Intraspecific neutral and adaptive variation
The persistence of populations that are increasingly isolated depends
largely upon the level of connectivity between them (Hodgson et
al. 2011). Thus, the high differentiation observed among some
populations within NIDGS might result from loss of suitable habitat and
dispersal corridors between populations, currently leading to the
isolation (and possible extinction) of populations (Yensen 1999; Sherman
& Runge 2002; Barrett 2005). Such patterns are frequent in other small
mammals with historically reduced ranges across altitudinal gradients
(Waterhouse et al. 2018; Bi et al. 2019). For NIDGS, the
neutral dataset identified two main groups (termed here ‘western’ and
‘eastern’, Figure 6A, K = 2) which corroborates previous studies
that used microsatellite loci (Garner et al. 2005;
Hoisington-Lopez et al. 2012; Zero et al. 2017). Our
results also identified more fine-scale structure within the eastern
part of the range than within the western part of the range, indicating
higher connectivity across the populations sampled from the western
region. This result is similar to that of previous microsatellite
analyses for the eastern part of the range (although this study did not
analyze the exact same populations; Garner et al. 2005), but contrasts
somewhat with our hypothesis (a) of IBD and the results of an allozyme
study, which found significant IBD within the western region (Gavinet al. 1999) and with unpublished results from Hoisington (2007)
which found evidence for additional substructure and restricted gene
flow within both the eastern and western groups. Very similar patterns
of differentiation have also been found using mitochondrial DNA
(Hoisington 2007). For SIDGS, the neutral dataset identified the highest
differentiation between populations on different sides of the Weiser
River, which corroborates previous studies (Garner et al. 2005;
Hoisington 2007; Zero et al. 2017). Interestingly, although Olds
Ferry was the most distinct population at the neutral level, it was not
substantially differentiated from other populations on the eastern side
of the Weiser River at the adaptive level, suggesting that its
distinction is mostly due to demographic (i.e. neutral) processes
(Garner et al. 2005; Hoisington-Lopez et al. 2012; Zeroet al. 2017). Previous studies sampled a larger number of sites
(10-11) and detected additional subgroups both east and west of the
Weiser River (Hoisington 2007; Zero et al. 2017). Earlier work on
SIDGS, which included a larger number of populations and larger spatial
area, found human disturbance (impervious surfaces and agriculture) and
small-scale topographic complexity to restrict gene flow while higher at
site heat load index, growing season precipitation and frost free period
facilitated gene flow (Zero et al. 2017). Translocations among
populations east of the Weiser River were performed to supplement small
and isolated populations, and might have led to an increased level of
genetic homogeneity at the neutral level (Yensen et al. 2010;
Weeks et al. 2011; Yensen & Tarifa 2012; Landguth & Balkenhol
2012). Successful translocations would result in low neutral and
adaptive differentiation, but previous studies have found low rates of
translocation success (Panek 2005; Busscher 2009; Yensen et al.2010; Smith et al. 2019). These translocations were performed
mainly into areas near the Weiser River population and might explain the
low genetic differentiation observed between this population and all
others east of the Weiser River (Figure S11C, Supporting information).
Similarly, adaptive differentiation was lowest for WR, suggesting some
benefits of translocations (increased genetic diversity and masking of
deleterious alleles) outweighing the potential negative effects such as
outbreeding depression (Weeks et al. 2011). Still, most of the
SIDGS populations showed lower than expected neutral heterozygosity
(Table 4), which suggests effects of inbreeding leading to reduced
genetic diversity. This agrees with previous studies that have found
lower genetic diversity in SIDGS than NIDGS, and point to the need of
increased protection of this species (Garner et al. 2005).