Exploring evolutionary mechanisms of genomic divergence in marine intertidal limpets

Abstract

Decades of research in population genetics have revealed that genetic divergence between populations and species is not uniformly distributed throughout the genome but rather exhibits a high degree of heterogeneity. Two main conceptual models—allopatric divergence and divergence with gene flow—have been proposed to explain this variability under natural selection. Here, we investigate patterns of genomic divergence in three marine limpet species, Scurria scurra, Scurria araucana, and Scurria ceciliana, across two major biogeographic breaks (30–34°S and 41–43°S). Genomic divergence varied among species, even between the two sympatric species S. scurra and S. araucana, which exhibited heterogeneous divergence patterns across the 30–34°S range. In S. ceciliana, the southernmost species (41–43°S), divergence was shaped by a combination of allopatric divergence and divergence with gene flow. This was unexpected given that its evolutionary history suggests past isolation in glacial refugia, which would have limited gene flow. However, the observed genomic divergence indicates that genetic exchange occurred between populations, challenging previous assumptions about its evolutionary dynamics. Divergence patterns appear species-specific, with few shared genomic regions, though more similarities were found among the sister species S. scurra and S. araucana. In highly divergent regions, genes associated with lipid metabolism were identified in S. scurra and S. araucana, whereas genes related to oxidative stress response and mitochondrial functions were found in S. ceciliana. These findings suggest that genomic divergence is not entirely stochastic but may be shaped by different selective pressures in each species, potentially reflecting adaptation to distinct ecological conditions.