Journal of Biogeography, 30, 71–86
The historical bridge between the Amazon
and the Atlantic Forest of Brazil: a study
of molecular phylogeography with small mammals
Leonora P. Costa Museum of Vertebrate Zoology, University of California, Berkeley,
Berkeley, CA, USA
Abstract
Aim To examine how the genetic diversity of selected taxa of forest-dwelling small
mammals is distributed between and within the major rain forest domains of Amazonia
and Atlantic Forest and the intervening interior forests of Brazil, as inferred by the
relationships between gene genealogies and geography. I also addressed the historical
importance of the central Brazilian forests in connecting Amazon and Atlantic Forest
populations of rodents and marsupials.
Methods I evaluated variation in the mitochondrial cytochrome b gene to estimate the
levels of sequence divergence between those taxa occurring throughout the Amazon,
Atlantic Forest, and forests in the Cerrado and Caatinga regions. I inferred the hierarchical relationships between haplotypes, populations and formal taxa using the cladistic
approach of maximum parsimony. I compared areas and the clades identified by
superimposing cladograms on the geographical distribution of samples. The degree of
concordance both in phylogeny and the depth of the nodes in these phylogenies, in
addition to patterns of geographical distribution of clades, permitted me to make
inferences on how, when and where the taxa differentiated.
Results Sequence similarity is often greater between samples from the Atlantic Forest
and either Amazon or central Brazilian forests than it is within each of the two rain
forest domains. The Atlantic Forest clades are either not reciprocally monophyletic or
are the sister group to all the other clades. There is some indication of northern and
southern components in the Atlantic Forest. Given the geographical distribution of
clades and the relatively deep levels of divergence, the central Brazilian area does not
behave as a separate region but is complementary to either Amazon or
Atlantic Forest. Patterns of area relationships differ across taxa, suggesting that
different processes and ⁄ or historic events affected the diversification within each
lineage.
Main conclusions The Amazon and the Atlantic forests are not exclusive in terms of
their small mammal faunas; both overlap broadly with taxa occurring in gallery forests
and dry forests in central Brazil. Central Brazilian forests are an integral part of the
evolutionary scenario of lowland small mammals, playing an important role as present
and past habitats for rain forest species. Therefore, representatives from this area should
always be included in analyses of the evolutionary history of lowland rain forest faunas.
The incongruence of branching patterns among areas is in agreement with recent results
presented for Neotropical passerine birds and indicates that a single hypothesis of
Neotropical area relationships is unlikely. These findings reinforce the idea that speciation in the Neotropics will not be explained by any single model of vicariance or
climatic changes.
Correspondence: Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, 31260-901 Belo
Horizonte, MG, Brazil. E-mail: [email protected]
2003 Blackwell Publishing Ltd
72
L. P. Costa
Keywords
Neotropical small mammals, Atlantic Forest, Amazon, Cerrado, Caatinga, phylogeography, evolutionary history of rain forest mammals.
INTRODUCTION
The aim of this paper is to investigate the biogeography and
evolutionary relationships of the non-volant, small-mammal
fauna distributed across the Amazon, Atlantic Forest and the
central Brazilian forests. The Amazon and the Atlantic forests morphoclimatic domains of South America (Ab’Saber,
1977) encompass the most diverse tropical forests in the
world. Between these two forests lies a belt of more open
vegetation, including the Argentinean and Paraguayan
Chaco, the Caatinga in north-eastern Brazil, and the central
Brazilian Cerrado, the latter being the second largest domain
in Brazil extending over 2 million km2. This dry corridor of
open vegetation, also called ÔThe major South American
disjunctionÕ (Brieger, 1969), has been considered as an
important restraint to species migration between the two
rain forest regions (Moojen, 1948; Raven & Axelrod, 1974;
Rizzini, 1979; Mori et al., 1981; Por, 1992). But if at first
glance, the Amazon and Atlantic forests appear widely isolated, maps of present-day vegetation clearly shows that the
ubiquitous gallery forests and series of deciduous and
semi-deciduous forest patches constitute a network of
interconnected forests through otherwise open landscape
(Oliveira-Filho & Ratter, 1995; Vivo, 1997). Other
particularities of the Cerrado and Caatinga regions provide
evidence of past connections as well.
Although dominated by a semi-deciduous arboreal
savanna, the Cerrado is composed of a mosaic of subunits
that vary from grasslands to dry forests. Along the rivers that
transect this mosaic, there are strips of mesic forests, the
gallery forests. Comprising <10% of the total area of the
Cerrado, gallery forests occur throughout the region.
Oliveira-Filho & Ratter (1995) provide many instances of
floristic links of gallery forest in the Cerrado region to either
Amazonian or Atlantic rain forests. Redford & Fonseca
(1986), based on a literature review, showed that the
greatest proportion of the Cerrado mammalian fauna is
composed of species characteristic of mesic domains, and
that the composition of mammal species in gallery forests is
very similar to that of both the Amazon and Atlantic rain
forests. Among the 100 species of mammals known to occur
in the Cerrado, only eleven are endemic to this domain, with
fifty-five being found also in the Amazon and sixty-four in
the Atlantic rain forests. The majority of the non-endemic
mammal species occur in the Cerrado mainly as a consequence of the presence of gallery forests (Redford &
Fonseca, 1986). A similar pattern of endemism and habitat
use was found by Silva (1995) for birds of the Cerrado, but
he pointed out that dry forests, additionally to gallery
forests, are keystone elements in maintaining avian diversity
in the Cerrado region. Therefore, dry forests should also be
investigated as important elements in the biogeographical
history of the region.
