Complex signatures of genomic variation of two non-model marine species in a homogeneous environment

Erica S. Nielsen, Romina Henriques, Robert J. Toonen, Ingrid S. S. Knapp, Baocheng Guo, Sophie von der Heyden

Genomic tools are increasingly being used on non-model organisms to provide insights into population structure and variability, including signals of selection. However, most studies are carried out in regions with distinct environmental gradients or across large geographical areas, in which local adaptation is expected to occur. Therefore, the focus of this study is to characterize genomic variation and selective signals over short geographic areas within a largely homogeneous region. To assess adaptive signals between microhabitats within the rocky shore, we compared genomic variation between the Cape urchin (Parechinus angulosus), which is a low to mid-shore species, and the Granular limpet (Scutellastra granularis), a high shore specialist. Using pooled restriction site associated DNA (RAD) sequencing, we described patterns of genomic variation and identified outlier loci in both species. We found relatively low numbers of outlier SNPs within each species, and identified outlier genes associated with different selective pressures than those previously identified in studies conducted over larger environmental gradients. The number of population-specific outlier loci differed between species, likely owing to differential selective pressures within the intertidal environment. Interestingly, the outlier loci were highly differentiated within the two northernmost populations for both species, suggesting that unique evolutionary forces are acting on marine invertebrates within this region. Our study provides a background for comparative genomic studies focused on non-model species, as well as a baseline for the adaptive potential of marine invertebrates along the South African west coast. We also discuss the caveats associated with Pool-seq and potential biases of sequencing coverage on downstream genomic metrics. The findings provide evidence of species-specific selective pressures within a homogeneous environment, and suggest that selective forces acting on small scales are just as crucial to acknowledge as those acting on larger scales. As a whole, our findings imply that future population genomic studies should expand from focusing on model organisms and/or studying heterogeneous regions to better understand the evolutionary processes shaping current and future biodiversity patterns, particularly when used in a comparative phylogeographic context.