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Genetic studies of the Eurasian brown bear (Ursus arctos) have so far focused on populations from Europe and North America, although the largest distribution area of brown bears is in Asia. In this study, we reveal population genetic parameters for the brown bear population inhabiting the Grand Kackar Mountains (GKM) in the north east of Turkey, western Lesser Caucasus. Using both hair (N = 147) and tissue samples (N = 7) collected between 2008 and 2014, we found substantial levels of genetic variation (10 microsatellite loci). Bear samples (hair) taken from rubbing trees worked better for genotyping than those from power poles, regardless of the year collected. Genotyping also revealed that bears moved between habitat patches, despite ongoing massive habitat alterations and the creation of large water reservoirs. This population has the potential to serve as a genetic reserve for future reintroduction in the Middle East. Due to the importance of the GKM population for on-going and future conservation actions, the impacts of habitat alterations in the region ought to be minimized; e.g., by establishing green bridges or corridors over reservoirs and major roads to maintain habitat connectivity and gene flow among populations in the Lesser Caucasus.
The Caucasian lynx, Lynx lynx dinniki, has one of the southernmost distributions in the Eurasian lynx range, covering Anatolian Turkey, the Caucasus and Iran. Little is known about the biology and the genetic status of this subspecies. To collect baseline genetic, ecological and behavioural data and benefit future conservation of L. l. dinniki, we monitored 11 lynx territories (396 km(2)) in northwestern Anatolia. We assessed genetic diversity of this population by non-invasively collecting 171 faecal samples and trapped and sampled 12 lynx individuals using box traps. We observed high allelic variation at 11 nuclear microsatellite markers, and found no signs of inbreeding despite the potential isolation of this population. We obtained similar numbers of distinct genotypes from the two sampling sources. Our results indicated that first order female relatives occupy neighbouring territories (female philopatry) and that territorial male lynx were highly unrelated to each other and to female territorial lynx, suggesting long distance male dispersal. Particular male and female resident territorial lynx and their offspring (kittens and subadults) were more likely to be trapped than resident floaters or dispersing (unrelated) lynx. Conversely, we obtained more data for unrelated lynx and higher numbers of territorials using non-invasive sampling (faeces). When invasive and non-invasive samples were analysed separately, the spatial organisation of lynx (in terms of female philopatry and females and males occupying permanent ranges) affected measures of genetic diversity in such a way that estimates of genetic diversity were reduced if only invasive samples were considered. It appears that, at small spatial scales, invasive sampling using box traps may underestimate the genetic diversity in carnivores with permanent ranges and philopatry such as the Eurasian lynx. As non-invasive sampling can also provide additional data on diet and spatial organisation, we advocate the use of such samples for conservation genetic studies of vulnerable, endangered or data deficient territorial species.
Distributions of mammals in Southeast Asia: The role of the legacy of climate and species body mass
(2019)
Aim Current species distributions are shaped by present and past biotic and abiotic factors. Here, we assessed whether abiotic factors (habitat availability) in combination with past connectivity and a biotic factor (body mass) can explain the unique distribution pattern of Southeast Asian mammals, which are separated by the enigmatic biogeographic transition zone, the Isthmus of Kra (IoK), for which no strong geophysical barrier exists. Location Southeast Asia. Taxon Mammals. Methods We projected habitat suitability for 125 mammal species using climate data for the present period and for two historic periods: mid-Holocene (6 ka) and last glacial maximum (LGM 21 ka). Next, we employed a phylogenetic linear model to assess how present species distributions were affected by the suitability of areas in these different periods, habitat connectivity during LGM and species body mass. Results Our results show that cooler climate during LGM provided suitable habitat south of IoK for species presently distributed north of IoK (in mainland Indochina). However, the potentially suitable habitat for these Indochinese species did not stretch very far southwards onto the exposed Sunda Shelf. Instead, we found that the emerged landmasses connecting Borneo and Sumatra provided suitable habitat for forest dependent Sundaic species. We show that for species whose current distribution ranges are mainly located in Indochina, the area of the distribution range that is located south of IoK is explained by the suitability of habitat in the past and present in combination with the species body mass. Main conclusions We demonstrate that a strong geophysical barrier may not be necessary for maintaining a biogeographic transition zone for mammals, but that instead a combination of abiotic and biotic factors may suffice.
