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Genetic basis of continuous variation in the levels and modular inheritance of pigmentation in cichlid fishes

Albertson, R. Craig, Powder, Kara E., Hu, Yinan, Coyle, Kaitlin P., Roberts, Reade B., Parsons, Kevin J.
Molecular ecology 2014 v.23 no.21 pp. 5135-5150
Cichlidae, biologists, color, epistasis, experimental design, fins, fish, genes, metagenomics, pigmentation, quantitative trait loci, sexual selection
Variation in pigmentation type and levels is a hallmark of myriad evolutionary radiations, and biologists have long been fascinated by the factors that promote and maintain variation in coloration across populations. Here, we provide insights into the genetic basis of complex and continuous patterns of colour variation in cichlid fishes, which offer a vast diversity of pigmentation patterns that have evolved in response to both natural and sexual selection. Specifically, we crossed two divergent cichlid species to generate an F₂ mapping population that exhibited extensive variation in pigmentation levels and patterns. Our experimental design is robust in that it combines traditional quantitative trait locus (QTL) analysis with population genomics, which has allowed us to move efficiently from QTL interval to candidate gene. In total, we detected 41 QTL and 13 epistatic interactions that underlie melanocyte‐ and xanthophore‐based coloration across the fins and flanks of these fishes. We also identified 2 QTL and 1 interaction for variation in the magnitude of integration among these colour traits. This finding in particular is notable as there are marked differences both within and between species with respect to the complexity of pigmentation patterns. While certain individuals are characterized by more uniform ‘integrated’ colour patterns, others exhibit many more degrees of freedom with respect to the distribution of colour ‘modules’ across the fins and flank. Our data reveal, for the first time, a genetic basis for this difference. Finally, we implicate pax3a as a mediator of continuous variation in the levels of xanthophore‐based colour along the cichlid flank.