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The genome of the Pyrenean desman and the effects of bottlenecks and inbreeding on the genomic landscape of an endangered species.

ABSTRACT: The Pyrenean desman (Galemys pyrenaicus) is a small semiaquatic mammal endemic to the Iberian Peninsula. Despite its limited range, this species presents a strong genetic structure due to past isolation in glacial refugia and subsequent bottlenecks. Additionally, some populations are highly fragmented today as a consequence of river barriers, causing substantial levels of inbreeding. These features make the Pyrenean desman a unique model in which to study the genomic footprints of differentiation, bottlenecks and extreme isolation in an endangered species. To understand these processes, the complete genome of the Pyrenean desman was sequenced and assembled using a Bloom filter-based approach. An analysis of the 1.83 Gb reference genome and the sequencing of five additional individuals from different evolutionary units allowed us to detect its main genomic characteristics. The population differentiation of the species was reflected in highly distinctive demographic trajectories. In addition, a severe population bottleneck during the postglacial recolonization of the eastern Pyrenees created one of the lowest genomic heterozygosity values recorded in a mammal. Moreover, isolation and inbreeding gave rise to a high proportion of runs of homozygosity (ROH). Despite these extremely low levels of genetic diversity, two key multigene families from an eco-evolutionary perspective, the major histocompatibility complex and olfactory receptor genes, showed heterozygosity excess in the majority of individuals, revealing that functional diversity can be maintained up to a certain extent. Furthermore, these two classes of genes were significantly less abundant than expected within ROH. In conclusion, the genomic landscape of each analysed Pyrenean desman turned out to be strikingly distinctive and was a clear reflection of its recent ancestry and current conservation conditions. These results may help characterize the genomic health of each individual, and can be crucial for the conservation and management of the species.

SUBMITTER: Escoda L

PROVIDER: S-EPMC8288019 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Molecular techniques allow non-invasive dietary studies from faeces, providing an invaluable tool to unveil ecological requirements of endangered or elusive species. They contribute to progress on important issues such as genomics, population genetics, dietary studies or reproductive analyses, essential knowledge for conservation biology. Nevertheless, these techniques require general methods to be tailored to the specific research objectives, as well as to substrate- and species-specific constraints. In this pilot study we test a range of available primers to optimise diet analysis from metabarcoding of faeces of a generalist aquatic insectivore, the endangered Pyrenean desman (Galemys pyrenaicus, É. Geoffroy Saint-Hilaire, 1811, Talpidae), as a step to improve the knowledge of the conservation biology of this species. Twenty-four faeces were collected in the field, DNA was extracted from them, and fragments of the standard barcode region (COI) were PCR amplified by using five primer sets (Brandon-Mong, Gillet, Leray, Meusnier and Zeale). PCR outputs were sequenced on the Illumina MiSeq platform, sequences were processed, clustered into OTUs (Operational Taxonomic Units) using UPARSE algorithm and BLASTed against the NCBI database. Although all primer sets successfully amplified their target fragments, they differed considerably in the amounts of sequence reads, rough OTUs, and taxonomically assigned OTUs. Primer sets consistently identified a few abundant prey taxa, probably representing the staple food of the Pyrenean desman. However, they differed in the less common prey groups. Overall, the combination of Gillet and Zeale primer sets were most cost-effective to identify the widest taxonomic range of prey as well as the desman itself, which could be further improved stepwise by adding sequentially the outputs of Leray, Brandon-Mong and Meusnier primers. These results are relevant for the conservation biology of this endangered species as they allow a better characterization of its food and habitat requirements.

Project description:The genetic structure of small semiaquatic animals may be influenced by dispersal across both rivers and land. The relative importance of these two modes of dispersal may vary across different species and with ecological conditions and evolutionary periods. The Pyrenean desman (Galemys pyrenaicus) is an endemic mammal of the Iberian Peninsula with a strong phylogeographic structure and semiaquatic habits, thus making it an ideal model to study the effects of river and overland dispersal on its genetic structure. Thanks to different types of noninvasive samples, we obtained an extensive sampling of the Pyrenean desman from the northwestern region of the Iberian Peninsula and sequenced two mitochondrial DNA fragments. We then analyzed, using an isolation-by-distance approach, the correlation between phylogenetic distances and geographical distances measured along both river networks and land to infer the relative importance of river and overland dispersal. We found that the correlations in the whole area and in a large basin were consistent with an effect of overland dispersal, which may be due to the postglacial colonization of new territories using terrestrial corridors and, possibly, a more extensive fluvial network that may have been present during the Holocene. However, in a small basin, likely to be less influenced by the impact of ancient postglacial dispersal, the correlations suggested significant overall effects of both overland and river dispersal, as expected for a semiaquatic mammal. Therefore, different scales and geographical regions reflect different aspects of the evolutionary history and ecology of this semiaquatic species using this isolation-by-distance method. The results we obtained may have crucial implications for the conservation of the Pyrenean desman because they reinforce the importance of interbasin dispersal for this species in the studied area and the need to protect the whole riverine ecosystem, including rivers, upland streams and terrestrial corridors between basins.

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The genome of the Pyrenean desman and the effects of bottlenecks and inbreeding on the genomic landscape of an endangered species.

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