novemcinctus. However, divergence times among
lineages have not been determined, and it is not known whether
there is any genetic connectivity across the Andes.
The brown-throated sloth, B. variegatus, is a wide-ranging
and highly variable species whose morphological diversity is
not clearly understood (Anderson and Handley 2001; Hautier
et al. 2014). Seven subspecies are recognized, with 2 restricted
to the west side of the Andes (Gardner 2008; Hayssen 2010;
Supporting Information S3). Genetic variation of B. variegatus
was explored using several nuclear and mitochondrial genes
(Moraes et al. 2002; Moraes-Barros et al. 2006, 2007, 2011).
A molecular phylogeny for the group suggests the existence of
distinct evolutionary lineages within the species, but because
only samples from South America (east of the Andes) were
included in those studies, that has not yet been conclusively
shown (Moraes-Barros et al. 2011).
The two-toed Hoffman’s sloth, C. hoffmanni, is represented by
2 disjunct populations. The northern one is restricted to Central
America and South America west of the Andes, whereas the
southern population occurs in the western Amazon, east of the
Andes. Five subspecies are described (Supporting Information
S3), and karyotypic analysis indicates a huge variation within
the genus (2N = 49 to 2N = 65), with chromosomal number
of C. hoffmanni ranging from 2N = 49 to 2N = 53 and that of
C. didactylus varying between 2N = 52 and 2N = 65 (Svartman
2012). No phylogeographic or population genetic studies of this
species have been conducted. Karyotypic and molecular differentiation of C. hoffmanni and C. didactylus suggest the existence of 2 phylogenetic lineages within C. hoffmanni (Steiner
et al. 2010), but because most of the individuals sampled in that
study could not be attributed to a specific geographical locality,
there is no current evidence that the 2 lineages actually represent a western and eastern population.
There are 3 other xenarthran species, all cingulates, occurring on both sides of the Andes but restricted to the central
and southern mountain range (Table 1). The armadillos C. villosus and Zaedyus pichiy are distributed across both sides of
the southern and south-central Andes, respectively. C. villosus
occurs from sea level to 1,500 m above sea level (asl), but it is
found west of the Andes only at the southern limit of its distribution. It is a monotypic species and, although its phylogeography has been studied, the authors only analyzed individuals
from east of the Andes, within Argentina (Poljak et al. 2010).
The results indicate a major differentiation between northern
and southern populations and a pattern of contiguous range
expansion towards south and east. Z. pichiy is found at 2,500
m asl (Gardner 2008). No population genetic or phylogeographic studies have been published for this species. It does
have 2 morphologically distinct subspecies (Z. p. pichiy and
Z. p. caurinus, the latter being smaller with a shorter rostrum—
Gardner 2008), but they are not geographically isolated by the
Andes. C. nationi is the 3rd armadillo occurring on both sides
of the central Andes; the species is restricted to high elevations
(2,400–4,000 m asl—Abba and Superina 2010). However, its
taxonomic status is now uncertain as the analyses of Abba
et al. (2015 indicate it may be a high elevation variant of C.
vellerosus. Although it may seem that these 3 species are not
good models in which to examine the effect of Andean uplift
on patterns of diversification, genetic analyses may provide
some insights. For example, a detailed phylogeographic study
of Z. pichiy might reveal the possible influence of Andean uplift
in promoting diversification of the subspecies Z. p. caurinus as
a result of its restriction to high elevations. Similarly, a detailed
study of phylogenetic relationships among species within
Chaetophractus and Dasypus would help understand the role of
the Andes in the diversification of species restricted to medium
to high elevations, such as D. yepesi, D. pilosus, and C. nationi.
The available data for xenarthrans do not allow us to fully
test the hypothesis that divergence processes were associated
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with isolation due to Andean uplift. Nevertheless, a congruent
pattern of intraspecific diversification among distinct crossAndean species, both in time and space, may reflect a possible association with the mountain range. Along this line, we
present an analysis of previously published and new genetic
data for sloths, using representatives from the west and east of
Andes, in a molecular phylogenetic approach (see Supporting
Informations S1 and S2 for methodological details).
