Evolution of the potassium channel gene Kcnj13 underlies colour pattern diversification in Danio fish

Marco Podobnik,Christiane Nüsslein-Volhard,Uwe Irion,Hans Georg Frohnhöfer,Christopher M Dooley,Anastasia Eskova

doi:10.1038/s41467-020-20021-6

Abstract

The genetic basis of morphological variation provides a major topic in evolutionary developmental biology. Fish of the genus Danio display colour patterns ranging from horizontal stripes, to vertical bars or spots. Stripe formation in zebrafish, Danio rerio, is a self-organizing process based on cell−contact mediated interactions between three types of chromatophores with a leading role of iridophores. Here we investigate genes known to regulate chromatophore interactions in zebrafish that might have evolved to produce a pattern of vertical bars in its sibling species, Danio aesculapii. Mutant D. aesculapii indicate a lower complexity in chromatophore interactions and a minor role of iridophores in patterning. Reciprocal hemizygosity tests identify the potassium channel gene obelix/Kcnj13 as evolved between the two species. Complementation tests suggest evolutionary change through divergence in Kcnj13 function in two additional Danio species. Thus, our results point towards repeated and independent evolution of this gene during colour pattern diversification.

Highlights

The genetic basis of morphological variation provides a major topic in evolutionary developmental biology
The vertical bars must develop in a different manner in D. erythromicron compared to D. aesculapii and D. choprae
In the Danio genus the pattern of D. nigrofasciatus, with fewer and interrupted dark stripes (Fig. 6), resembles the mutant phenotype of weak alleles involved in endothelin signalling in D. rerio

Summary

Introduction

The genetic basis of morphological variation provides a major topic in evolutionary developmental biology. Pattern formation by neural crest-derived pigment cells involves direct contact-based interactions among cells of the same type or between different types of pigment cells These interactions control cell proliferation, shape changes and migration resulting in superimposed layers of differently coloured pigment cells under the skin generating a large variety of patterns, rich in fishes. The zebrafish, Danio rerio, has emerged as an excellent system to study colour pattern development in a vertebrate[7,8,13,17,18,19] In this model organism a fair number of genes have been identified in mutant screens that are required for the formation of the pattern[7,8], which is composed of a series of horizontal light and dark stripes on the flank of the fish as well as in the anal and tail fins (Fig. 1a). In Meox[1] (choker) mutants, which lack this structure, the horizontal orientation of the stripes is lost, but they form of normal width and composition (Fig. 1b), indicating that stripe formation is a process of self-organisation of the pigment cells[32]

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