Conserved but flexible modularity in the zebrafish skull: implications for craniofacial evolvability

Morphological variation is the outward manifestation of development and provides fodder for adaptive evolution. Because of this contingency, evolution is often thought to be biased by developmental processes and functional interactions among structures, which are statistically detectable through forms of covariance among traits. This can take the form of substructures of integrated traits, termed modules, which together comprise patterns of variational modularity. While modularity is essential to an understanding of evolutionary potential, biologists currently have little understanding of its genetic basis and its temporal dynamics over generations. To address these open questions, we compared patterns of craniofacial modularity among laboratory strains, defined mutant lines and a wild population of zebrafish ( Danio rerio ). Our findings suggest that relatively simple genetic changes can have profound effects on covariance, without greatly affecting craniofacial shape. Moreover, we show that instead of completely deconstructing the covariance structure among sets of traits, mutations cause shifts among seemingly latent patterns of modularity suggesting that the skull may be predisposed towards a limited number of phenotypes. This new insight may serve to greatly increase the evolvability of a population by providing a range of ‘preset’ patterns of modularity that can appear readily and allow for rapid evolution.

Challenges in Identifying and Interpreting Organizational Modules in Morphology

Form is a rich concept that agglutinates information about the proportions and topological arrangement of body parts. Modularity is readily observable in both the variation of proportions (variational modules) and the organization of topology (organizational modules). The study of variational modularity and of organizational modularity faces similar challenges regarding the identification of meaningful modules and the validation of generative processes; however, most studies in morphology focus solely on variational modularity, while organizational modularity is much less understood. A possible cause for this bias is the successful development in the last twenty years of morphometrics, and specially geometric morphometrics, to study patters of variation. This contrasts with the lack of a similar mathematical framework to deal with patterns of organization. Recently, a new mathematical framework has been proposed to study the organization of anatomical parts using tools from Network Theory, so-called anatomical network analysis. This essay explores the potential use of this new framework – and the challenges it faces in identifying and validating biologically meaningful modules in morphological systems –, by providing an example of a complete analysis of modularity of the human skull and upper limb. Finally, we suggest further directions of research that may bridge the gap between variational and organizational modularity studies.

Modularity of the Oral Jaws Is Linked to Repeated Changes in the Craniofacial Shape of African Cichlids

The African cichlids of the East-African rift-lakes provide one of the most dramatic examples of adaptive radiation known. It has long been thought that functional decoupling of the oral and pharyngeal jaws in cichlids has facilitated their explosive evolution. Recent research has also shown that craniofacial evolution from radiations in lakes Victoria, Malawi, and Tanganyika has occurred along a shared primary axis of shape divergence, whereby the preorbital region of the skull changes in a manner that is, relatively independent from other head regions. We predicted that the preorbital region would comprise a variational module and used an extensive dataset from each lake that allowed us to test this prediction using a model selection approach. Our findings supported the presence of a preorbital module across all lakes, within each lake, and for Malawi, within sand and rock-dwelling clades. However, while a preorbital module was consistently present, notable differences were also observed among groups. Of particular interest, a negative association between patterns of variational modularity was observed between the sand and rock-dwelling clades, a patter consistent with character displacement. These findings provide the basis for further experimental research involving the determination of the developmental and genetic bases of these patterns of modularity.