New data on molecular phylogeny of sloths.—We analyzed
previously published molecular data with newly generated
DNA sequences for the sloths B. variegatus and C. hoffmanni
(see Supporting Informations S1 and S2). We observed a
congruent pattern of divergence among lineages within each
species for both methods used. The B. variegatus phylogeny,
based on representatives from the same localities described in
Moraes-Barros et al. (2011) plus new localities from the west
side of the Andes and Central America, confirms the high diversity of evolutionary lineages and indicates 2 more highly divergent lineages that are found only on the west side of the Andes
(Figs. 1 and 2a; Supporting Information S4a). For C. hoffmanni,
we obtained 2 lineages, 1 for localities in Central America and
South America and the other for localities in South America
east of the Andes (Figs. 1 and 2b; Supporting Information S4b).
For both species of sloths, these data indicate a marked divergence between samples from the west and east side of the Andes.
Each lineage also corresponds to a different subspecies (Figs. 1
and 2; Supporting Information S4). Divergence times between
the west and east Andean lineages are also congruent. For both
B. variegatus and C. hoffmanni, the 1st split between the western and eastern lineages is estimated at around 8 mya (about
8.5 and 7.5 mya, respectively). For B. variegatus, a 2nd split is
estimated around 4.6 mya (Fig. 2; Supporting Information S4).
This 2nd split represents the divergence between a lineage from
northern Colombia, in the inter-Andean region, and all other
B. variegatus lineages on the east side of the eastern mountain
range. The 1st split event observed for both C. hoffmanni and
B. variegatus in the late Miocene is coincident with the most
intense Andean mountain building in the western mountain
range of Colombia (Hoorn et al. 2010). At that time, the eastern
Andean mountain range in Colombia was no more than 40%
of its modern elevation. About 5 mya, a rapid uplift resulted
in a significant elevation, which culminated at around 2.7 mya
when it reached its present day elevation (Gregory-Wodzicki
2000). This may explain the 2nd split event observed in B. variegatus between the inter-Andean region and the east Andean
lineages.
Fig. 1.—Spatial location of the 18 samples from Bradypus and Choloepus hoffmanni analyzed for the cytochrome oxidase I gene (white dots:
Bradypus variegatus, black squares: C. hoffmanni, and black triangles: Bradypus torquatus). Numbers in sampling localities correspond to specimens in phylogenetic trees of Fig. 2. Hatched areas represent Neotropical moist broadleaf forests according to Olson et al. (2001).
SPECIAL FEATURE—XENARTHRAN GENETIC DIVERSITY AND PATTERNS695
Fig. 2.—Phylogenetic analysis and divergence times inferred for cross-Andes and forest-dependent xenarthrans. Trees were estimated from
cytochrome oxidase I sequences using both neighbor-joining and Bayesian approaches for a) Bradypus and b) Choloepus hoffmanni; the 2
approaches resulted in similar topologies and inferred divergence times. Branch lengths are proportional to time units. Divergence estimates
obtained after neighbor-joining analysis are indicated in the scale as intervals, according to maximum and minimum values of calibration points
(solid lines = split between west and east Andean lineages; dashed lines = split between northern and southern lineages within the Atlantic forest). Numbers at the nodes indicate bootstrap values from 10,000 replications. Most nodes were supported by maximum posterior probabilities
of Bayesian inferences, except those indicated by symbols: star (), 0.95–0.99; dot (•), ≤0.90. Terminals are identified according to subspecies
(Supporting Information S2). Numbers in parentheses indicate sampling localities shown in Fig. 1. For some C. hoffmanni sequences the subspecies could not be determined because the exact geographic origin of the samples was unknown (indicated by number sign, #). For the C. h. hoffmanni sequence, only the country of origin was known. Previously published DNA sequences are identified with an asterisk (*). See Supporting
Informations S1, S2, and S4 for details on methodology, DNA sequences and individuals analyzed, and Bayesian analysis.
With just a few representatives of such widely distributed
species, and using only 1 mitochondrial gene (cytochrome oxidase c subunit I), the geographic extent of each lineage and
the degree of isolation due to the Andes cannot be determined.
