Ana Carolina Loss

Neotropical forest expansion during the last glacial period challenges refuge hypothesis

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. 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.

Mitogenomic phylogeny, diversification, and biogeography of South American spiny rats

Echimyidae is one of the most speciose and ecologically diverse rodent families in the world, occupying a wide range of habitats in the Neotropics. However, a resolved phylogeny at the genus-level is still lacking for these 22 genera of South American spiny rats, including the coypu (Myocastorinae), and 5 genera of West Indian hutias (Capromyidae) relatives. Here, we used Illumina shotgun sequencing to assemble 38 new complete mitogenomes, establishing Echimyidae, and Capromyidae as the first major rodent families to be completely sequenced at the genus-level for their mitochondrial DNA. Combining mitogenomes and nuclear exons, we inferred a robust phylogenetic framework that reveals several newly supported nodes as well as the tempo of the higher level diversification of these rodents. Incorporating the full generic diversity of extant echimyids leads us to propose a new higher level classification of two subfamilies: Euryzygomatomyinae and Echimyinae. Of note, the enigmatic Carterodon displays fast-evolving mitochondrial and nuclear sequences, with a long branch that destabilizes the deepest divergences of the echimyid tree, thereby challenging the sister-group relationship between Capromyidae and Euryzygomatomyinae. Biogeographical analyses involving higher level taxa show that several vicariant and dispersal events impacted the evolutionary history of echimyids. The diversification history of Echimyidae seems to have been influenced by two major historical factors, namely (1) recurrent connections between Atlantic and Amazonian Forests and (2) the Northern uplift of the Andes.

Pequenos mamíferos não voadores em fragmentos de Mata Atlântica e áreas agrícolas em Viana, Espírito Santo, Brasil

We surveyed non-flying small mammals at Viana, Espirito Santo, southeastern Brazil, in 1981-1982 and 2006-2007. We trapped 439 non-flying small mammals belonging to three orders (Didelphimorphia, Rodentia, and Lagomorpha) and six families (Didelphidae, Sciuridade, Cricetidae, Muridae, Echimyidae, and Leporidae). The most abundant species were the rodents Akodon cursor and Nectomys squamipes and the marsupial Metachirus nudicaudatus. We recorded the echimyid rodent Euryzygomatomys spinosus for the first time in the state of Espirito Santo. The species richness (S = 21) and Shannon diversity index (H = 2.23) are among the highest recorded for Atlantic Forest small mammals in the state, even when compared to values from protected areas. These higher richness and diversity values are probably related to habitat heterogeneity and highlight the need for conservation of Vianas forest fragments, which are an important source of Atlantic Forest biodiversity.

Evolutionary diversification of Phyllomys (Rodentia: Echimyidae) in the Brazilian Atlantic Forest

Abstract Tree rats of the genus Phyllomys are arboreal rodents endemic to the Brazilian Atlantic Forest. Previous phylogenetic analysis of mitochondrial DNA resulted in a basal polytomy of species in this genus, suggesting rapid speciation. Here we expanded this data matrix by adding specimens and both nuclear and mitochondrial genes. We found 2 basal clades: P. pattoni + P. mantiqueirensis; and a clade split into 6 lineages: southern clade ([P. sulinus + P. nigrispinus] + P. dasythrix); northeastern clade ([P. brasiliensis + P. lamarum] + P. blainvilii); Phyllomys sp. 1; Phyllomys sp. 2; Phyllomys sp. 3; and P. lundi. The discovery of 3 potentially new species calls for a reevaluation of the taxonomy of Phyllomys species. The combination of nuclear and mitochondrial markers increased the resolution of the tree, although the basal topology is poorly supported. The patterns of geographic distribution and phylogenetic relationships are compatible with parapatric diversification within Phyllomys through ecological gradients of latitude beginning 3.69 million years ago and of altitude 4.34 million years ago.

Mitochondrial genome of Plasmodium vivax/simium detected in an endemic region for malaria in the Atlantic Forest of Espírito Santo state, Brazil: do mosquitoes, simians and humans harbour the same parasite?

BackgroundThe transmission of malaria in the extra-Amazonian regions of Brazil, although interrupted in the 1960s, has persisted to the present time in some areas of dense Atlantic Forest, with reports of cases characterized by particular transmission cycles and clinical presentations. Bromeliad-malaria, as it is named, is particularly frequent in the state of Espírito Santo, with Plasmodium vivax being the parasite commonly recognized as the aetiologic agent of human infections. With regard to the spatial and temporal distances between cases reported in this region, the transmission cycle does not fit the traditional malaria cycle. The existence of a zoonosis, with infected simians participating in the epidemiology, is therefore hypothesized. In the present study, transmission of bromeliad-malaria in Espírito Santo is investigated, based on the complete mitochondrial genome of DNA extracted from isolates of Plasmodium species, which had infected humans, a simian from the genus Allouata, and Anopheles mosquitoes. Plasmodium vivax/simium was identified in the samples by both nested PCR and real-time PCR. After amplification, the mitochondrial genome was completely sequenced and compared with a haplotype network which included all sequences of P. vivax/simium mitochondrial genomes sampled from humans and simians from all regions in Brazil.ResultsThe haplotype network indicates that humans and simians from the Atlantic Forest become infected by the same haplotype, but some isolates from humans are not identical to the simian isolate. In addition, the plasmodial DNA extracted from mosquitoes revealed sequences different from those obtained from simians, but similar to two isolates from humans.ConclusionsThese findings strengthen support for the hypothesis that in the Atlantic Forest, and especially in the state with the highest frequency of bromeliad-malaria in Brazil, parasites with similar molecular backgrounds are shared by humans and simians. The recognized identity between P. vivax and P. simium at the species level, the sharing of haplotypes, and the participation of the same vector in transmitting the infection to both host species indicate interspecies transference of the parasites. However, the intensity, frequency and direction of this transfer remain to be clarified.

