The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals

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

                                          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 hierar-
                                          chical 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
                                          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 speci-
                                          ation 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:

 2003 Blackwell Publishing Ltd
72   L. P. Costa

                                    Neotropical small mammals, Atlantic Forest, Amazon, Cerrado, Caatinga, phylogeo-
                                    graphy, evolutionary history of rain forest mammals.

                                                                    investigated as important elements in the biogeographical
                                                                    history of the region.
The aim of this paper is to investigate the biogeography and           The Caatinga is a xerophytic vegetation type characterized
evolutionary relationships of the non-volant, small-mammal          by spiny deciduous trees and shrubs in association with
fauna distributed across the Amazon, Atlantic Forest and the        succulent plants, cacti and bromeliads (Kuhlmann, 1977; De
central Brazilian forests. The Amazon and the Atlantic for-         Oliveira et al., 1999). This near-desert vegetation surrounds
ests morphoclimatic domains of South America (Ab’Saber,             inland ÔbrejoÕ forests, enclaves of moist forest caused by
1977) encompass the most diverse tropical forests in the            precipitation on the slopes of various plateaus (Mori, 1989).
world. Between these two forests lies a belt of more open           Botanical studies of these mesic enclaves and the north-
vegetation, including the Argentinean and Paraguayan                eastern coastal forests revealed floristic disjunction with
Chaco, the Caatinga in north-eastern Brazil, and the central        either the Amazon or the Atlantic Forest (Rizzini, 1963;
Brazilian Cerrado, the latter being the second largest domain       Bigarella et al., 1975; Coimbra-Filho & Câmara, 1996).
in Brazil extending over 2 million km2. This dry corridor of        Species of small mammals typical of rain forests [such as the
open vegetation, also called ÔThe major South American              slender mouse opossum Marmosops incanus (Lund) and the
disjunctionÕ (Brieger, 1969), has been considered as an             murid rodent Rhipidomys mastacalis (Lund)] are currently
important restraint to species migration between the two            found in ÔbrejoÕ forests in the states of Ceará and Bahia (Y.
rain forest regions (Moojen, 1948; Raven & Axelrod, 1974;           Leite and L. P. Costa, unpublished data). Based on mam-
Rizzini, 1979; Mori et al., 1981; Por, 1992). But if at first       malian distributional patterns, the fossil record and ecolog-
glance, the Amazon and Atlantic forests appear widely iso-          ical physiology, Vivo (1997) suggested that a mesic forest
lated, maps of present-day vegetation clearly shows that the        capable of supporting arboreal rain forest mammals existed
ubiquitous gallery forests and series of deciduous and              in the area presently occupied by the Caatinga, connecting
semi-deciduous forest patches constitute a network of               the eastern Amazonian and the Atlantic rain forests.
interconnected forests through otherwise open landscape                Therefore, forests are far from a negligible component of
(Oliveira-Filho & Ratter, 1995; Vivo, 1997). Other                  central Brazilian vegetation, and their role as migration
particularities of the Cerrado and Caatinga regions provide         routes for forest species must be recognized, especially when
evidence of past connections as well.                               evidence exists for a previously wider forest cover (Oliveira-
   Although dominated by a semi-deciduous arboreal                  Filho & Ratter, 1995; Vivo, 1997). The Amazon and
savanna, the Cerrado is composed of a mosaic of subunits            Atlantic forests were probably once continuous in the past,
that vary from grasslands to dry forests. Along the rivers that     becoming separated as increasing aridity in the Tertiary
transect this mosaic, there are strips of mesic forests, the        formed the belt of xeromorphic formations between them
gallery forests. Comprising
Phylogeography of Neotropical forest small mammals 73

