Divergence at the IRX gene cluster underlies extreme trophic polymorphism in a cichlid fish (Herichthys minckleyi)

The origin of the extensive phenotypic divergence characterizing adaptive radiation could often be geographically localized and genetically simple. In a classic case of a trophically polymorphic cichlid fish (Herichthys minckleyi), we investigated alternative genomic processes that could have produced its extreme within-population variation in pharyngeal jaw tooth size. First, we generated a high-quality reference genome for its close relative (H. cyanoguttatus) to dissect the genetic architecture of this dental polymorphism. Then, using whole genome resequencing across the small Cuatro Ciénegas valley where H. minckleyi is endemic, we found substantial micro-geographic subdivision and effectively no genetic structure due to pharyngeal morphotype. We also employed quantitative trait loci mapping and genome wide association to pinpoint a single peak in an Iroquois-related (IRX) gene cluster associated with H. minckleyi's dental divergence. Interspecific introgression in this genomic region appears negligible, suggesting the genomic basis of the polymorphism likely arose within cichlids confined to Cuatro Ciénegas. Because H. minckleyi tooth size disparity is comparable to that found in all Central American cichlids, this offers a striking example of how genomic divergence at a single locus could produce a punctuated burst of eco-morphological divergence that generates phenotypic breadth comparable to a highly diverse cichlid adaptive radiation.