Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influenced whether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.
Patterns of intraspecific geographic variation of signaling systems provide insight into the microevolutionary processes driving phenotypic divergence. The acoustic calls of bats are sensitive to diverse evolutionary forces, but processes that shape call variation are largely unexplored. In China, Rhinolophus ferrumequinum displays a diverse call frequency and inhabits a heterogeneous landscape, presenting an excellent opportunity for this kind of research. We quantified geographic variation in resting frequency (RF) of echolocation calls, estimated genetic structure and phylogeny of R. ferrumequinum populations, and combined this with climatic factors to test three hypotheses to explain acoustic variation: genetic drift, cultural drift, and local adaptation. Our results demonstrated significant regional divergence in frequency and phylogeny among the bat populations in China's northeast (NE), central-east (CE) and southwest (SW) regions. The CE region had higher frequencies than the NE and SW regions. Drivers of RF divergence were estimated in the entire range and just the CE/NE region (since these two regions form a clade). In both cases, RF divergence was not correlated with mtDNA or nDNA genetic distance, but was significantly correlated with geographic distance and mean annual temperature, indicating cultural drift and ecological selection pressures are likely important in shaping RF divergence among different regions in China.
Globalization has facilitated the worldwide movement and introduction of pathogens, but epizoological reconstructions of these invasions are often hindered by limited sampling and insufficient genetic resolution among isolates. Pseudogymnoascus destructans, a fungal pathogen causing the epizootic of white-nose syndrome in North American bats, has exhibited few genetic polymorphisms in previous studies, presenting challenges for both epizoological tracking of the spread of this fungus and for determining its evolutionary history. We used single nucleotide polymorphisms (SNPs) from whole-genome sequencing and microsatellites to construct high-resolution phylogenies of P. destructans. Shallow genetic diversity and the lack of geographic structuring among North American isolates support a recent introduction followed by expansion via clonal reproduction across the epizootic zone. Moreover, the genetic relationships of isolates within North America suggest widespread mixing and long-distance movement of the fungus. Genetic diversity among isolates of P. destructans from Europe was substantially higher than in those from North America. However, genetic distance between the North American isolates and any given European isolate was similar to the distance between the individual European isolates. In contrast, the isolates we examined from Asia were highly divergent from both European and North American isolates. Although the definitive source for introduction of the North American population has not been conclusively identified, our data support the origin of the North American invasion by P. destructans from Europe rather than Asia.
Predicting species' fates following the introduction of a novel pathogen is a significant and growing problem in conservation. Comparing disease dynamics between introduced and endemic regions can offer insight into which naive hosts will persist or go extinct, with disease acting as a filter on host communities. We examined four hypothesized mechanisms for host–pathogen persistence by comparing host infection patterns and environmental reservoirs for Pseudogymnoascus destructans (the causative agent of white-nose syndrome) in Asia, an endemic region, and North America, where the pathogen has recently invaded. Although colony sizes of bats and hibernacula temperatures were very similar, both infection prevalence and fungal loads were much lower on bats and in the environment in Asia than North America. These results indicate that transmission intensity and pathogen growth are lower in Asia, likely due to higher host resistance to pathogen growth in this endemic region, and not due to host tolerance, lower transmission due to smaller populations, or lower environmentally driven pathogen growth rate. Disease filtering also appears to be favouring initially resistant species in North America. More broadly, determining the mechanisms allowing species persistence in endemic regions can help identify species at greater risk of extinction in introduced regions, and determine the consequences for disease dynamics and host–pathogen coevolution.
The most striking feature of peafowl (Pavo) is the males' elaborate train, which exhibits ocelli (ornamental eyespots) that are under sexual selection. Two additional genera within the Phasianidae (Polyplectron and Argusianus) exhibit ocelli, but the appearance and location of these ornamental eyespots exhibit substantial variation among these genera, raising the question of whether ocelli are homologous. Within Polyplectron, ocelli are ancestral, suggesting ocelli may have evolved even earlier, prior to the divergence among genera. However, it remains unclear whether Pavo, Polyplectron and Argusianus form a monophyletic clade in which ocelli evolved once. We estimated the phylogeny of the ocellated species using sequences from 1966 ultraconserved elements (UCEs) and three mitochondrial regions. The three ocellated genera did form a strongly supported clade, but each ocellated genus was sister to at least one genus without ocelli. Indeed, Polyplectron and Galloperdix, a genus not previously suggested to be related to any ocellated taxon, were sister genera. The close relationship between taxa with and without ocelli suggests multiple gains or losses. Independent gains, possibly reflecting a pre-existing bias for eye-like structures among females and/or the existence of a simple mutational pathway for the origin of ocelli, appears to be the most likely explanation.
Aim The goals of our study were to assess the population history and genetic structure of the widespread bat Hipposideros armiger, and to evaluate the effect of palaeoclimatic changes and dispersal patterns on this species.Location South China, mainland Southeast Asia and the South Himalayas.Methods We amplified two mitochondrial DNA (mtDNA) regions (cyt b and D-loop) and seven nuclear microsatellite loci (nSSRs) from 216 individuals of H. armiger. To examine the evolutionary history of this species, we constructed maximum likelihood and Bayesian phylogenetic trees based on the two mtDNA regions. From the mtDNA and/or nSSR data, we assessed population genetic structure using analysis of molecular variance (AMOVA) and median-joining network and structure analyses. We also estimated demographic history and gene flow using a Bayesian skyline plot and the program IMa2.Results Phylogenetic and median-joining network analyses revealed that H. armiger comprises two distinct mtDNA clades divided into seven subclades. The results of AMOVA suggested strong population genetic structure based on mtDNA, but weak structure based on nSSRs. structure analysis identified three population clusters and also showed weak genetic structure at the nuclear level. Demographic analyses revealed two population expansion events c. 0.62 Ma and c. 0.25 Ma. The basic phylogeographical structure of H. armiger was established by 0.24 Ma. IMa2 analysis demonstrated that substantial gene flow has occurred between different regions since then. Additionally, non-significant population structure and significant gene flow were detected between Taiwan and Hainan island populations and those from mainland China.Main conclusions Our results suggest that divergence and population expansion of H. armiger occurred in association with Pleistocene climatic changes and that multiple refugia may have existed for this species. Post-glacial malebiased dispersal was likely to be the primary contributor to the contemporary genetic structure of H. armiger populations. Gene flow may have contributed greatly to the genetic structure of insular populations and populations from mainland China.
Epigenetic modifications are considered to have an important role in evolution. DNA methylation is one of the best studied epigenetic mechanisms and methylation variability is crucial for promoting phenotypic diversification of organisms in response to environmental variation. A critical first step in the assessment of the potential role of epigenetic variation in evolution is the identification of DNA methylation polymorphisms and their relationship with genetic variations in natural populations. However, empirical data is scant in animals, and particularly so in wild mammals. Bats are considered as bioindicators because of their sensitivity to environmental perturbations and they may present an opportunity to explore epigenetic variance in wild mammalian populations. Our study is the first to explore these questions in the female great roundleaf bat (Hipposideros armiger) populations using the methylation-sensitive amplified polymorphism (MSAP) technique. We obtained 868 MSAP sites using 18 primer combinations and found (1) a low genomic methylation level (21.3 % on average), but extensive DNA methylation polymorphism (90.2 %) at 5'-CCGG-3' sites; (2) epigenetic variation that is structured into distinct between- (29.8 %) and within- (71.2 %) population components, as does genetic variation; and (3) a significant correlation between epigenetic and genetic variations (P < 0.05). These results may also apply to other wild mammalian populations. The possible causes for the correlation between epigenetic and genetic variations are discussed.
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