Molecular parallelisms between pigmentation in the avian iris and the integument of ectothermic vertebrates.

Pedro Andrade,Pedro M Araújo,M Thomas P Gilbert,Jacob A Rasmussen,Cristiana I Marques,Małgorzata A Gazda,Miguel Carneiro,Ricardo J Lopes,Sandra Afonso

doi:10.1371/journal.pgen.1009404

Abstract

Birds exhibit striking variation in eye color that arises from interactions between specialized pigment cells named chromatophores. The types of chromatophores present in the avian iris are lacking from the integument of birds or mammals, but are remarkably similar to those found in the skin of ectothermic vertebrates. To investigate molecular mechanisms associated with eye coloration in birds, we took advantage of a Mendelian mutation found in domestic pigeons that alters the deposition of yellow pterin pigments in the iris. Using a combination of genome-wide association analysis and linkage information in pedigrees, we mapped variation in eye coloration in pigeons to a small genomic region of ~8.5kb. This interval contained a single gene, SLC2A11B, which has been previously implicated in skin pigmentation and chromatophore differentiation in fish. Loss of yellow pigmentation is likely caused by a point mutation that introduces a premature STOP codon and leads to lower expression of SLC2A11B through nonsense-mediated mRNA decay. There were no substantial changes in overall gene expression profiles between both iris types as well as in genes directly associated with pterin metabolism and/or chromatophore differentiation. Our findings demonstrate that SLC2A11B is required for the expression of pterin-based pigmentation in the avian iris. They further highlight common molecular mechanisms underlying the production of coloration in the iris of birds and skin of ectothermic vertebrates.

Highlights

Coloration plays a vital role in the life history of many animals, so understanding the cellular and molecular underpinnings of traits related to ornamentation, camouflage or aposematic signals is key to shed light on major questions in evolutionary research [1]
We took advantage of variation in eye color found in domestic pigeons, which can be either pigmented or unpigmented
Using a combination of genomic and transcriptomic analyses, we show that the ability to express pterin pigmentation is explained by SLC2A11B, a gene that has been previously implicated in the differentiation of pigment cells in the skin of fish

Summary

Introduction

Coloration plays a vital role in the life history of many animals, so understanding the cellular and molecular underpinnings of traits related to ornamentation, camouflage or aposematic signals is key to shed light on major questions in evolutionary research [1]. In many species of vertebrates, colorful ornaments are linked to the development of specialized dermal cell types termed chromatophores, typically organized in a so-called “dermal chromatophore unit” whose basic structure is largely conserved in fish, amphibians and reptiles [2] With few exceptions, this unit is formed by several types of chromatophores, including pterin and carotenoidcontaining xanthophores, iridophores with reflecting guanine platelets, and melanophores containing melanin pigments. Iris pigmentation is frequently associated with the deposition of pterins [13], a class of pigments that is common in the skin of ectothermic vertebrates, but virtually absent in the integument of birds and mammals This observation together with the presence of all dermal chromatophore types in the avian iris–similar to those found in the skin of fish, amphibians and reptiles–have led previous authors to propose the iris as an “evolutionary refugium” for pigment cells in endothermic vertebrates [3]. Investigating genes associated with eye color variation in birds could shed light on this hypothesis, but finding suitable biological models is difficult given that differences in eye color are generally fixed between species [14]

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