The Caatinga is a xerophytic vegetation type characterized
by spiny deciduous trees and shrubs in association with
succulent plants, cacti and bromeliads (Kuhlmann, 1977; De
Oliveira et al., 1999). This near-desert vegetation surrounds
inland ÔbrejoÕ forests, enclaves of moist forest caused by
precipitation on the slopes of various plateaus (Mori, 1989).
Botanical studies of these mesic enclaves and the northeastern coastal forests revealed floristic disjunction with
either the Amazon or the Atlantic Forest (Rizzini, 1963;
Bigarella et al., 1975; Coimbra-Filho & Câmara, 1996).
Species of small mammals typical of rain forests [such as the
slender mouse opossum Marmosops incanus (Lund) and the
murid rodent Rhipidomys mastacalis (Lund)] are currently
found in ÔbrejoÕ forests in the states of Ceará and Bahia (Y.
Leite and L. P. Costa, unpublished data). Based on mammalian distributional patterns, the fossil record and ecological physiology, Vivo (1997) suggested that a mesic forest
capable of supporting arboreal rain forest mammals existed
in the area presently occupied by the Caatinga, connecting
the eastern Amazonian and the Atlantic rain forests.
Therefore, forests are far from a negligible component of
central Brazilian vegetation, and their role as migration
routes for forest species must be recognized, especially when
evidence exists for a previously wider forest cover (OliveiraFilho & Ratter, 1995; Vivo, 1997). The Amazon and
Atlantic forests were probably once continuous in the past,
becoming separated as increasing aridity in the Tertiary
formed the belt of xeromorphic formations between them
(Bigarella et al., 1975). The palynological record of the
Quaternary showed that between 33,000 and 25,000 BP, the
central Brazilian region was moister than today and was
covered by rain forests (Ledru, 1993), and during the last
glacial maximum (18,000–12,000 yr BP), the present-day
corridor of xeric vegetation was covered by extensive
woodland (Prado & Gibbs, 1993). These findings indicate
the predominance of seasonal arboreal vegetation during
most of the Pleistocene. A palynological profile from the
latest Pleistocene (10,990–10,540 yr BP) from the Caatinga
region revealed pollen of taxa found in the present Amazonian and Atlantic forests; the pollen concentration is high,
probably reflecting a large and well-drained watershed under
a climate conducive for a dense forest cover (De Oliveira
et al., 1999). The extent to which these climatic fluctuations
and associated vegetation changes affected the patterns of
distribution and diversification of the small mammal fauna
remains a central question in understanding the evolution of
lowland forest communities.
Recent developments in the field of molecular biology
provide the tools to further investigate phylogenetic
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
Phylogeography of Neotropical forest small mammals 73
relationships among organisms. When associated with geographical distributions, this information enables us to
understand processes of diversification, to construct patterns
of phylogenetic relationships and to test explicit hypotheses
of biogeographical history (e.g. Smith & Patton, 1993;
Patton et al., 1994). The study of the principles and processes governing the geographical distributions of genealogical lineages constitutes the new field of phylogeography, as
defined by Avise et al. (1987). Previous work on phylogeography of small mammals has addressed the relationships
among taxa distributed across Amazonian and Atlantic
forests. In a preliminary analysis, Patton et al. (1997) utilized Cracaft’s (Cracraft, 1985, 1988; Cracraft & Prum,
1988) framework for small mammals, and found the samples from the Atlantic Forest to form a monophyletic group
that was also the most divergent phylogenetically. A high
degree of genetic divergence (above 12%) between Atlantic
Forest and Amazonian clades of three marsupial taxa
(Micoureus Lesson, Philander Tiedemann, and Didelphis
Linnaeus) and one rodent [Oryzomys capito (Olfers)]
suggested that these two domains have been isolated for a
long period of time. Mustrangi & Patton (1997) examined
alternative hypotheses of relationships between Atlantic
Forest and Amazonian species of Marmosops Matschie, and
in this case the monophyly of the Atlantic Forest species
could not be confirmed.
The considerations above raise several questions regarding
the evolutionary history of the Neotropical rain forest
mammal fauna. How much diversification has occurred
exclusively within the Amazon or the Atlantic Forest and
how much diversification has been shared among these two
rain forest domains (Fig. 1)? Have the central Brazilian
forests played a historical role as extensions of the rain forest
domains for small mammal species, enabling gene exchange
through two regions otherwise isolated? Is there a common
pattern of diversification across different mammal lineages,
such as marsupials and murid rodents? One way to answer
these questions is to integrate molecular data under a phy-
Figure 1 Diagram showing the distribution of the Amazon (Am)
and the Atlantic Forest (AF), the Cerrado (hatched) and the Caatinga (stippled). In order to examine the evolutionary distinctiveness
of the rain forest biomes, a cladistic approach was employed to
determine if the sister-group relationships of small mammals were
found within (left) or between (right) the Amazon and the Atlantic
forests.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
logenetic framework for multiple taxa with present-day
geographical distributions.
