Discussion
Migration and environmental change can drive adaptation (Rankin
and Burchsted 1992; Charlesworth et al. 2003;
Gillespie 2004; Excoffier et al. 2009;
Porretta et al. 2012; White et al.2013). Species with somewhat isolated or divided populations are likely
to adapt to their differing local environments. Migration can both
facilitate and hinder such adaptation, allowing new variation (including
potentially beneficial variants) to be spread between populations and
preventing inbreeding depression. Strong migration can also import
locally nonadaptive variants and prevent the fixation of the most fit
variants in local populations. We sought to examine the extent that
these processes take place in a species of Drosophila found
across four forests separated by large expanses of desert.
We characterized the phylogeographic history of four populations ofDrosophila innubila , a mycophagous species endemic to the
Arizonan Sky islands using whole genome resequencing of wild-caught
individuals. D. innubila expanded into its current range during
or following the previous glacial maximum (Figure 1, Supplementary
Figure 1). We find some evidence of local adaptation, primarily in the
cuticle development genes and antifungal immune genes (Figure 2,
Supplementary Figure 2). Interestingly, there is very little support for
population structure across the nuclear genome (Figures 1 & 2,
Supplementary Figures 1 & 2), including in the repetitive content
(Supplementary Figure 11), but some evidence of population structure in
the mitochondria, as found previously in D. innubila(Dyer and Jaenike 2005). This suggests that if gene flow is
occurring, it could be primarily males migrating, as is seen in other
non-Drosophila species (Rankin and Burchsted 1992;
Searle et al. 2009; Ma et al. 2013;
Avgar and Fryxell 2014). Based on the polymorphism data
available, coalescent times are not deep, and given our estimated
population history, this suggests that variants aren’t ancestrally
maintained and are instead transmitted through migration between
locations (Charlesworth et al. 2003).
Segregating inversions are often associated with population structure
and could explain the abnormalities seen on Muller element B here
(Supplementary Figures 2-5). Our detection of several putative
segregating inversions on Muller element B relative to all other
chromosomes (Figure 3A) supports this assertion. However, few of the
putative inversions support this hypothesis, in that all are large and
common inversions characterized in all populations, suggesting the
inversions are not driving the elevated FST. We suspect
that the actual causal inversions may not have been characterized due to
the limitations of detecting inversions in repetitive regions with short
read data (Marzo et al. 2008; Chakrabortyet al. 2017). The elevated FST could also be
caused by other factors, such as extensive duplication and divergence on
Muller element B being misanalysed as just divergence. In fact, the
broken and split read pairs used to detect inversions are very similar
to the signal used to detect duplications (Ye et al.2009; Rausch et al. 2012; Chen et al.2016), suggesting some misidentification may have occurred. If a large
proportion of Muller B was duplicated, we would see elevated mean
coverage of Muller element B in all strains compared to other autosomes,
which is not the case (Supplementary Table 1). Further study is
necessary to disentangle if inversions or other factors are causing this
elevated FST and the selective and/or demographic
pressures driving this differentiation. However, it is worth noting thatD. pseudoobscura segregates for inversions on Muller element C
and these segregate by population in the same Sky island populations
(and beyond) as the populations described here (Dobzhansky and
Sturtevant 1937; Dobzhansky et al. 1963;
Fuller et al. 2016). Thus, the inversion polymorphism
among populations is a plausible area for local adaptation and may
provide an interesting contrast to the well-studied D.
pseudoobscura inversions.
We find very few signatures of divergence between samples from 2001 and
2017 (Supplementary Figure 8). Though the environment has changed in the
past few decades, there may have been little impact on the habitat ofD. innubila in the Chiricahuas, resulting in few changes in
selection pressures in this short period of time, unlike most bird and
mammal’s species in the same area (Coe et al. 2012).
Interestingly, there was an extensive forest fire in 2011 which could
plausibly have been a strong selective force but we see no genome-wide
signature of such (Arechederra-Romero 2012). Alternatively,
seasonal fluctuations in allele frequencies may swamp out directional
selection. Excessive allele frequency change is limited to a few genes
with no known association to each other, and little overlap with the
diverging genes between populations. Some of the genes with elevated
FST (and differing in allele frequency) between time
points overlap with divergent genes between sexes, primarily at the
telomere of the X chromosome (Muller element A, Supplementary Figure 8).
In fact, FST is significantly correlated on Muller
element A between the two surveys (Pearson’s correlation t = 82.411,
p-value = 1.2e-16), even with the 2001-2017 survey only considering male
samples, supporting an association between the factors driving
divergence between sexes and over time. Given the sex bias of SNPs in
this region, this could suggest that a selfish factor with differential
effects in the sexes is located on the X chromosome near the telomere
(Burt and Trivers 2006). Often these selfish elements also
accumulate inversions to prevent the breakdown of synergistic genetic
components (Burt and Trivers 2006), and the Muller A telomere
appears to have accumulated several inversions (Figure 3A). However,
populations of D. innubila are already female-biased due to the
male-killing Wolbachia infection found in 30-35% of females
(Dyer 2004; Dyer and Jaenike 2005; Jaenike and
Dyer 2008). Thus D. innubila could be simultaneously parasitized
by both the male-killing Wolbachia and a selfish X chromosome.
Alternatively, the strong signals associated with the telomere of the X
could be a signature of selection related to the Wolbachiainfection (Unckless 2011b).
Ours is one of few studies that sequences individual wild-caughtDrosophila and therefore avoids several generations of inbreeding
that would purge recessive deleterious alleles (Gillespie 2004;
Mackay et al. 2012; Pool et al. 2012).
The excess of putatively deleterious alleles harkens back to early
studies of segregating lethal mutations in populations as well as recent
work on humans (Dobzhansky et al. 1963;
Marinkovic 1967; Dobzhansky and Spassky 1968;
Watanabe et al. 1974; Gao et al. 2015).
To date, most of the genomic work concerning the phylogeography and
dispersal of different Drosophila species has been limited to themelanogaster supergroup (Pool et al. 2012;
Pool and Langley 2013; Behrman et al. 2015;
Lack et al. 2015; Machado et al. 2015),
with some work in other Sophophora species (Fulleret al. 2016). This limits our understanding of how non-commensal
species disperse and behave, and what factors seem to drive population
demography over time. Here we have glimpsed into the dispersal and
history of a species of mycophageous Drosophila and found
evidence of changes in population distributions potentially due to the
changing climate (Survey 2005) and population structure
possibly driven by segregating inversions and selfish elements. Because
many species have recently undergone range changes or expansions
(Excoffier et al. 2009; Porretta et al.2012; White et al. 2013), we believe examining how this
has affected genomic variation is important for population modelling and
even for future conservation efforts (Excoffier et al.2009; Coe et al. 2012).