Multiple pigment cell types contribute to the black, blue, and orange ornaments of male guppies (Poecilia reticulata).

Iris Koch,Kevin Mcgraw,Verena A Kottler,Matthias Flötenmeyer,Hisashi Hashimoto,Detlef Weigel,Christine Dreyer

doi:10.1371/journal.pone.0085647

Iris Koch, Kevin Mcgraw + Show 5 more

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https://doi.org/10.1371/journal.pone.0085647

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Abstract

The fitness of male guppies (Poecilia reticulata) highly depends on the size and number of their black, blue, and orange ornaments. Recently, progress has been made regarding the genetic mechanisms underlying male guppy pigment pattern formation, but we still know little about the pigment cell organization within these ornaments. Here, we investigate the pigment cell distribution within the black, blue, and orange trunk spots and selected fin color patterns of guppy males from three genetically divergent strains using transmission electron microscopy. We identified three types of pigment cells and found that at least two of these contribute to each color trait. Further, two pigment cell layers, one in the dermis and the other in the hypodermis, contribute to each trunk spot. The pigment cell organization within the black and orange trunk spots was similar between strains. The presence of iridophores in each of the investigated color traits is consistent with a key role for this pigment cell type in guppy color pattern formation.

Highlights

The spectacular orange, yellow, white, and black along with the blue to green iridescent colors of male guppies (Poecilia reticulata) have attracted the attention of biologists and hobby breeders for almost a century [1,2,3,4,5]
Our study demonstrates that at least two of the three types of pigment cells contribute to each of the investigated ornamental traits of Cumana, Quare6, and Maculatus guppy males, suggesting that complex interactions between different chromatophore types both may be involved in establishing color patterns and enhance color signals in these strains
It would be especially interesting to investigate whether natural guppy populations that differ in the production of drosopterins and orange coloration [14] show differences in the ultrastructure of their orange ornaments

Summary

Introduction

The spectacular orange, yellow, white, and black along with the blue to green iridescent colors of male guppies (Poecilia reticulata) have attracted the attention of biologists and hobby breeders for almost a century [1,2,3,4,5]. Mate choice experiments have demonstrated that guppy females, which are camouflaged by an inconspicuous reticulate pattern [4,8], prefer males with high amounts of orange and iridescent pigments [6,9,10]. Both orange and iridescent ornaments can indicate a male’s current physical condition and genetic quality. Iridescent ornaments increase the risk of being noticed by predators and provide information on a male’s capability to evade these [6,9,15] Males intensify their black pigmentation during courtship, which might emphasize orange areas [6,16]. Studies have demonstrated that guppy females favor males with rare or novel color patterns over males with familiar phenotypes, suggesting that negative frequencydependent selection contributes to the maintenance of male color polymorphisms within guppy populations [19,20,21,22,23]

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