When structure leads to sex: Untangling signals in population genetic data sets

A robust signal of population structure often provides the first glimpse into the evolutionary history of a species and its populations. In this issue of Molecular Ecology, new work from Louis Bernatchez’s group (Benestan et al., 2017) starts with an investigation of apparent structure in two marine species and concludes with an identification of sex-linked genes, and in the process provides a model for robust analysis. Structure is the genetic signal left by natural selection as well as by neutral processes like migration and gene flow. Neutral areas of the genome can reveal the geographical relationships and related gene flow between populations over time and space, while selection can resist the natural genomic turnover created by recombination and generate adaptive structure between populations that can be detected. However, artefacts in a data set can easily hide the true signal of structure; muta-tion, whether it is a true appearance of a recent, minor allele, or more commonly, an error in SNP calling or molecular library construction, can easily conceal patterns of population structure (e.g., geographical structure in mackerel, Rodriguez-Ezpeleta et al. (2016)). A demographic structure that results from the most “forceful” evolutionary processes can overwhelm another signal generated by other, unrelated phe-notypes. For example, the structure among diverged freshwater and marine threespine stickleback populations results from such strong selection and linkage disequilibrium across the genome that it impairs the ability to disentangle the genetic basis of particular evolved morphological traits (e.g., opercle development, Alligood (2017)). Finally, there might be conflicting inferences for what underlies structure patterns. Structure may be created by differential patterns of meiotic recombination, and genetic maps are a reliable means for identifying genomic regions that resist recombination. But, without additional information (Anderson et al., 2012), it can be difficult to distinguish the recombination-suppressing effect of a segregating genomic inversion (Small et al., 2016) from that of sex-linked selec-tion.