relationships among organisms. When associated with geo-                logenetic framework for multiple taxa with present-day
graphical distributions, this information enables us to                 geographical distributions.
understand processes of diversification, to construct patterns             The work I report here is an extension of that previously
of phylogenetic relationships and to test explicit hypotheses           carried out by Patton et al. (1997), and the specific topics
of biogeographical history (e.g. Smith & Patton, 1993;                  covered in this paper are: (1) How phylogenetically distinct
Patton et al., 1994). The study of the principles and pro-              are the small mammal taxa of the Amazon with respect to
cesses governing the geographical distributions of genealo-             their Atlantic Forest relatives, and vice-versa? (2) Do the
gical lineages constitutes the new field of phylogeography, as          central Brazilian gallery and dry forests play a role in large-
defined by Avise et al. (1987). Previous work on phylogeo-              scale patterns of geographical distribution of the genetic
graphy of small mammals has addressed the relationships                 diversity and differentiation of lowland rain forest small
among taxa distributed across Amazonian and Atlantic                    mammals, acting as connections between the Amazon and
forests. In a preliminary analysis, Patton et al. (1997) util-          the Atlantic Forest? If so, what are the phylogenetic affinities
ized Cracaft’s (Cracraft, 1985, 1988; Cracraft & Prum,                  of the small mammals living in these interior forests with
1988) framework for small mammals, and found the sam-                   respect to the mammals living in the two rain forest
ples from the Atlantic Forest to form a monophyletic group              domains? (3) Given the geographical distribution of clades,
that was also the most divergent phylogenetically. A high               is there a consistent pattern of area-relationship across taxa?
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)]                     I focused my analysis on geographical clades of eleven
suggested that these two domains have been isolated for a               monophyletic groups of small mammals, including repre-
long period of time. Mustrangi & Patton (1997) examined                 sentatives of five genera (Caluromys J. A. Allen, Philander,
alternative hypotheses of relationships between Atlantic                Micoureus, Marmosops, Gracilinanus Gardner and
Forest and Amazonian species of Marmosops Matschie, and                 Creighton) and two widespread species of marsupials
in this case the monophyly of the Atlantic Forest species               [Metachirus nudicaudatus (Desmarest) and Marmosa
could not be confirmed.                                                 murina (Linnaeus)], two groups of Oryzomyini rodents
   The considerations above raise several questions regarding           (Oryzomys megacephalus group and O. macconnelli
the evolutionary history of the Neotropical rain forest                 group), and two arboreal sigmodontine rodent genera
mammal fauna. How much diversification has occurred                     (Rhipidomys Tschudi and Oecomys Thomas). Twenty-two
exclusively within the Amazon or the Atlantic Forest and                collection sites within gallery forests, semi-deciduous forests
how much diversification has been shared among these two                and dry forests in central and north-eastern areas in Brazil
rain forest domains (Fig. 1)? Have the central Brazilian                were sampled. Non-volant small mammals were trapped
forests played a historical role as extensions of the rain forest       using live- and snap-traps, and prepared according to
domains for small mammal species, enabling gene exchange                standardized museum procedures. Liver tissue samples were
through two regions otherwise isolated? Is there a common               collected in the field and preserved in alcohol or liquid
pattern of diversification across different mammal lineages,            nitrogen. DNA was extracted using the Chelex (Bio-Rad,
such as marsupials and murid rodents? One way to answer                 Hercules, CA, USA) method (Walsh et al., 1991), amplified
these questions is to integrate molecular data under a phy-             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 mam-
                                                                        mals 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
Figure 1 Diagram showing the distribution of the Amazon (Am)
and the Atlantic Forest (AF), the Cerrado (hatched) and the Caat-
                                                                        occurring throughout the Amazon, the Atlantic Forest, and
inga (stippled). In order to examine the evolutionary distinctiveness   forests in the Cerrado and Caatinga regions. Sequence di-
of the rain forest biomes, a cladistic approach was employed to         vergence was calculated using the Kimura two-parameter
determine if the sister-group relationships of small mammals were       (K2p) algorithm (Kimura, 1980) as implemented in PAUP*
found within (left) or between (right) the Amazon and the Atlantic      version 4.0b8 (Swofford, 1999). Hierarchical relationships
forests.                                                                among haplotypes, populations and formal taxa were

