The origin and maintenance of intraspecific variation in vocal signals is important for population divergence and speciation. Where vocalizations are transmitted by vertical cultural inheritance, similarity will reflect co-ancestry, and thus vocal divergence should reflect genetic structure. Horseshoe bats are characterized by echolocation calls dominated by a constant frequency component that is partly determined by maternal imprinting. Although previous studies showed that constant frequency calls are also influenced by some non-genetic factors, it is not known how frequency relates to genetic structure. To test this, we related constant frequency variation to genetic and non-genetic variables in the Formosan lesser horseshoe bat (Rhinolophus monoceros). Recordings of bats from across Taiwan revealed that females called at higher frequencies than males; however, we found no effect of environmental or morphological factors on call frequency. By comparison, variation showed clear population structure, with frequencies lower in the centre and east, and higher in the north and south. Within these regions, frequency divergence was directional and correlated with geographical distance, suggesting that call frequencies are subject to cultural drift. However, microsatellite clustering analysis showed that broad differences in constant frequency among populations corresponded to discontinuities in allele frequencies resulting from vicariant events. Our results provide evidence that the processes shaping genetic subdivision have concomitant consequences for divergence in echolocation call frequency.
Intraspecific phylogenies can provide useful insights into how populations have been shaped by historical and contemporary processes. Taiwan formed around 5 million years ago from tectonic uplift, and has been connected to mainland Asia several times since its emergence. A central mountain range runs north to south, bisecting the island, and potentially impedes gene flow along an east-west axis. The Formosan lesser horseshoe bat (Rhinolophus monoceros) is endemic to Taiwan, where it is found mainly at low altitude. To determine the population structure and the demographic and colonization history of this species, we examined variation in the mitochondrial DNA control region in 203 bats sampled at 26 sites. We found very high haplotype and nucleotide diversity, which decreased from the centre to the south and north. Population differentiation followed a pattern of isolation by distance, though most regional genetic variance was attributable to differences between the relatively isolated southern population and those from other regions. A haplotype network was consistent with these findings and also suggested a southward colonization, followed by subsequent secondary contact between the south and other regions. Mismatch distributions were used to infer a past population expansion predating the last glacial maximum, and a neighbour-joining tree showed that R. monoceros formed a monophyletic grouping with respect to its sister taxa. Taken together, our results suggest that this taxon arose from a single period of colonization, and that demographic growth followed in the late Pleistocene. Current genetic structure reflects limited gene flow, probably coupled with stepwise colonization in the past. We consider explanations for the persistence of the species through multiple glacial maxima.
Sex-biased behaviours are expected to play an important role in partitioning genetic variance in animal populations. Comparing genetic structure at markers with different modes of inheritance provides a means of detecting these behaviours and their consequences for population genetic structure. In colonially breeding mammals, the common combination of female philopatry and male vagility can promote contrasting patterns of genetic differentiation between the sexes, both via their effects on recurrent gene flow and on colonization. We examined sex differences in gene flow and structure by comparing maternally inherited mitochondrial DNA (mtDNA) and biparentally inherited autosomal loci in the Formosan lesser horseshoe bat Rhinolophus monoceros. We found that genetic partitioning was higher at mtDNA than autosomal markers in both sexes, indicative of female-biased philopatry and male-biased dispersal. Across Taiwan, isolation-by-distance was detected for all sex/marker combinations but was steeper for mtDNA than for nuclear markers. We suggest that isolation-by-distance shown from mtDNA at large scales is likely to reflect the stepwise founding of new breeding colonies by females during colonization. In contrast, no isolation-bydistance was found at smaller distances of up to 100 km, indicating that gene flow and/or recent shared ancestry homogenises genetic structure among nearby sites. Our results highlight the value of an indirect genetic approach to understanding sex-biased behaviours and their consequences in a little-studied species.
