A tale of two genomes: contrasting patterns of phylogeographic structure in a widely distributed bat (original) (raw)
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Conflicting Evolutionary Histories of the Mitochondrial and Nuclear Genomes in New World Myotis Bats
Systematic Biology
The rapid diversification of Myotis bats into more than 100 species is one of the most extensive mammalian radiations available for study. Efforts to understand relationships within Myotis have primarily utilized mitochondrial markers and trees inferred from nuclear markers lacked resolution. Our current understanding of relationships within Myotis is therefore biased towards a set of phylogenetic markers that may not reflect the history of the nuclear genome. To resolve this, we sequenced the full mitochondrial genomes of 37 representative Myotis, primarily from the New World, in conjunction with targeted sequencing of 3648 ultraconserved elements (UCEs). We inferred the phylogeny and explored the effects of concatenation and summary phylogenetic methods, as well as combinations of markers based on informativeness or levels of missing data, on our results. Of the 294 phylogenies generated from the nuclear UCE data, all are significantly different from phylogenies inferred using mitochondrial genomes. Even within the nuclear data, quartet frequencies indicate that around half of all UCE loci conflict with the estimated species tree. Several factors can drive such conflict, including incomplete lineage sorting, introgressive hybridization, or even phylogenetic error. Despite the degree of discordance between nuclear UCE loci and the mitochondrial genome and among UCE loci themselves, the most common nuclear topology is recovered in one quarter of all analyses with strong nodal support. Based on these results, we reexamine the evolutionary history of Myotis to better understand the phenomena driving their unique nuclear, mitochondrial, and biogeographic histories.
Leaf-nosed bats (Phyllostomidae) are one of the most studied groups within the order Chiroptera mainly because of their outstanding species richness and diversity in morphological and ecological traits. Rapid diversification and multiple homoplasies have made the phylogeny of the family difficult to solve using morphological characters. Molecular data have contributed to shed light on the evolutionary history of phyllostomid bats, yet several relationships remain unresolved at the intra-familial level. Complete mitochondrial genomes have proven useful to deal with this kind of situation in other groups of mammals by providing access to a large number of molecular characters. At present, there are only two mitogenomes available for phyllostomid bats hinting at the need for further exploration of the mitogenomic approach in this group. We used both standard Sanger sequencing of PCR products and next-generation sequencing (NGS) of shotgun genomic DNA to obtain new complete mitochondrial genomes from 10 species of phyllostomid bats, including representatives of major subfamilies, plus one outgroup belonging to the closely-related mormoopids. We then evaluated the contribution of mitogenomics to the resolution of the phylogeny of leaf-nosed bats and compared the results to those based on mitochondrial genes and the RAG2 and VWF nuclear makers. Our results demonstrate the advantages of the Illumina NGS approach to efficiently obtain mitogenomes of phyllostomid bats. The phylogenetic signal provided by entire mitogenomes is highly comparable to the one of a concatenation of individual mitochondrial and nuclear markers, and allows increasing both resolution and statistical support for several clades. This enhanced phylogenetic signal is the result of combining markers with heterogeneous evolutionary rates representing a large number of nucleotide sites. Our results illustrate the potential of the NGS mitogenomic approach for resolving the evolutionary history of phyllostomid bats based on a denser species sampling.
Mitochondrial DNA Part B, 2020
The geographic distributions of eastern and western Lasionycteris noctivagans populations suggest they could be genetically isolated, but this has rarely been assessed using genetic data. Here, we evaluate this possibility by sequencing the complete mitochondrial genome of four silver-haired bats from eastern and western populations. The three usable mitogenomes were closely associated with other Vespertilionid bats and the phylogenetic tree revealed the two western individuals grouping together to form their own clade. Our results support the idea of small but significant genetic differences between eastern and western populations of these bats, but this should be tested further.
Implications for Bat Evolution from Two New Complete Mitochondrial Genomes
Molecular Biology and Evolution, 2001
Mitochondrial genomes are useful in the quantitative analysis of vertebrate evolution. We report here the complete mitochondrial genomes for a megabat (the flying fox, Pteropus scapulatus) and a microbat (the New Zealand long-tailed bat, Chalinolobus tuberculatus). The evolutionary history of bats (chiroptera) has been uncertain, and even the monophyly of this group has been questioned. The new sequences allow five questions to be addressed: the position of bats within eutheria, whether bats are monophyletic, whether microbats are paraphyletic with respect to megabats, the approximate timing of the origin of bats, and whether some insectivores (e.g., moles) form a sister group with bats. In order to examine these questions, we analyzed two data sets (both separately and combined), one with 12 protein-coding regions and the other with RNA (combined ribosomal RNAs and tRNAs). The results are congruent, support bat monophyly, and place bats close to the cetferungulates (whales [cetaceans] plus ferungulates [carnivores, ungulates, and perissodactyls]).