 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
74   L. P. Costa

inferred using the cladistic approach of maximum parsimony                     I compared areas and the clades identified by superimpo-
using PAUP*. Trees were constructed using the heuristic search              sing cladograms on maps of the geographical location of
option via stepwise addition, with ten replicates and random                samples. The concordance of area cladograms and the depth
addition sequence of taxa. The support for internal branches                of the nodes in these phylogenies permitted me to make
was evaluated by decay indices (Bremer, 1988) and bootstrap                 inferences on how, when and where the taxa differentiated
analyses (Felsenstein, 1985), with 100 bootstrap replicates                 and thereby to address the historical importance of the
each consisting of a full heuristic search as described above.              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            (Fig. 2a), was the Atlantic Forest (AF) clade the sister group
of phylogenetic distinctiveness of the rain forest domains            to all other areas. In four of eight cases, the Atlantic Forest
was examined under a cladistic evolutionary approach. In              clade was deeply nested in a more inclusive clade (Fig. 2b),
other words, I asked if sister-group relationships were con-          while in three cases it showed up as a composite area
centrated within or between the Amazon and the Atlantic               (Fig. 2c). A more detailed example of the last case can be seen
Forest (Fig. 1).                                                      in Fig. 3, which depicts the phylogeographical relationships
  To explore the discrepancy in time of splitting events in           of five species of the climbing rat Rhipidomys. There are two
the many taxa utilized in the analyses, I estimated branch            species in the Atlantic Forest, Rhipidomys mastacalis in the
lengths of the trees by maximum likelihood using third                north and an undescribed species in the south. These two
position changes only, constraining and not constraining a            species are not sister groups. Rather, the southern species has
molecular clock. Then, I performed a likelihood ratio test            a sister relationship with R. leucodactylus Tschudi, a species
(LRT) of the molecular clock, and used only the taxa for              from the west-central Amazon, while R. mastacalis is closely
which the LRT was not significantly different (Huelsenbeck            related to R. nitela Thomas, a species occurring in the central
& Rannala, 1997). Calibration of the clock was carried out            Brazilian area, the two forming the sister group to the species
for marsupials using the estimates of Mustrangi & Patton              of the south-western Amazon, R. gardneri Patton, da Silva
(1997) for Marmosops, and for the rodents using the para-             and Malcolm.
meters of Smith & Patton (1999).                                         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
RESULTS                                                               mammals, K2p distances are commonly greater among
                                                                      localities within domains than across domains. An example of
The phylogeographical relationships between
                                                                      this is the woolly mouse opossum, Micoureus demerarae
the Amazon and the Atlantic Forest
                                                                      (Thomas). This species occurs throughout the Amazon and
From the eleven groups analysed, three (Micoureus, Graci-             the central Brazilian forests, reaching the Atlantic Forest in
linanus and Oryzomys macconnelli group) showed poly-                  coastal Brazil (Fig. 4a). Haplotypes from the most eastern
tomic relationships, and for that reason could not be used in         Amazon locality are closer to those from the northern Atlantic
the inference of sister-group relationships between geo-              Forest than they are to haplotypes from other Amazonian
graphical clades in the two rain forest domains. Among the            localities (Fig. 5). Similarly, haplotypes of the brown four-
eight taxa remaining (Fig. 2), in only one group, Philander           eyed opossum, Metachirus nudicaudatus (Figs 4b & 5), and

Figure 3 Phylogeographical relationships
among cytochrome b haplotypes of five spe-
cies of the climbing rat, genus Rhipidomys.
The map shows the range of the genus
Rhipidomys and the geographical distribu-
tion 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. Per-
centages are average Kimura two-parameter

