Females and males have conflicting evolutionary interests. Selection favors the evolution of different phenotypes within each sex, yet divergence between the sexes is constrained by the shared genetic basis of female and male traits. Current theory predicts that such “sexual antagonism” should be common: manifesting rapidly during the process of adaptation, and slow in its resolution. However, these predictions apply in temporally stable environments. Environmental change has been shown empirically to realign the direction of selection acting on shared traits and thereby alleviate signals of sexually antagonistic selection. Yet there remains no theory for how common sexual antagonism should be in changing environments. Here, we analyze models of sex-specific evolutionary divergence under directional and cyclic environmental change, and consider the impact of genetic correlations on long-run patterns of sex-specific adaptation. We find that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima. Nevertheless, some forms of environmental change generate persistent sexually antagonistic selection that is difficult to resolve. Our results reinforce recent empirical observations that changing environmental conditions alleviate conflict between males and females. They also generate new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.
The evolutionary interests are very much conflicting when it comes to males and females. The evolution of distinct phenotypes within each sex is favored by selection, yet the shared genetic basis of female and male traits is a constraint upon the divergence between sexes. Now, the present theory suggests that such “sexual antagonism” is ordinary: manifesting rapidly in the adaptation process, and with slow resolution. However, this theory is applicable in temporally stable environments. There is no theory as to how ordinary sexual antagonism is in the environment which is changing and not stable. Still, some forms of environmental change result in persistent sexually antagonistic selection which is difficult to solve. Sex-specific fitness data from 202 fully sequenced hemiclonal Drosophila melanogaster fly lines was used to perform a genome-wide association study (GWAS) of sexual antagonism. The results reinstate recent empirical observations that changing environmental conditions fortify the confliction between males and females.
The reproductive roles of males and females are very divergent and favor different phenotypes. However, responses to these selective pressures have a shared genome as the constraint, leading to ‘sexual antagonism’, where different alleles at given loci are favored in the two sexes. A great amount of quantitative genetic studies has suggested sexual antagonism as like being omnipresent, being in birds, reptiles, plants, mammals. Sexual antagonism can be recognized as an important constraint on adaptation and an important mechanism for the maintenance of fitness variation within the variety of species.
As each sex employs different techniques in reproduction, selection often favors the evolution of different phenotypes in males and females (e.g. Andersson 1994). The traits that each sex expresses are encoded in a shared genome, and most phenotypes display strong and positive additive genetic correlations between the sexes (hereafter rmf; see Poissant et al. 2010; Griffin et al. 2013)). Although a positive between-sex genetic correlation (rmf > 0) promotes adaptation when directional selection aligns between the sexes, it reduces adaptation in each sex when selection is sexually antagonistic (Chenoweth 2009), giving rise to a form of evolutionary constraint known as intra locus sexual conflict (or sexual antagonism; see Rice 1992; Rice and Chippindale 2001). Such constraints manifest in patterns of opposing directional selection between the sexes and genetic tradeoffs between male and female fitness (Lande 1980; Connallon and Clark 2014) – patterns that have now been documented in several animal and plant populations.
Various recent empirical studies show that changes in environmental conditions can change the empirical signals of sexually antagonistic selection, such as sex-specific directional selection gradients and genetic correlations between female and male fitness components (Delph et al. 2011; Long et al. 2012; Berger et al. 2014). In Drosophila and in seed beetles, for instance, if they are in favorable lab conditions, it increases the genetic correlation between female and male fitness, relative to those which have adapted to stable lab conditions (Long et al. 2012; Berger et al. 2014). Conversely, stable or benign lab conditions often show relatively pronounced signals of sexually antagonistic selection (Rice and Chippindale 2001; Innocenti and Morrow 2010; Long et al. 2012; Berger et al. 2014). These recent empirical studies convey that changes in environmental conditions may often align the direction of selection in females and males, and thus, alleviate evolutionary constraints related with sexually antagonistic selection.
Contradictorily, a well-developed theory of adaptation to stable environmental conditions suggests that sexually antagonistic selection should rise rapidly during the process of adaptation toward sex-specific phenotypic optima, and persist across long evolutionary timescales. In Lande’s (1980) original treatment of this scenario, sexual antagonism rapidly increases during the early evolution of sexual dimorphism, in which the average phenotype of each sex evolves rapidly to a compromised position between the female and male fitness optima (i.e. the “fast phase” of evolutionary change). Sexual dimorphism evolves slowly, mostly when male and female traits are strongly genetically correlated, leading to a compacted period of sexually antagonistic selection (i.e. the “slow phase”). With time, the mean phenotypes of each sex finally evolve to their respective optima, yet as the evolution of sexual dimorphism is slow, it leads to sexual antagonism over a large period of time during adaptation. To oppose directional selection between the sexes, it may therefore portray the norm rather than the exception during bouts of adaptation towards sex-specific phenotypic optima.
LHM is a laboratory-adapted population of D. melanogaster that has been maintained under a highly controlled rearing regime since 1996. A random sample of 223 genetic lines was created from the population using a hemiclonal approach. Individuals of each line carry an identical haploid genome comprising the major chromosomes X, 2, and 3. Crosses with flies from custom stocks enable the replication of individuals—males and females—that carry a line’s X-2-3 haplotype alongside a random chromosomal complement from the LHM population that can be assayed for fitness. We used 16 random samples of LHM females to supply the chromosomal complements for each line, sex, and block.
