Evolving developmental trajectories to generate phenotypic diversity in Lake Malawi Cichlids

Thesis

A significant question in evolutionary developmental biology is how morphogenesis and gene regulation interact to achieve phenotypic diversity. In this thesis, I tackle this question using two complementary approaches.

First, I investigate how morphological diversity is generated in the near absence of genetic diversity. Lake Malawi cichlid fishes are an excellent system with which to study this problem, varying in phenotype but having extremely limited genetic diversity. In particular, cichlid species vary in somite and vertebral number, with Astatotilapia calliptera and Rhamphochromis chilingali forming 32 and 40 somites respectively. I characterized in detail the process of axial development during somitogenesis in both species, and found that both species differ only at the onset of segmentation: at the early stages of segmentation, the R. chilingali PSM is longer, greater in volume, and contains more cells, than that of A. calliptera. Other aspects of development, such as the anatomy and gene expression patterning of the PSM, are identical between these species. This suggests that R. chilingali have evolved an increased somite count by evolving the initial conditions of somitogenesis, and not the process of somitogenesis itself. This suggests that minor modifications of initial conditions can result in dramatic phenotypic innovations.

Secondly, I investigate how morphogenesis in the form of cell movements influences pattern formation during zebrafish somitogenesis. I develop and validate a method to reverse-engineer gene regulatory networks in a tissue undergoing extensive cell movements and rearrangements: the zebrafish presomitic mesoderm (PSM) during T-box pattern formation. Combining static and dynamic microscopy data, I reverse-engineer GRNs which are able to recapitulate key aspects of the T-box GRN, including pattern formation, the sign of known genetic interactions, and the response to perturbations in signalling. Characterizing these networks reveals that the tbox GRN could act as a cell-autonomous timer of differentiation as cells adopt a somitic fate. This finding explains a surprising ability of cells in the zebrafish PSM, to autonomously differentiate and upregulate tbx6/mesp-ba expression when isolated from the tailbud.

Altogether, this investigates how morphogenesis and genetic processes co-operate to produce phenotypic diversity during embryonic development.

Authors: Taylor, S

• DOI: 10.5287/ora-5jjjkegq0
• Type of award: DPhil
• Level of award: Doctoral
• Awarding institution: University of Oxford
• Language: English
• Keywords: evolvability; axial elongation; evo-devo; somitogenesis; Cichlid
• Subjects: Computational biology; Evolutionary developmental biology