 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
76   L. P. Costa

                                                                                       Figure 4 Maps of the range and geograph-
                                                                                       ical 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 compo-
                                                                                       nents in the Atlantic Forest. For Micoureus,
                                                                                       solid lines circumscribing samples correspond
                                                                                       to species boundaries and dashed lines indi-
                                                                                       cate clades within species; symbols corres-
                                                                                       pond to each of the five species. For
                                                                                       Metachirus, solid lines circumscribe intra-
                                                                                       specific 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 &          two geographically structured clades of the species in the
6a), from different localities in the Atlantic Forest are        Atlantic Forest. The break in the distribution of species and
genetically more similar to those compared from the Amazon       clades of these taxa is nearly coincidental. Nevertheless, the
than the Amazonian haplotypes are to each other. This pat-       K2p distances within each of these clades are different,
tern can also be observed for species within the same complex.   suggesting that vicariant events affected taxa at different
As an example, Oryzomys megacephalus Fisher from the             times. Cyclic climatic fluctuations are one plausible explan-
northern Amazon and central Brazil is more closely related       ation for this coincidental pattern in space but not in time.
to O. laticeps (Lund) from the Atlantic Forest than to
O. perenensis (Allen) from the western Amazon (Fig. 7).
                                                                 The phylogeographical affinities of the Cerrado and
   In terms of the Atlantic Forest itself, there are northern
                                                                 Caatinga domains
and southern components, as exemplified by Rhipidomys
(Fig. 3), Micoureus (Fig. 4a) and Metachirus Burmeister          The samples from the intervening region between the
(Fig. 4b). In both Rhipidomys and Micoureus, clades cor-         Atlantic Forest and Amazonia, including the Cerrado and
responding to two different species replace one another from     Caatinga domains and for simplification called here the
north to south, while in Metachirus nudicaudatus, there are      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, Metachi-
rus 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           thesis, I took into account all localities within the Cerrado
this broad area in the diversification of rain forest small           and Caatinga, and those in the transition areas between
mammals. Animals inhabiting this region could have their              these two domains and the lowland rain forests, but exclu-
closest relatives in the Atlantic Forest, in the Amazon, or be        ded those from the central Amazon and Atlantic Forest
basal relative to the two rain forest domains (Fig. 8). The           themselves. At each CA locality, only taxa that had rela-
results, derived from analyses of all trees in Figs 2–7, are          tionships with either the Amazon or the Atlantic Forest were
summarized in Table 1. Five of eleven groups could not be             considered. These comparisons (Fig. 9) do not present the
used in this analysis, because two of them are absent in one          clear-cut trend hypothesized above. Rather, in some cases
of the areas and three showed polytomic relationships (for            specimens in localities near the Atlantic Forest share a more
details on these taxa, see Table 1). As one might expect              recent common ancestor with Amazonian groups, whereas
when dealing with forest animals living in a somewhat                 in the transition zone between the Cerrado and the Amazon,
more foreign environment, the samples from the CA were                specimens were often related to Atlantic Forest individuals.
never basal to their relatives in the forest domains. More            It is also interesting to note that localities to the southwest of
often the CA clade was the sister to an Atlantic Forest clade         the CA tend to be more affiliated to the Amazon, while
than to an Amazonian clade, as is the case for Marmosa                localities in the northeast are more often related to the
murina (Figs 2b & 6a), Caluromys (Figs 2c & 6b),                      Atlantic Forest (Fig. 9). This observation suggests possible
Rhipidomys (Figs 2c & 3) and the Oecomys trinitatis group             routes and directions of interchange between the Amazon
(Fig. 2b).                                                            and the Atlantic Forest.
   I also looked at individual localities in the CA to see if the
affiliation of this area and the two rain forest domains was
                                                                      Patterns and timing of diversification
only a matter of geographical distance from the source in
either the Atlantic Forest or the Amazon (Fig. 9). Under the          One of the aims of this paper was to search for congruent
assumption of isolation by distance, samples from localities          patterns of diversification linking subareas in each domain.
in the CA situated near the Amazon should share a more                Nevertheless, while some genera or group of species show a
recent common ancestor with Amazonian samples, whereas                strong hierarchical structure over the whole sampled geo-
those from localities closer to the Atlantic Forest should be         graphical area, others, although geographically structured,
related to those in Atlantic Forest. To explore this hypo-            show little resolution with respect to the relationships

 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
78   L. P. Costa

                                                                                      Figure 6 Maps showing the range and geo-
                                                                                      graphical distribution of the samples of spe-
                                                                                      cies 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-param-
                                                                                      eter distances.

among species or geographical clades within species. Two        (Fig. 10c) are structured into three sharply defined clades
closely related species groups of the rice rat and repre-       hierarchically organized, while the geographical clades of
sentatives of two sister genera of didelphids illustrate this   Micoureus demerarae (Fig. 10d) are linked in the form of a
situation in Fig. 10. The Oryzomys megacephalus group           basal polytomy. Other taxa examined present similar
(Fig. 10a) is comprised of three species that replace one       contrasts. Among eight taxa that are widespread in the
another from east to west, with two (O. laticeps and            Amazon, Atlantic Forest and CA, five show resolved area
O. megacephalus) more closely related species in the At-        relationships while four do not (Table 2). Among the taxa
lantic Forest and northern Amazon ⁄ south central Brazil,       that have restricted distributions or are absent in one of
and a more distant one (O. perenensis) in the western           the domains, two have resolved area relationships
Amazon. In contrast, rice rats of the Oryzomys macconelli       while one does not (Table 2). As groups of closed
group (Fig. 10b), although strongly divergent and geo-          related taxa (e.g. sister groups Marmosa ⁄ Micoureus and
graphically bounded, do not show the same level of reso-        Gracilinanus ⁄ Marmosops) can present resolved or unre-
lution among the five species included in the complex.          solved area relationships, independently of the geograph-
Similarly, the geographical clades of Marmosa murina            ical 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.

