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Posting Policy. It inhabits all the biomes that exist in the Neotropics, from seasonally flooded forests to semi-arid environments, and from sea level to meters of altitude. Therefore there are no identifiable physical barriers for dispersal and gene flow in the distributional range of this bat. In this case, it is likely that ecological barriers serve as a possible explanation to the structure found for this bat. All the divergence times estimated using coalescent and non-coalescent approaches fall within the Pleistocene epoch, suggesting that this bat is indeed susceptible to forest fragmentation.
On the other hand the lack of resolution regarding the phylogenetic relationships between these three clades may reflect concomitant historical events of divergence. In this case, there would be an interesting corridor for gene flow along the eastern slopes of the Andes cordillera, that generated the clade formed by PAN and CA that showed high bootstrap support as shown in Figure 1.
The other ancestral clade would be formed along the Guiana and Brazilian shields that originated the AMC and the Atlantic forest clades. The high levels of sequence divergence may also be responsible for low bootstrap values showed by the AMC clade; but since this clade was consistently present with the exact same topology in all methods employed in this study, we consider this clade to be reflecting the true relationship between the sampled haplotypes. The Atlantic forest has become separated of the other area clades during the Pleistocene epoch, a result that is congruent with the appearance of a dry belt separating this forested area from the Amazon.
This is the first study to suggest a Pleistocene separation of the Atlantic forest and the Amazon based on the phylogeographic data collected on a vertebrate species using molecular-based estimates of divergence times. This work describes the Atlantic forest of Brazil as a composite area, with northern and southern components. The latitudinal division of this area has been recognized using parsimonious analysis of endemicity in amphibians [ 62 , 63 ], reptiles [ 64 ], birds [ 65 ] and harvestmen [ 66 ].
More recently, phylogeographic studies that used mtDNA described this structure in organisms as diverse as birds [ 67 ], pit vipers [ 68 ], non-volant small mammals [ 69 ], canids [ 70 ] and the bat species Carollia perspicillata [ 14 ].
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All the studies that implemented time estimates yielded Pleistocene divergence times for this event. There are numerous paleopalinological and sediment studies that describe that this region has been fragmented with dry open areas related to glaciation-driven events during the Pleistocene [ 71 — 74 ].
In a recent study, Carnaval and Moritz [ 75 ] generated climatic simulation data and cross-referenced their results with phylogeographic and paleopalinological studies. The authors describe a scenario where in its northern portion the Atlantic forest have always supported an evergreen forest even during the driest conditions, while south of the Doce river the climatic conditions would not support a forest formation.
The authors suggest that in its current southern distribution, the Atlantic forest was probably fragmented in several small patches in the wettest areas, a scenario that was proposed before by Whitmore and Prance [ 76 ]. The results shown here are congruent with this scenario: the SAF clade is the only one with significant evidence of population expansion for two different markers.
According to Lessa et al. The results obtained here reflect the predictions of Pleistocene forest dynamics: the time divergence estimates all fall within this epoch and the estimated historical demography is congruent with refugia.
The existence of a Atlantic forest lineage that is basal to both SAF and NAF comes as a surprise, specially because this lineage is at the southernmost end of the Atlantic forest distribution - where according to the Carnaval-Moritz model, there should be no forests at the last glacial maximum. This particular haplotype could represent another lineage and a possible contact zone between this lineage and the SAF. The incongruence between the results observed for the mitochondrial and nuclear markers could be due to two different scenarios: complete fragmentation and incongruence between markers due to the nature and characteristics of each molecular marker or long-term female philopatry and male-biased dispersal.
We will discuss each of these hypotheses in detail. The first possibility - of complete isolation between populations but no footprints in nuclear markers due to larger effective size and lower mutation rates - was the reason behind the coalescent simulations carried in this study. The results of the simulations have shown that given the mutation rate, time of separation and effective population size calculated for these bats, an average nuclear marker might or might not reflect the true demographic history of this species with similar probabilities. Given that, we believe that the best way to approach the question on whether the structure found is valid or the outcome of long-term female philopatry would be to sequence a larger number of loci - at least 16 according to Moore [ 79 ] - in search of more accurate phylogenetic reconstructions or use other nuclear markers such as the Y chromosome or microsatellites, all of which are beyond the scope of the present analysis.
The DRB intron was chosen due to the possibility of studying balancing selection on the common vampire bat - as described for many of the genes that comprise the major histocompatibility complex MHC in vertebrates. This work shows that these two markers do not seem appropriate for intraspecific phylogeographic studies. Females of D. In addition, females do occasionally migrate among roosts, so there is evidence of some adult female dispersal.
Under these conditions of female philopatry with restricted dispersal, the expected pattern of differentiation would be one of isolation by distance [ 9 ]. However, in our analyses we find low sequence divergence among localities at large geographic distances over km , and large increases in genetic differentiation taking place over relatively short distances. This pattern is particularly clear in the analysis of the Atlantic forest. The NCA results point towards the same direction in opposition to isolation by distance.
We believe that if the sampling gaps were filled, this outcome on the inference key allopatric fragmentation would be observed repeatedly among all clades. The results observed for the mtDNA marker show strong evidence of historical fragmentation, even with limited information on the extent of historical and current male-mediated gene flow.
Vampire Origin Traits
The phylogeographic pattern described for the common vampire bat Desmodus rotundus is characterized by Pleistocene ecological vicariance. The mitochondrial marker showed deep divergence between reciprocally monophyletic clades representing distinct ecodomains within the Neotropics. The times of separation between the lineages are all within the Pleistocene epoch. The phylogenetic pattern is congruent with many other Neotropical clades. In addition, the historical demography, with a population expansion at the southern end of the distribution, is compatible with the Carnaval-Moritz model of historic Atlantic forest dynamics.