The work I report here is an extension of that previously
carried out by Patton et al. (1997), and the specific topics
covered in this paper are: (1) How phylogenetically distinct
are the small mammal taxa of the Amazon with respect to
their Atlantic Forest relatives, and vice-versa? (2) Do the
central Brazilian gallery and dry forests play a role in largescale patterns of geographical distribution of the genetic
diversity and differentiation of lowland rain forest small
mammals, acting as connections between the Amazon and
the Atlantic Forest? If so, what are the phylogenetic affinities
of the small mammals living in these interior forests with
respect to the mammals living in the two rain forest
domains? (3) Given the geographical distribution of clades,
is there a consistent pattern of area-relationship across taxa?
METHODS
I focused my analysis on geographical clades of eleven
monophyletic groups of small mammals, including representatives of five genera (Caluromys J. A. Allen, Philander,
Micoureus, Marmosops, Gracilinanus Gardner and
Creighton) and two widespread species of marsupials
[Metachirus nudicaudatus (Desmarest) and Marmosa
murina (Linnaeus)], two groups of Oryzomyini rodents
(Oryzomys megacephalus group and O. macconnelli
group), and two arboreal sigmodontine rodent genera
(Rhipidomys Tschudi and Oecomys Thomas). Twenty-two
collection sites within gallery forests, semi-deciduous forests
and dry forests in central and north-eastern areas in Brazil
were sampled. Non-volant small mammals were trapped
using live- and snap-traps, and prepared according to
standardized museum procedures. Liver tissue samples were
collected in the field and preserved in alcohol or liquid
nitrogen. DNA was extracted using the Chelex (Bio-Rad,
Hercules, CA, USA) method (Walsh et al., 1991), amplified
by the polymerase-chain reaction (PCR) (Saiki et al., 1988),
and sequenced using an automated sequencer (ABI-Prism
377, Perkin Elmer, Foster City, CA, USA) in the Laboratory
of Evolutionary Genetics of the Museum of Vertebrate
Zoology. The data set varied from 327 to 801 bp of the
cytochrome b (cyt b) gene. One hundred and sixty new
sequences were added to an existing data base of 194
sequences of Amazonian and Atlantic Forest small mammals gathered by J. L. Patton and collaborators (Patton
et al., 1996, 2000; Mustrangi & Patton, 1997; Smith &
Patton, 1999; Patton & Costa, in press; Costa et al., in
press). A list of specimens and locality data used in the
present report can be found in Costa (2001).
Variation in the cyt b gene was evaluated in order to
estimate the levels of sequence divergence between those taxa
occurring throughout the Amazon, the Atlantic Forest, and
forests in the Cerrado and Caatinga regions. Sequence divergence was calculated using the Kimura two-parameter
(K2p) algorithm (Kimura, 1980) as implemented in PAUP*
version 4.0b8 (Swofford, 1999). Hierarchical relationships
among haplotypes, populations and formal taxa were
74
L. P. Costa
inferred using the cladistic approach of maximum parsimony
using PAUP*. Trees were constructed using the heuristic search
option via stepwise addition, with ten replicates and random
addition sequence of taxa. The support for internal branches
was evaluated by decay indices (Bremer, 1988) and bootstrap
analyses (Felsenstein, 1985), with 100 bootstrap replicates
each consisting of a full heuristic search as described above.
I compared areas and the clades identified by superimposing cladograms on maps of the geographical location of
samples. The concordance of area cladograms and the depth
of the nodes in these phylogenies permitted me to make
inferences on how, when and where the taxa differentiated
and thereby to address the historical importance of the
central Brazilian forests in connecting Amazon and Atlantic
Figure 2 Area relationships of eight taxa of small mammals. (a) All Amazonian areas form a clade relative to the Atlantic Forest (Philander).
(b) The Atlantic Forest is deeply nested in a more inclusive clade in four cases (M. nudicaudatus, M. murina, O. megacephalus group and
O. trinitatis group). (c) In three cases (Rhipidomys, Caluromys and Marmosops) the Atlantic Forest has a paraphyletic status. The samples from the
central area (CA) are also deeply nested in all phylograms in which they appear. Tree topologies are based on bootstrap consensus trees; therefore
clades shown are supported by at least 50% bootstrap values. The black dots indicate clades supported by more than 75% bootstrap values.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
Phylogeography of Neotropical forest small mammals 75
Forest populations of rodents and marsupials. The question
of phylogenetic distinctiveness of the rain forest domains
was examined under a cladistic evolutionary approach. In
other words, I asked if sister-group relationships were concentrated within or between the Amazon and the Atlantic
Forest (Fig. 1).
To explore the discrepancy in time of splitting events in
the many taxa utilized in the analyses, I estimated branch
lengths of the trees by maximum likelihood using third
position changes only, constraining and not constraining a
molecular clock. Then, I performed a likelihood ratio test
(LRT) of the molecular clock, and used only the taxa for
which the LRT was not significantly different (Huelsenbeck
& Rannala, 1997). Calibration of the clock was carried out
for marsupials using the estimates of Mustrangi & Patton
(1997) for Marmosops, and for the rodents using the parameters of Smith & Patton (1999).
