Microsatellite length variation in candidate genes correlates with habitat in the gilthead sea bream Sparus aurata

Abstract

The genetic basis and evolutionary implications of local adaptation in high gene flow marine organisms are still poorly understood. In several Mediterranean fish species, alternative migration patterns exist between individuals entering coastal lagoons that offer favourable conditions for growth and those staying in the sea where environmental conditions are less subject to rapid and stressful change. Whether these coexisting strategies are phenotypically plastic or include a role for local adaptation through differential survival needs to be determined. Here, we explore the genetic basis of alternate habitat use in western Mediterranean populations of the gilthead sea bream (Sparus aurata). Samples from lagoonal and open-sea habitats were typed for three candidate gene microsatellite loci, seven anonymous microsatellites and 44 amplified fragment length polymorphism markers to test for genotype-environment associations. While anonymous markers globally indicated high levels of gene flow across geographic locations and habitats, non-neutral differentiation patterns correlated with habitat type were found at two candidate microsatellite loci located in the promoter region of the growth hormone and prolactin genes. Further analysis of these two genes revealed that a mechanism based on habitat choice alone could not explain the distribution of genotype frequencies at a regional scale, thus implying a role for differential survival between habitats. We also found an association between allele size and habitat type, which, in the light of previous studies, suggests that polymorphisms in the proximal promoter region could influence gene expression by modulating transcription factor binding, thus providing a potential explanatory link between genotype and growth phenotype in nature.

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

“…A particular focus was made on microsatellite markers located close to 2 candidate genes, GH and Prl, that are functionally related to growth and osmoregulatory capacities in fish (Streelman & Kocher 2002, Almuly et al 2008, Quéré et al 2010) and have been previously showed to be involved in habitat-based genetic differentiation in sea bream (Chaoui et al 2012). This latter study suggested that GH and Prl genotypes with varying selective advantage among lagoons impact mortality in juvenile sea breams that spent their first year of life in ecologically contrasted lagoons (i.e.…”

“…We hypothesised that under habitat-based selection, genetic differentiation would be higher in older juveniles caught in autumn than in younger ones caught soon after entering coastal lagoons. Therefore, we randomly selected 12 autumn individuals from MA and 12 autumn individuals from TH to evaluate genetic differentiation between the 2 most extreme habitats (Chaoui et al 2012). New primers were designed to amplify the full gene sequences of GH and Prl genes using long-range PCR (LR-PCR) (see LR-PCR pri mers in Table S1 in Supplement 1).…”

“…The gilthead sea bream Sparus aurata is a euryhaline coastal marine fish in which spatially varying selection between marine and lagoon habitats has been reported in the northwestern Mediterranean (Chaoui et al 2012). After hatching at sea from De cember to February, a large proportion of the juveniles colonise coastal lagoons in March and April for foraging (Mercier et al 2011, Isnard et al 2015 before returning to the open sea in October and November to overwinter, when lagoon water temperatures drop (Audouin 1962, Lasserre 1974, Mercier et al 2012).…”

“…Using candidate gene markers located in the proximal promoter of the growth hormone (GH) and prolactin (Prl) genes, Chaoui et al (2012) found non-neutral allele frequency shifts between young juveniles caught in marine and lagoon habitats and interpreted these patterns as a footprint of post-settlement selection. Because cis-regulatory polymorphisms have been described for both GH (Astola et al 2003) and Prl (Almuly et al 2008) genes in sea bream, Chaoui et al (2012) hypothesised that functional variants affecting gene expression might be selected differently among habitats due to their phenotypic effects on growth and/or osmoregulation (e.g. Streelman & Kocher 2002, Blel et al 2010, Shimada et al 2011.…”

Fitness difference between cryptic salinity-related phenotypes of sea bass (<em>Dicentrarchus labrax</em>)

“…Indeed, lagoon individuals were found to be genetically differentiated from individuals inhabiting the buffered open sea environment (Allegrucci et al 1997, Lemaire et al 2000. Further studies of other marine, coastal, euryhaline fish species by, e.g., Blel et al (2010;Mugil cephalus), Chaoui et al (2012;Sparus aurata), González-Wangüemert and Pérez-Ruzafa (2012; Diplodus sargus) and González-Wangüemert and Vergara-Chen (2014; Pomatoschistus minutus) reported similar (but still not fully understood) observations. However, the absence of recognized polymorphic markers in GHR, and the non-significant relationship between gene expression level of IGF-1 and genotypes at the μIGF-1 locus in UFW, SSW and SFW individuals does not allow us to go any further with regard to a possible genotype-phenotype relationship in sea bass.…”