Introduction
In the past 25,000 years, the earth has undergone substantial
environmental changes due to both human-mediated events (anthropogenic
environment destruction, desert expansion, extreme weather and the
growing anthropogenic climate crisis) (Cloudsley-Thompson 1978;
Rosenzweig et al. 2008) and events unrelated to humans
(glaciation and tectonic shifts) (Hewitt 2000;
Holmgren et al. 2003; Survey 2005). These
environmental shifts can fundamentally reorganize habitats, influence
organism fitness, rates of migration between locations, and population
ranges (Smith et al. 1995; Astanei et
al. 2005; Rosenzweig et al. 2008; Searleet al. 2009; Cini et al. 2012; Porrettaet al. 2012; Antunes et al. 2015). Signatures of
the way organisms adapt to these events are often left in patterns of
molecular variation within and between species (Charlesworthet al. 2003; Wright et al. 2003;
Excoffier et al. 2009).
When a population migrates to a new location it first goes through a
population bottleneck (as only a small proportion of the population will
establish in the new location) (Charlesworth et al.2003; Excoffier et al. 2009; Li and Durbin
2011). These bottlenecks result in the loss of rare alleles in the
population (Tajima 1989; Gillespie 2004). After the
bottleneck, the population will grow to fill the carrying capacity of
the new niche and adapt to the unique challenges in the new environment,
both signaled by an excess of rare alleles (Excoffier et
al. 2009; White et al. 2013). This adaptation can
involve selective sweeps from new mutations or standing genetic
variation, and signatures of adaptive evolution and local adaptation in
genes key to the success of the population in this new location
(Charlesworth et al. 2003; Hermisson and
Pennings 2005; McVean 2007; Messer and Petrov 2013).
However, these signals can confound each other making inference of
population history difficult. For example, both population expansions
and adaptation lead to an excess of rare alleles, meaning more thorough
analysis is required to identify the true cause of the signal
(Wright et al. 2003).
Signatures of demographic change are frequently detected in species that
have recently undergone range expansion due to human introduction
(Astanei et al. 2005; Excoffier et al.2009) or the changing climate (Hewitt 2000; Parmesan
and Yohe 2003; Guindon et al. 2010; Walshet al. 2011; Cini et al. 2012). Other hallmarks
of invasive species population genomics include signatures of
bottlenecks visible in the site frequency spectrum, and differentiation
between populations (Charlesworth et al. 2003;
Li and Durbin 2011). This can be detected by a deficit of rare
variants, a decrease in population pairwise diversity and an increase in
the statistic, Tajima’s D (Tajima 1989). Following the
establishment and expansion of a population, there is an excess of rare
variants and local adaptation results in divergence between the invading
population and the original population. These signatures are also
frequently utilized in human populations to identify traits which have
fixed upon the establishment of a humans in a new location, or to
identify how our human ancestors spread globally (Li and Durbin
2011).
The Madrean archipelago, located in southwestern USA and northwestern
Mexico, contains numerous forested mountains known as ‘Sky islands’,
separated by large expanses of desert (McCormack et al.2009; Coe et al. 2012). These ‘islands’ were connected
by lush forests during the previous glacial maximum which then
retreated, leaving forest habitat separated by hundreds of miles of
desert, presumably limiting migration between locations for most species
(Survey 2005; McCormack et al. 2009). The
islands are hotbeds of ecological diversity. However, due to the
changing climate in the past 100 years, they have become more arid,
which may drive migration and adaptation (McCormack et
al. 2009; Coe et al. 2012).
Drosophila innubila is a mycophageous Drosophila species
found throughout these Sky islands and thought to have arrived during
the last glacial maximum (Dyer and Jaenike 2005; Dyeret al. 2005). Unlike the lab model D. melanogaster ,D. innubila has a well-studied ecology (Lachaise and
Silvain 2004; Dyer and Jaenike 2005; Dyer et
al. 2005; Jaenike and Dyer 2008; Unckless 2011a;
Unckless and Jaenike 2011; Coe et al. 2012). In
fact, in many ways the ‘island’ endemic, mushroom-feeding ecological
model D. innubila represent a counterpoint to the human
commensal, cosmopolitan, genetic workhorse D. melanogaster .
We sought to reconstruct the demographic and migratory history ofD. innubila inhabiting the Sky islands. Isolated populations with
limited migration provide a rare opportunity to observe replicate bouts
of evolutionary change and this is particularly interesting regarding
the coevolution with pathogens (Dyer and Jaenike 2005;
Unckless 2011a). We also wanted to understand how D.
innubila adapt to their local climate and if this adaptation is
recurrent or recent and specific to local population. We resequenced
whole genomes of wild-caught individuals from four populations ofD. innubila in four different Sky island mountain ranges.
Surprisingly, we find little evidence of population structure by
location, with structure limited to the mitochondria and a single
chromosome (Muller element B which is syntenic with 2L in D.
melanogaster) (Markow and O’Grady 2006). However, we find some
signatures of local adaptation, such as for cuticle development and
fungal pathogen resistance, suggesting potentially a difference in
fungal pathogens and toxins between locations. We also find evidence of
mitochondrial translocations into the nuclear genome, with strong
evidence of local adaptation of these translocations, suggesting
potential adaptation to changes in metabolic process of the host between
location, and possibly even as a means of compensating for reduced
efficacy of selection due to Wolbachia infection (Jaenike
and Dyer 2008).