The coalescent simulations showed that, given the population parameters estimated for this species, a nuclear marker may or may not recover Pleistocene population history with similar probabilities. The next step in revealing the true nature of the interactions between the mitochondrial clades indentified and the species status within D. This study would consider not only a multiloci approach but also field observations on ecology and behavior. We are also on the way to conduct experiments with bats genotyped for the different clades under controlled laboratory conditions, to test for reproductive isolation and the possible ramification of the hybridization between the animals belonging to different clades.
We also would like to thank Dr. Also thanks for Adalberto Cesari for english revisions. Part of this work was carried out by using the resources of the Computational Biology Service Unit from Cornell University which is partially funded by Microsoft Corporation. We would like to thank two anonymous reviewers for detailed and helpful suggestions. This article is published under license to BioMed Central Ltd. Research article Open Access. Phylogeography of the common vampire bat Desmodus rotundus : Marked population structure, Neotropical Pleistocene vicariance and incongruence between nuclear and mtDNA markers.
BMC Evolutionary Biology 9 Abstract Background The common vampire bat Desmodus rotundus is an excellent model organism for studying ecological vicariance in the Neotropics due to its broad geographic range and its preference for forested areas as roosting sites. Conclusions We therefore conclude that the pattern exhibited by the common vampire bat, with marked geographical structure for a mitochondrial marker and no phylogeographic structure for nuclear markers is compatible with a historical scenario of complete isolation of refuge-like populations during the Pleistocene.
Phasing of nuclear genotypes and recombination tests Heterozygous nucleotide positions were identified by conspicuous double peaks in the electropherograms of both L and R strands. Phylogenetic analyses Four different methods of phylogenetic inference were used. Population level and coalescent analyses Analysis of molecular variance AMOVA [ 41 ] was used to quantify the extent of population subdivision using the Arlequin software [ 42 ]. Coalescent simulations of nuclear sequence data According to Hare [ 20 ], the average nuclear marker will not trace Pleistocene events in the same manner as mitochondral markers due to its larger effective size, lower mutation rates and diploid nature.
Molecular variation For the mitochondrial marker, individuals were sampled from 54 localities. Phylogenetic inference: mitochondrial marker Figure 1 shows the MP phylogenetic reconstruction for the haplotypes described. The NJ phylogenetic tree was identical to the MP tree. The ML and bayesian analyses are largely congruent with this tree, with the exception of the relationships among a few terminal taxa.
The figure shows that there are five major monophyletic clades representing distinct geographical regions and biomes. A single sample from Ecuador could not be assigned to any of the clades. The distribution of each of these clades in the American continent can be seen in Figure 2. Although the clades had high bootsptrap and bayesian posterior probability support except for the basal haplotypes on the AMC clade, which is discussed later , the relationship between the major clades - excluding the Atlantic forest monophyly - received very weak support and was not the same across all methods of phylogenetic reconstruction.
Figure 1 Phylogenetic reconstruction of mtDNA haplotypes.
Figure 2 Geographical representation of the mtDNA phylogenetic groups. On the nested clade analysis, the TCS software identified the same clades as the tree-based methods. The haplotype network is presented on Figure 3. This decision was made based on the fact that the relationship between these three clades is poorly resolved. Both clusters were made independent on where and how these clades would connect. High and significant correlations between the haplotypes and their geographical localities were identified by the software GEODIS.
The inference key identified the pattern observed to the Atlantic forest as a whole as allopatric fragmentation.
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In the case of the last step clade, our sampling does not allow to discriminate between allopatric fragmentation and isolation by distance - which was predictable, given the large gaps in sampling, especially in central Brazil and northwestern South America. Figure 3 mtDNA haplotype network. The structure found in the phylogenetic analyses for the mitochondrial marker was also observed in the population-level analyses.
All pairwise comparison between the clades identified were also significant. The time divergence estimates for these clades are in Table 1. This result yields flat likelihood surfaces for the parameter t making it impossible to calculate coalescent time divergence estimates. The coalescent and non-coalescent time estimates for each comparison are very similar and all within the Pleistocene epoch. Table 1 Pairwise divergence times for the mtDNA clades described.
Given the results obtained for the mtDNA, we decided to conduct further analyses utilizing the mtDNA clades as populations for the nuclear markers. Even with this extensive sharing of haplotypes, Fst values between the locations demarcated by the mitochondrial clades were all significant for both markers. This result could not be replicated by the DRB intron, probably due to poor sampling for these localities only ten individuals.
Table 2 summarizes the population genetics results for the RAG2 marker. Table 2 Population genetics analysis results for the nuclear marker RAG2. The outfiles generated had similar haplotype diversity average 0. Given these conditions we ran the iterations on the TNT software using maximum parsimony. The results of these analyses are summarized in Table 3.
The results show that there is no clear distinction between all possible scenarios involving reciprocal monophyly of the clades, i. Therefore, no scenarios could be confirmed or excluded. Table 3 Coalescent simulations and clade monophyly. Biogeographic pattern It comes as no surprise that species with wide geographical distributions consist of two or more evolutionary units when molecular markers are studied. Mitochondrial and nuclear incongruence The incongruence between the results observed for the mitochondrial and nuclear markers could be due to two different scenarios: complete fragmentation and incongruence between markers due to the nature and characteristics of each molecular marker or long-term female philopatry and male-biased dispersal.
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