Academic journal article Genetics

Genome-Wide Patterns of Differentiation among House Mouse Subspecies

Academic journal article Genetics

Genome-Wide Patterns of Differentiation among House Mouse Subspecies

Article excerpt

(ProQuest: ... denotes formulae omitted.)

UNDERSTANDING the genetic basis of speciation is a fundamental goal of evolutionary biology. This problem has primarily been approached in two ways: through laboratory studies using crosses and through studies of genetic variation in natural populations. Laboratory studies control for genetic background and environment, and they make it possible to connect genotype and phenotype. These types of studies have produced some spectacular successes including the identification of individual genes underlying postzygotic isolation in Drosophila (e.g., Ting et al. 1998; Presgraves et al. 2003; Brideau et al. 2006; Masly et al. 2006), Arabidopsis (Bomblies et al. 2007; Bikard et al. 2009), Mus (Mihola et al. 2009), and others (reviewed in Presgraves 2010 and Nosil and Schluter 2011).

Studies of natural populations rely on the idea that regions of the genome that are important in reproductive isolation may be more differentiated than other regions of the genome. Therefore, by studying patterns of differentiation, one may gain insight into the genomic regions that underlie isolation. The idea that the genomes of closely related species are mosaics of differentiated and less differentiated regions is not new and first emerged in the literature on hybrid zones (e.g., Key 1968; Harrison 1986; Tucker et al. 1992; Rieseberg et al. 1999; reviewed in Harrison 2012). The advent of genomic methods has fueled a renewed interest in studying patterns of differentiation between closely related species, including work on mosquitoes (Turner et al. 2005; Lawniczak et al. 2010; Neafsey et al. 2010), mice (Harr 2006), Drosophila (Kulathinal et al. 2009), Heliconius butterflies (Nadeau et al. 2012), flycatchers (Ellegren et al. 2012), crickets (Andrés et al. 2013), sunflowers (Renaut et al. 2013), and others.

Despite their appeal, genome scans present a number of challenges. One is correctly identifying genomic regions that show unexpectedly high levels of differentiation. This has typically been done either by specifying an appropriate null demographic model against which an observed distribution can be compared or by simply identifying extreme values as potential candidate regions. Another challenge is interpreting the biological meaning of a genomic region showing a high level of differentiation. Shared polymorphism can result from retained ancestral variation or from gene flow; conversely, differentiation can result from sorted ancestral variation (due to drift or selection) or from absence of gene flow. Charlesworth (1998) pointed out that reduced variation within a population will inflate estimates of differentiation, such as F st, that are based on both within- and between-population components of variation. As a result, background selection (Charlesworth 1993) and genetic hitchhiking (Maynard Smith and Haigh 1974) may lead to localized high values of Fst even for regions that are not involved in reproductive isolation (Cruickshank and Hahn 2014). Therefore, genomic "islands of differentiation" may reflect (1) stochastic variation in lineage sorting; (2) regions of reduced gene flow; (3) regions in which the effects of selection at linked sites are more pronounced, regardless of involvement with reproductive isolation; or (4) some combination of these processes.

House mice provide a valuable system for the study of speciation. Mus musculus consists of three subspecies that are distributed parapatrically: M. m. domesticus in western Europe, M. m. musculus in eastern Europe and northern Asia, and M. m. castaneus in southeast Asia. These subspecies are believed to have diverged in allopatry at roughly the same time-~350,000 years ago (Bonhomme et al. 2007; Geraldes et al. 2008, 2011; White et al. 2009)-and come into secondary contact much more recently (e.g., Cucchi et al. 2005; Duvaux et al. 2011). Each subspecies meets and hybridizes with the other two species where their ranges come into contact (e. …

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