Yuri Leite

The forest refuge hypothesis (FRH) has long been a paradigm for explaining the extreme biological diversity of tropical forests. According to this hypothesis, forest retraction and fragmentation during glacial periods would have promoted reproductive isolation and consequently speciation in forest patches (ecological refuges) surrounded by open habitats. The recent use of paleoclimatic models of species and habitat distributions revitalized the FRH, not by considering refuges as the main drivers of allopatric speciation, but instead by suggesting that high contemporary diversity is associated with historically stable forest areas. However, the role of the emerged continental shelf on the Atlantic Forest biodiversity hotspot of eastern South America during glacial periods has been ignored in the literature. Here, we combined results of species distribution models with coalescent simulations based on DNA sequences to explore the congruence between scenarios of forest dynamics through time and the genetic structure of mammal species cooccurring in the central region of the Atlantic Forest. Contrary to the FRH predictions, we found more fragmentation of suitable habitats during the last interglacial (LIG) and the present than in the last glacial maximum (LGM), probably due to topography. We also detected expansion of suitable climatic conditions onto the emerged continental shelf during the LGM, which would have allowed forests and forest-adapted species to expand. The interplay of sea level and land distribution must have been crucial in the biogeographic history of the Atlantic Forest, and forest refuges played only a minor role, if any, in this biodiversity hotspot during glacial periods. last glacial maximum | sea level | Atlantic Forest | Quaternary | continental shelf T he extreme biological diversity of tropical forests has inspired and puzzled naturalists and scientists for centuries, and the forest refuge hypothesis (FRH) has long been one of the major paradigms to explain it. According to the FRH, forest retraction and fragmentation during glacial periods would have promoted isolation and consequently allopatric speciation in forest patches, or ecological refuges, surrounded by open habitats in the Amazon (1). Although originally based on climate fluctuations in the Pleistocene, the FRH was subsequently invoked for climate changes irrespective of the time period (2). The FRH was also applied to South America's Atlantic Forest (3), one of the top-five biodiversity hotspots on Earth (4). The FRH gained broad acceptance during the 1980s when empirical paleoecological data from neotropical rainforests were still lacking. Nevertheless, heavy criticism came upon the FRH because some paleobotanical data showed that forests had persisted throughout glacial cycles (5). As paleoclimatic models of species and habitats became widely used, recent studies revitalized the FRH, not by considering refuges as the main drivers of allopatric speciation, but instead by suggesting that high contemporary diversity and endemism are associated with historically stable Atlantic Forest areas (6). This hypothesis is based on the assumption that populations were restricted to refugia within the bounds of the current observed distribution of a species, thus disregarding paleogeography. Here, we used coalescent simulations to test alternative demographic models and found potentially larger past distributions. Contrary to the refuge models, here, we show that forest specialist small mammal populations actually expanded during the last glacial period, after the expansion of the Atlantic Forest onto the Brazilian continental shelf, a process that has been neglected in paleoenvironmental reconstructions. This new idea is what we call the Atlantis Forest hypothesis , in homage to Plato's legendary continent, which was eventually swallowed up by the sea. We combined the results of distribution models with coalescent simulations based on DNA sequences to explore the congruence between scenarios of forest dynamics through time and the genetic diversity of mammal species cooccurring in the central region of the Atlantic Forest. First, we used climatic models to estimate range shifts from the last interglacial (LIG) [∼120,000 y before present (120 kybp)], through the last glacial maximum (LGM) (∼21 kybp), to the present. For LGM simulations, we extended the baseline climate data onto the exposed continental shelf, in contrast to other studies (6). Then, we used coalescent simulations to test the genetic data for congruence with historic demographic Significance The tropical forests of South America are among the most diverse and unique habitats in the world in terms of plant and animal species. One of the most popular explanations for this diversity and endemism is the idea that forests retracted and fragmented during glacial periods, forming ecological refuges, surrounded by dry lands or savannas. These historically stable forest refuges would have been responsible for maintaining the pattern of diversity and endemism observed today. Here, we show that the Atlantic Forest of eastern South America probably expanded, rather than contracted, during the last glacial period. In addition, the emerged Brazilian continental shelf played a major, yet neglected, role on the evolution of this biodiversity hotspot during the last glacial period.

One or two diversification models alone cannot explain biodiversity evolution in the Atlantic Forest, or any other megadiverse biome, as we (1, 2) pointed out long before Raposo do Amaral et al. (3). In our recent paper (4), we present the Atlantis Forest hypothesis (AFH), which is an additional perspective to the Atlantic Forest evolution, beyond the forest refuge hypothesis (FRH). The AFH incorporates irrefutable Quaternary sea-level changes, which had been overlooked in the literature, and this is the main point of our paper. Support for the AFH came from small mammal distribution modeling and coalescent simulations based on mitochondrial DNA (mtDNA) sequences, which have been success- fully used in thousands of biogeographical studies for over 30 y, forming the basis of the booming field of phylogeography (5) and providing support for the FRH (6). We agree that analyses based on a single locus might be subject to stochastic error, and a recent re- view found mito-nuclear discordance in 18% of biogeo- graphical studies (7). This is not a negligible number, but most mtDNA results can be taken as reliable indi- cators of geographical population structure and phylo- geographical patterns (8).