Phylogenomic Analyses Elucidate the Evolutionary Relationships of Bats
Molecular phylogenetics has rapidly established the evolutionary positions of most major mammal groups , yet analyses have repeatedly failed to agree on that of bats (order Chiroptera) . Moreover, the relationship among the major bat lineages has proven equally contentious, with ongoing disagreements about whether echolocating bats are paraphyletic [7-9] or a true group [10] having profound implications for whether echolocation evolved once or possibly multiple times. By generating new bat genome data and applying model-based phylogenomic analyses designed to accommodate heterogeneous evolutionary processes , we show that-contrary to recent suggestions-bats are not closely related to odd-toed ungulates but instead have a more ancient origin as sister group to a large clade of carnivores, ungulates, and cetaceans. Additionally, we provide the first genome-scale support showing that laryngeal echolocating bats are not a true group and that this paraphyly is robust to their position within mammals. We suggest that earlier disagreements in the literature may reflect model misspecification, long-branch artifacts, poor taxonomic coverage, and differences in the phylogenetic markers used. These findings are a timely reminder of the relevance of experimental design and careful statistical analysis as we move into the phylogenomic era.
Contrasting Genetic Structure in Two Co-Distributed Species of Old World Fruit Bat
PloS one, 2010
The fulvous fruit bat (Rousettus leschenaulti) and the greater short-nosed fruit bat (Cynopterus sphinx) are two abundant and widely co-distributed Old World fruit bats in Southeast and East Asia. The former species forms large colonies in caves while the latter roots in small groups in trees. To test whether these differences in social organization and roosting ecology are associated with contrasting patterns of gene flow, we used mtDNA and nuclear loci to characterize population genetic subdivision and phylogeographic histories in both species sampled from China, Vietnam and India. Our analyses from R. leschenaulti using both types of marker revealed little evidence of genetic structure across the study region. On the other hand, C. sphinx showed significant genetic mtDNA differentiation between the samples from India compared with China and Vietnam, as well as greater structuring of microsatellite genotypes within China. Demographic analyses indicated signatures of past rapid population expansion in both taxa, with more recent demographic growth in C. sphinx. Therefore, the relative genetic homogeneity in R. leschenaulti is unlikely to reflect past events. Instead we suggest that the absence of substructure in R. leschenaulti is a consequence of higher levels of gene flow among colonies, and that greater vagility in this species is an adaptation associated with cave roosting.
Assemblages of bats are phylogenetically clustered on a regional scale
Basic and Applied Ecology, 2013
Phylogenetically related species are assumed to be ecologically similar. Ecological similarity might lead to competition and to low distributional overlap. Therefore, if competitive interactions drive assemblages, we expect a decrease in distributional overlap with increasing phylogenetic relatedness and phylogenetic over-dispersion in assemblages. We tested this hypothesis by evaluating the mean phylogenetic distance of bat assemblages within grid cells of ≈36 km 2 across Bavaria, Germany (887 grids; 20,023 records). To calculate phylogenetic distance between species, we used a phylogenetic tree derived from sequences of three mitochondrial genes (cytb, COI, ND1), two nuclear-protein-encoding genes (vWF, RAG2) and the genes encoding16S rRNA, 12S rRNA and tRNA-Val. Overall, bat species co-occurring within grid cells were more similar than expected from null models (phylogenetic clustering). This suggests that on the considered scale, bat assemblages are triggered more by environmental filters than by competition. Furthermore, mean phylogenetic distance decreased with the amount of anthropogenic habitats within grids. This contrasts with species richness of bats, which increased with anthropogenic habitats.
Molecular …, 2009
Phylogeographical studies are typically based on haplotype data, occasionally on nuclear markers such as microsatellites, but rarely combine both. This is unfortunate because the use of markers with contrasting modes of inheritance and rates of evolution might provide a more accurate and comprehensive understanding of a species' history. Here we present a detailed study of the phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum, using 1098 bp of the mitochondrial ND2 gene from 45 localities from across its Palaearctic range to infer population history. In addition, we re-analysed a large microsatellite data set available for this species and compared the results of both markers to infer population relationships and the historical processes influencing them. We show that mtDNA, the most popular marker in phylogeography studies, yielded a misleading result, and would have led us to conclude erroneously that a single expansion had taken place in Europe. Only by combining the mitochondrial and microsatellite data sets are we able to reconstruct the species' history and show two colonization events in Europe, one before the Last Glacial Maximum (LGM) and one after it. Combining markers also revealed the importance of Asia Minor as an ancient refugium for this species and a source population for the expansion of the greater horseshoe bat into Europe before the LGM.