                                                                        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 con-
                                                                        cordance which indicates concurrent vicariant events: the
Figure 8 Area cladograms depicting possible phylogeographical
                                                                        split of the Atlantic Forest species Philander frenatus (Olfers)
affinities of the central area (CA) under three hypotheses: the sam-    from all others in the genus is nearly coincidental with the
ples from the CA could be more closely related to those from the        split of the three species of Gracilinanus. Similarly, there is a
Atlantic Forest (left), to Amazon samples (middle), or be basal rel-    simultaneous split between the north-western Amazonian
ative to the two forest biomes (right).                                 species of Rhipidomys (R. macconelli de Winton and
                                                                        R. wetzeli Gardner) and western Amazonian species of
                                                                        Marmosops [M. neblina Gardner and M. noctivagus
cladogram resolution is neither a matter of phylogenetic                (Tschudi)] from other species in their complex.
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.               Cracraft & Prum (1988) hypothesized historical relation-
Although cladogenesis and gene divergence are not neces-                ships among putative centres of endemism in the Neo-
sarily coincident (Edwards & Beerli, 2000), the magnitude               tropics through successive vicariant events for four clades
of the differences in coalescence times observed in Fig. 11             of birds. Interestingly, the only discordant pattern between

 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
80     L. P. Costa

                                                                                                Table 1 Sister-group relationships of six
                                 Central area                                                   groups of small mammals distributed in the
                                                                                                Amazon, Atlantic Forest (AF) and central
                                 Sister to the     Sister to the   Basal to the Atlantic
Taxa                             Atlantic Forest   Amazon          Forest and to the Amazon

Oryzomys megacephalus group                        •
Oecomys trinitatis group         •
Marmosa murina                   •
Philander                                          •
Caluromys                        •
Rhipidomys                       •

*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 local-
                                                                                                ities 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,                    distribution of clades and the levels of divergence found,
which appeared in their analysis as a composite, or bio-                 the central Brazilian area does not behave as a separate
geographical ÔhybridÕ area, having some component taxa                   region, but is complementary to either Amazon or Atlantic
nested within the Amazonian clade while others were                      forests. As a consequence, the central Brazilian forests are
outside this clade. Patton et al. (1997) found the Atlantic              an integral part of the evolutionary history of lowland
Forest as basal or polytomic in relation to other areas in               small mammals. Their role as present and past habitats for
the Amazon basin and Central America, for six generic or                 forest species must be recognized, and representatives from
infrageneric groups of didelphid marsupials and two spe-                 this area should always be included in the analyses of the
cies complexes of the murid rodent Oryzomys Baird. In                    evolutionary history of lowland rain forest faunas.
my expanded analyses, including the same taxa examined                      In terms of the affinities of the central Brazilian area, there
by Patton et al. (1997) as well as additional taxa, the                  is a slight trend towards a closer association of the small
Atlantic Forest was often nested in a more inclusive clade               mammals living in forest habitats in the central region with
(Fig. 2b), but similar to Cracaft and Prum’s results, it also            those from the Atlantic Forest, as revealed by the analyses of
showed up as a composite area (Fig. 2c). The main dif-                   sister group relationships (Table 1). Nevertheless, the ana-
ference between my work and the previous analyses by                     lyses of individual localities summarized in Fig. 9 did not
Patton and collaborators is the inclusion of samples from                indicate the same result. Hence, at this point the data suggest
the region between the Amazon and Atlantic Forest. As a                  that the CA region has affinities with both the Atlantic
result, if earlier we viewed the Atlantic Forest as a dis-               Forest and the Amazon. This result is not unexpected,
connected area, long separated from the Amazon, this                     because many taxa contemplated in this study belong to old
view has drastically changed with the inclusion of samples               lineages (Fig. 11) that experienced numerous contractions
from the central Brazilian forests. Given the geographical               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                                                  Area relationships
                                                   Pattern of distribution                Resolved                        Not resolved