However, the patterns and divergence times observed for both
C. hoffmanni and B. variegatus are congruent with previous
molecular phylogenetic studies on several other vertebrate species. Those studies indicate an association of diversification
events and the last stages of the Andean uplift. For instance,
a west and east divergence was observed for Alouatta (howler
monkeys) lineages (Cortés-Ortiz et al. 2003), woodcreepers of
the genus Dendrocincla (Weir and Price 2011), and moths of the
genus Eois (Strutzenberger and Fielder 2011). Some other studies show a different phylogeographic pattern, indicating crossAndean migration of lowland species that may have occurred
after the Andean uplift (bats—Ditchfield 2000; Hoffmann and
Baker 2003; bees—Dick et al. 2004; birds—Marks et al. 2002;
Miller et al. 2008). However, these events seem to be restricted
to species with superior dispersal capacities. On the other hand,
although we have not observed any shared lineage between
sloths west and east of the Andes, we cannot refute the possibility of cross-Andean migration. There are records for both
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B. variegatus (Costa Rica—Ureña et al. 1986) and C. hoffmanni
(Colombia—Alberico et al. 2000; Moreno 2003; Acevedo and
Sanchez 2007) occurring at high elevations (2,400–3,000 m
asl); moreover, our sampling through the northern Andes was
sparse. Therefore, a wider sampling of both sloth species across
forests of the Andes is needed in order to further evaluate the
extent of isolation promoted by Andean uplift. Likewise, similar studies of the other species of Xenarthra with a cross-Andes
distribution are needed in order to determine how widespread
the impact of Andean uplift was on diversification of lineages
and to identify factors that may have enhanced or ameliorated
those effects.
Great American Biotic Interchange
During the Great American Biotic Interchange, several species of Xenarthra participated in dispersal waves from South
America to North America. Extinct genera of various families
of armadillos, sloths, and anteaters moved into northern regions,
in what is today Mexico and the United States, throughout the
Pleistocene (Shaw and McDonald 1987; McDonald 2002).
Currently, only 8 species of Xenarthra occur outside of South
America. The nine-banded armadillo, D. novemcinctus, was
the only species to reach the southern United States (Taulman
and Robbins 2014). The anteaters T. mexicana and C. didactylus and the armadillo C. centralis are present as far north as
the tropical regions of Mexico, whereas the sloths B. variegatus, C. hoffmanni, and the giant anteater M. tridactyla reach
northern Central America. The pygmy sloth B. pygmaeus is
restricted to Escudo de Veraguas Island off the Atlantic coast of
Panama (Voirin 2015). The isolation of a B. variegatus population on Escudo is presumed to have led to B. pygmaeus speciation (Anderson and Handley 2002). This is the only xenarthran
speciation event known to have occurred in Central America,
although the southern Central American region harbors unique
genetic endemism in several other taxa (Wang et al. 2008).
Studies on the assembly and diversification of biota in Central
America have revealed a complex set of phylogeographical patterns. According to Bagley and Johnson (2014), some patterns
are temporally consistent with Pliocene–Pleistocene dispersal
and vicariance events matching the timeline of isthmus emergence, but long-term mechanisms of genetic isolation have been
an important process in diversification too. Bagley and Johnson
(2014) reviewed more than 50 phylogeographic analyses representing almost 100 nominal taxa, but none was a xenarthran.
The only phylogeographic study of a xenarthran found in
Central America was focused on D. novemcinctus. During the
expansion of its range, the nine-banded armadillo was part of at
least 2 dispersal waves to North America (Arteaga et al. 2012).
This is reflected in the presence of 2 divergent lineages that are
found from Central America and Mexico to Colombia. In addition to divergence, range expansion, at least into the United States,
also impacted genetic diversity. Several studies have reported
low genetic diversity in nine-banded armadillo populations from
the United States (Moncrief 1988; Huchon et al. 1999), which is
probably the result of a recent founder effect. D. novemcinctus
was first recorded in the United States in 1854 (Audubon and
Bachman 1854), and colonization of the country was likely the
result of the initial spread of a small number of individuals out
of the Rio Grande Valley (Loughry and McDonough 2013). This
scenario is supported by a study that documented higher genetic
variation in Mexican populations, suggesting that there was a
larger population size than in populations in the United States
(Arteaga et al. 2012). Populations from Paraguay (Frutos and
Van Den Bussche 2002), French Guiana (Huchon et al. 1999),
and Colombia (Caballero et al. 2013) have even higher levels of
genetic diversity, which is probably related to both population
size and the long period of time D. novemcinctus has occupied
these regions. Overall, the phylogeographic structure and genetic
diversity levels of nine-banded armadillos at broad geographic
scales appear to reflect the effects of the colonization process
after the Great American Biotic Interchange.
