Transcriptomics of morphological color change in polychromatic Midas cichlids

Frederico Henning,Axel Meyer,Julia C Jones,Paolo Franchini

doi:10.1186/1471-2164-14-171

Abstract

BackgroundAnimal pigmentation has received much attention in evolutionary biology research due to its strong implications for adaptation and speciation. However, apart from a few cases the genetic changes associated with these evolutionary processes remain largely unknown. The Midas cichlid fish from Central America are an ideal model system for investigating pigmentation traits that may also play a role in speciation. Most Midas cichlids maintain their melanophores and exhibit a grayish (normal) color pattern throughout their lives. A minority of individuals, however, undergo color change and exhibit a distinctive gold or even white coloration in adulthood. The ontogenetic color change in the Midas cichlids may also shed light on the molecular mechanisms underlying pigmentation disorders in humans.ResultsHere we use next-generation sequencing (Illumina) RNAseq analyses to compare skin transcriptome-wide expression levels in three distinct stages of color transformation in Midas cichlids. cDNA libraries of scale tissue, for six biological replicates of each group, were generated and sequenced using Illumina technology. Using a combination of three differential expression (DE) analyses we identified 46 candidate genes that showed DE between the color morphs. We find evidence for two key DE patterns: a) genes involved in melanosomal pathways are up-regulated in normally pigmented fish; and b) immediate early and inflammatory response genes were up-regulated in transitional fish, a response that parallels some human skin disorders such as melanoma formation and psoriasis. One of the DE genes segregates with the gold phenotype in a genetic cross and might be associated with incipient speciation in this highly “species-rich” lineage of cichlids.ConclusionsUsing transcriptomic analyses we successfully identified key expression differences between different color morphs of Midas cichlid fish. These differentially expressed genes have important implications for our understanding of the molecular mechanisms underlying speciation in this lineage of extremely young species since they mate strongly assortatively, and new species may arise by sexual selection due to this color polymorphism. Some of the human orthologues of the genes identified here may also be involved in pigmentation differences and diseases and therefore provide genetic markers for the detection of human pigmentation disorders.

Highlights

Animal pigmentation has received much attention in evolutionary biology research due to its strong implications for adaptation and speciation
Transitional and gold phenotypes were studied in mature, age matched, sibling fish (Figure 1) using six biological replicates of each phenotype, and two technical replicates of each library. We identify both well-known and uncharacterized genes associated with melanophore maintenance, cell death and build the de novo assembly
The Midas cichlid fish system provides a rare example of sympatric speciation, where color-based assortative mating is one of the processes thought to be driving divergence in these fish [21,23,24]

Summary

Introduction

Animal pigmentation has received much attention in evolutionary biology research due to its strong implications for adaptation and speciation. The Midas cichlid fish from Central America are an ideal model system for investigating pigmentation traits that may play a role in speciation. Animal pigmentation is a tractable and relevant trait for understanding key issues in evolutionary biology such as adaptation, speciation and the maintenance of balanced polymorphisms. While these evolutionary processes themselves have attracted much research attention, apart from a few cases [1,2,3,4,5,6,7] the genetic changes associated underlie speciation-with-gene flow in Neotropical cichlids (Figure 1A). The timing of the onset of this color change is variable and can begin when an individual is only a few months old, but can in a few individuals happen at a much older age - up to several years [25,26]

Objectives

Methods

Results

Conclusion