Role of the Cranial Neural Crest in the Adaptive Radiation of Cichlid Jaw Shape
The cichlid model: A natural mutant screen for craniofacial shape.
Cichlid radiations are characterized by extensive trophic diversity. Closely related species exhibit dramatic variation in head shape, providing a unique opportunity to study patterns of natural variation in jaw morphogenesis. We view cichlid radiations as a collection of craniofacial mutants. Like mutants identified in chemical mutagenesis screens, natural variants can be used to investigate an extremely broad spectrum of traits. However, unlike traditional screens, mutants screened by natural selection are non-lethal and can therefore be studied beyond embryonic stages of development. Moreover, because mutations fixed by natural selection will likely affect regulatory elements, a natural mutant screen is more discerning of subtle differences in morphology. Thus, where traditional mutagenesis screens have been used to study craniofacial patterning, natural mutants will provide insights into factors that underlie craniofacial shape.
Cichlids as a collection of craniofacial mutants. Images from: www.malawicichlids.com
The cranial neural crest in evolution and development.
The progenitor cells of most of the craniofacial skeleton, including the jaw, are the cranial neural crest (CNC), a ‘key innovation’ contributing both to the origin and evolutionary success of vertebrates. Development of the CNC has been well studied in several vertebrate models. In bony fishes, the CNC migrate in three distinct streams from the putative mid- and hindbrain into a bilateral series of endodermal pouches, called pharyngeal arches. The iterative segmentation of the posterior-most arch into four additional arches is achieved through a complex morphogenic process that involves coordinated signaling from the pharyngeal endoderm and the CNC. CNC cells within each pharyngeal arch condense and differentiate to form the skeletal anatomy of the head.
Jaw morphogenesis may therefore be partitioned into series of distinct developmental stages that involve the CNC:
We want to know which of these developmental stages contribute to the production of adaptive variation in cichlid jaw shape.
An embryological approach to the study of adaptive radiation.
The characterization of patterns of CNC migration and segmentation in various cichlid species suggests that while the timing of CNC migration is relatively conserved, patterns of segmentation differ among species with divergent jaw morphologies. For example, species with thin jaws possess elongate CNC segments (A), whereas species with stout jaws possess robust CNC masses (B). These data suggest that adaptive variation in cichlid jaw shape is evident during CNC segmentation stages of embryological development. Since pharyngeal arch morphogenesis involves reciprocal signaling from the CNC and the surrounding epithelia, it is unclear whether this difference is due to changes in crest cells themselves or their environment.
Cichlid species with alternate jaw morphologies exhibit distinct patterns of CNC development.
A genetic approach to studying adaptive radiation.
Because of the recent origin of cichlid radiations, most interspecific and many intergeneric crosses will produce fertile hybrids, providing a unique opportunity to cross radically different ecomorphs to identify the genes that underlie differences in craniofacial shape.
We have used quantitative trait loci (QTL) analysis to identify the approximate number, effect and chromosomal position of loci that affect differences in cichlid jaw shape. Of particular interest are QTL that co-segregate with genes known to regulate jaw morphogenesis; Bone morphogenic protein 4 (bmp4) is one such factor.
Differences in cichlid jaw shape map to an interval on linkage group 19 that contains bmp4.
Work in several model organisms suggests that bmp4 plays an important role during jaw morphogenesis. For example, levels of bmp4 in the developing jaw will affect CNC condensation size as well as the transition from condensation growth to overt differentiation of chondroblasts. In cichlids, we find that species with distinct jaw morphologyies exhibit distinct patterns of bmp4 expression in the mandibular arch: higher levels of bmp4 are observed in species with robust jaws, whereas lower levels are observed in species with thin jaws. These data suggest that differences in CNC condensation and/or differentiation, regulated by bmp4, underlie differences in cichlid jaw shape.
Species with high levels of bmp4 in the mandibular arch (red arrowhead, cross section through the embryonic head) develop short robust jaws, whereas species with low levels of bmp4 develop thin elongate jaws.
Our studies show that cichlid species are divergent in various aspects of CNC development. Our approach integrates comparative embryology and quantitative genetics.
An embryological approach provides the opportunity to study the evolution of developmental pathways among closely related species (i.e., divergence in CNC segmentation). Genetic analyses, on the other hand, will point to the causative loci that result in divergent jaw shapes. These loci will be targets for natural selection and may therefore be studied in the broader context of cichlid evolution. A genetic approach will also serve to identify candidate genes that underlie adaptive variation in CNC-derived jaw morphogenesis (i.e., bmp4 mediated divergence in CNC condensation/differentiation). The goal of our lab is to expand this integrative approach to a broader taxonomic sampling to reveal the hierarchy of developmental changes that have contributed to the adaptive radiation of cichlid jaw shape.
Specific areas of research:
If you are interested in participating in one or more of these projects please contact me: rcalbert@syr.edu
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