Immunological responses of hibernating mammals are suppressed at low body temperatures, a possible explanation for the devastating effect of the white-nose syndrome on hibernating North American bats. However, European bats seem to cope well with the fungal causative agent of the disease. To better understand the immune response of hibernating bats, especially against fungal pathogens, we challenged European greater mouse-eared bats (Myotis myotis) by inoculating the fungal antigen zymosan. We monitored torpor patterns, immune gene expressions, different aspects of the acute phase response and plasma oxidative status markers, and compared them with sham-injected control animals at 30 min, 48 h and 96 h after inoculation. Torpor patterns, body temperatures, body masses, white blood cell counts, expression of immune genes, reactive oxygen metabolites and non-enzymatic antioxidant capacity did not differ between groups during the experiment. However, zymosan injected bats had significantly higher levels of haptoglobin than the control animals. Our results indicate that hibernating greater mouse-eared bats mount an inflammatory response to a fungal challenge, with only mild to negligible consequences for the energy budget of hibernation. Our study gives a first hint that hibernating European bats may have evolved a hibernation-adjusted immune response in order to balance the trade-off between competent pathogen elimination and a prudent energy-saving regime.
In this study we compared the phylogeographic patterns of two Rusa species, Rusa unicolor and Rusa timorensis, in order to understand what drove and maintained differentiation between these two geographically and genetically close species and investigated the route of introduction of individuals to the islands outside of the Sunda Shelf. We analyzed full mitogenomes from 56 archival samples from the distribution areas of the two species and 18 microsatellite loci in a subset of 16 individuals to generate the phylogeographic patterns of both species. Bayesian inference with fossil calibration was used to estimate the age of each species and major divergence events. Our results indicated that the split between the two species took place during the Pleistocene, similar to 1.8Mya, possibly driven by adaptations of R. timorensis to the drier climate found on Java compared to the other islands of Sundaland. Although both markers identified two well-differentiated clades, there was a largely discrepant pattern between mitochondrial and nuclear markers. While nDNA separated the individuals into the two species, largely in agreement with their museum label, mtDNA revealed that all R. timorensis sampled to the east of the Sunda shelf carried haplotypes from R. unicolor and one Rusa unicolor from South Sumatra carried a R. timorensis haplotype. Our results show that hybridization occurred between these two sister species in Sundaland during the Late Pleistocene and resulted in human-mediated introduction of hybrid descendants in all islands outside Sundaland.
Background
The members of the genus Muntiacus are of particular interest to evolutionary biologists due to their extreme chromosomal rearrangements and the ongoing discussions about the number of living species. Red muntjacs have the largest distribution of all muntjacs and were formerly considered as one species. Karyotype differences led to the provisional split between the Southern Red Muntjac (Muntiacus muntjak) and the Northern Red Muntjac (M. vaginalis), but uncertainties remain as, so far, no phylogenetic study has been conducted. Here, we analysed whole mitochondrial genomes of 59 archival and 16 contemporaneous samples to resolve uncertainties about their taxonomy and used red muntjacs as model for understanding the evolutionary history of other species in Southeast Asia.
Results
We found three distinct matrilineal groups of red muntjacs: Sri Lankan red muntjacs (including the Western Ghats) diverged first from other muntjacs about 1.5 Mya; later northern red muntjacs (including North India and Indochina) and southern red muntjacs (Sundaland) split around 1.12 Mya. The diversification of red muntjacs into these three main lineages was likely promoted by two Pleistocene barriers: one through the Indian subcontinent and one separating the Indochinese and Sundaic red muntjacs. Interestingly, we found a high level of gene flow within the populations of northern and southern red muntjacs, indicating gene flow between populations in Indochina and dispersal of red muntjacs over the exposed Sunda Shelf during the Last Glacial Maximum.
