An intronic transposon insertion associates with a trans-species color polymorphism in Midas cichlid fishes

Claudius F Kratochwil,Yipeng Liang,Alexander Nater,Axel Meyer,Andreas F Kautt,Andreas Härer,Frederico Henning

doi:10.1038/s41467-021-27685-8

Abstract

Polymorphisms have fascinated biologists for a long time, but their genetic underpinnings often remain elusive. Here, we aim to uncover the genetic basis of the gold/dark polymorphism that is eponymous of Midas cichlid fish (Amphilophus spp.) adaptive radiations in Nicaraguan crater lakes. While most Midas cichlids are of the melanic “dark morph”, about 10% of individuals lose their melanic pigmentation during their ontogeny and transition into a conspicuous “gold morph”. Using a new haplotype-resolved long-read assembly we discover an 8.2 kb, transposon-derived inverted repeat in an intron of an undescribed gene, which we term goldentouch in reference to the Greek myth of King Midas. The gene goldentouch is differentially expressed between morphs, presumably due to structural implications of inverted repeats in both DNA and/or RNA (cruciform and hairpin formation). The near-perfect association of the insertion with the phenotype across independent populations suggests that it likely underlies this trans-specific, stable polymorphism.

Highlights

Polymorphisms have fascinated biologists for a long time, but their genetic underpinnings often remain elusive
The presence of “gold” and “dark” individuals (Fig. 1a) in the Midas cichlid species complex (Amphilophus spp.) is a striking example of a stable color polymorphism that has been studied for almost half a century[3,4]
In order to narrow down candidates for the causal genetic variant, we performed genome-wide association mapping separately in individual lake populations

Summary

Introduction

Polymorphisms have fascinated biologists for a long time, but their genetic underpinnings often remain elusive. The presence of “gold” and “dark” individuals (Fig. 1a) in the Midas cichlid species complex (Amphilophus spp.) is a striking example of a stable color polymorphism that has been studied for almost half a century[3,4]. Between 3 months and 4 years of age or more[6], genetically “gold” individuals transition into the gold phenotype by losing the black pigmentation in their skin (usually within a few weeks) and become uniformly orange, red, yellow, or later sometimes even white[7]. During this process, melanophores, the melanin-bearing pigment cells, progressively undergo cell death[6]. Convincing candidates for the causally underlying mutation(s) or genes had been lacking so far

Objectives

Methods

Results