Speciation, species persistence and the goals of studying genomic barriers to gene flow

The processes generating regions of elevated genomic divergence during speciation have been extensively debated and discussed as our ability to collect data to address this subject has undergone wholesale revolution during the past decade (Noor & Bennett, 2009; Nosil & Feder, 2012; Seehausen et al., 2014). Ravinet et al. (2017, this issue) thoroughly review and discuss the progress we have made in identifying and understanding genomic barriers to gene flow, including the cases in which making these interpretations is challenging, and review the prospects of this field moving forward. As a complement to the message in Ravinet et al. (2017), we highlight an important need to clearly define the goals of studying patterns and processes of genomic divergence, and in particular, to understand when studying genomic divergence has direct links to the mechanisms of speciation, and when it may not. One challenge that Ravinet et al. (2017) identify is that although it is now relatively easy to identify candidate barrier loci using genome scan methods, it is far more difficult to determine which of these candidate loci, if any, contribute to reproductive isolation between a pair of species. Making this next conceptual advance is crucial if genomic data are to help us truly understand the genetic basis of reproductive isolation between species. Progress towards understanding speciation mechanisms will depend on applying appropriate analyses for the questions and goals at hand, and clearly placing these results into the applicable evolutionary context (Fig. 1). Although analyses of divergent regions of the genome and the search for barrier loci can be useful in understanding evolutionary processes, the exact relevance and significance of such analyses to speciation mechanisms will depend on the evolutionary scenario. It is now clear that in many evolutionary scenarios there is an inability to uniquely identify process from patterns of genomic divergence, and it is important to consider these cases in refining appropriate questions to pursue in a given study system or with a given sampling design. One simple framework for refining appropriate goals given the study taxa of interest, and generally for understanding how to realistically approach the study of barrier loci in the context of studying the genetic basis of speciation, is to consider both the magnitude of evolutionary divergence between focal taxa, and the level of contemporary gene flow between taxa. We can place upon this framework many of the lessons we have learned about the successes and limitations of inferring process from patterns of genomic divergence (Fig. 1). In Fig. 1a,b, we find situations with low divergence between populations, but which vary in the presence (Fig. 1b) or absence (Fig. 1a) of contemporary gene flow. Young allopatric populations fall into the first category (Fig. 1a), whereas young sympatric or parapatric populations with gene flow fall in the second category (Fig. 1b). Because of low background genomic differentiation in both scenarios, in contrast with situations with more divergent taxa (Fig. 1c,d), there are fewer confounding factors at play contributing to population differences, making it potentially easier to identify the genomic differences underlying phenotypic population differentiation (e.g. Marques et al., 2016). However, without gene flow (Fig. 1a) there is no opportunity for differential introgression. These scenarios are then equivalent to detecting local adaptation from genome scans (e.g. Jensen et al., 2016), where detecting regions of the genome under selection may not have relevance to reproductive isolation of divergent populations. For populations that have recently stopped exchanging genes, the signature of differential introgression may persist for some time, but as genomic divergence proceeds, it becomes increasingly difficult to distinguish differential introgression from other processes that may leave similar genomic patterns (extensively reviewed in Ravinet et al., 2017). Furthermore, a major challenge in studies of young taxa is distinguishing gene flow from shared ancestral polymorphism (Noor & Bennett, 2009; Nachman & Payseur, 2012; Sousa & Hey, 2013; Martin et al., 2015). One additional challenge in linking the case with ongoing gene flow in young taxa (Fig. 1b) to speciation is that it is not clear whether the forces leading to differential introgression will ultimately lead to full reproductive isolation between the populations, or whether these populations will continue to exchange genes and/or ultimately collapse. The latter may be particularly likely for cases in which population differentiation is dependent on stable directional selection, and thus where environmental changes may lead to Correspondence: Catherine E. Wagner, Department of Botany, University of Wyoming, Laramie, WY 82071, USA. Tel. : +1 307 766 4158; fax: +1 307 766 2851; e-mail: catherine.wagner@uwyo.edu Commentary on Ravinet et al.: Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.