Experimental evolution of a novel sexually antagonistic allele.

Evolutionary conflict permeates biological systems. In sexually reproducing organisms, sex-specific optima mean that the same allele can have sexually antagonistic expression, i.e. beneficial in one sex and detrimental in the other, a phenomenon known as intralocus sexual conflict. Intralocus sexual...

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Main Authors: Rebecca Dean, Jennifer C Perry, Tommaso Pizzari, Judith E Mank, Stuart Wigby
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3431318?pdf=render
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spelling doaj-ca52648b2a49457489817da46953d27b2020-11-24T21:47:52ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-0188e100291710.1371/journal.pgen.1002917Experimental evolution of a novel sexually antagonistic allele.Rebecca DeanJennifer C PerryTommaso PizzariJudith E MankStuart WigbyEvolutionary conflict permeates biological systems. In sexually reproducing organisms, sex-specific optima mean that the same allele can have sexually antagonistic expression, i.e. beneficial in one sex and detrimental in the other, a phenomenon known as intralocus sexual conflict. Intralocus sexual conflict is emerging as a potentially fundamental factor for the genetic architecture of fitness, with important consequences for evolutionary processes. However, no study to date has directly experimentally tested the evolutionary fate of a sexually antagonistic allele. Using genetic constructs to manipulate female fecundity and male mating success, we engineered a novel sexually antagonistic allele (SAA) in Drosophila melanogaster. The SAA is nearly twice as costly to females as it is beneficial to males, but the harmful effects to females are recessive and X-linked, and thus are rarely expressed when SAA occurs at low frequency. We experimentally show how the evolutionary dynamics of the novel SAA are qualitatively consistent with the predictions of population genetic models: SAA frequency decreases when common, but increases when rare, converging toward an equilibrium frequency of ∼8%. Furthermore, we show that persistence of the SAA requires the mating advantage it provides to males: the SAA frequency declines towards extinction when the male advantage is experimentally abolished. Our results empirically demonstrate the dynamics underlying the evolutionary fate of a sexually antagonistic allele, validating a central assumption of intralocus sexual conflict theory: that variation in fitness-related traits within populations can be maintained via sex-linked sexually antagonistic loci.http://europepmc.org/articles/PMC3431318?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Rebecca Dean
Jennifer C Perry
Tommaso Pizzari
Judith E Mank
Stuart Wigby
spellingShingle Rebecca Dean
Jennifer C Perry
Tommaso Pizzari
Judith E Mank
Stuart Wigby
Experimental evolution of a novel sexually antagonistic allele.
PLoS Genetics
author_facet Rebecca Dean
Jennifer C Perry
Tommaso Pizzari
Judith E Mank
Stuart Wigby
author_sort Rebecca Dean
title Experimental evolution of a novel sexually antagonistic allele.
title_short Experimental evolution of a novel sexually antagonistic allele.
title_full Experimental evolution of a novel sexually antagonistic allele.
title_fullStr Experimental evolution of a novel sexually antagonistic allele.
title_full_unstemmed Experimental evolution of a novel sexually antagonistic allele.
title_sort experimental evolution of a novel sexually antagonistic allele.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2012-01-01
description Evolutionary conflict permeates biological systems. In sexually reproducing organisms, sex-specific optima mean that the same allele can have sexually antagonistic expression, i.e. beneficial in one sex and detrimental in the other, a phenomenon known as intralocus sexual conflict. Intralocus sexual conflict is emerging as a potentially fundamental factor for the genetic architecture of fitness, with important consequences for evolutionary processes. However, no study to date has directly experimentally tested the evolutionary fate of a sexually antagonistic allele. Using genetic constructs to manipulate female fecundity and male mating success, we engineered a novel sexually antagonistic allele (SAA) in Drosophila melanogaster. The SAA is nearly twice as costly to females as it is beneficial to males, but the harmful effects to females are recessive and X-linked, and thus are rarely expressed when SAA occurs at low frequency. We experimentally show how the evolutionary dynamics of the novel SAA are qualitatively consistent with the predictions of population genetic models: SAA frequency decreases when common, but increases when rare, converging toward an equilibrium frequency of ∼8%. Furthermore, we show that persistence of the SAA requires the mating advantage it provides to males: the SAA frequency declines towards extinction when the male advantage is experimentally abolished. Our results empirically demonstrate the dynamics underlying the evolutionary fate of a sexually antagonistic allele, validating a central assumption of intralocus sexual conflict theory: that variation in fitness-related traits within populations can be maintained via sex-linked sexually antagonistic loci.
url http://europepmc.org/articles/PMC3431318?pdf=render
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