                                                   Widespread in the Amazon,              Oryzomys megacephalus           Oryzomys macconnelli
                                                   Atlantic Forest and central area        group                           group
                                                                                          Marmosa murina                  Micoureus demerarae
                                                                                          Caluromys                       Philander
                                                                                          Oecomys trinitatis group
                                                   Restricted or absent in                Gracilinanus                    Marmosops
                                                    one of the areas                      Metachirus

cene and preceding geological eras. Nevertheless, a decisive                 (2000) have noted a latitudinal break in the distribution of
assessment of the affinities of the CA with the rain forest                  Atlantic Forest vertebrates, which separates the north from
domains will have to wait until more phylogenies are                         the south in reptiles, lowland birds and lowland mammals,
available.                                                                   the latter two using parsimony analysis of endemicity.
  The partitioning of the Amazon into several highly                         Although these analyses found a strong sister-group
divergent phylogeographical areas has already been docu-                     relationship between the northern and the southern Atlantic
mented (Cracraft & Prum, 1988; Patton et al., 1997,                          Forest clades, in my analysis I found a different pattern:
2000). In contrast, the division of the Atlantic Forest as                   often, taxa occurring in northern and southern Atlantic
indicated by the phylogenetic analyses in this paper has                     Forest were not sister taxa. Species of Rhipidomys and
been unrecognized for small mammals until very recently.                     Micoureus illustrate this situation in Figs 3 and 4a. The
Vanzolini (1988), Bates et al. (1998) and Costa et al.                       species relationships of the genus Marmosops are likely

 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
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            cussed by Zink et al. (2001) and include differences in levels
results further strengthen the likelihood that the Atlantic      of gene flow among populations, different responses of
Forest is a composite area.                                      species to the same environmental or geological feature that
   One of the main observations from the data presented          could have acted or not as a barrier to gene flow, or different
here is the lack of congruence of area cladograms across         Ôresponse timesÕ of species effectively isolated by the same
taxa, a result concordant with recent data for other groups      barrier, because of differences in their effective population
of taxa. To date, the question of area relationships between     size. All the above explanations assume vicariance as the
and within the Atlantic Forest and Amazonia has addressed        historical process shaping the distribution of taxa and ulti-
primarily avian taxa. Bates et al. (1998), studying Neo-         mately leading to phylogeographical congruence. Neverthe-
tropical lowland passerine birds and using raw geographical      less, the effects of dispersal confounding the signal in a
distributions of species and subspecies, found many different    phylogeographical analysis cannot be ignored (Avise, 2000).
hypotheses of area relationships and concluded that a single     As pointed out by Ronquist (1997), dispersal barriers appear
network of Neotropical area relationships is not likely. Zink    and disappear throughout earth history and may have dif-
et al. (2000) examined six lineages of birds occurring in the    ferent effects on the evolutionary history of different species.
arid lands of North America and obtained different area          Zink et al. (2000) evaluated the relative roles of vicariance
cladograms depending on how widespread and missing taxa          and dispersal for a series of avian lineages from the arilands
were coded. Nonetheless, no cladogram was obtained in            of North America, and found that although vicariance was
which all lineages were congruent. Are these results just an     the dominant mode of evolution, at least 25% of speciation
artefact of the materials and methods utilized or do they        events could have been derived from dispersal across a pre-
reflect reality? I argued above that the lack of congruence in   existing barrier.
cladograms obtained for the many taxa examined here was             In contrast to the scarcity of investigations about the sig-
not because of phylogenetic constraints or the patterns of       nificance of potential forest corridors linking populations of
distribution of taxa. Other reasons for the lack of congru-      mammals and Neotropical faunas in general, botanists have
ence in phylogeographical patterns were thoroughly dis-          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 migra-
tion 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 connec-
tions between these two rain forest domains are seen in the
phylogeography of individual species. For both Micoureus
demerarae (Figs 4a & 5) and Caluromys philander (Lin-
naeus) (Fig. 6b), populations from coastal Brazil are linked
with those in eastern Amazonia (Fig. 12), while for Meta-
chirus 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             Figure 12 The distribution of lowland rain forests in South America.
Pleistocene vegetation shifts in the region.                          The Amazon is divided into the four regions initially recognized in
   In addition to the factors responsible for incongruence in         1852 by Alfred Russel Wallace. The ÔpathwaysÕ connecting the
area cladograms discussed above, many other events could              Amazon and the Atlantic Forest of coastal Brazil hypothesized by
have affected the history of the lineages discussed here. In          Por (1992) are indicated. For these, the thickness of the arrows
general, the old idea of biological and geological stability of       indicates the degree of past biogeographical connection. Below are
the tropics (Sanders, 1969) has been replaced in a view of            two hypothetical cladograms depicting area relationships between
                                                                      the Amazon (AM) and the Atlantic Forest (AF). Top: south-eastern
historical dynamism. There are ecologically orientated
                                                                      AM exhibits connection to Atlantic Forest; bottom: south-western
hypotheses, like the Ecological Gradients Hypothesis                  AM exhibits connection to Atlantic Forest. Beside each cladogram
(Endler, 1982); there are hypotheses dealing with river               are examples of didelphid species with phylogeographical patterns
dynamics (Wallace, 1952; Salo et al., 1986); there are those          that fit each hypothesis.
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 (Klam-
mer, 1984; Marroig & Cerqueira, 1997) and finally there is            events occurred. It is apparent from Fig. 11 that there are
the idea of climatic changes favouring the formation of               major differences in times of lineage diversification and that
forest refuges (Haffer, 1969; Vanzolini & Williams, 1970).            most of these small-mammal lineages are very old, some
These various hypotheses are not mutually exclusive and,              going back at least 8 Myr. These age estimates are so old
indeed, several could have influenced the evolutionary his-           that one of the more influential hypotheses formulated to
tory of any particular lineage. It should not be surprising           explain Neotropical diversity, the Pleistocene Refugia
that separate taxon lineage could have been affected by               Hypothesis (Haffer, 1969; Vanzolini & Williams, 1970),
different events.                                                     cannot be responsible for most of the speciation events in
   There is also a temporal component to be accounted for,            these lineages, because times of divergence are mostly pre-
specifically the age of each lineage and when the splitting           Pleistocene. A molecular systematic study of passerine birds