Phylogeographic reconstructions of codistributed taxa can help reveal the interplay between abiotic factors, such as altitude and climate, and species-specific attributes, in shaping patterns of population genetic structure. Recent studies also demonstrate the value of both rangewide sampling and species distribution modelling (SDM) in comparative phylogeography. Here, we combine these approaches to study the population histories of four phylogenetically related forest-dependent bat species. All are endemic to the mountainous island of Taiwan but show differences in their tolerance to altitude, with Murina gracilis considered to be a high-altitude specialist, M. recondita and Kerivoula sp. low-altitude specialists, and M. puta an altitudinal generalist. We tested the prediction that contrasting habitat preferences would impact on patterns of past and contemporary gene flow and found broad concordance between the results of population genetic analyses and species distribution models based on the Model for Interdisciplinary Research on Climate. Both lowland species showed evidence of genetic divergence between the east and west of the island, consistent with SDMs that indicated the Central Mountain Range (CMR) has presented a long-term and continuous barrier to gene flow since before the Last Glacial Maximum. In contrast, Murina gracilis and M. puta showed lower degrees of historical isolation and genetic differentiation associated with the CMR, reflecting greater gene flow, possibly coupled with past population growth in M. puta. Together our results highlight the usefulness of combining distribution models with phylogeographic analyses to understand the drivers of genetic structure.
Cases of geographically restricted co-occurring sister taxa are rare and may point to potential divergence with gene flow. The two bat species Murina gracilis and Murina recondita are both endemic to Taiwan and are putative sister species. To test for nonallopatric divergence and gene flow in these taxa, we generated sequences using Sanger and next-generation sequencing, and combined these with microsatellite data for coalescent-based analyses. MtDNA phylogenies supported the reciprocally monophyletic sister relationship between M. gracilis and M. recondita; however, clustering of microsatellite genotypes revealed several cases of species admixture suggesting possible introgression. Sequencing of microsatellite flanking regions revealed that admixture signatures stemmed from microsatellite allele homoplasy rather than recent introgressive hybridization, and also uncovered an unexpected sister relationship between M. recondita and the continental species Murina eleryi, to the exclusion of M. gracilis. To dissect the basis of these conflicts between ncDNA and mtDNA, we analysed sequences from 10 anonymous ncDNA loci with *beast and isolation-with-migration and found two distinct clades of M. eleryi, one of which was sister to M. recondita. We conclude that Taiwan was colonized by the ancestor of M. gracilis first, followed by the ancestor of M. recondita after a period of allopatric divergence. After colonization, the mitochondrial genome of M. recondita was replaced by that of the resident M. gracilis. This study illustrates how apparent signatures of sympatric divergence can arise from complex histories of allopatric divergence, colonization and hybridization, thus highlighting the need for rigorous analyses to distinguish between such scenarios.
Interactions among multiple species form complex networks of interdependences and are considered primary factors in the generation and maintenance of biodiversity. Pteropodid bats are keystone species that provide important ecosystem services of pollination and seed dispersal in the tropics and subtropics. In this study, we investigated the utilization and preference of food resources by the insular frugivorous flying fox Pteropus dasymallus. We found that fig species constituted the major portion of the diet of the flying fox (94.6%). When foraging, the flying fox preferred seed figs from female trees over gall figs from male trees in functionally dioecious fig species. Germination experiments showed a significantly higher percentage of germination for fig seeds in feces than those from pellets and ripe figs (feces: 80.2%, pellets: 23.4%, ripe figs: 32.9%). Considering the active selection of seed figs and avoidance of gall figs by foraging flying foxes, we suggest that the abundance of seed figs accurately represents food availability for dioecy. This preference for seed figs or viable seeds can effectively promote the survival of pollinating wasps and might reinforce the evolution of dioecism in figs. In addition, the effects of gut passage on seed germination, in combination with the capacity of flying foxes to travel long distances, may substantially contribute to the efficiency of flying foxes as seed dispersers.
Recordings of bat echolocation and social calls are used for many research purposes from ecological studies to taxonomy. Effective use of these relies on identification of species from the recordings, but comparative recordings or detailed call descriptions to support identification are often lacking for areas with high biodiversity. The ChiroVox website (www.chirovox.org) was created to facilitate the sharing of bat sound recordings together with their metadata, including biodiversity data and recording circumstances. To date, more than 30 researchers have contributed over 3,900 recordings of nearly 200 species, making ChiroVox the largest open-access bat call library currently available. Each recording has a unique identifier that can be cited in publications; hence the acoustic analyses are repeatable. Most of the recordings available through the website are from bats whose species identities are confirmed, so they can be used to determine species in recordings where the bats were not captured or could not be identified. We hope that with the help of the bat researcher community, the website will grow rapidly and will serve as a solid source for bat acoustic research and monitoring.
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