RESULTS
The phylogeographical relationships between
the Amazon and the Atlantic Forest
From the eleven groups analysed, three (Micoureus, Gracilinanus and Oryzomys macconnelli group) showed polytomic relationships, and for that reason could not be used in
the inference of sister-group relationships between geographical clades in the two rain forest domains. Among the
eight taxa remaining (Fig. 2), in only one group, Philander
Figure 3 Phylogeographical relationships
among cytochrome b haplotypes of five species of the climbing rat, genus Rhipidomys.
The map shows the range of the genus
Rhipidomys and the geographical distribution of the samples. Note that the two species
that occur in the Atlantic Forest are not sister
groups. Bold numbers at nodes are bootstrap
values and decay indices, respectively. Percentages are average Kimura two-parameter
distances.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
(Fig. 2a), was the Atlantic Forest (AF) clade the sister group
to all other areas. In four of eight cases, the Atlantic Forest
clade was deeply nested in a more inclusive clade (Fig. 2b),
while in three cases it showed up as a composite area
(Fig. 2c). A more detailed example of the last case can be seen
in Fig. 3, which depicts the phylogeographical relationships
of five species of the climbing rat Rhipidomys. There are two
species in the Atlantic Forest, Rhipidomys mastacalis in the
north and an undescribed species in the south. These two
species are not sister groups. Rather, the southern species has
a sister relationship with R. leucodactylus Tschudi, a species
from the west-central Amazon, while R. mastacalis is closely
related to R. nitela Thomas, a species occurring in the central
Brazilian area, the two forming the sister group to the species
of the south-western Amazon, R. gardneri Patton, da Silva
and Malcolm.
Another way to examine the evolutionary distinctiveness of
the domains is to compare the genetic distances among
haplotypes of widely distributed species. For these small
mammals, K2p distances are commonly greater among
localities within domains than across domains. An example of
this is the woolly mouse opossum, Micoureus demerarae
(Thomas). This species occurs throughout the Amazon and
the central Brazilian forests, reaching the Atlantic Forest in
coastal Brazil (Fig. 4a). Haplotypes from the most eastern
Amazon locality are closer to those from the northern Atlantic
Forest than they are to haplotypes from other Amazonian
localities (Fig. 5). Similarly, haplotypes of the brown foureyed opossum, Metachirus nudicaudatus (Figs 4b & 5), and
76
L. P. Costa
Figure 4 Maps of the range and geographical distribution of the samples of species of
Micoureus (a) and Metachirus nudicaudatus
(b). The phylogenetic relationships among
haplotypes (shown to the right) indicate the
existence of northern and southern components in the Atlantic Forest. For Micoureus,
solid lines circumscribing samples correspond
to species boundaries and dashed lines indicate clades within species; symbols correspond to each of the five species. For
Metachirus, solid lines circumscribe intraspecific phylogeographical units represented
by different symbols and dashed lines indicate
clades within such units. Bold numbers at
internal nodes are bootstrap values and decay
indices, respectively; percentages are average
Kimura two-parameter distances.
the murine opossum, Marmosa murina (Linnaeus) (Figs 5 &
6a), from different localities in the Atlantic Forest are
genetically more similar to those compared from the Amazon
than the Amazonian haplotypes are to each other. This pattern can also be observed for species within the same complex.
As an example, Oryzomys megacephalus Fisher from the
northern Amazon and central Brazil is more closely related
to O. laticeps (Lund) from the Atlantic Forest than to
O. perenensis (Allen) from the western Amazon (Fig. 7).
In terms of the Atlantic Forest itself, there are northern
and southern components, as exemplified by Rhipidomys
(Fig. 3), Micoureus (Fig. 4a) and Metachirus Burmeister
(Fig. 4b). In both Rhipidomys and Micoureus, clades corresponding to two different species replace one another from
north to south, while in Metachirus nudicaudatus, there are
two geographically structured clades of the species in the
Atlantic Forest. The break in the distribution of species and
clades of these taxa is nearly coincidental. Nevertheless, the
K2p distances within each of these clades are different,
suggesting that vicariant events affected taxa at different
times. Cyclic climatic fluctuations are one plausible explanation for this coincidental pattern in space but not in time.
The phylogeographical affinities of the Cerrado and
Caatinga domains
The samples from the intervening region between the
Atlantic Forest and Amazonia, including the Cerrado and
Caatinga domains and for simplification called here the
central area (CA), were deeply nested in all phylogenies
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
Phylogeography of Neotropical forest small mammals 77
Figure 5 Maps of the geographical location
and average Kimura 2-parameter distances of
selected haplotypes of three taxa of didelphid
marsupials (Micoureus demerarae, Metachirus nudicaudatus and Marmosa murina).
Note the small genetic distances between
samples from the Atlantic Forest and the
Amazon, especially when compared with the
genetic distances separating samples from
localities within the Amazon itself. The
Amazon and the Atlantic Forest are shown in
dense stippling, the Cerrado hatched and the
Caatinga in sparse stippling.
obtained (Figs 2–7). This fact attests to the importance of
this broad area in the diversification of rain forest small
mammals. Animals inhabiting this region could have their
closest relatives in the Atlantic Forest, in the Amazon, or be
basal relative to the two rain forest domains (Fig. 8). The
results, derived from analyses of all trees in Figs 2–7, are
summarized in Table 1. Five of eleven groups could not be
used in this analysis, because two of them are absent in one
of the areas and three showed polytomic relationships (for
details on these taxa, see Table 1). As one might expect
when dealing with forest animals living in a somewhat
more foreign environment, the samples from the CA were
never basal to their relatives in the forest domains. More
often the CA clade was the sister to an Atlantic Forest clade
than to an Amazonian clade, as is the case for Marmosa
murina (Figs 2b & 6a), Caluromys (Figs 2c & 6b),
Rhipidomys (Figs 2c & 3) and the Oecomys trinitatis group
(Fig. 2b).
