Haplotype-resolved genome and population genomics of the threatened garden dormouse in Europe [RESOURCES]

Paige A. Byerly1,2,16, Alina von Thaden1,2,16, Evgeny Leushkin1,3, Leon Hilgers1,3, Shenglin Liu1,3, Sven Winter4,5, Tilman Schell1,3, Charlotte Gerheim1,3, Alexander Ben Hamadou1,3, Carola Greve1,3, Christian Betz6, Hanno J. Bolz6, Sven Büchner7, Johannes Lang7, Holger Meinig7, Evax Marie Famira-Parcsetich7, Sarah P. Stubbe7, Alice Mouton8, Sandro Bertolino9, Goedele Verbeylen10, Thomas Briner11, Lídia Freixas12, Lorenzo Vinciguerra13, Sarah A. Mueller14, Carsten Nowak1,2 and Michael Hiller1,3,15 1LOEWE Centre for Translational Biodiversity Genomics, 60325 Frankfurt, Germany; 2Conservation Genetics Group, Senckenberg Research Institute and Natural History Museum Frankfurt, 63571 Gelnhausen, Germany; 3Senckenberg Research Institute, 60325 Frankfurt, Germany; 4Senckenberg Biodiversity and Climate Research Centre, 60325 Frankfurt am Main, Germany; 5Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, 1160 Vienna, Austria; 6Bioscientia Human Genetics, Institute for Medical Diagnostics GmbH, 55218 Ingelheim, Germany; 7Justus-Liebig-University Giessen, Clinic for Birds, Reptiles, Amphibians and Fish, Working Group for Wildlife Research, 35392 Giessen, Germany; 8Socio-économie, Environnement et Développement (SEED), University of Liege (Arlon Campus Environment), 81001 Arlon, Belgium; 9Department of Life Sciences and Systems Biology, University of Turin, 10123 Torino, Italy; 10Natuurpunt Studie vzw, Mammal Working Group, 2800 Mechelen, Belgium; 11Naturmuseum Solothurn, 4500 Solothurn, Switzerland; 12BiBio Research Group, Natural Sciences Museum of Granollers, 08402 Granollers, Catalonia, Spain; 13Naturmuseum St. Gallen, 9016 St. Gallen, Switzerland; 14Division of Evolutionary Biology, Faculty of Biology, LMU Munich, 80539 Munich, Germany; 15Institute of Cell Biology and Neuroscience, Faculty of Biosciences, Goethe University Frankfurt, 60438 Frankfurt, Germany

16 These authors contributed equally to this work.

Corresponding authors: paige.byerlysenckenberg.de, michael.hillersenckenberg.de Abstract

Genomic resources are important for evaluating genetic diversity and supporting conservation efforts. The garden dormouse (Eliomys quercinus) is a small rodent that has experienced one of the most severe modern population declines in Europe. We present a high-quality haplotype-resolved reference genome for the garden dormouse, and combine comprehensive short and long-read transcriptomics data sets with homology-based methods to generate a highly complete gene annotation. Demographic history analysis of the genome reveal a sharp population decline since the last interglacial, indicating an association between colder climates and population declines before anthropogenic influence. Using our genome and genetic data from 100 individuals, largely sampled in a citizen-science project across the contemporary range, we conduct the first population genomic analysis for this species. We find clear evidence for population structure across the species’ core Central European range. Notably, our data show that the Alpine population, characterized by strong differentiation and reduced genetic diversity, is reproductively isolated from other regions and likely represents a differentiated evolutionary significant unit (ESU). The predominantly declining Eastern European populations also show signs of recent isolation, a pattern consistent with a range expansion from Western to Eastern Europe during the Holocene, leaving relict populations now facing local extinction. Overall, our findings suggest that garden dormouse conservation may be enhanced in Europe through the designation of ESUs.

Received February 21, 2024. Accepted September 12, 2024.

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