Quantitative Genetic Analyses of Male Color Pattern and Female Mate Choice in a Pair of Cichlid Fishes of Lake Malawi, East Africa.

Baoqing Ding,Patrick D Danley,Aimee E Howe,Ming Chen,Martin Husemann,Daniel W Daugherty

doi:10.1371/journal.pone.0114798

Abstract

The traits involved in sexual selection, such as male secondary sexual characteristics and female mate choice, often co-evolve which can promote population differentiation. However, the genetic architecture of these phenotypes can influence their evolvability and thereby affect the divergence of species. The extraordinary diversity of East African cichlid fishes is often attributed to strong sexual selection and thus this system provides an excellent model to test predictions regarding the genetic architecture of sexually selected traits that contribute to reproductive isolation. In particular, theory predicts that rapid speciation is facilitated when male sexual traits and female mating preferences are controlled by a limited number of linked genes. However, few studies have examined the genetic basis of male secondary sexual traits and female mating preferences in cichlids and none have investigated the genetic architecture of both jointly. In this study, we artificially hybridized a pair of behaviorally isolated cichlid fishes from Lake Malawi and quantified both melanistic color pattern and female mate choice. We investigated the genetic architecture of both phenotypes using quantitative genetic analyses. Our results suggest that 1) many non-additively acting genetic factors influence melanistic color patterns, 2) female mate choice may be controlled by a minimum of 1–2 non-additive genetic factors, and 3) F2 female mate choice is not influenced by male courting effort. Furthermore, a joint analysis of color pattern and female mate choice indicates that the genes underlying these two traits are unlikely to be physically linked. These results suggest that reproductive isolation may evolve rapidly owing to the few genetic factors underlying female mate choice. Hence, female mate choice likely played an important role in the unparalleled speciation of East African cichlid fish.

Highlights

The genetic architecture of traits experiencing sexual selection influences phenotypic evolution and speciation [1]
In this study, using a pair of closely related, yet reproductively isolated Malawian cichlids as the model, we investigated the genetic architecture of two evolutionary significant traits, male color pattern and female mate choice, with quantitative genetic analyses
Our results suggest that melanistic color patterns are influenced by many non-additively acting genetic factors, while female mate choice may be controlled by a few non-additive genetic factors

Summary

Introduction

The genetic architecture of traits experiencing sexual selection influences phenotypic evolution and speciation [1]. The pattern and rate of response of a trait to selection depends on several factors including the strength of selection, the presence of genetic variation, the mode of inheritance, genetic correlations with other traits, the numbers of genes and alleles underlying a phenotype, the distribution of allelic effects, and patterns of pleiotropy, dominance, and epistasis [1,2,3,4]. Despite their importance, empirical studies examining these factors within the context of sexual selection and speciation are sparse, in vertebrates. Some have suggested that color patterns may have evolved in response to ecological pressures [16,17,18,19] or male-male competition [20,21,22], many empirical studies have documented the role that male color patterns, i.e. colored ornamentation [23], body hue [24, 25], and melanistic patterns [26,27,28], play in sexual selection via female mate choice

Methods

Results

Conclusion