Candidate gene variation in gilthead sea bream reveals complex spatiotemporal selection patterns between marine and lagoon habitats

Abstract

In marine fishes, the extent to which spatial patterns induced by selection remain stable across generations remains largely unknown. In the gilthead sea bream (Sparus aurata), polymorphisms in the growth hormone (GH) and prolactin (Prl) genes can display high levels of differentiation between marine and lagoon habitats. These genotype-environment associations have been attributed to differential selection following larval settlement, but it remains unclear whether selective mortality during later juvenile stages further shapes genetic differences among habitats. We addressed this question by analysing differentiation patterns at GH and Prl markers together with a set of twenty-one putatively neutral microsatellite loci. We compared genetic variation of spring juveniles that had just settled in three ecologically different lagoons, against older juveniles sampled from the same sites in autumn, at the onset of winter outmigration. In spring, genetic differentiation among lagoons was greater than expected from neutrality, for both candidate gene markers. Surprisingly, this signal disappeared completely in the older juveniles, with no significant differentiation for either locus a few months later in autumn. We searched for signals of haplotype structure within GH and Prl genes using next-generation amplicon deep-sequencing. Both genes contained two groups of haplotypes, but high similarities among groups indicated that signatures of selection, if any, had largely been erased by recombination. Our results are consistent with the view that differential selection operates during early juvenile life in sea bream, and highlight the importance of temporal replication in studies of post-settlement selection in marine fish.