Population genetic structure shaped by isolation-by-distance and
historical dynamics
The population genetic pattern that we observe is partly consistent with
isolation-by-distance (IBD). The Mantel test showed a significant,
positive correlation between pairwise geographic distance and genetic
distance although the effect size is very small when individuals with
high kinship values are removed from the dataset. Individuals located
within 1 km have significantly lower pairwise genetic distances than
expected by chance, and this significance drops off by 2 km (Figure S4).
Additionally, pairwise F ST between the
non-adjacent MT summit and MK clusters is greater than the value between
neighboring clusters (Table 2a). High rates of gene flow between
adjacent demes across the landscape, with relatively short dispersal
distances as suggested by the correlogram and ANOVA (Figure S4, Table
1), could have generated the clinal pattern we observe (Figure 5);
however, this does not explain the distinctiveness of the summit MT
cluster. The Euclidean distance between the lowest and highest sampled
points on MK (ca. 13.5 km) is greater than the distance between the
lowest and highest sampling points on MT (ca. 4.5 km), yet there is more
population genetic differentiation on MT. This indicates that the
structure we observe is not due to isolation-by-distance or
isolation-by-elevation alone, and that genetic similarity decays with
geographic distance at unequal rates in this landscape (Figure S5a).
Historical population dynamics, in addition to IBD, likely contributed
to the observed population genetic structure. Without data from other
locations in Borneo, it is difficult to determine what process(es)
generated the pattern. However, we suggest a plausible scenario given
known information about the relative ages of MT and MK and the degree of
divergence between the mountain treeshrew and its sister species.MT reached its current elevation earlier (ca. 11–7 Mya) than MK (ca. 1
Mya) (Collenette, 1964; Hall, 1998; Liew et al. 2010). This suggests
that MT was available for colonization prior to the split of mountain
treeshrews from ruddy treeshrews ca. 4 Mya (Roberts et al., 2011). If
mountain treeshrews were resident on MT prior to the major uplift of MK,
and a second colonization event occurred later, this would explain the
signature of two population clusters. We find higher-than-average
genetic diversity among individuals at high elevation MT despite its
smaller habitat area (Figures 1a & S5b), which is consistent with our
hypothesis that this region maintained a relatively stable, or recently
reduced, effective population size over time relative to MK. Lower gene
flow upslope to high elevation MT relative to gene flow towards MK may
have preserved the signature of this cluster.
In the MIGRATE-N analysis, the estimated rate of migration upslope to
high elevation MT was lower than migration downslope and toward MK
(Table S6). We suggest that reduced gene flow to high elevation MT may
be related to shifts in the plant community that occur between 1450 masl
and the summit (van der Ent, Cardace, Tibbett, & Echevarria, 2018).
Supporting this hypothesis, trapping success of mountain treeshrews and
other small mammals is low from 1500 to 1800 masl, and increases above
2000 masl (Camacho-Sanchez et al., 2019).
By contrast, lack of differentiation across MK could have been
influenced by an upslope shift at the mountain treeshrew’s upper
elevational limit, enabled by climate warming and upslope shifts in
montane forest since the Last Glacial Maximum (LGM). During late
Quaternary glacial cycles, MK’s summit alternated between ice-free
(during glacial minima) and ice-covered (during glacial maxima) periods
(Hall et al., 2008). After the LGM ca. 20,000 ybp, the ice began to melt
and by 9,200 ybp the summit was likely ice-free (Hall et al., 2008).
Upslope shifts in montane forest during this period of warming could
have enabled range expansion at high elevations by mountain
treeshrews. Mountain treeshrews on MT likely did not experience a
concurrent upslope range shift since MT has a much lower summit than MK
which was never covered in ice (Hall et al., 2008). The lack of a
population expansion signature in the mountain treeshrew mitogenome data
could be explained by unrestricted gene flow between adjacent areas
during expansion (Pierce, Gutierrez, Rice, & Pfennig, 2017). As
predicted for a recent expansion, we find lower-than-average genetic
diversity among high elevation MK individuals (≥1600 masl) using
estimated effective migration surface modeling (Petkova, Novembre, &
Stephens, 2016) to visualize genetic diversity on the landscape (Figure
S5b).