Identifying the loci of speciation: the challenge beyond genome scans

In their review on the genomic landscape of speciation, Ravinet et al. (in press) highlight difficulties when attempting to draw inferences about speciation based on heterogeneous patterns of genome differentiation. These problems arise because various factors that are either causally unlinked or only spuriously associated with speciation can induce genomic heterogeneity and thus complicate the interpretation of genome scans. In the light of these difficulties, it is important to not restrict speciation research to genome scans but to view them as an additional tool that can be applied complementary to more traditional methodologies, for example field observations, experiments and crosses. In our opinion, interpreting the genomic landscape of speciation faces additional difficulties that were not addressed by Ravinet et al. (in press), mainly due to limitations in our understanding of whether genomic patterns caused by processes involved in speciation can be differentiated from those associated with adaptation within lineages. While the latter likely play an important role in many cases of speciation (Gavrilets, 2003; Schluter & Conte, 2009; Nosil, 2012), in other cases, they might not (Presgraves, 2010; Maheshwari & Barbash, 2011). We thus argue that reduced gene flow attributable to divergent adaptation, and potentially noticeable in genome scans, might contain limited information about speciation, as it is difficult to predict the future role of adaptive alleles in facilitating the evolution of reproductive isolation. This parallels the notion that current isolating barriers may be uninformative about their past importance during speciation (Coyne & Orr, 2004). The unpredictable future holds for any isolation barrier, but specifically so for those solely relying on environmental factors (e.g. Seehausen et al., 2008). We thus focus here on whether genome scans can identify barriers to gene flow that are potentially able to keep species separated in the long run and that may be less susceptible to or independent of environmental changes, for example intrinsic hybrid incompatibilities or mating preferences (Seehausen et al., 2014). While environmentally independent processes that potentially advance speciation (e.g. genomic conflict or assortative mating) can differ from processes involved in divergent adaptation between lineages, their genomic signatures may be difficult to distinguish in an empirical context. However, it is critical to understand the relative importance and interaction of different classes of barriers for the evolution of reproductive isolation and speciation.

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