I also looked at individual localities in the CA to see if the
affiliation of this area and the two rain forest domains was
only a matter of geographical distance from the source in
either the Atlantic Forest or the Amazon (Fig. 9). Under the
assumption of isolation by distance, samples from localities
in the CA situated near the Amazon should share a more
recent common ancestor with Amazonian samples, whereas
those from localities closer to the Atlantic Forest should be
related to those in Atlantic Forest. To explore this hypo 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
thesis, I took into account all localities within the Cerrado
and Caatinga, and those in the transition areas between
these two domains and the lowland rain forests, but excluded those from the central Amazon and Atlantic Forest
themselves. At each CA locality, only taxa that had relationships with either the Amazon or the Atlantic Forest were
considered. These comparisons (Fig. 9) do not present the
clear-cut trend hypothesized above. Rather, in some cases
specimens in localities near the Atlantic Forest share a more
recent common ancestor with Amazonian groups, whereas
in the transition zone between the Cerrado and the Amazon,
specimens were often related to Atlantic Forest individuals.
It is also interesting to note that localities to the southwest of
the CA tend to be more affiliated to the Amazon, while
localities in the northeast are more often related to the
Atlantic Forest (Fig. 9). This observation suggests possible
routes and directions of interchange between the Amazon
and the Atlantic Forest.
Patterns and timing of diversification
One of the aims of this paper was to search for congruent
patterns of diversification linking subareas in each domain.
Nevertheless, while some genera or group of species show a
strong hierarchical structure over the whole sampled geographical area, others, although geographically structured,
show little resolution with respect to the relationships
78
L. P. Costa
Figure 6 Maps showing the range and geographical distribution of the samples of species of Marmosa murina (a) and Caluromys
(b). The phylogenetic relationships among
haplotypes are shown to the right. For
Caluromys, solid lines circumscribing
samples correspond to species boundaries
and dashed lines indicate clades within
species; symbols correspond to each of the
two species. For M. murina, solid lines
circumscribe intraspecific phylogeographical
units represented by different symbols and
dashed lines indicate clades within such units.
Bold numbers at internal nodes are bootstrap
values and decay indices, respectively;
percentages are average Kimura two-parameter distances.
among species or geographical clades within species. Two
closely related species groups of the rice rat and representatives of two sister genera of didelphids illustrate this
situation in Fig. 10. The Oryzomys megacephalus group
(Fig. 10a) is comprised of three species that replace one
another from east to west, with two (O. laticeps and
O. megacephalus) more closely related species in the Atlantic Forest and northern Amazon ⁄ south central Brazil,
and a more distant one (O. perenensis) in the western
Amazon. In contrast, rice rats of the Oryzomys macconelli
group (Fig. 10b), although strongly divergent and geographically bounded, do not show the same level of resolution among the five species included in the complex.
Similarly, the geographical clades of Marmosa murina
(Fig. 10c) are structured into three sharply defined clades
hierarchically organized, while the geographical clades of
Micoureus demerarae (Fig. 10d) are linked in the form of a
basal polytomy. Other taxa examined present similar
contrasts. Among eight taxa that are widespread in the
Amazon, Atlantic Forest and CA, five show resolved area
relationships while four do not (Table 2). Among the taxa
that have restricted distributions or are absent in one of
the domains, two have resolved area relationships
while one does not (Table 2). As groups of closed
related taxa (e.g. sister groups Marmosa ⁄ Micoureus and
Gracilinanus ⁄ Marmosops) can present resolved or unresolved area relationships, independently of the geographical range of these taxa, I conclude that the lack of area
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
Phylogeography of Neotropical forest small mammals 79
Figure 7 Phylogeographical relationships and geographical distribution of three species of the rice rat Oryzomys of the group megacephalus.
Oryzomys megacephalus from northern Amazon and central Brazil is more closely related to O. laticeps from the Atlantic Forest than to
O. perenensis from western Amazon. Bold numbers at internal nodes are bootstrap values and decay indices, respectively; percentages are
average Kimura two-parameter distances. Solid lines circumscribing samples on the map correspond to species boundaries and dashed lines
indicate the northern and southern clades within O. megacephalus.
Figure 8 Area cladograms depicting possible phylogeographical
affinities of the central area (CA) under three hypotheses: the samples from the CA could be more closely related to those from the
Atlantic Forest (left), to Amazon samples (middle), or be basal relative to the two forest biomes (right).
cladogram resolution is neither a matter of phylogenetic
constraint nor of distributional pattern.
In Fig. 11 I present clock-constrained trees for all taxa for
which the clock was not rejected by the LRT. Clearly, the
gene trees of different taxa coalesce at different times.
