Morphometric and Genetic Description of Trophic Adaptations in Cichlid Fishes

SIMPLE SUMMARY: Skull and jaw shape are critical to how an animal eats. The goal of this work was to examine how facial variation evolves and the genetic basis of these changes. We used two species of Lake Malawi cichlids with different facial shapes, one which has evolved to eat prey by suction feeding, a second that bites algae from rocks, as well as hybrid individuals generated by artificial mating of the two species. We found a series of changes in craniofacial structure including the shape of the lower jaw and throat region that impact how animals perform at suction feeding and biting. We then identified genetic regions that regulate these facial shapes. These genetic regions suggested that evolution of the senses, among other traits, may play an important role in facial evolution. Also, evolution of different parts of the face are controlled by distinct genetic regions. Despite this, cichlids that eat similar ways have similar facial shapes, suggesting that the function of jaw movement places certain limits on facial evolution in cichlid fishes. Overall, this work provides insights into how the face evolves, how these changes relate to feeding, and the genes and molecules that regulate craniofacial variation. ABSTRACT: Since Darwin, biologists have sought to understand the evolution and origins of phenotypic adaptations. The skull is particularly diverse due to intense natural selection on feeding biomechanics. We investigated the genetic and molecular origins of trophic adaptation using Lake Malawi cichlids, which have undergone an exemplary evolutionary radiation. We analyzed morphological differences in the lateral and ventral head shape among an insectivore that eats by suction feeding, an obligate biting herbivore, and their F(2) hybrids. We identified variation in a series of morphological traits—including mandible width, mandible length, and buccal length—that directly affect feeding kinematics and function. Using quantitative trait loci (QTL) mapping, we found that many genes of small effects influence these craniofacial adaptations. Intervals for some traits were enriched in genes related to potassium transport and sensory systems, the latter suggesting co-evolution of feeding structures and sensory adaptations for foraging. Despite these indications of co-evolution of structures, morphological traits did not show covariation. Furthermore, phenotypes largely mapped to distinct genetic intervals, suggesting that a common genetic basis does not generate coordinated changes in shape. Together, these suggest that craniofacial traits are mostly inherited as separate modules, which confers a high potential for the evolution of morphological diversity. Though these traits are not restricted by genetic pleiotropy, functional demands of feeding and sensory structures likely introduce constraints on variation. In all, we provide insights into the quantitative genetic basis of trophic adaptation, identify mechanisms that influence the direction of morphological evolution, and provide molecular inroads to craniofacial variation.