Population genomics of parallel evolution in gene expression and gene sequence during ecological adaptation

Abstract

Natural selection often produces parallel phenotypic changes in response to a similar adaptive challenge. However, the extent to which parallel gene expression differences and genomic divergence underlie parallel phenotypic traits and whether they are decoupled or not remains largely unexplored. We performed a population genomic study of parallel ecological adaptation among replicate ecotype pairs of the rough periwinkle (Littorina saxatilis) at a regional geographical scale (NW Spain). We show that genomic changes underlying parallel phenotypic divergence followed a complex pattern of both repeatable differences and of differences unique to specific ecotype pairs, in which parallel changes in expression or sequence are restricted to a limited set of genes. Yet, the majority of divergent genes were divergent either for gene expression or coding sequence, but not for both simultaneously. Overall, our findings suggest that divergent selection significantly contributed to the process of parallel molecular differentiation among ecotype pairs, and that changes in expression and gene sequence underlying phenotypic divergence could, at least to a certain extent, be considered decoupled processes.

Thermal Plasticity in Insects’ Response to Climate Change and to Multifactorial Environments

“…These studies search to investigate phenotypic effects when variation in temperature is combined with variation in other environmental variables (Figure 2), including biotic and abiotic factors (Bubliy et al, 2013;Schou et al, 2013;Arambourou and Stoks, 2015;Saeed et al, 2018;Kutz et al, 2019). Some studies extend the analysis of plasticity in multifactorial environments to include: (1) multiple traits and/or to multiple genotypes (e.g,., Saastamoinen et al, 2013;Verspagen et al, 2020), (2) threeway environmental interactions (e.g., temperature × humidity × food; Bomble and Nath, 2019), and (3) quantifying underlying changes in gene expression (e.g., candidate genes, Rivas et al, 2018, and whole transcriptome, Koch and Guillaume, 2020). The results to date paint a complex picture, with distinct types of additive (e.g., Koch and Guillaume, 2020) and nonadditive (e.g., Yoshii et al, 2009;Arambourou and Stoks, 2015;Piggott et al, 2015) effects of multifactorial environments, and differences between traits and between genotypes.…”

The effects of diadromy and its loss on genomic divergence: The case of amphidromous Galaxias maculatus populations

“…In Patagonia too, lakes that were ice-covered during the last glacial maximum (LGM) were colonized soon after deglaciation (Vera-Escalona, Habit, & Ruzzante, 2015Zemlak et al, 2011). An earlier colonization of lakes for the northernmost populations can explain their higher genetic differentiation from their TA B L E 3 Blast annotation results from the top 25 outliers that have a potential function described in Table S3 diadromous counterparts, while in the southern populations, recent colonization can explain the weak differentiation as the standing genetic variation from the ancestral population (diadromous ecotype) will likely be the source of variation (Rivas et al, 2018).…”

Phenotypic and genotypic parallel evolution in parapatric ecotypes ofSenecio

“…In such systems, divergent loci are difficult to detect as they contain low FST, which further makes detecting genetic parallelism highly unlikely in these systems. Finally, traditional approaches that sample SNPs across the genome will fail to detect variation in gene expression levels, which may also be involved in adaptation during parallel evolution (e.g., Rivas et al, 2018;Verta & Jones, 2019).…”