The Araguaia River as an Important Biogeographical Divide for Didelphid Marsupials in Central Brazil

The riverine barrier model suggests that rivers play a significant role in separating widespread organisms into isolated populations. In this study, we used a comparative approach to investigate the phylogeography of 6 didelphid marsupial species in central Brazil. Specifically, we evaluate the role of the mid-Araguaia River in differentiating populations and estimate divergence time among lineages to assess the timing of differentiation of these species, using mitochondrial DNA sequence data. The 6 didelphid marsupials revealed different intraspecific genetic patterns and structure. The 3 larger and more generalist species, Didelphis albiventris, Didelphis marsupialis, and Philander opossum, showed connectivity across the Araguaia River. In contrast the genetic structure of the 3 smaller and specialist species, Gracilinanus agilis, Marmosa (Marmosa) murina, and Marmosa (Micoureus) demerarae was shaped by the mid-Araguaia. Moreover, the split of eastern and western bank populations of the 2 latter species is consistent with the age of Araguaia River sediments formation. We hypothesize that the role of the Araguaia as a riverine barrier is linked to the level of ecological specialization among the 6 didelphid species and differences in their ability to cross rivers or disperse through the associated habitat types.

Syntopy of cryptic Phyllomys (Rodentia: Echimyidae) species: description of the karyotype of Phyllomys nigrispinus and an expansion of the geographic distribution of Phyllomys sulinus

Abstract The echimyid rodents of the genus Phyllomys are medium-sized arboreal spiny rats endemic to the Atlantic Forest of Brazil. The genus is currently composed of 13 species, although there are at least four other undescribed species. The ecology, zoogeography and diversity of the genus are still poorly understood. Here, we provide the first record of Phyllomys sulinus from the Brazilian state of Rio de Janeiro, based on a specimen collected in the Serra da Bocaina National Park, which extends the known geographic range of the species approximately 130 km to the northeast. At this site, P. sulinus occurred in syntopy with the cryptic Phyllomys nigrispinus. We describe the karyotype of P. nigrispinus for the first time and identify two different diploid numbers (2n=84 and 85). We also conducted a molecular analysis of the cytochrome b gene of five specimens, which we identified by phylogenetic reconstruction. Our findings reinforce the importance of molecular data, such as DNA sequences, and karyotypes for the differentiation of cryptic, syntopic species.

Phylogeny and biogeography of Phyllomys (Rodentia: Echimyidae) reveal a new species from the Cerrado and suggest Miocene connections of the Amazon and Atlantic Forest

Phyllomys is the most species-rich genus among spiny tree rats of the family Echimyidae and includes members widely distributed throughout the Atlantic Forest of South America. Among recognized species recovered in previous studies, 4 lineages are unnamed and their taxonomic distinctness needs further investigation. Biogeographic analyses recovered an Amazonian ancestor of the basal lineage leading to living Phyllomys, suggesting ancient connections between the 2 largest South American rainforests, and presence of rainforest corridors within the central Brazilian dry biomes. Based on exhaustive taxonomic sampling of Phyllomys, applying multigene phylogenetic methods, and morphological and karyological data, we described a new species of Phyllomys from central Brazil. Geographical records from the center of the Cerrado biome of central Brazil indicate an unexpected location for the distribution of the genus, given the contrast between the physical and biological characteristics of the Cerrado and Atlantic Forest habitats. Contrary to previous studies, the analysis of the ancestral geographic range performed here suggests a Cerrado ancestral distribution for Phyllomys during the late Miocene. This result favors the hypothesis of a past link between the Amazon and Atlantic Forest in central Brazil, through the region occupied today by the dry Cerrado, and that forest expansions and contractions may have occurred in Brazilian dry biomes over the course of the Tertiary.

Correction to: Acanthamoeba of three morphological groups and distinct genotypes exhibit variable and weakly inter-related physiological properties

The authors recognized a mistake in Abstract and in the Discussion section.

Neither barriers nor refugia explain genetic structure in a major biogeographic break: phylogeography of praying mantises in the Brazilian Atlantic Forest

Abstract The Atlantic Forest is one of the world’s top biodiversity hotspots, but the diversification processes of its biota are still poorly known, with competing models attributing dominant roles to either Quaternary climatic changes or geographic barriers. Many studies identify the Doce river as a major phylogeographic break, but the reasons for this phenomenon are highly debated. Here we test the predictions of the refugial and barrier models for a common species of praying mantis, Miobantia fuscata, focusing in the areas immediately south and north of the Doce river. Our analyses show high intraspecific genetic diversity, deep coalescence times and no evidence for recent population expansion. Phylogeographic structure is inconsistent with a refugial hypothesis. Significant gene flow between northern and southern populations also conflicts with a strong role for geographic barriers. This study highlights the need for considering invertebrate taxa to infer recent landscape changes, and points towards a more complex picture of genetic diversification in the Atlantic Forest.