Although cladogenesis and gene divergence are not necessarily coincident (Edwards & Beerli, 2000), the magnitude
of the differences in coalescence times observed in Fig. 11
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
suggests that speciation in many taxa could have been
affected by different historical events. Although molecular
clocks are not always reliable indicators of absolute time
(Ayala, 1997), taxon-specific local clocks are probably
widespread (Edwards & Beerli, 2000). Therefore, one can
infer from Fig. 11 that several splits occurred prior to the
Pleistocene (shaded area). Alternatively, there is some concordance which indicates concurrent vicariant events: the
split of the Atlantic Forest species Philander frenatus (Olfers)
from all others in the genus is nearly coincidental with the
split of the three species of Gracilinanus. Similarly, there is a
simultaneous split between the north-western Amazonian
species of Rhipidomys (R. macconelli de Winton and
R. wetzeli Gardner) and western Amazonian species of
Marmosops [M. neblina Gardner and M. noctivagus
(Tschudi)] from other species in their complex.
DISCUSSION
Cracraft & Prum (1988) hypothesized historical relationships among putative centres of endemism in the Neotropics through successive vicariant events for four clades
of birds. Interestingly, the only discordant pattern between
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L. P. Costa
Central area
Taxa
Oryzomys megacephalus group
Oecomys trinitatis group
Marmosa murina
Philander
Caluromys
Rhipidomys
Sister to the
Atlantic Forest
Sister to the
Amazon
Basal to the Atlantic
Forest and to the Amazon
Table 1 Sister-group relationships of six
groups of small mammals distributed in the
Amazon, Atlantic Forest (AF) and central
area*
•
•
•
•
•
•
*Marmosops and Metachirus are absent in the central area, and the relationship is polytomic
for Micoureus, Gracilinanus and taxa in the Oryzomys macconnelli group.
Figure 9 Pie-charts showing sister-group
relationships of samples at individual localities in the central area of Brazil. At each
locality, only taxa that had relationships with
either the Amazon or the Atlantic Forest were
considered. Samples from each locality were
scored as either sister to Amazon or Atlantic
Forest samples. The size of the pie is
proportional to the number of samples
examined at each locality.
phylogeny and geography involved the Atlantic Forest,
which appeared in their analysis as a composite, or biogeographical ÔhybridÕ area, having some component taxa
nested within the Amazonian clade while others were
outside this clade. Patton et al. (1997) found the Atlantic
Forest as basal or polytomic in relation to other areas in
the Amazon basin and Central America, for six generic or
infrageneric groups of didelphid marsupials and two species complexes of the murid rodent Oryzomys Baird. In
my expanded analyses, including the same taxa examined
by Patton et al. (1997) as well as additional taxa, the
Atlantic Forest was often nested in a more inclusive clade
(Fig. 2b), but similar to Cracaft and Prum’s results, it also
showed up as a composite area (Fig. 2c). The main difference between my work and the previous analyses by
Patton and collaborators is the inclusion of samples from
the region between the Amazon and Atlantic Forest. As a
result, if earlier we viewed the Atlantic Forest as a disconnected area, long separated from the Amazon, this
view has drastically changed with the inclusion of samples
from the central Brazilian forests. Given the geographical
distribution of clades and the levels of divergence found,
the central Brazilian area does not behave as a separate
region, but is complementary to either Amazon or Atlantic
forests. As a consequence, the central Brazilian forests are
an integral part of the evolutionary history of lowland
small mammals. Their role as present and past habitats for
forest species must be recognized, and representatives from
this area should always be included in the analyses of the
evolutionary history of lowland rain forest faunas.
In terms of the affinities of the central Brazilian area, there
is a slight trend towards a closer association of the small
mammals living in forest habitats in the central region with
those from the Atlantic Forest, as revealed by the analyses of
sister group relationships (Table 1). Nevertheless, the analyses of individual localities summarized in Fig. 9 did not
indicate the same result. Hence, at this point the data suggest
that the CA region has affinities with both the Atlantic
Forest and the Amazon. This result is not unexpected,
because many taxa contemplated in this study belong to old
lineages (Fig. 11) that experienced numerous contractions
and expansions of the Cerrado vegetation over the Pleisto 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
Phylogeography of Neotropical forest small mammals 81
Figure 10 Differences in hierarchical structure among the cladograms of taxa of the rice rat Oryzomys and the didelphid species Marmosa
murina and Micoureus demerarae. Relationships among species of the O. megacephalus group and the geographically structured clades of
M. murina are fully resolved, while the same level of resolution is not observed for the species in the O. macconnelli group and the intraspecific
clades of M. demerarae. Symbols on the maps and cladograms correspond to the different species of Oryzomys, and to intraspecific
phylogeographical units of M. murina and M. demerarae. Numbers at nodes are bootstrap values (above) and decay indices (below).
Table 2 Pattern of distribution and area
relationships for eleven groups of small
mammals
Area relationships
Pattern of distribution
Resolved
Not resolved
Widespread in the Amazon,
Atlantic Forest and central area
Oryzomys megacephalus
group
Marmosa murina
Caluromys
Oecomys trinitatis group
Rhipidomys
Oryzomys macconnelli
group
Micoureus demerarae
Philander
Restricted or absent in
one of the areas
Gracilinanus
Metachirus
Marmosops
cene and preceding geological eras. Nevertheless, a decisive
assessment of the affinities of the CA with the rain forest
domains will have to wait until more phylogenies are
available.
