Genome-Wide Divergence among Populations in Distinct Ocean Habitats of the Mesopelagic Copepod Pleuromamma xiphias

Abstract

Although the ecological and evolutionary responses of marine zooplankton to climate change have the potential to strongly influence commercially important species, we know very little about the processes that drive adaptive genetic divergence and evolution in these species. Selection is likely a dominant driver of evolution in marine zooplankton, and population genomics provides a powerful approach to investigate selection and adaptive evolution in non- model species. Using single nucleotide polymorphism (SNP) loci assayed in 322 animals collected across a latitudinal basin-scale transect in the Atlantic Ocean (49 °N – 45 °S, 12 sites), we document divergence among populations of the planktonic copepod Pleuromamma xiphias in equatorial and subtropical/temperate waters. FST outlier tests identified 57 loci putatively under directional selection, and when these loci were removed, differentiation between equatorial and subtropical/temperate populations persisted, suggesting that these parapatric and partially co- occurring populations are not driven by outlier loci. Genetic differentiation among northern and southern gyre sites also was observed in Bayesian clustering, principal component, and pairwise FST analyses, with a total of three genetically distinct populations detected across the Atlantic basin. Prior work on this species using mitochondrial (mt) polymorphisms had identified 2 primary mt clades in the Atlantic Ocean (clades 2, 3). Combining the SNP data and mitochondrial markers revealed discordant patterns: mt clade 2 animals only occur within SNP cluster 1 (equatorial), whereas mt clade 3 animals occur in both SNP clusters (equatorial & subtropical/temperate). Widespread sharing of identical haplotypes among SNP clusters may suggest recent or ongoing mitochondrial introgression among these incipient species, with both phylogenetic and biogeographic patterns indicative of introgression from the subtropical/temperate species into the equatorial endemic. Such mitochondrial-nuclear discordance has not been previously reported in marine zooplankton. Our results yield insight into the processes of population divergence and mitochondrial introgression among plankton populations in distinct ocean habitats, and suggest that geographically proximate populations can diverge even in very high dispersal systems.