Integration and evolution of the cichlid pharyngeal skeleton: seeking the causes and consequences of trait covariation

The evolutionary success of animals has been facilitated by the expansion and diversification of serially homologous elements. The vertebrate pharyngeal skeleton exemplifies this process. Evolved from a uniform series of cartilaginous rods, different elements have evolved distinct shapes and functions over time. This process implies that the evolution of the pharyngeal skeleton involved the decoupling of its constituent elements; however, to ensure functionality, a level of connectivity must be maintained. Thus, the evolution of the pharyngeal skeleton is likely influenced by a balance of diversifying and unifying forces. We probe these ideas using East African cichlid fishes. Shape analyses in a sample of 75 ecologically diverse species and a large F5 hybrid population showed a conspicuous lack of independence. Nearly all elements were correlated, a pattern reflected in the genotype-phenotype map and associated with co-expression of the candidate gene, smad7. Results are discussed in the context of the palimpsest model, whereby trait covariation is the result of numerous, hierarchical forces of covariation. Given its broad regulatory roles, we suggest that smad7 may be involved in several layers of the palimpsest, providing molecular insights into how serially homologous elements may diversify while also maintaining functionality.