An allelic series at pax7a is associated with colour polymorphism diversity in Lake Malawi cichlid fish

Abstract

Despite longstanding interest in the evolution and maintenance of discrete phenotypic polymorphisms, the molecular genetic basis of such polymorphism in the wild is largely unknown. Female sex-associated blotched color polymorphisms found in cichlids of Lake Malawi, East Africa represent a highly successful polymorphic phenotype, found and maintained in four genera across the geographic expanse of the lake. Previously, we identified an association with an allelic variant of the paired-box transcription factor gene pax7a and blotched color morphs in Lake Malawi cichlid fishes. Though a diverse range of blotched phenotypes are present in Lake Malawi cichlid species, they all appeared to result from an allele of pax7a that produces increased levels of transcript. Here, we examine the developmental and genetic basis of variation among blotched morphs. First, we confirm that pax7a-associated blotch morphs result primarily from modulation of melanophore development and survival. From lab crosses and natural population studies, we identify at least three alleles of pax7a associated with discrete subtypes of blotched morphs, in addition to the ancestral pax7a allele. Genotypes at pax7a support initial evolution of a novel pax7a allele to produce the blotched class of morphs, followed by subsequent evolution of that pax7a blotched allele to produce additional alleles associated with discrete color morphs. Variant alleles of pax7a produce different levels of pax7a transcript, correlating with pigmentation phenotype at the cellular level. This naturally selected allelic series should serve as a case study for understanding the molecular genetic control of pax7a expression and the evolution of sex-associated alleles.

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

“…A chimeric, polyallelic origin can explain the cis-regulatory evolution of optix (Wallbank et al 2015) (see also chapter by CD Jiggins in this volume), a transcription factor locus that, like WntA, shows extensive parallelism and multiallelism in the Heliconius genus (Reed et al 2011;Papa et al 2013;Kronforst and Papa 2015;Zhang et al 2016). We expect that further examples of phenotypic radiations will uncover a multiallelic basis, as recently proposed in cichlid fishes (Roberts et al 2016). The fact that we observe genetic heterogeneity shows that multiple variants can swarm in a gene pool and may thus provide the bricks of change to build novel cis-regulatory activities.…”

Evolutionary diversity as a catalyst for biological discovery

“…To date, the majority of comparative genetic investigations in cichlids have focused on speciation, trophic morphology, and vision/color patterning (Albertson et al, 2005; Brawand et al, 2014; Gante et al, 2016; Hauser et al, 2017; Hulsey, 2009; Lee et al, 2005; Loh et al, 2008; Owens & Rennison, 2017; Parsons et al, 2014; Roberts et al, 2017; Spady et al, 2005; Streelman et al, 2003). Additional studies have investigated the diverse genetic mechanisms regulating sex determination, and differences in brain organization associated with ecology (Bohne et al, 2013; Sylvester et al, 2013).…”

One gene, multiple alleles: insights into the microevolution of pigmentation polymorphisms

“…Roberts et al . () studied a widespread female‐associated pigmentation polymorphism—the blotched class of morphs (Fig. A).…”

“…In the present study, Roberts et al . () take a novel approach and combine developmental and population genetics methods to study the emergence and diversification of a colour polymorphism found in four genera, comprising 20 species, of Lake Malawi cichlids (Fig. ).…”

“…Schematic representation of the Roberts et al . () study. (A) Species and morphs used in the study depicting the diversity within the blotched morphs.…”