Spotting genome-wide pigmentation variation in a brown trout admixture context

Variation in body pigmentation attracted fish biologists for a while, but high-throughput genomic studies investigating its molecular basis remain limited to few species and associated conservation issues ignored. Using 75,684 SNPs, we explored the genomic basis of pigmentation pattern variation among individuals of the Atlantic and Mediterranean clades of the brown trout (Salmo trutta), a polytypic species in which Atlantic hatchery individuals are commonly used to supplement local wild populations. Using redundancy analyses and genome-wide association studies, a set of 337 independent "colour patterning loci" (CPLs) significantly associated with pigmentation traits such as the number of red and black spots on flanks, or the presence of a black spot on the pre-opercular bone was identified. CPLs map onto 35 out of 40 brown trout linkage groups indicating a polygenic basis to pigmentation patterns. They are mostly located in coding regions (43.4%) of 223 candidate genes, and correspond to GO-terms known to be involved in pigmentation (e.g. calcium and ion-binding, cell adhesion). Annotated candidates include genes with known pigmentation effects (e.g. SOX10, PEML, SLC45A2), but also the Gap-junction {otimes}2 (GJD2) gene already shown differentially expressed in trout skin. Patterns of admixture were found significantly distinct when using either the full SNP data set or the set of CPLs, indicating that pigmentation patterns accessible to practitioners are not a reliable proxy of genome-wide admixture. Consequences for management are discussed.