The partitioning of the Amazon into several highly
divergent phylogeographical areas has already been documented (Cracraft & Prum, 1988; Patton et al., 1997,
2000). In contrast, the division of the Atlantic Forest as
indicated by the phylogenetic analyses in this paper has
been unrecognized for small mammals until very recently.
Vanzolini (1988), Bates et al. (1998) and Costa et al.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
(2000) have noted a latitudinal break in the distribution of
Atlantic Forest vertebrates, which separates the north from
the south in reptiles, lowland birds and lowland mammals,
the latter two using parsimony analysis of endemicity.
Although these analyses found a strong sister-group
relationship between the northern and the southern Atlantic
Forest clades, in my analysis I found a different pattern:
often, taxa occurring in northern and southern Atlantic
Forest were not sister taxa. Species of Rhipidomys and
Micoureus illustrate this situation in Figs 3 and 4a. The
species relationships of the genus Marmosops are likely
82
L. P. Costa
Figure 11 Clock-constrained phylogenetic
trees for six genera of didelphid marsupials
(above) and three genera of sigmodontine
rodents (below). Only taxa for which the
clock was not rejected by the likelihood ratio
test were included. The results indicate that
most of the splits probably occurred prior to
the Pleistocene (shaded area).
another example (see Mustrangi & Patton, 1997). These
results further strengthen the likelihood that the Atlantic
Forest is a composite area.
One of the main observations from the data presented
here is the lack of congruence of area cladograms across
taxa, a result concordant with recent data for other groups
of taxa. To date, the question of area relationships between
and within the Atlantic Forest and Amazonia has addressed
primarily avian taxa. Bates et al. (1998), studying Neotropical lowland passerine birds and using raw geographical
distributions of species and subspecies, found many different
hypotheses of area relationships and concluded that a single
network of Neotropical area relationships is not likely. Zink
et al. (2000) examined six lineages of birds occurring in the
arid lands of North America and obtained different area
cladograms depending on how widespread and missing taxa
were coded. Nonetheless, no cladogram was obtained in
which all lineages were congruent. Are these results just an
artefact of the materials and methods utilized or do they
reflect reality? I argued above that the lack of congruence in
cladograms obtained for the many taxa examined here was
not because of phylogenetic constraints or the patterns of
distribution of taxa. Other reasons for the lack of congruence in phylogeographical patterns were thoroughly dis-
cussed by Zink et al. (2001) and include differences in levels
of gene flow among populations, different responses of
species to the same environmental or geological feature that
could have acted or not as a barrier to gene flow, or different
Ôresponse timesÕ of species effectively isolated by the same
barrier, because of differences in their effective population
size. All the above explanations assume vicariance as the
historical process shaping the distribution of taxa and ultimately leading to phylogeographical congruence. Nevertheless, the effects of dispersal confounding the signal in a
phylogeographical analysis cannot be ignored (Avise, 2000).
As pointed out by Ronquist (1997), dispersal barriers appear
and disappear throughout earth history and may have different effects on the evolutionary history of different species.
Zink et al. (2000) evaluated the relative roles of vicariance
and dispersal for a series of avian lineages from the arilands
of North America, and found that although vicariance was
the dominant mode of evolution, at least 25% of speciation
events could have been derived from dispersal across a preexisting barrier.
In contrast to the scarcity of investigations about the significance of potential forest corridors linking populations of
mammals and Neotropical faunas in general, botanists have
addressed the question of corridors for plants since the early
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
Phylogeography of Neotropical forest small mammals 83
1960s, and two possible migration routes between the
Amazon and the Atlantic forests have been suggested.
Rizzini (1963) and Andrade-Lima (1964) refer to a migration route through a mesophytic forest corridor that would
have crossed the Caatinga at certain periods since the late
Tertiary. The montane forests (brejos) that presently exist
within the semi-arid region would be in fact relicts of an
ancient and wider forest cover (Andrade-Lima, 1982).
Bigarella et al. (1975) added a second route, which they
called the Southeast-Northwest bridge, based on floristic
similarity between the eastern Amazon and south-eastern
Atlantic Forest. As suggested by Oliveira-Filho & Ratter
(1995), this route could have run through central Brazil,
either as a continuous forest corridor or as a series of forest
patches between which island-hopping would have occurred.
Finally, Por (1992) has noted three historical ÔpathwaysÕ of
connection between Amazonia and the Atlantic Forest: a
major southern route through the Paraná River basin, a
secondary route to the northeast around the horn of Brazil,
and a minor route via the gallery forests along rivers of the
central Brazilian Cerrado (Fig. 12). All three routes could
have been important for small mammals, because connections between these two rain forest domains are seen in the
phylogeography of individual species. For both Micoureus
demerarae (Figs 4a & 5) and Caluromys philander (Linnaeus) (Fig. 6b), populations from coastal Brazil are linked
with those in eastern Amazonia (Fig. 12), while for Metachirus nudicaudatus (Figs 4b & 5) and Caluromys lanatus
(Olfers) (Fig. 6b), the linkage is between coastal Brazil and
south-western Amazonia (Fig. 12). For Marmosa murina,
the path of linkage is equivocal as each of the three routes
between the coastal and Amazon forests are supported
(Fig. 6a & 12). Levels of sequence divergence in each of
these cases are relatively low (1–5%), suggesting that the
connections are more recent, and quite likely result from
Pleistocene vegetation shifts in the region.