Regarding sloths of the genus Bradypus, Moss et al. (2012)
described new microsatellites and estimated relatively high
values of genetic diversity for a single population of B. variegatus from Costa Rica. A similar study focusing on B. variegatus, but with a larger set of loci and several populations,
found similar high values of diversity from just the Brazilian
Amazon forest, and lower values for a Central American population sampled in Panama (Silva 2013). The same study showed
that when using microsatellites that are polymorphic only at
the population level, there is an overestimation of diversity
levels. Overestimation was not consistent across populations
and created a bias when ranking populations based on their
genetic diversity. Nonetheless, the pattern of higher diversity
in Amazonian populations and high distinctiveness among
populations of B. variegatus was corroborated by analyses of
mitochondrial DNA (Moraes-Barros et al. 2006, 2007, 2011).
Therefore, a comparative analysis using all available molecular
markers and covering all previously sampled Central and South
American populations is needed to elucidate the hypothesis of
bias in values of genetic diversity in sloths from Costa Rica.
Such a study will also provide the data necessary to evaluate
the role of the Great American Biotic Interchange in shaping
patterns of genetic diversity in sloths.
Linkages Between the Amazon and
Atlantic Forest
The Amazon and the Atlantic forests are among the most
diverse biomes in the world. Today, they are separated by open
vegetation landscapes such as the Caatinga, a xeric shrubland in
northeastern Brazil, and the Cerrado, a tropical savanna in central Brazil. However, in the past, due to climatic oscillations,
these forested areas were episodically connected. Evidence for
such links can be observed in the faunal distributions of forests
and gallery forests within the Cerrado (Costa 2003).
Among xenarthrans, B. variegatus is the most likely candidate in which to explore linkages between the Amazon and
Atlantic forests. Although 9 xenarthrans occur exclusively in
forested habitats (Table 1), for various reasons 8 of these species are less suitable subjects for such an analysis. For example,
SPECIAL FEATURE—XENARTHRAN GENETIC DIVERSITY AND PATTERNS697
some, such as the armadillo D. pilosus, are restricted to particular habitats that do not include the Amazon and Atlantic
forests (Abba and Superina 2010). In fact, only 2 species occur
in both Amazon and Atlantic forests, the brown-throated sloth
(B. variegatus) and pygmy anteater (C. didactylus). However,
C. didactylus is only found in a segment of the northeastern
Brazilian Atlantic forest and its genetic diversity has not been
properly evaluated yet (F. Miranda, Universidade de São Paulo,
in litt.; Superina et al. 2010a) . The maned sloth B. torquatus,
which will be discussed below, is restricted to just the Atlantic
forest (Gardner 2008).
The phylogenetic relationships between Amazonian and
Atlantic forest sloths were first discussed by Barros et al.
(2003), who determined the split between B. torquatus and the
clade of B. variegatus + B. tridactylus to be at 8 mya. A further
and more detailed molecular phylogeny of Bradypus indicates
the divergence of the B. torquatus lineage as the 1st split within
the genus occurred around 12.5 mya (Moraes-Barros et al.
2011). This divergence pattern is similar to that observed in
primates of the genera Brachyteles, which was restricted to the
Atlantic forest, and Lagothrix, which occurred in the Amazon
forest; both of these lineages split around 10 mya (Schneider
et al. 1993, 1996; Goodman et al. 1998). However, our analysis also indicates a 2nd split event in the Pleistocene (around
0.8–1.0 mya, depending on the method of time inference) that
led to the diversification of a B. variegatus lineage exclusive
to the Atlantic forest (Figs. 1 and 2a; Supporting Information
S4a). Within B. variegatus, the Central American and western
Amazon lineages were the first to diverge, followed by the split
of an eastern Amazon lineage, and the final split of an Atlantic
forest lineage (Figs. 1 and 2a; Supporting Information S4a).
