ABSTRACT
Developmental evolution and diversification of morphology can arise through changes in the regulation of gene expression or protein-coding sequence. To unravel mechanisms underlying early developmental evolution in cavefish of the species Astyanax mexicanus, we compared transcriptomes of surface-dwelling and blind cave-adapted morphs at the end of gastrulation. Twenty percent of the transcriptome was differentially expressed. Allelic expression ratios in cave X surface hybrids showed that cis-regulatory changes are the quasi-exclusive contributors to inter-morph variations in gene expression. Among a list of 108 genes with change at the cis-regulatory level, we explored the control of expression of rx3, which is a master eye gene. We discovered that cellular rx3 levels are cis-regulated in a cell-autonomous manner, whereas rx3 domain size depends on non-autonomous Wnt and Bmp signalling. These results highlight how uncoupled mechanisms and regulatory modules control developmental gene expression and shape morphological changes. Finally, a transcriptome-wide search for fixed coding mutations and differential exon use suggested that variations in coding sequence have a minor contribution. Thus, during early embryogenesis, changes in gene expression regulation are the main drivers of cavefish developmental evolution.
Footnotes
Author contributions
Conceptualization: J.L., J.T.-P., S.R.; Methodology: J.L., J.T.-P., F.A.; Software: M.P.; Validation: J.L., J.T.-P., S.R.; Formal analysis: J.L., J.T.-P., S.R.; Investigation: J.L., J.T.-P., M.P., F.A.; Resources: J.L., S.R.; Data curation: J.L., S.R.; Writing - original draft: J.L., S.R.; Writing - review & editing: J.T.-P., M.P., F.A., S.R.; Visualization: J.L., J.T.-P., S.R.; Supervision: S.R.; Project administration: S.R.; Funding acquisition: S.R.
Funding
This work was supported by grants to S.R. from Equipe Fondation pour la Recherche Médicale (EQU202003010144), Retina France and the Agence Nationale pour la Recherche (Cavemom).
Data availability
The RNA-seq data have been deposited in the Sequence Read Archive on NCBI under BioProject ID PRJNA848099.
Special Issue
This article is part of the Special Issue ‘Uncovering developmental diversity’, edited by Cassandra Extavour, Liam Dolan and Karen Sears. See related articles at https://journals.biologists.com/dev/issue/151/20.
