Genomic signatures of adaptive divergence in lacustrine copepods

Abstract

Abstract Ecological speciation, the formation of reproductive barriers as a consequence of adaptive divergence, can be a widespread diversification process in lacustrine landscapes, where the interplay of multiple biotic and abiotic factors generates a lavish array of divergent environments. Copepods are a major component of aquatic ecosystems and have remarkable evolvability, but the effects of adaptation to divergent environments at the genomic level and their implications for diversification in lakes are unknown. We studied four populations of calanoid copepods (Leptodiaptomus group sicilis) inhabiting three permanent deep lakes and one ephemeral playa lake; despite their geographical closeness, they display adaptation to local conditions of salinity, potential immigrant inviability and divergent life‐history traits. Using a reduced representation of the genome, we describe the genomic signatures of ecological divergence (salinity and habitat permanence), genome‐wide differentiation and population structure. We found that the four populations are genetically well‐differentiated and constitute four monophyletic lineages with individual evolutionary trajectories. Candidate adaptive loci showed clear signatures of diversifying selection, and the relationship between neutral and adaptive genetic variation suggested a pattern of isolation‐by‐adaptation. Interestingly, most neutral and adaptive differentiation was associated with habitat permanence, not with salinity divergence. We concluded that local adaptation to salinity promoted reduced gene flow via immigrant inviability, reinforcing the adaptation to other factors associated with the permanence/ephemerality of lakes and fostering the accumulation of genomic differentiation due to neutral evolution, ultimately leading to speciation. Our results show how divergent ecological conditions such as salinity and permanence/ephemerality of water regime produce significant genomic differentiation in copepod populations, paving the way for their diversification and speciation.