In addition to the factors responsible for incongruence in
area cladograms discussed above, many other events could
have affected the history of the lineages discussed here. In
general, the old idea of biological and geological stability of
the tropics (Sanders, 1969) has been replaced in a view of
historical dynamism. There are ecologically orientated
hypotheses, like the Ecological Gradients Hypothesis
(Endler, 1982); there are hypotheses dealing with river
dynamics (Wallace, 1952; Salo et al., 1986); there are those
that incorporate tectonic history (Patton et al., 2000); still
others link the glacial cycles with sea-level changes creating
marine incursions or continental freshwater lakes (Klammer, 1984; Marroig & Cerqueira, 1997) and finally there is
the idea of climatic changes favouring the formation of
forest refuges (Haffer, 1969; Vanzolini & Williams, 1970).
These various hypotheses are not mutually exclusive and,
indeed, several could have influenced the evolutionary history of any particular lineage. It should not be surprising
that separate taxon lineage could have been affected by
different events.
There is also a temporal component to be accounted for,
specifically the age of each lineage and when the splitting
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
Figure 12 The distribution of lowland rain forests in South America.
The Amazon is divided into the four regions initially recognized in
1852 by Alfred Russel Wallace. The ÔpathwaysÕ connecting the
Amazon and the Atlantic Forest of coastal Brazil hypothesized by
Por (1992) are indicated. For these, the thickness of the arrows
indicates the degree of past biogeographical connection. Below are
two hypothetical cladograms depicting area relationships between
the Amazon (AM) and the Atlantic Forest (AF). Top: south-eastern
AM exhibits connection to Atlantic Forest; bottom: south-western
AM exhibits connection to Atlantic Forest. Beside each cladogram
are examples of didelphid species with phylogeographical patterns
that fit each hypothesis.
events occurred. It is apparent from Fig. 11 that there are
major differences in times of lineage diversification and that
most of these small-mammal lineages are very old, some
going back at least 8 Myr. These age estimates are so old
that one of the more influential hypotheses formulated to
explain Neotropical diversity, the Pleistocene Refugia
Hypothesis (Haffer, 1969; Vanzolini & Williams, 1970),
cannot be responsible for most of the speciation events in
these lineages, because times of divergence are mostly prePleistocene. A molecular systematic study of passerine birds
84
L. P. Costa
(Zink & Slowinski, 1995) also showed that diversification
rates were lower in the Pleistocene than for the preceding
period.
All the reasons discussed above indicate that many
regional events, varying in scale and age, were responsible
for the patterns we observe today. Therefore, I suggest that
the incongruence of area relationships reflects reality. These
findings also reinforce the idea that speciation in the Neotropics will not be explained by any single model of vicariance or climatic changes. As a result, and given the general
scarcity of phylogenies for Neotropical lineages, at this time
we should focus on recording specific biogeographical patterns rather than seeking to identify processes of diversification of the whole Neotropical fauna.
ACKNOWLEDGMENTS
I thank each of the following colleagues for providing
specimens used in the research and ⁄ or for aiding in the
field collections: Y. L. R. Leite, J. L. Patton, L. H.
Emmons, L. Geise, R. T. de Moura, M. D. Engstrom, A. L.
Gardner, L. Lessa, J. R. Malcolm, A. Paglia, M. J. de
J. Silva, N. da Silva, M. N. F. da Silva, R. M. Timm, R. S.
Voss, T. A. Yates, N. Cáceres, M. T. da Fonseca, A. M.
Fernandes, D. C. Bianchini, L. G. Vieira, F. P.C. Santos,
R. L. Dias and M. A. L. Sábato. J. L. Patton, D. B. Wake,
R. Gillespie, Y. L. R. Leite and P. Stott read the manuscript and provided helpful comments for its improvement.
M. F. Smith, S. Morshed and Y. Chaver provided essential
help in the laboratory and Y. L. R. Leite aided in the
preparation of figures. Financial support for either laboratory or field work was obtained from the National Geographic Society, World Wildlife Foundation, Berkeley
Chapter of Sigma-Xi, Museum of Vertebrate Zoology of
the University of California, Berkeley, John D. and Catherine T. MacArthur Foundation, and grants from the
National Science Foundation to J. L. Patton. Permits for
collection of specimens were kindly provided by IBAMA
(Instituto Brasileiro do Meio Ambiente) and by the Instituto Estadual de Florestas de Minas Gerais. During
four years of my doctoral studies, I was supported by a
fellowship from CAPES (Fundação Coordenação de
Aperfeiçoamento de Pessoal de Nı́vel Superior).
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BIOSKETCH
Leonora Pires Costa has a PhD in integrative biology
from the University of California at Berkeley. Her current
areas of research interest include evolution, phylogeography and systematics of Neotropical small mammals.
She has worked on ecology and systematics of small
mammals for the last 14 years, with extensive field work
carried out in the Atlantic Forest, the Amazon, Cerrado,
and Caatinga regions in Brazil. She is now a curatorial
and research associate at the Zoology Department of the
Institute of Biological Sciences, Federal University of
Minas Gerais, Brazil.
2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86