 2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
84   L. P. Costa

(Zink & Slowinski, 1995) also showed that diversification            Avise, J.C., Arnold, J., Ball, R.M., Bermingham, E., Lamb, T.,
rates were lower in the Pleistocene than for the preceding             Neigel, J.E., Reeb, C.A. & Saunders, N.C. (1987) Intraspe-
period.                                                                cific phylogeography the mitochondrial DNA bridge between
   All the reasons discussed above indicate that many                  population genetics and systematics. Annual Review of
regional events, varying in scale and age, were responsible            Ecology and Systematics, 18, 489–522.
for the patterns we observe today. Therefore, I suggest that         Ayala, F.J. (1997) Vagaries of the molecular clock. Proceed-
the incongruence of area relationships reflects reality. These         ings of the National Academy of Science, USA, 94, 7776–
findings also reinforce the idea that speciation in the Neo-           7783.
                                                                     Bates, J.M., Hackett, S.J. & Cracraft, J. (1998) Area-relation-
tropics will not be explained by any single model of vicar-
                                                                       ships in the neotropical lowlands: an hypothesis based on raw
iance or climatic changes. As a result, and given the general
                                                                       distributions of passerine birds. Journal of Biogeography, 25,
scarcity of phylogenies for Neotropical lineages, at this time
we should focus on recording specific biogeographical pat-
                                                                     Bigarella, J.J., Andrade-Lima, D. & Riehs, P.J. (1975) Con-
terns rather than seeking to identify processes of diversifi-          siderações a respeito das mudanças paleoambientais na
cation of the whole Neotropical fauna.                                 distribuição de algumas espécies vegetais e animais no Brasil.
                                                                       Anais da Academia Brasileira de Ciências, 47, 411–464.
ACKNOWLEDGMENTS                                                      Bremer, K. (1988) The limits of amino-acid sequence data in
                                                                       angiosperm phylogenetic reconstruction. Evolution, 42, 795–
I thank each of the following colleagues for providing                 803.
specimens used in the research and ⁄ or for aiding in the            Brieger, F.G. (1969b) Contribuição à fitogeografia do Brasil com
field collections: Y. L. R. Leite, J. L. Patton, L. H.                 referência especial as orquı́deas. Anais do XX Congresso
Emmons, L. Geise, R. T. de Moura, M. D. Engstrom, A. L.                Nacional de Botânica, 41–44.
Gardner, L. Lessa, J. R. Malcolm, A. Paglia, M. J. de                Coimbra-Filho, A.F. & Câmara, I.G. (1996) Os limites originais
J. Silva, N. da Silva, M. N. F. da Silva, R. M. Timm, R. S.            do bioma Mata Atlântica na Região Nordeste do Brasil,
Voss, T. A. Yates, N. Cáceres, M. T. da Fonseca, A. M.                p. 86. FBCN Fundação Brasileira para a Conservação da
Fernandes, D. C. Bianchini, L. G. Vieira, F. P.C. Santos,              Natureza, Rio de Janeiro.
R. L. Dias and M. A. L. Sábato. J. L. Patton, D. B. Wake,           Costa, L.P. (2001) Phylogeographic studies on Neotropical
R. Gillespie, Y. L. R. Leite and P. Stott read the manu-               small mammals, PhD Thesis, University of California, Berke-
script and provided helpful comments for its improvement.              ley.
M. F. Smith, S. Morshed and Y. Chaver provided essential             Costa, L.P., Leite, Y.L.R., Fonseca, G.A.B.d. & Fonseca, M.T.d.
                                                                       (2000) Biogeography of South American forest mammals:
help in the laboratory and Y. L. R. Leite aided in the
                                                                       endemism and diversity in the Atlantic Forest. Biotropica, 32,
preparation of figures. Financial support for either labor-