These results allow us to propose a western South American
origin and a west to east dispersal through Amazonia for
B. variegatus diversification. Northwestern South America
was dominated by a permanent and widespread lacustrine
landscape during the Early to early Late Miocene (about 23–9
mya), known as the Pebas system (Wesselingh and Salo 2006).
Although this system mostly acted as a barrier for dispersal
between western and eastern South America, there were some
land connections on its southern limit (Hoorn et al. 2010).
These connections may have allowed dispersal of the ancestral
lineage leading to B. torquatus. The subsequent uplift of the
northern Andes and isolation of the northern region between 10
and 7 mya facilitated allopatric speciation (Hoorn et al. 2010)
and probably promoted the divergence of Bradypus lineages in
the Amazon (B. variegatus + B. tridactylus) and Atlantic forests
(B. torquatus). Further draining of the wetlands in the western
Amazon was followed by a rapid diversification and then dispersion of B. variegatus toward the eastern Amazon, culminating with the connection to the Atlantic forest, probably in the
northeastern region of Brazil, during the Pleistocene (Fig. 2a;
Supporting Information S4a). The hypothesis of a northeastern
connection was first proposed by Moraes-Barros et al. (2007)
and is supported by observations in other vertebrates (Costa
2003). By the time B. variegatus reached the Atlantic forest,
B. torquatus was probably already established there, as we discuss next.
Latitudinal Divergence Within the
Brazilian Atlantic Forest
The spatial organization of vertebrate diversity within the
Atlantic forest has been investigated in several studies based
both on molecular and morphological data. One of the first studies focused on genetic variation in medium-sized mammals and
described a pattern of latitudinal differentiation for 2 species
of sloths, B. variegatus and B. torquatus (Moraes-Barros et al.
2006). Further identification of distinct northern and southern lineages for various vertebrates led researchers to accept a 2-component hypothesis for the Brazilian Atlantic forest (Patterson and
Costa 2012). However, the situation may be more complex. Silva
et al. (2012) reviewed phylogeographic and endemism studies
for Brazilian Atlantic forest vertebrates and described 3 large
regions, subdivided into 9 components that were latitudinally
and longitudinally organized. The authors confirmed the complex history of the Brazilian Atlantic forest, both in space and
time. Also, the time of diversification events within the Brazilian
Atlantic forest, although not empirically estimated for most vertebrates, was not restricted to the Pleistocene.
Among xenarthrans, the 2 forest-dependent species occurring in distinct regions of the Atlantic forest are also the best
known regarding phylogeographic patterns. B. torquatus, a species listed as Vulnerable (International Union for Conservation
of Nature 2014), shows a narrower geographic distribution
within the Atlantic forest than B. variegatus. B. torquatus is
currently distributed in 3 disjunct segments of the Atlantic
forest (Chiarello and Moraes-Barros 2013), each one encompassing a genetically distinct population, grouped in 2 main
lineages, northern and southern (Moraes et al. 2002; MoraesBarros et al. 2006; Lara-Ruiz et al. 2008). Lara-Ruiz et al.
(2008) estimated the divergence time between the 2 lineages at
around 2.48 mya. Our present analysis, which combined DNA
sequences from Lara-Ruiz et al. (2008) with newly generated
sequences from both B. torquatus and B. variegatus, indicates
divergence occurred somewhat earlier, around 4.9–3.9 mya
(Fig. 2a; Supporting Information S4a). This difference is probably due to the substitution rate values used to calibrate the
molecular clock, as those in Lara-Ruiz et al. (2008) are much
higher than the ones we used. Nevertheless, both divergence
estimates are in agreement with split times between northern
and southern Brazilian Atlantic forest lineages inferred for
other vertebrate species (Silva et al. 2012).
Previously published analyses of B. variegatus do not provide divergence time estimates, but they do suggest that climatic
and environmental changes during the Pleistocene may have
shaped the distribution of genetic diversity within the Atlantic
forest (Moraes-Barros et al. 2006, 2007). Our analysis supports
these inferences, pointing to divergence between northern and
southern B. variegatus populations in the Pleistocene at around
0.51–0.4 mya (Fig. 2a; Supporting Information S4a). As mentioned in the previous section, B. torquatus likely inhabited the
biome before colonization by B. variegatus. This is supported
by comparative genetic analyses that show diversity values are
higher for B. torquatus than for B. variegatus (Moraes et al.
