Academic journal article Genetics

A Coalescent Model for a Sweep of a Unique Standing Variant

Academic journal article Genetics

A Coalescent Model for a Sweep of a Unique Standing Variant

Article excerpt

(ProQuest: ... denotes formulae omitted.)

IN recent decades, an understanding of how positive directional selection and the associated hitchhiking effect influence patterns of genetic variation has become a valuable tool for evolutionary geneticists. The reductions in genetic diversity and long extended haplotypes that are characteristic of a recentselective sweep can allowfor boththe identification of individual genes that have contributed to recent adaptation within a population (i.e., hitchhiking mapping) and understanding the rate and dynamics of adaptation at a genome-wide level (Wiehe and Stephan 1993; Andolfatto 2007; Eyre-Walker and Keightley 2009; Elyashiv et al. 2014).

While the contribution of many different modes to the adaptive process has long been recognized, early work on the hitchhiking effect focused largely on the scenario where a single codominant mutation arose and was immediately beneficial, rapidly sweeping to fixation (Maynard Smith and Haigh 1974; Kaplan et al. 1989). Both simulation studies and analytical explorations during the last decade, however, have drawn attention to models in which adaptation proceeds from alleles present in the standing variation or arising via recurrent mutation once the sweep has already begun (Innan and Kim 2004; Przeworski et al. 2005; Hermisson and Pennings 2005; Pennings and Hermisson 2006a,b; Barrett and Schluter 2008; Hermisson and Pfaffelhuber 2008; Ralph and Coop 2010; Pokalyuk 2012; Roesti et al. 2014; Wilson et al. 2014). Collectively, these phenomena have come to be known as "soft sweeps," a term originally coined by Hermisson and Pennings (2005) and now often used as a catchall phrase to refer to any sweep for which the most recent common ancestor at the locus of the beneficial allele(s) predates the onset of positive selection (Messer and Petrov 2013).

Empiricalwork occurring largelyin parallel with thetheory discussed above suggests that soft sweeps of one variety or another likely make a substantial contribution to adaptation. For example, many freshwater stickleback populations have independently lost the bony plating of their marine ancestors due to repeated selection on an ancient standing variant at the Eda gene (Colosimo 2005), and a substantial fraction of the increased apical dominance in maize relative to teosinte can be traced to a standing variant that predates domestication by at least 10,000 years (Studer et al. 2011). Additional examples of adaptation from standing variation have been documented in Drosophila (Magwire et al. 2011), Peromyscus (Domingues et al. 2012), and humans (Peter et al. 2012), among others. Adaptations involving simultaneous selection on multiple alleles of independent origin at the same locus have also been documented across a wide array of species (Menozzi et al. 2004; Nair et al. 2006; Karasov et al. 2010; Salgueiro et al. 2010; Schmidt et al. 2010; Jones et al. 2013). Nonetheless, the general importance of soft sweeps for the adaptive process remains somewhat contentious (see, e.g., Jensen 2014; Schrider et al. 2015).

While models of the hitchhiking effect under soft sweeps involving multiple independent mutations have received a fair amount of analytical attention (Pennings and Hermisson 2006a,b; Hermisson and Pfaffelhuber 2008; Pokalyuk 2012; Wilson et al. 2014), the model of a uniquely derived mutation that segregates as a standing variant before sweeping in response to an environmental change is less well characterized. Present understanding of the hitchhiking effect in a single population under this model comes primarily from two sources. The first one is a pair of simulation studies (Innan and Kim 2004; Przeworski et al. 2005), which focused largely on simple summaries of diversity and the allele frequency spectrum, and the second one is the general verbal intuition that, similar to the multiple-mutation case, the beneficial allele should be found on "multiple haplotypes." In contrast to the multiple-mutation case, these additional haplotypes are created as a result of recombination events during the period before the sweep when the allele was present in the standing variation, rather than due to recurrent mutations on different ancestral haplotypes (Barrett and Schluter 2008; Messer and Petrov 2013). …

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