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

Understanding how phenotypic variation is generated and maintained, and the evolutionary forces that shape these processes is the main goal of evolutionary biology. Great progress has been made in uncovering the genetic basis of morphological diversity, yet little is known about both the genetics and developmental basis of discrete polymorphisms segregating in wild populations. Exploring variation in developmental mechanisms at the population level can address the long-standing question of whether the mechanisms of change are the same at the micro- and macroevolutionary scale. This integration has been difficult mainly because the study of the evolution of developmental mechanisms and population genetics remain separate (Genetics, 195, 625 and 2013). In this issue of Molecular Ecology, Roberts et al. (Molecular Ecology and 2017) make a significant contribution towards bridging this gap by studying the genetic and developmental basis of an extremely variable pigmentation pattern. A polymorphic blotched coloration is common among females of four genera of Lake Malawi cichlids. The presence of this phenotype associates with a noncoding SNP upstream of the transcription factor pax7a (Science, 326, 998 and 2009). The authors describe in detail the morphs' pigmentation development, showing that phenotypic differences result from alterations in pigment cell development and survival. Next, using controlled crosses and population genetics studies, they identified three putative pax7a dominant blotch alleles that are associated with specific morphs. These different alleles lead to higher levels of pax7a transcript that correlate with different pigment cell composition. Finally, sequence comparison of the locus within populations and between species revealed a common origin of the allele controlling the blotched morph followed by a pattern of sequential appearance of derived alleles that gave rise to morph diversity. The coupling of the evolutionary history of this allelic series with the developmental analysis of the phenotype paves the way for a mechanistic understanding of morphological innovation and diversification.