Lifetime adult reproductive fitness of males and females of each line was measured using proven assays designed to mimic the LHM rearing regime. For male fitness, we measured competitive fertilization success by setting up competition vials containing 5 hemiclonal males from a given line, 10 competitor bw males, and 15 virgin bw females. After two days, bw females were isolated into individual vials containing no additional yeast and left to oviposit for 18 hours. On day 12 post egg laying, progeny was scored for eye color. Male fitness was calculated as the proportion of offspring sired by the 5 hemiclonal males (those with wild-type eye color), combining progeny data from the 15 oviposition vials. This assay was repeated five times in a blocked design; estimates for each line were therefore based on fitness measurements from 25 hemiclonal males. As expected for flies carrying a homozygous phenotypic marker mutation, bw males are slightly inferior to wild-type males (they sired approximately 46.4% instead of the expected two thirds of offspring across all fitness assays). They provide a meaningful competitive standard for our male fitness measures, as proved by the significant heritability in male mating success.
Quality control of whole-genome sequences
We used previously published whole-genome sequences generated from the hemiclonal lines analyzed here (available at https://zenodo.org/record/159472). Details about DNA extraction, library preparation, sequencing, read processing, and SNP calling are provided in the original publication. Prior to the association analysis performed here, further site-level quality filtering steps were performed in VCF tools and PLINK. First, individual variant calls based on depth <10 and genotype quality <30 were removed. Second, individuals with >15% missing positions were removed. Third, positions with poor genotype information (<95% call rate) across all retained individuals were not considered. Finally, given the comparatively small sample size of the dataset as a whole and the low power of an association test for rare variants, we kept only common variants (MAF > 0.05) for further analysis. From an initial dataset of 220 HEMICLONES containing 1,312,336 SNPs, this yielded a quality-filtered dataset of 765,980 SNPs from 203 HEMICLONES.
Quantification and association analysis of sexual antagonism
To recognize loci underlying sexual antagonism, we followed the approach of Berger and colleagues and consequent research and created an ‘antagonism index’. To be specific, we rotated the coordinates of the male and female fitness plane by 45 degrees, by multiplying the matrix of fitness coordinates (average male and female fitness estimate for each hemiclonal line) by a rotation matrix:
The matrix of hemiclonal male and female fitness values is transformed into positions on a bivariate coordinate system (of dimension 2 × 202 lines) with one sexually antagonistic and one sexually concordant axis. These positions display the values of the ‘antagonism index’ used to map antagonistic genetic variation, as well as the ‘concordant index’ used for comparative purposes.
The sex-specific fitness of hemiclonal fly lines (N = 223) that had been extracted from LHM as part of a previous study was measured. Individuals from each hemiclonal line carry an identical haploid genome comprising all major chromosomes (X, 2, and 3; i.e., about 99% of the total genomic content) paired with a random chromosomal complement from LHM. For each line, we measured male fitness as competitive fertilization success and female fitness as competitive fecundity. The fitness estimates obtained are based on measurements from 25 individual males and females for each hemiclonal line. Assays closely mimic the rearing regime experienced by flies in the base population, thus providing a good proxy for lifetime reproductive success in each sex.
Quantitative genetic analyses confirm the presence of significant amounts of genetic variation for male and female fitness among the lines assayed. To understand putative antagonistic SNPs, we performed a GWAS based on the antagonism index and sequence polymorphism data for 765,764 common (minor allele frequency [MAF] > 0.05) and stringently quality-filtered SNPs across 202 of the 223 lines. We used a linear mixed model that corrects for between-line relatedness and population structure by incorporating a genetic similarity matrix as a random effect. The genomic inflation factor ( = 0.967) and analyses using alternative, permutation-based significance tests confirmed that the parametric P values obtained are robust.
This study analyses the identity, function, and evolution of genome-wide sexually antagonistic sequence polymorphisms. Remarkably, we find that genetic variation at antagonistic loci is stably maintained across D. melanogaster populations throughout the species’ distribution range, and across species boundaries into D. simulans. These results show that the targets of antagonistic selection have been largely conserved for many millennia and hundreds of thousands of generations—and that a number of antagonistic polymorphisms have arisen and persisted since the speciation event between D. melanogaster and D. simulans, around 1 million years ago. It is possible that our GWAS only captures a subset of antagonistic variants, i.e., those that remain polymorphic in the constant laboratory environment to which asdthe LHM population has adapted.
By recognizing genome-wide antagonistic variants and linking these loci to signatures of balancing selection in independent populatasdions, our results supplement a growing body of evidence suggesting that balancing selection can influence patterns of genetic variation on a genome-wide scale, rather than a very limited number of isolated loci, as is sometimes assumed. For example, previous quantitative genetic analyses have shown that levels of genetic variation observed among populations of Drosophila and other species far exceed the levels predicted under mutation-selection balance alone, implying an important role for balanced polymorphisms. Moreover, a recent genomic study in D. melanogaster has linked candidate loci under opposing selection between seasons with long-term elevations in genome-wide polymorphism, emphasizing the importance of fluctuating balancing selection across the genome. Sexually antagonistic selection should contribute particularly strongly to the buildup of balanced polymorphisms, given that there is abundant evidence for sex-specific selection in nature and that many traits portray strong positive genetic correlations between the sexes. Together, these factors create permissive conditions for the evolution of sexually antagonistic polymorphisms relative to alternative sources of balancing selection.
This research clarifies the relative role of antagonistic and non-antagonistic modes of balancing selection towards the maintenance of genetic variation. But it also provides the foundation for further work on the genetics of sexual antagonism, including elucidating its functional basis and testing theories regarding its resolution. These future studies will help us understand better how males and females can, or cannot, respond to sex-specific selection and adapt to their respective reproductive roles.
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