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Evolution of Female Choice Under Intralocus Sexual Conflict and Rstb.Royalsocietypublishing.Org Genotype-By-Environment Interactions Downloaded from http://rstb.royalsocietypublishing.org/ on August 27, 2018 Evolution of female choice under intralocus sexual conflict and rstb.royalsocietypublishing.org genotype-by-environment interactions Xiang-Yi Li1 and Luke Holman2 1Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, Research 8057 Zurich, Switzerland 2School of BioSciences, University of Melbourne, Parkville, Victoria 3010, Australia Cite this article: Li X-Y, Holman L. 2018 Evolution of female choice under intralocus X-YL, 0000-0001-8662-0865 sexual conflict and genotype-by-environment In many species, females are hypothesized to obtain ‘good genes’ for their interactions. Phil. Trans. R. Soc. B 373: offspring by mating with males in good condition. However, female pre- 20170425. ferences might deplete genetic variance and make choice redundant. http://dx.doi.org/10.1098/rstb.2017.0425 Additionally, high-condition males sometimes produce low-fitness offspring, for example because of environmental turnover and gene-by-environment interactions (GEIs) for fitness, or because fit males carry sexually antagonistic Accepted: 24 July 2018 alleles causing them to produce unfit daughters. Here, we extend previous theory by investigating the evolution of female mate choice in a spatially One contribution of 14 to a theme issue explicit evolutionary simulation implementing both GEIs and intralocus ‘Linking local adaptation with the evolution of sexual conflict (IASC), under sex-specific hard or soft selection. We show sex differences’. that IASC can weaken female preferences for high-condition males or even cause a preference for males in low condition, depending on the relative benefits of producing well-adapted sons versus daughters, which in turn Subject Areas: depends on the relative hardness of selection on males and females. We evolution, theoretical biology, ecology, discuss the relevance of our results to conservation genetics and empirical computational biology evolutionary biology. This article is part of the theme issue ‘Linking local adaptation with the evolution of sex differences’. Keywords: environmental stochasticity, GEI and GxE, lek paradox, local adaptation, mate preference, sexual antagonism 1. Introduction Selection resulting from mate choice preferences can profoundly affect evolution Author for correspondence: and demography, and can favour striking adaptations such as song, dance and Xiang-Yi Li elaborated coloration [1]. One hypothesis is that mate choice preferences evolved e-mail: [email protected] to allow the choosy sex (hereafter ‘females’ for brevity) to select mates carrying ‘good genes’ (using associated phenotypic cues, such as condition-dependent sexual signals [2]), such that alleles encoding mate choice will be found in high-fitness females more often than alleles encoding random mating [3]. A perennial problem for good genes models is that mate preferences tend to deplete genetic variance, making choice redundant and selecting against choosi- ness whenever it has a cost (the ‘lek paradox’, e.g. [4]). Another problem is that the notion of good genes is subjective. Because gene-by-environment interactions (GEIs) are ubiquitous [5], many alleles only confer high fitness in certain environ- ments. Choosy females may, therefore, obtain alleles that were advantageous in the male’s environment, but which are disadvantageous in the environment experienced by their offspring, due to spatial and/or temporal environmental turnover. Similarly, many alleles confer high fitness when expressed in the ‘environment’ of a male body, but low fitness in a female body, or vice versa [6,7]. Such intralocus sexual conflict (IASC) means that females selecting high- condition males may, therefore, produce fit sons but unfit daughters, reducing or reversing the net fitness of mate choice [8]. Electronic supplementary material is available Alternatively, IASC might sometimes drive the evolution of female choice. online at https://dx.doi.org/10.6084/m9. Seger & Trivers [9] showed that females can evolve to prefer males carrying figshare.c.4183508. female-beneficial/male-detrimental alleles, due to either a build-up of linkage & 2018 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from http://rstb.royalsocietypublishing.org/ on August 27, 2018 disequilibrium between female preference and sexual antagon- time series), where (i) E values are static and homogeneous 2 istic loci, or partial population-mixing by migration between across habitat patches, (ii) E values are static but heterogeneous rstb.royalsocietypublishing.org demes. Albert & Otto [10] studied the effects of IASC on across habitats, (iii) E values are heterogeneous and fluctuate female-choice evolution under different sex-determination sys- mildly across patches or (iv) E values are heterogeneous and fluc- tems. They found that if both the IASC locus and the female tuate strongly across patches. In the last two types, E values are temporally and spatially autocorrelated such that nearby patches choice