Genetic and developmental origins of a unique foraging adaptation in a Lake Malawi cichlid genus.

Phenotypic novelties are an important but poorly understood category of morphological diversity. They can provide insights into the origins of phenotypic variation, but we know relatively little about their genetic origins. Cichlid fishes display remarkable diversity in craniofacial anatomy, including several novelties. One aspect of this variation is a conspicuous, exaggerated snout that has evolved in a single Malawi cichlid lineage and is associated with foraging specialization and increased ecological success. We examined the developmental and genetic origins for this phenotype and found that the snout is composed of two hypertrophied tissues: the intermaxillary ligament (IML), which connects the right and left sides of the upper jaw, and the overlying loose connective tissue. The IML is present in all cichlids, but in its exaggerated form it interdigitates with the more superficial connective tissue and anchors to the epithelium, forming a unique ligament-epithelial complex. We examined the Transforming growth factor ß (Tgfß) → Scleraxis (Scx) candidate pathway and confirmed a role for these factors in snout development. We demonstrate further that experimental up-regulation of Tgfß is sufficient to produce an expansion of scx expression and concomitant changes in snout morphology. Genetic and genomic mapping show that core members of canonical Tgfß signaling segregate with quantitative trait loci (QTL) for snout variation. These data also implicate a candidate for ligament development, adam12, which we confirm using the zebrafish model. Collectively, these data provide insights into ligament morphogenesis, as well as how an ecologically relevant novelty can arise at the molecular level.

Evolution of a soft-tissue foraging adaptation in African cichlids: Roles for novelty, convergence, and constraint.

Understanding the origins of biodiversity demands consideration of both extrinsic (e.g., ecological opportunity) and intrinsic (e.g., developmental constraint) factors. Here, we use a combination of phylogenetic and genetic tools to address the origin of novelty in African cichlids. In particular, we focus on an extreme hypertrophied snout that is structurally integrated with the upper jaw. We show that this bizarre trait has evolved independently in at least two distinct and ecologically successful cichlid clades. We find that snout dimensions are decoupled both phenotypically and genetically, which has enabled it to evolve independently in multiple directions. Further, patterns of variation among species and within a genetic mapping pedigree suggest that relative to snout length, depth is under greater genetic and/or developmental constraint. Models of evolution suggest that snout shape is under selection for feeding behavior, with snout depth being important for algae scraping and snout length for sand sifting. Indeed, the deep snout of some algivores is achieved via an expansion of the intermaxillary ligament, which is important for jaw stability and may increase feeding performance. Overall, our data imply that the evolution of exaggerated snout depth required overcoming a genetic/developmental constraint, which led to expanded ecological opportunity via foraging adaptation.