Nested Levels of Adaptive Divergence: The Genetic Basis of Craniofacial Divergence and Ecological Sexual Dimorphism

Exemplary systems for adaptive divergence are often characterized by their large degrees of phenotypic variation. This variation represents the outcome of generations of diversifying selection. However, adaptive radiations can also contain a hierarchy of differentiation nested within them where species display only subtle phenotypic differences that still have substantial effects on ecology, function, and ultimately fitness. Sexual dimorphisms are also common in species displaying adaptive divergence and can be the result of differential selection between sexes that produce ecological differences between sexes. Understanding the genetic basis of subtle variation (between certain species or sexes) is therefore important for understanding the process of adaptive divergence. Using cichlids from the dramatic adaptive radiation of Lake Malawi, we focus on understanding the genetic basis of two aspects of relatively subtle phenotypic variation. This included a morphometric comparison of the patterns of craniofacial divergence between two ecologically similar species in relation to the larger adaptive radiation of Malawi, and male–female morphological divergence between their F(2) hybrids. We then genetically map craniofacial traits within the context of sex and locate several regions of the genome that contribute to variation in craniofacial shape that is relevant to sexual dimorphism within species and subtle divergence between closely related species, and possibly to craniofacial divergence in the Malawi radiation as a whole. To enhance our search for candidate genes we take advantage of population genomic data and a genetic map that is anchored to the cichlid genome to determine which genes within our QTL regions are associated with SNPs that are alternatively fixed between species. This study provides a holistic understanding of the genetic underpinnings of adaptive divergence in craniofacial shape.