Conclusions
Our results provide new insights into the evolution of species in South and Southeast Asia as we found clear genetic differentiation in a widespread and generalist species, corresponding to two known biogeographical barriers: The Isthmus of Kra and the central Indian dry zone. In addition, our molecular data support either the delineation of three monotypic species or three subspecies, but more importantly these data highlight the conservation importance of the Sri Lankan/South Indian red muntjac.
Over the past ~40 years, several attempts were made to reintroduce Eurasian lynx to suitable habitat within their former distribution range in Western Europe. In general, limited numbers of individuals have been released to establish new populations. To evaluate the effects of reintroductions on the genetic status of lynx populations we used 12 microsatellite loci to study lynx populations in the Bohemian–Bavarian and Vosges–Palatinian forests. Compared with autochthonous lynx populations, these two reintroduced populations displayed reduced genetic diversity, particularly the Vosges–Palatinian population. Our genetic data provide further evidence to support the status of ‘endangered’ and ‘critically endangered’ for the Bohemian–Bavarian and Vosges–Palatinian populations, respectively. Regarding conservation management, we highlight the need to limit poaching, and advocate additional translocations to bolster genetic variability.
Background: Findings: Approximately 55 gigabases of raw sequence were generated. From this data we assembled 72 complete mitogenome sequences, with an average depth of coverage of 102.9x and 55.2x for modern samples and historical samples, respectively. This dataset represents 52 species, of which 30 species had no previous mitogenome data available. The mitogenomes were geotagged to their sampling location, where known, to display a detailed geographical distribution of the species. Conclusion:
Epigenetic modifications, of which DNA methylation is the most stable, are a mechanism conveying environmental information to subsequent generations via parental germ lines. The paternal contribution to adaptive processes in the offspring might be crucial, but has been widely neglected in comparison to the maternal one. To address the paternal impact on the offspring’s adaptability to changes in diet composition, we investigated if low protein diet (LPD) in F0 males caused epigenetic alterations in their subsequently sired sons. We therefore fed F0 male Wild guinea pigs with a diet lowered in protein content (LPD) and investigated DNA methylation in sons sired before and after their father’s LPD treatment in both, liver and testis tissues. Our results point to a ‘heritable epigenetic response’ of the sons to the fathers’ dietary change. Because we detected methylation changes also in the testis tissue, they are likely to be transmitted to the F2 generation. Gene-network analyses of differentially methylated genes in liver identified main metabolic pathways indicating a metabolic reprogramming (‘metabolic shift’). Epigenetic mechanisms, allowing an immediate and inherited adaptation may thus be important for the survival of species in the context of a persistently changing environment, such as climate change.
Epigenetic mechanisms convey environmental information through generations and can regulate gene expression. Epigenetic studies in wild mammals are rare, but enable understanding adaptation processes as they may occur in nature. In most wild mammal species, males are the dispersing sex and thus often have to cope with differing habitats and thermal changes more rapidly than the often philopatric females. As temperature is a major environmental selection factor, we investigated whether genetically heterogeneous Wild guinea pig (Cavia aperea) males adapt epigenetically to an increase in temperature, whether that response will be transmitted to the next generation(s), and whether it regulates mRNA expression. Five (F0) adult male guinea pigs were exposed to an increased ambient temperature for 2 months, corresponding to the duration of the species' spermatogenesis. To study the effect of heat, we focused on the main thermoregulatory organ, the liver. We analyzed CpG-methylation changes of male offspring (F1) sired before and after the fathers' heat treatment (as has recently been described in Weyrich et al. [Mol. Ecol., 2015]). Transcription analysis was performed for the three genes with the highest number of differentially methylated changes detected: the thermoregulation gene Signal Transducer and Activator of Transcription 3 (Stat3), the proteolytic peptidase gene Cathepsin Z (Ctsz), and Sirtuin 6 (Sirt6) with function in epigenetic regulation. Stat3 gene expression was significantly reduced (P < 0.05), which indicated a close link between CpG-methylation and expression levels for this gene. The two other genes did not show gene expression changes. Our results indicate the presence of a paternal transgenerational epigenetic effect. Quick adaptation to climatic changes may become increasingly relevant for the survival of wildlife species as global temperatures are rising.