locus are autosomal, female choice cannot evolve. and time points tend to have similar E. Similarly, modelling work has shown that GEIs can both help and hinder the spread of alleles encoding female prefer- ence [11,12]. However, few if any previous models have (c) Condition, mate choice and reproduction simultaneously examined the effects of IASC and GEIs on We model discrete generations in which individuals are born, female-choice evolution. Since GEIs help maintain genetic disperse, reproduce and then die. We assume that an individ- variance, they help resolve the lek paradox by maintaining ual’s condition is determined by (i) the match between its Phil. Trans. R. Soc. B locally maladapted alleles. Conversely, GEIs lead to ‘mistakes’ genotype at the local adaptation locus and the environment(s) whereby females choose a male whose alleles are poorly it encounters and (ii) its genotype at the sexual conflict locus. j adapted to the environment that their offspring will experi- Specifically, the condition ( ) of an individual in the reproduc- tion phase is a weighted average of its conditions in the natal ence, reducing the benefits of being choosy. Interestingly, and breeding patches. In equation (2.1), the subscripts N and B these two effects do not cancel out: occasional mistakes actually represent the effects on condition of the environmental states in 373 promote the evolution of mate choice, as they help maintain a the natal and breeding patches, respectively, while C (concordant) pool of maladapted males for choosy females to avoid. and A (antagonistic) represent the effects on condition of the : 20170425 We hypothesize that when individual condition depends local adaptation and sexual conflict loci. The relative importance on both local adaptation and IASC, a female preference for of the natal versus breeding habitats in determining condition is high-condition males may yield locally adapted offspring, weighted by knatal, while kLA (local adaptation) controls the but runs the risk of producing unfit daughters. An additional relative contributions of local adaptation versus sexual conflict complication is that the proportion of genetic variance in to individual condition. The condition of an individual at the fitness that is sexually antagonistic is not fixed, but varies time of breeding is then dynamically in response to processes such as migration, j ¼ knatal(kLAjNÁC þ (1 À kLA)jNÁA) local adaptation, environmental changes and assortative þ (1 À knatal)(kLAjBÁC þ (1 À kLA)jBÁA): ð2:1Þ mating (e.g. empirical evidence [13–16] and theory [17,18]). Here, we use individual-based simulations to jointly For the local adaptation locus, condition is maximized when study the evolution of female mate preferences, local adap- the individual’s genotype (f) exactly matches the environmental tation under GEIs, IASC and sex-specific (potentially state E, and decreases exponentially as the phenotype deviates co-evolving) dispersal behaviour. Our principal aims are to from it, so that jiÁC ¼ Exp( 2 10jf 2 Ej), where i can take either test whether female preferences evolve more or less easily N (on natal patch) or B (on breeding patch). For the sexual in populations carrying sexually antagonistic alleles and to conflict locus, we consider two different causes of sexual antag- onistic selection. In the first scenario, sexual conflict arises from determine whether the conclusions of past work regarding IASC, and we assume that an individual with allelic value x at mate choice under GEIs are robust to the addition of co- the locus has the condition component jiÁA ¼ x if the individual evolving sexual conflict loci. We consider a range of is male, and jiÁA ¼ 1 2 x (i[fN, Bg) if the individual is female. assumptions about sex-specific dispersal, the scale of compe- In the second scenario, sexual conflict arises from different tition, and the relative importance of IASC and local environmental optima for males and females. In this case, we adaptation to individual condition. consider an independent environmental state E0 (details in electronic supplementary material, §A), and males have the 0 condition component jiÁA ¼ E while females have jiÁA ¼ 1 2 E0 (i[fN, Bg), so that male condition is better at higher E0 2. Material and methods values while female condition is better at lower E0 values. For males, condition affects fitness by influencing the prob- (a) The meta-population ability of mating, assuming that at least one of the females in We model a population of sexually reproducing, dioecious the patch is choosy. We model the relative preference of a haploids subdivided over K discrete habitat patches. The habitat female for a male of condition j using a beta distribution func- patches are arranged linearly in a ring, such that every patch has tion B(j; a, b) ¼ G(a)G(b)=G(a þ b), where j [(0, 1), and a and two neighbours and there are no ‘edge effects’. Each patch has an b are female preference factors that determine the shape of environmental state E, which can be thought of as an ecological the preference curve. Random mating occurs when a ¼ b ¼ 1. variable that affects fitness.
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