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Cichlid fishes exhibit rapid, extensive, and replicative adaptive radiation in feeding morphology. Plasticity of the cichlid jaw has also been well documented, and this combination of iterative evolution and developmental plasticity has led to the proposition that the cichlid feeding apparatus represents a morphological “flexible stem.” Under this scenario, the fixation of environmentally sensitive genetic variation drives evolutionary divergence along a phenotypic axis established by the initial plastic response. Thus, if plasticity is predictable then so too should be the evolutionary response. We set out to explore these ideas at the molecular level by identifying genes that underlie both the evolution and plasticity of the cichlid jaw. As a first step, we fine-mapped an environment-specific quantitative trait loci for lower jaw shape in cichlids, and identified a nonsynonymous mutation in the ciliary rootlet coiled-coil 2 (crocc2), which encodes a major structural component of the primary cilium. Given that primary cilia play key roles in skeletal mechanosensing, we reasoned that this gene may confer its effects by regulating the sensitivity of bone to respond to mechanical input. Using both cichlids and zebrafish, we confirmed this prediction through a series of experiments targeting multiple levels of biological organization. Taken together, our results implicate crocc2 as a novel mediator of bone formation, plasticity, and evolution.

SynopsisWhen novel or extreme morphologies arise, they are oft met with the burden of functional trade-offs in other aspects of anatomy, which may limit phenotypic diversification and make particular adaptive peaks inaccessible. Bramids (Perciformes: Bramidae) comprise a small family of 20 extant species of fishes, which are distributed throughout pelagic waters worldwide. Within the Bramidae, the fanfishes (Pteraclis and Pterycombus) differ morphologically from the generally stout, laterally compressed species that typify the family. Instead, Pteraclis and Pterycombus exhibit extreme anterior positioning of the dorsal fin onto the craniofacial skeleton. Consequently, they possess fin and skull anatomies that are radically different from other bramid species. Here, we investigate the anatomy, development, and evolution of the Bramidae to test the hypothesis that morphological innovations come at functional (proximate) and evolutionary (ultimate) costs. Addressing proximate effects, we find that the development of an exaggerated dorsal fin is associated with neurocrania modified to accommodate an anterior expansion of the dorsal fin. This occurs via reduced development of the supraoccipital crest (SOC), providing a broad surface area on the skull for insertion of the dorsal fin musculature. While these anatomical shifts are presumably associated with enhanced maneuverability in fanfishes, they are also predicted to result in compromised suction feeding, possibly limiting the mechanisms of feeding in this group. Phylogenetic analyses suggest craniofacial and fin morphologies of fanfishes evolved rapidly and are evolutionarily correlated across bramids. Furthermore, fanfishes exhibit a similar rate of lineage diversification as the rest of the Bramidae, lending little support for the prediction that exaggerated medial fins are associated with phylogenetic constraint. Our phylogeny places fanfishes at the base of the Bramidae and suggests that nonfanfish bramids have reduced medial fins and re-evolved SOCs. These observations suggest that the evolution of novel fin morphologies in basal species has led to the phylogenetic coupling of head and fin shape, possibly predisposing the entire family to a limited range of feeding. Thus, the evolution of extreme morphologies may have carryover effects, even after the morphology is lost, limiting ecological diversification of lineages.

Since the time of Darwin, biologists have sought to understand the origins and maintenance of life’s diversity of form. However, the nature of the exact DNA mutations and molecular mechanisms that result in morphological differences between species remains unclear. Here, we characterize a nonsynonymous mutation in a transcriptional coactivator, limb bud and heart homolog (lbh), which is associated with adaptive variation in the lower jaw of cichlid fishes. Using both zebrafish and Xenopus, we demonstrate that lbh mediates migration of cranial neural crest cells, the cellular source of the craniofacial skeleton. A single amino acid change that is alternatively fixed in cichlids with differing facial morphologies results in discrete shifts in migration patterns of this multipotent cell type that are consistent with both embryological and adult craniofacial phenotypes. Among animals, this polymorphism in lbh represents a rare example of a coding change that is associated with continuous morphological variation. This work offers novel insights into the development and evolution of the craniofacial skeleton, underscores the evolutionary potential of neural crest cells, and extends our understanding of the genetic nature of mutations that underlie divergence in complex phenotypes.