atory or field work was obtained from the National Ge-
                                                                     Costa, L.P., Leite, Y.L.R. & Patton, J.L. (in press) Phylogeo-
ographic Society, World Wildlife Foundation, Berkeley
                                                                       graphy and systematic notes on two species of Gracilinanus
Chapter of Sigma-Xi, Museum of Vertebrate Zoology of                   (Marsupialia, Didelphidae). Proceedings of the Biology
the University of California, Berkeley, John D. and Cath-              Society of Washington.
erine T. MacArthur Foundation, and grants from the                   Cracraft, J. (1985) Historical Biogeography and patterns of
National Science Foundation to J. L. Patton. Permits for               differentiation within the South American avifauna: areas of
collection of specimens were kindly provided by IBAMA                  endemism. Ornithological Monographs, 36, 49–84.
(Instituto Brasileiro do Meio Ambiente) and by the Insti-            Cracraft, J. (1988) Deep-history biogeography retrieving the
tuto Estadual de Florestas de Minas Gerais. During                     historical pattern of evolving continental biotas. Systematic
four years of my doctoral studies, I was supported by a                Zoology, 37, 221–236.
fellowship from CAPES (Fundação Coordenação de                   Cracraft, J. & Prum, R.O. (1988) Patterns and processes of
Aperfeiçoamento de Pessoal de Nı́vel Superior).                       diversification: speciation and historical congruence in some
                                                                       Neotropical birds. Evolution, 42, 603–620.
                                                                     De Oliveira, P.E., Franca Barreto, A.M. & Suguio, K. (1999)
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Wallace, A.R. (1952) On the monkeys of the Amazon. Proceed-
  ings of the Zoological Society of London, 20, 107–110.
Walsh, P.S., Metzger, D.A. & Higuchi, R. (1991) Chelex 100 as
  a medium for simple extraction of DNA for PCR-based
                                                                    Leonora Pires Costa has a PhD in integrative biology
  typing from forensic material. Biotechniques, 10, 506–513.
                                                                    from the University of California at Berkeley. Her current
Zink, R.M., Blackwell-Rago, R.C. & Ronquist, F. (2000) The
                                                                    areas of research interest include evolution, phylogeo-
  shifting roles of dispersal and vicariance in biogeography.
                                                                    graphy and systematics of Neotropical small mammals.
  Proceedings of the Royal Society Biological Sciences Series B,
                                                                    She has worked on ecology and systematics of small
  267, 497–503.
                                                                    mammals for the last 14 years, with extensive field work
Zink, R.M., Kessen, A.E., Line, T.V. & Blackwell-Rago, R.C.
                                                                    carried out in the Atlantic Forest, the Amazon, Cerrado,
  (2001) Comparative phylogeography of some aridland bird
                                                                    and Caatinga regions in Brazil. She is now a curatorial
  species. Condor, 103, 1–10.
                                                                    and research associate at the Zoology Department of the
Zink, R.M. & Slowinski, J.B. (1995) Evidence from molecular
                                                                    Institute of Biological Sciences, Federal University of
  systematics for decreased avian diversification in the Pleisto-   Minas Gerais, Brazil.
  cene Epoch. Proceedings of the National Academy of
  Sciences, 92, 5832–5835.

                                                                     2003 Blackwell Publishing Ltd, Journal of Biogeography, 30, 71–86
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