2002; Moraes-Barros et al. 2006, 2007; Lara-Ruiz et al. 2008).
698
JOURNAL OF MAMMALOGY
The lower genetic diversity values of B. variegatus can be
explained as a founder effect associated with the colonization
of the Atlantic forest by a single lineage, which presumably
contained only part of the genetic diversity of the species. Even
though both sloth species present a similar pattern of latitudinal differentiation, divergence between northern and southern
lineages are not coincident in time. Likewise, other vertebrate
diversification events within the Atlantic forest are not restricted
to the Pleistocene (Moritz et al. 2000; Silva et al. 2012).
Conclusions
In Xenarthra, the information currently available on molecular phylogeny, phylogeography, and population genetics indicates possible associations between paleoenvironmental events
and genetic diversification of many lineages. Documented
patterns include isolation and diversification associated with
Andean uplift, west to east dispersal in the Amazon region for
forest-dependent species, and colonization pathways within the
Atlantic forest. Representative sampling of xenarthrans and
the use of multiple molecular markers in phylogeographic and
population genetic studies will be key to testing the hypotheses
developed to explain these patterns. Likewise, such analyses
will be critical in determining the true extent of genetic diversity within Xenarthra and whether the patterns we have reported
represent real effects of paleoenvironmental events or just the
result of sampling bias. Based on available data, 31 extant species of Xenarthra are recognized, but this may underestimate
the diversity contained within the group. For example, we
have presented evidence of distinct evolutionary lineages for
B. torquatus, B. variegatus, C. hoffmanni, and D. novemcinctus. However, for many species, we still have no information
on intraspecific diversity or how this may have been shaped by
paleoenvironmental events.
By documenting the extent of diversity within taxa, genetic
data may also help identify populations most in need of conservation attention (Delsuc and Douzery 2008). At the practical
level, such analyses can provide insight into how to allocate
conservation efforts by helping define, for instance, wildlife
management units (Moraes-Barros et al. 2007; Lara-Ruiz et al.
2008). In addition, it may be possible to predict the possible
consequences of climatic change on the gene pool of particular
species with studies of potential areas of distribution and habitat suitability (Anacleto et al. 2006; Moraes-Barros et al. 2010;
Arteaga et al. 2011; Abba et al. 2012; Feng and Papeş 2015;
Moreira et al. 2014).
Genetic studies at the intraspecific level are particularly
important for the 6 xenarthrans currently classified in a threatened category (B. pygmaeus, B. torquatus, C. nationi, M. tridactyla, Priodontes maximus, Tolypeutes tricinctus—International
Union for Conservation of Nature 2014). An example is the
giant anteater, M. tridactyla. The species has disappeared
from most of its original range in Central America (Superina
et al. 2010a), and in the Brazilian Cerrado, a recent population
genetic study indicated high levels of inbreeding and possible
negative consequences for population viability (Collevatti et al.
2007). Two other examples are the pygmy sloth, B. pygmaeus,
the only xenarthran endemic to Central America (Voirin 2015),
and T. tricinctus, the Brazilian three-banded armadillo, which
is endemic to the open biomes of Brazil. B. pygmaeus is represented by a single population, likely to be quite small, and
is considered Critically Endangered, wheraes T. tricinctus is
Vulnerable (International Union for Conservation of Nature
2014). Population genetic studies are underway on these 2
threatened species, but our preliminary results suggest low levels of genetic diversity for both species. In the case of pygmy
sloths, the low genetic diversity may lead to endogamic depression if the population size decreases any further (Superina et al.
2010b). Indeed, of the 6 species considered threatened, only 1,
B. torquatus, has had its genetic diversity investigated across
most of its geographic range (Moraes et al. 2002; MoraesBarros et al. 2006; Lara-Ruiz et al. 2008). Not only threatened
xenarthrans can benefit from genetic diversity studies focused
on identifying possible targets for conservation at the intraspecific level. The protection of historically isolated lineages
should be a conservation priority, as has already been proposed
for some xenarthrans (Moraes-Barros et al. 2007, 2011; LaraRuiz et al. 2008; Abba et al. 2015).