Epigenetic modifications, of which DNA methylation is the best studied one, can convey environmental information through generations via parental germ lines. Past studies have focused on the maternal transmission of epigenetic information to the offspring of isogenic mice and rats in response to external changes, whereas heterogeneous wild mammals as well as paternal epigenetic effects have been widely neglected. In most wild mammal species, males are the dispersing sex and have to cope with differing habitats and thermal changes. As temperature is a major environmental factor we investigated if genetically heterogeneous Wild guinea pig (Cavia aperea) males can adapt epigenetically to an increase in temperature and if that response will be transmitted to the next generation(s). Five adult male guinea pigs (F0) were exposed to an increased ambient temperature for 2 months, i.e. the duration of spermatogenesis. We studied the liver (as the main thermoregulatory organ) of F0 fathers and F1 sons, and testes of F1 sons for paternal transmission of epigenetic modifications across generation(s). Reduced representation bisulphite sequencing revealed shared differentially methylated regions in annotated areas between F0 livers before and after heat treatment, and their sons’ livers and testes, which indicated a general response with ecological relevance. Thus, paternal exposure to a temporally limited increased ambient temperature led to an ‘immediate’ and ‘heritable’ epigenetic response that may even be transmitted to the F2 generation. In the context of globally rising temperatures epigenetic mechanisms may become increasingly relevant for the survival of species.
Epigenetic modifications are a mechanism conveying environmental information to subsequent generations via parental germ lines. Research on epigenetic responses to environmental changes in wild mammals has been widely neglected, as well as studies that compare responses to changes in different environmental factors. Here, we focused on the transmission of DNA methylation changes to naive male offspring after paternal exposure to either diet (~40% less protein) or temperature increase (10 °C increased temperature). Because both experiments focused on the liver as the main metabolic and thermoregulation organ, we were able to decipher if epigenetic changes differed in response to different environmental changes. Reduced representation bisulfite sequencing (RRBS) revealed differentially methylated regions (DMRs) in annotated genomic regions in sons sired before (control) and after the fathers’ treatments. We detected both a highly specific epigenetic response dependent on the environmental factor that had changed that was reflected in genes involved in specific metabolic pathways, and a more general response to changes in outer stimuli reflected by epigenetic modifications in a small subset of genes shared between both responses. Our results indicated that fathers prepared their offspring for specific environmental changes by paternally inherited epigenetic modifications, suggesting a strong paternal contribution to adaptive processes.
Genetic studies of the Eurasian brown bear (Ursus arctos) have so far focused on populations from Europe and North America, although the largest distribution area of brown bears is in Asia. In this study, we reveal population genetic parameters for the brown bear population inhabiting the Grand Kaçkar Mountains (GKM) in the north east of Turkey, western Lesser Caucasus. Using both hair (N = 147) and tissue samples (N = 7) collected between 2008 and 2014, we found substantial levels of genetic variation (10 microsatellite loci). Bear samples (hair) taken from rubbing trees worked better for genotyping than those from power poles, regardless of the year collected. Genotyping also revealed that bears moved between habitat patches, despite ongoing massive habitat alterations and the creation of large water reservoirs. This population has the potential to serve as a genetic reserve for future reintroductions in the Middle East. Due to the importance of the GKM population for on-going and future conservation actions, the impacts of habitat alterations in the region ought to be minimized; e.g., by establishing green bridges or corridors over reservoirs and major roads to maintain habitat connectivity and gene flow among populations in the Lesser Caucasus.
