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

Abstract

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.

Differences in spectral selectivity between stages of visually-guided mating approaches in a buprestid beetle

“…This study shows a similar gradation of coloration from green to red in A. angustulus. Furthermore, the ability to select for more extreme color morph variants in the A. planipennis colony affirms a degree of heritable polymorphism that in other systems has been associated with high speciation rates (Hugall and Stuart-Fox, 2012;McLean and Stuart-Fox, 2014) and particular speciation scenarios (Richards-Zawacki et al, 2012;Albertson et al, 2014). Finally, the spectral response preference of A. angustulus males was shown to include red targets (∼694 nm), which have a chromatic content well outside the normal range of peak wavelength emission of conspecifics (542-650 nm).…”

Molecular ecology studies of species radiations: current research gaps, opportunities and challenges

“…They address some of the most hotly debated evolutionary radiations in animals and plants, including cichlids (e.g. Schliewen et al 2001;Colombo et al 2013;Keller et al 2013;Manousaki et al 2013;Albertson et al 2014;Ford et al 2015), sticklebacks (Gow et al 2006;Berner et al 2010;Deagle et al 2013;Feulner et al 2013), Anolis lizards (Glor et al 2005;Ng & Glor 2011;Muñoz et al 2013), Heliconius butterflies (Nadeau et al 2013), Darwin 0 s finches (Petren et al 2005), plants of the Hawaiian silversword alliance (Lawton-Rauh et al 2007), oak trees (Cavender-Bares et al 2015) and bromeliads (Palma-Silva et al 2011). Due to the targeted nature of our search and the specific search terms used, our literature review is certainly not exhaustive.…”

Cichlid fishes as a model to understand normal and clinical craniofacial variation

“…Recently, investigators have begun to address these methodological limitations by combining both population genomics and QTL mapping into a single experiment, thereby leveraging the advantages while mitigating the disadvantages of each approach (Albertson, et al 2014; Barrett and Hoekstra 2011; Parsons and Albertson 2013). For example, we previously used this approach to implicate pax3a in cichlid coloration (Albertson, et al 2014).…”

“…For example, we previously used this approach to implicate pax3a in cichlid coloration (Albertson, et al 2014). We first used QTL mapping to associate a 28cM region with levels of red/yellow pigmentation.…”