Introduction
Understanding how organisms adapt to their local environment is one of
the central questions of evolutionary biology, which is becoming
increasingly important in a world of human-induced rapid climate and
environmental change (HIREC). It is generally accepted that genetic
variation within and among populations is influenced by the local
environment in which organisms reside. For example, populations along an
environmental gradient may be adapted to their local conditions if
selection is strong enough relative to drift and gene flow between
populations (Kawecki & Ebert, 2004). Since local adaptation arises
from natural selection on adaptive phenotypic traits, it can be
demonstrated by genetic differentiation at the genetic loci underlying
those traits (Phifer-Rixey et al., 2018; Stillwell, 2010; Stinchcombe et
al., 2004). The genetic basis for environmental adaptation has been
uncovered for a few obvious traits with distinct phenotypic
characteristics, such as variation in coat colour in mice in relation to
environmental background colour (Linnen et al., 2009; Nachman et al.,
2003) or reduction in armour plating in sticklebacks in response to
freshwater colonization (Colosimo et al., 2005; Cresko et al., 2004),
or body size and blood chemistry (Phifer-Rixey et al., 2018).
Theoretical and empirical studies suggest that many adaptive processes
have a polygenic basis and are controlled by many genes of small effect
(Barghi et al., 2020; Yeaman, 2015). Conventional genome scans are good
at detecting signals from adaptive loci with large effects, but their
ability to detect weak signals of polygenic selection acting across many
loci is rather limited, because they focus on only one locus at a time
(Rellstab et al., 2015; Wellenreuther & Hansson, 2016). In contrast,
multivariate genotype-environment association (GEA) methods offer the
possibility of analysing many loci simultaneously together with several
environmental predictors. These are therefore suitable for detecting
signals of polygenic selection (Capblancq et al., 2018; Forester et al.,
2018), but have not yet been widely used in evolutionary ecology. In
addition, these multivariate approaches also allow quantification of
spatial patterns of adaptive genetic variation associated with
environmental variables (Lasky et al., 2012; Micheletti et al., 2018;
Nadeau et al., 2016).
Small forest mammals provide an ideal biological model to investigate
the relative roles of selective and neutral factors in response to
clinal environmental gradients, because they have large geographic
ranges and individuals are not highly mobile within the range (Haasl &
Payseur, 2016). Such gradients, and their respective genetic responses,
include climate, and divergence in gene regulatory regions and genes
related to metabolism and immunity (Phifer-Rixey et al., 2018) or body
size and extremities ratio (Ballinger & Nachman, 2022); rural-urban
gradients, and signals of selection in genes involved in lipids and
carbohydrates metabolism (S. E. Harris & Munshi-South, 2017); as well
as altitudinal gradients, and genes related to metabolic function and
oxygen transport (Beckman et al., 2022; Waterhouse et al., 2018).
The bank vole Myodes glareolus (also known asClethrionomys glareolus ; Kryštufek et al., 2020) is a
small Eurasian forest-dwelling rodent with a broad geographic
distribution in Europe, ranging from the Mediterranean peninsulas and
the southern coast of the Black Sea in the south almost to the northern
edge of Scandinavia (Figure 1). This distribution covers a wide
temperature gradient (Figure 1). Bank voles survived in several refugia
during the Last Glacial Maximum, including the well known refugia on the
Mediterranean peninsulas and cryptic refugia in the Carpathians (Kotlik
et al., 2006; Wójcik et al., 2010) and the Ural Mountains (Abramson et
al., 2009; Deffontaine et al., 2005). Their subsequent recolonization
of Europe, when the climate became more favourable at the beginning of
the Holocene, resulted in a complex genetic structure, with several
distinct phylogeographic lineages, first described based on
mitochondrial DNA sequences (Filipi et al., 2015) and later confirmed by
genome-wide SNP analyses (Horniková et al., 2021; Marková et al., 2020).
Bank voles have limited dispersal capabilities (Deter et al., 2008;
Viitala et al., 1994) and short generation times, resulting in large
local effective population sizes. Together with their limited capacity
to disperse, these factors result in a large evolutionary potential for
genetic responses to local conditions. Therefore, bank voles are a
suitable system to study signatures of local adaptation in response to
spatially varying climate-induced selective pressures along an
environmental gradient. They have been the target of GEA-studies in
relation to geographic expansion (White et al., 2013) and tolerance toPuumala orthohantavirus infection (Rohfritsch et al., 2018).
However, the specific selection forces driving adaptations, as well as
the genetic loci involved, are not well understood for wide latitudinal
gradients.