Epigenetic modifications, of which DNA methylation is the most stable, are a mechanism conveying environmental information to subsequent generations via parental germ lines. The paternal contribution to adaptive processes in the offspring might be crucial, but has been widely neglected in comparison to the maternal one. To address the paternal impact on the offspring's adaptability to changes in diet composition, we investigated if low protein diet (LPD) in F0 males caused epigenetic alterations in their subsequently sired sons. We therefore fed F0 male Wild guinea pigs with a diet lowered in protein content (LPD) and investigated DNA methylation in sons sired before and after their father's LPD treatment in both, liver and testis tissues. Our results point to a 'heritable epigenetic response' of the sons to the fathers' dietary change. Because we detected methylation changes also in the testis tissue, they are likely to be transmitted to the F2 generation. Gene-network analyses of differentially methylated genes in liver identified main metabolic pathways indicating a metabolic reprogramming ('metabolic shift'). Epigenetic mechanisms, allowing an immediate and inherited adaptation may thus be important for the survival of species in the context of a persistently changing environment, such as climate change.
The Leopard cat Prionailurus bengalensis is a habitat generalist that is widely distributed across Southeast Asia. Based on morphological traits, this species has been subdivided into 12 subspecies. Thus far, there have been few molecular studies investigating intraspecific variation, and those had been limited in geographic scope. For this reason, we aimed to study the genetic structure and evolutionary history of this species across its very large distribution range in Asia. We employed both PCR-based (short mtDNA fragments, 94 samples) and high throughput sequencing based methods (whole mitochondrial genomes, 52 samples) on archival, noninvasively collected and fresh samples to investigate the distribution of intraspecific genetic variation. Our comprehensive sampling coupled with the improved resolution of a mitochondrial genome analyses provided strong support for a deep split between Mainland and Sundaic Leopard cats. Although we identified multiple haplogroups within the species’ distribution, we found no matrilineal evidence for the distinction of 12 subspecies. In the context of Leopard cat biogeography, we cautiously recommend a revision of the Prionailurus bengalensis subspecific taxonomy: namely, a reduction to 4 subspecies (2 mainland and 2 Sundaic forms).
Do cities represent sources, sinks or isolated islands for urban wild boar population structure?
(2017)
Biodiversity has suffered a dramatic global decline during the past decades, and monitoring tools are urgently needed providing data for the development and evaluation of conservation efforts both on a species and on a genetic level. However, in wild species, the assessment of genetic diversity is often hampered by the lack of suitable genetic markers. In this article, we present Random Amplicon Sequencing (RAMseq), a novel approach for fast and cost-effective detection of single nucleotide polymorphisms (SNPs) in nonmodel species by semideep sequencing of random amplicons. By applying RAMseq to the Eurasian otter (Lutra lutra), we identified 238 putative SNPs after quality filtering of all candidate loci and were able to validate 32 of 77 loci tested. In a second step, we evaluated the genotyping performance of these SNP loci in noninvasive samples, one of the most challenging genotyping applications, by comparing it with genotyping results of the same faecal samples at microsatellite markers. We compared (i) polymerase chain reaction (PCR) success rate, (ii) genotyping errors and (iii) Mendelian inheritance (population parameters). SNPs produced a significantly higher PCR success rate (75.5% vs. 65.1%) and lower mean allelic error rate (8.8% vs. 13.3%) than microsatellites, but showed a higher allelic dropout rate (29.7% vs. 19.8%). Genotyping results showed no deviations from Mendelian inheritance in any of the SNP loci. Hence, RAMseq appears to be a valuable tool for the detection of genetic markers in nonmodel species, which is a common challenge in conservation genetic studies.
