High genomic diversity in the bank vole at the northern apex of a range expansion: The role of multiple colonizations and end‐glacial refugia

Abstract

The history of repeated northern glacial cycling and southern climatic stability has long dominated explanations for how genetic diversity is distributed within temperate species in Eurasia and North America. However, growing evidence indicates the importance of cryptic refugia for northern colonization dynamics. An important geographic region to assess this is Fennoscandia, where recolonization at the end of the last glaciation was restricted to specific routes and temporal windows. We used genomic data to analyse genetic diversity and colonization history of the bank vole (Myodes glareolus) throughout Europe (>800 samples) with Fennoscandia as the northern apex. We inferred that bank voles colonized Fennoscandia multiple times by two different routes; with three separate colonizations via a southern land-bridge route deriving from a "Carpathian" glacial refugium and one via a north-eastern route from an "Eastern" glacial refugium near the Ural Mountains. Clustering of genomewide SNPs revealed high diversity in Fennoscandia, with eight genomic clusters: three of Carpathian origin and five Eastern. Time estimates revealed that the first of the Carpathian colonizations occurred before the Younger Dryas (YD), meaning that the first colonists survived the YD in Fennoscandia. Results also indicated that introgression between bank and northern red-backed voles (Myodes rutilus) took place in Fennoscandia just after end-glacial colonization. Therefore, multiple colonizations from the same and different cryptic refugia, temporal and spatial separations and interspecific introgression have shaped bank vole genetic variability in Fennoscandia.Together, these processes drive high genetic diversity at the apex of the northern expansion in this emerging model species. K E Y W O R D S approximate Bayesian computation, Clethrionomys glareolus, climate change, cryptic refugia, genotyping-by-sequencing, population genomics | 1731 MARKOVÁ et Al.

Gene Expression Variation of Candidate Endogenous Control Genes Across Latitudinal Populations of the Bank Vole (Clethrionomys glareolus)

“…Furthermore, when studying gene expression in wild populations there are additional sources of variation due to the natural heterogeneity of the sample (Kozera and Rapacz, 2013;Huang and Agrawal, 2016). In this study we have identified two strong pairs of RGs for the use in RT-qPCR studies of the bank vole, an emerging model species for evolutionary and epidemiological studies (Marková et al, 2020).…”

“…studies and represented the three latitudinal zones identified based on the combined information from phylogenetic analyses of mitochondrial DNA sequences (Filipi et al, 2015) and clustering of genomic data (Marková et al, 2020): southern refugial (n = 6), which includes the areas of glacial refugia in the Mediterranean region, northern apex (n = 7), which includes Great Britain and Fennoscandia as the apex areas of the northward end-glacial colonization; and central (n = 8), including samples from the area between southern and northern regions, which has a mixed history of glacial survival and post-glacial colonization (Filipi et al, 2015;Marková et al, 2020).…”

“…The bank vole displays one of the most complex geographical patterns of population structure in any small mammal studied to date (Pedreschi et al, 2019), likely as the result of isolation and adaptation of populations during and after the glacial periods of the Pleistocene (Deffontaine et al, 2005;Kotlík et al, 2014;Filipi et al, 2015). While suitable glacial refugia for the bank vole have persisted in southern Mediterranean regions of Europe and in the vicinity of the major mountain ranges (such as the Carpathians), facilitating population divergence and accumulation of genetic diversity, recurrent founder events during end-glacial colonization of northern areas resulted in a reassortment and/or reduction of diversity away from the refugial areas (Marková et al, 2020). The broad range and complex history made the bank vole one of the key mammals used in genetic studies of the response to climate change at the end of the last glaciation (Wójcik et al, 2010;Colangelo et al, 2012;Kotlík et al, 2018;Marková et al, 2020) including local adaptation to environmental heterogeneity (Kotlík et al, 2014;Strážnická et al, 2018).…”

“…While suitable glacial refugia for the bank vole have persisted in southern Mediterranean regions of Europe and in the vicinity of the major mountain ranges (such as the Carpathians), facilitating population divergence and accumulation of genetic diversity, recurrent founder events during end-glacial colonization of northern areas resulted in a reassortment and/or reduction of diversity away from the refugial areas (Marková et al, 2020). The broad range and complex history made the bank vole one of the key mammals used in genetic studies of the response to climate change at the end of the last glaciation (Wójcik et al, 2010;Colangelo et al, 2012;Kotlík et al, 2018;Marková et al, 2020) including local adaptation to environmental heterogeneity (Kotlík et al, 2014;Strážnická et al, 2018). Additionally, bank vole is an important zoonotic reservoir of various emerging pathogens such as Puumala orthohantavirus (PUUV) (Khalil et al, 2019;Madriéres et al, 2019) Ljungan virus (Hauffe et al, 2010) and cowpox virus (Franke et al, 2017), with significant differences in the level of host immune-related gene expression reported between bank voles from PUUV endemic and non-endemic regions of Europe (Guivier et al, 2014).…”

Mitochondrial Genome Evolution, Genetic Diversity, and Population Structure in British Water Voles (Arvicola amphibius)

“…MtDNA control region sequences of Myodes glareolus were used as a comparison to A. amphibius. All sequences were obtained from [26,27] and multiple alignments were computed based on location, before calculating population genetics statistics for each.…”