Trinomys is a genus of terrestrial spiny rats from the Atlantic Forest, and three species occur in the state of Espírito Santo, eastern Brazil: T. gratiosus, T. paratus, and T. setosus. The levels of morphological variation within and among these species are virtually unknown, and their geographic ranges have not been properly assessed. These three species are externally very similar, hampering their identification in surveys and ecological studies that are not based on voucher specimens. We evaluated 162 specimens of Trinomys spp. from eastern Brazil, especially from the state of Espírito Santo, and used data from skulls, skins, and bacula to examine morphological variation and its taxonomic implications. We found extensive morphological variation in the skins and skulls even when diagnostic characters were examined, such as the number of dental lophs and bones contributing to the postorbital process. We also found variation in bacular shape among and within species, including polymorphism among individuals from the same population. The geographic range of each species in Espírito Santo was well defined: T. setosus occurred on the left (north) bank of the Doce River, and the other two species, T. gratiosus and T. paratus, occurred on the right (south) bank of this river; however, T. gratiosus was found at altitudes above 500 m, whereas T. paratus occurred below 580 m. Despite difficulties in species identification, the results of morphological and morphometric analyses are compatible with the current classification of these three species. In addition, the level of morphological variation found in specimens identified as T. g. panema—including types—falls within the range of T. g. gratiosus, confirming the taxonomic status of the former as a junior synonym of the latter.

ABSTRACT AimTo investigate the biogeographical history of the Pantepui region based on the phylogenetic relationships and divergence dates of a tepui-endemic small mammal: the Roraima mouse, Podoxymys roraimae. This mouse is one of the rarest and most restricted mammals in terms of geographical distribution, and its evolutionary position has never been evaluated within a rigorous phylogenetic framework. LocationThe Pantepui biogeographical region of northern South America, which harbours a remarkable flora and fauna in one of the most dramatic landscapes on Earth. Methods We used maximum-likelihood and Bayesian analyses of mitochondrial (cytb) and nuclear (irbp) DNA sequences from a specimen of P. roraimae to infer phylogenetic affinities and estimate divergence times of Podoxymys from its closest relatives based on a relaxed molecular clock model. ResultsPodoxymys lies within the Akodontini tribe of the rodent subfamily Sigmodontinae, closely related to Thalpomys and Necromys, two taxa found on the Brazilian Plateau. The divergence of Podoxymys from its closely related genera was estimated at 2.47-3.68Ma, at the end of the Neogene (Pliocene) and before the start of the Pleistocene climatic oscillations. Main conclusionsPodoxymys roraimae is a relict species restricted to tepui summits, and its closest relatives are taxa found in open-vegetation biomes, especially the Cerrado vegetation on the Brazilian Plateau. Our results do not conform to the predictions of currently proposed models of Pantepui faunal evolution, but instead indicate a possible relationship between the Guiana and Brazilian shields during the Pliocene.

Research on the biology of Neotropical small mammals has increased in recent decades, and many studies have emphasized ecological and population attributes, but information on reproduction is still scarce. Reproduction is one of the most important natural history attributes because it is related to almost every structural, physiological and behavioral adaptation of an individual or a species. Most research on rodent reproduction concentrates in temperate areas and there is an evident lack of data from the Neotropical region. We compared reproductive patterns of sigmodontine and echimyid rodents using necropsy data from 135 specimens collected in the field and belonging to 22 species of sigmodontine and 8 species of echimyid rodents. We estimated embryonic litter size by counting the number of embryos or the number and placement of placental scars in pregnant and parous females. Although smaller in body size, sigmodontines have larger litter sizes (3.6 ± 1.2) than echimyids (2.1 ± 0.7), indicating a tendency toward r and K reproductive strategies, respectively. Embryonic litter size in pregnant females was not statistically different from the number of placental scars, so the latter is a reliable estimate of the former in both sigmodontines and echimyids. Embryo implantation is asymmetric regarding uterine horns in sigmodontines, with predominance in the right horn, but not in echimyids. The data obtained in this study are relevant in understanding the life history of two of the most diverse clades of neotropical mammals.

We report the discovery of a new species of Coendou (Rodentia, Erethizontidae), here designated Coendou speratus sp. nov. This small porcupine, locally known as coandumirim, is found in the Pernambuco Endemism Centre in the Atlantic coast of northeastern Brazil north of the São Francisco river, one of the most important known biodiversity hotspots. The geographic range of C. speratus overlaps with that of the larger, widespread C. prehensilis, but not with that of C. insidiosus from the southeastern Atlantic forest, nor with that of C. nycthemera, an eastern Amazonian species. Coendou speratus is a small-bodied, long-tailed species that appears to be completely spiny because it lacks long dorsal fur. The dorsal quills have conspicuously brownish red tips that contrast with the blackish dorsal background color. The new species is overall similar to C. nycthemera, but the dorsal body quills are typically tricolored in the former and bicolored in the latter. The new species is externally very distinct from C. insidiosus, especially because the latter has bicolored dorsal quills that are almost completely hidden beneath longer and homogeneous pale or dark hairs.

Although codistributed species are affected by the same abiotic factors, such as rivers and seasonal flooding regimes, ecological traits, such as locomotion habits and habitat preferences, may also influence differences in levels of genetic diversity and differentiation. We examined population genetic structure and diversity of Hylaeamys megacephalus and Oecomys aff. roberti, two cricetid rodent species from the mid-Araguaia River in central Brazil, using mitochondrial DNA sequence data. Specifically, we aim to test whether the Araguaia River acts as a barrier to the gene flow of these two species and to assess how ecological traits, such as locomotion habits and habitat preferences, may influence differences in levels of genetic diversity and differentiation. As both species occur in flooded forests, neither showed genetic differences related to river banks. Oecomys aff. roberti showed stronger population structure that appears to be associated with isolation by distance. This arbo...