Besides conservation issues, ecological questions can arise
from molecular analyses. For instance, analyses of patterns of
gene flow between 2 divergent lineages of D. novemcinctus in
Mexico led to additional insights on niche conservatism and
its impacts on species dispersion (Arteaga et al. 2011). Also,
discerning evolutionary patterns from ecological associations
is possible. For instance, Jiménez et al. (2012) reconstructed 3
events of dispersal to the Nearctic in Aspidoderidae, a family
of nematodes that infest mammals that participated in the Great
American Biotic Interchange. The results suggest that 2 different lineages of Dasypodidae parasites entered the Northern
Hemisphere at different times, which is consistent with the
presence of 2 lineages of armadillos in Mexico.
Further investigation of xenarthran molecular phylogenies
and phylogeography will substantially contribute to discussions in 2 topics, the effect of the Andean uplift on diversification and speciation processes, especially for those species and
subspecies restricted to high elevations; and patterns of genetic
diversity in Central America and how they are related to emergence of the Isthmus of Panama and climatic changes during
the Pleistocene. Ultimately though, the success of such projects
will depend on obtaining samples from large numbers of individuals from multiple localities. Despite the elusive nature of
most xenarthrans and the difficulties in capturing them, there
is a growing number of studies on potential distribution areas
which can help prioritize areas to survey. Regarding genetic
analysis, new technologies, especially those related to nextgeneration sequencing methodologies (Davey et al. 2011),
may overcome difficulties in selecting molecular markers for
population genetic studies. In addition, more robust inferences
of phylogenetic and split time may be obtained by analyzing
complete genomes (e.g., mitochondrial genomes). Therefore,
we expect that in the near future a growing number of phylogeographic and population genetic studies will contribute substantially to our understanding of the rich evolutionary history
and patterns of diversity found in xenarthrans.
SPECIAL FEATURE—XENARTHRAN GENETIC DIVERSITY AND PATTERNS699
Acknowledgments
We thank W. J. Loughry and M. Superina for inviting us to contribute to this special feature and their critical review of the manuscript. Thanks also to the following institutions and researchers
who contributed sloth DNA samples: B. Voirin, T. Plese from
Fundación AIUNAU, the Museum of Vertebrate Zoology at
Berkeley, and the American Museum of Natural History. We
especially thank R. S. Voss for taxonomic review of the C. hoffmanni specimen, A. G. Chiarello for valuable comments on the
manuscript, and F. Diaz and R. P. Ramirez for their hard work on
the Neotropics map. NM-B was partially funded by Fundação
de Amparo à Pesquisa do Estado de São Paulo, Brazil (FAPESP
06/52220 and 03/03212-7) and Coordenação de Aperfeiçoamento
de Pessoal de Nivel Superior–Programa de Apoio a Projetos
Institucionais com a Participação de Recém-Doutores, Brazil
(Capes-Prodoc 1910/2008–23038.040875/2008–88). We dedicate this article to Rodrigo Vieira Moraes Barros and Máximo
Emilio Bello Arteaga.
Supporting Information
The Supporting Information documents are linked to this
manuscript and are available at Journal of Mammalogy online
(jmammal.oxfordjournals.org). The materials consist of data
provided by the author that are published to benefit the reader.
The posted materials are not copyedited. The contents of all
supporting data are the sole responsibility of the authors.
Questions or messages regarding errors should be addressed
to the author.
Supporting Information S1.—Survey of previously published papers on Xenarthra, and phylogenetic analysis based
on previously published and newly generated xenarthran DNA
sequences.
Supporting Information S2.—Detailed description of DNA
samples used in this study.
Supporting Information S3.—Detailed description of the
5 Xenarthra species occurring on both sides of the northern
Andes and their subspecies.
Supporting Information S4.—Trees and divergence times
inferred for cross-Andes and forest-dependent xenarthrans
according to Bayesian analysis.
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Editor for Special Feature was Barbara H. Blake.