Phylogeography of the Small Indian Civet and Origin of Introductions to Western Indian Ocean Islands
(2016)
The biogeographic dynamics affecting the Indian subcontinent, East and Southeast Asia during the Plio-Pleistocene has generated complex biodiversity patterns. We assessed the molecular biogeography of the small Indian civet (Viverricula indica) through mitogenome and cytochrome b + control region sequencing of 89 historical and modern samples to (1) establish a time-calibrated phylogeography across the species’ native range and (2) test introduction scenarios to western Indian Ocean islands. Bayesian phylogenetic analyses identified 3 geographic lineages (East Asia, sister-group to Southeast Asia and the Indian subcontinent + northern Indochina) diverging 3.2–2.3 million years ago (Mya), with no clear signature of past demographic expansion. Within Southeast Asia, Balinese populations separated from the rest 2.6–1.3 Mya. Western Indian Ocean populations were assigned to the Indian subcontinent + northern Indochina lineage and had the lowest mitochondrial diversity. Approximate Bayesian computation did not distinguish between single versus multiple introduction scenarios. The early diversification of the small Indian civet was likely shaped by humid periods in the Late Pliocene–Early Pleistocene that created evergreen rainforest barriers, generating areas of intra-specific endemism in the Indian subcontinent, East, and Southeast Asia. Later, Pleistocene dispersals through drier conditions in South and Southeast Asia were likely, giving rise to the species’ current natural distribution. Our molecular data supported the delineation of only 4 subspecies in V. indica, including an endemic Balinese lineage. Our study also highlighted the influence of prefirst millennium AD introductions to western Indian Ocean islands, with Indian and/or Arab traders probably introducing the species for its civet oil.
Deciphering the genes involved in disease resistance is essential if we are to understand host-pathogen coevolutionary processes. The rabbit haemorrhagic disease virus (RHDV) was imported into Australia in 1995 as a biocontrol agent to manage one of the most successful and devastating invasive species, the European rabbit (Oryctolagus cuniculus). During the first outbreaks of the disease, RHDV caused mortality rates of up to 97%. Recently, however, increased genetic resistance to RHDV has been reported. Here, we have aimed to identify genomic differences between rabbits that survived a natural infection with RHDV and those that died in the field using a genomewide next-generation sequencing (NGS) approach. We detected 72 SNPs corresponding to 133 genes associated with survival of a RHD infection. Most of the identified genes have known functions in virus infections and replication, immune responses or apoptosis, or have previously been found to be regulated during RHD. Some of the genes identified in experimental studies, however, did not seem to play a role under natural selection regimes, highlighting the importance of field studies to complement the genomic background of wildlife diseases. Our study provides a set of candidate markers as a tool for the future scanning of wild rabbits for their resistance to RHDV. This is important both for wild rabbit populations in southern Europe where RHD is regarded as a serious problem decimating the prey of endangered predator species and for assessing the success of currently planned RHDV variant biocontrol releases in Australia.
Conservation genetics can provide data needed by conservation practitioners for their decisions regarding the management of vulnerable or endangered species, such as the sun bear Helarctos malayanus. Throughout its range, the sun bear is threatened by loss and fragmentation of its habitat and the illegal trade of both live bears and bear parts. Sharply declining population numbers and population sizes, and a lack of natural dispersal between populations all threaten the genetic diversity of the remaining populations of this species. In this first population genetics study of sun bears using microsatellite markers, we analyzed 68 sun bear samples from Cambodia to investigate population structure and genetic diversity. We found evidence for two genetically distinct populations in the West and East of Cambodia. Ongoing or recent gene flow between these populations does not appear sufficient to alleviate loss of diversity in these populations, one of which (West Cambodia) is characterized by significant inbreeding. We were able to assign 85% of sun bears of unknown origin to one of the two populations with high confidence (assignment probability >= 85%), providing valuable information for future bear reintroduction programs. Further, our results suggest that developed land (mostly agricultural mosaics) acts as a barrier to gene flow for sun bears in Cambodia. We highlight that regional sun bear conservation action plans should consider promoting population connectivity and enforcing wildlife protection of this threatened species.