Genomic signatures of positive selection and relaxed selective constraints associated with convergent dietary specialisation

Abstract

Island radiations provide ideal frameworks for studying the molecular basis of convergent evolution. The rapid diversification of Dysdera spiders in Canary Islands provides a striking example, with repeated dietary shifts towards specialisation on woodlice, accompanied by morphological, metabolic, and behavioural modifications that facilitate the exploitation of this heavy-metal-rich prey. Here, we investigate two independent events of dietary specialisation on different islands. By analysing six high-quality genome-assemblies, including three newly generated in this study, we investigate the genomic signals of positive selection and relaxed selection in protein-coding genes, upstream regulatory regions, and gene family turnover rates. We detected signatures of positive selection associated with the two specialists, accompanied by a twofold increase in gene loss rates relative to generalist ancestors. Notably, positive selection targeted a smaller, functionally coherent set of genes, potentially involved in detoxification likely through heavy metal excretion. In contrast, relaxation of selection affected a broader set of genes associated with functions that may have become dispensable under the new dietary regime. Furthermore, we found contractions in gene families associated with vesicular transport, potentially reflecting a reduced reliance on vesicle-mediated metal accumulation. Overall, our findings suggest that similar ecological pressures can drive parallel, yet non-identical, adaptive and non-adaptive responses, pointing to partially predictable evolutionary trajectories in an island radiation.