Epigenetics and the evolution of form: Experimental manipulation of a chromatin modification causes species-specific changes to the craniofacial skeleton.

A central question in biology is the molecular origins of phenotypic diversity. While genetic changes are key to the genotype-phenotype relationship, alterations to chromatin structure and the physical packaging of histone proteins may also be important drivers of vertebrate divergence. We investigate the impact of such an epigenetic mechanism, histone acetylation, within a textbook example of an adaptive radiation. Cichlids of Lake Malawi have adapted diverse craniofacial structures, and here we investigate how histone acetylation influences morphological variation in these fishes. Specifically, we assessed the effect of inhibiting histone deacetylation using the drug trichostatin A (TSA) on developing facial structures. We examined this during three critical developmental windows in two cichlid species with alternate adult morphologies. Exposure to TSA during neural crest cell (NCC) migration and as postmigratory NCCs proliferate in the pharyngeal arches resulted in significant changes in lateral and ventral shape in Maylandia, but not in Tropheops. This included an overall shortening of the head, widening of the lower jaw, and steeper craniofacial profile, all of which are paedomorphic morphologies. In contrast, treatment with TSA during early chondrogenesis did not result in significant morphological changes in either species. Together, these data suggest a sensitivity to epigenetic alterations that are both time- and species-dependent. We find that morphologies are due to nonautonomous or potentially indirect effects on NCC development, including in part a global developmental delay. Our research bolsters the understanding that proper histone acetylation is essential for early craniofacial development and identifies a species-specific robustness to developmental change. Overall, this study demonstrates how epigenetic regulation may play an important role in both generating and buffering morphological variation.

Genetic basis of ecologically relevant body shape variation among four genera of cichlid fishes.

Divergence in body shape is one of the most widespread and repeated patterns of morphological variation in fishes and is associated with habitat specification and swimming mechanics. Such ecological diversification is the first stage of the explosive adaptive radiation of cichlid fishes in the East African Rift Lakes. We use two hybrid crosses of cichlids (Metriaclima sp. × Aulonocara sp. and Labidochromis sp. × Labeotropheus sp., >975 animals total) to determine the genetic basis of body shape diversification that is similar to benthic-pelagic divergence across fishes. Using a series of both linear and geometric shape measurements, we identified 34 quantitative trait loci (QTL) that underlie various aspects of body shape variation. These QTL are spread throughout the genome, each explaining 3.2-8.6% of phenotypic variation, and are largely modular. Further, QTL are distinct both between these two crosses of Lake Malawi cichlids and compared to previously identified QTL for body shape in fishes such as sticklebacks. We find that body shape is controlled by many genes of small effect. In all, we find that convergent body shape phenotypes commonly observed across fish clades are most likely due to distinct genetic and molecular mechanisms.

Morphometric and Genetic Description of Trophic Adaptations in Cichlid Fishes.

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 F2 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.

Using 3D-digital photogrammetry to examine scaling of the body axis in burrowing skinks.

Three-dimensional (3D) modeling techniques have been increasingly utilized across disciplines for the visualization and analysis of complex structures. We employ 3D-digital photogrammetry for understanding the scaling of the body axis of 12 species of scincid lizards in the genus Brachymeles. These skinks represent a diverse radiation which shows tremendous variation in body size and degree of axial elongation. Because of the complex nature of the body axis, 3D-methods are important for understanding how the body axis evolves. 3D-digital photogrammetry presents a flexible, inexpensive, and portable system for the reconstruction of biological forms. As body size increased among species, the cross-sectional area and circumference of the head and other portions of the body axis increased isometrically, which indicates that species of differing sizes possess proportionally similar head and body shapes. These results suggest that there are no substantial head and body shape changes with body size among the sampled species, but further comparative studies with larger sample sizes and functional studies of size and morphology effects on burrowing or above-ground locomotion are needed.