Comparing the intersex genetic correlation for fitness across novel environments in the fruit fly, Drosophila serrata

Punzalan, David; Delcourt, Matthieu; Rundle, Howard D.

doi:10.1038/hdy.2013.85

Cited by 60 publications

(105 citation statements)

References 40 publications

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“…Finally, both theory and data suggest that the severity of sexual antagonism should generally increase during the course of adaptation, with sexually antagonistic mutations being rare in poorly adapted populations and common in well-adapted ones (e.g., Long et al 2012;Berger et al 2014;Connallon and Clark 2014), but this is not always so (see Delcourt et al 2009;Punzalan et al 2014). The relative probability of balancing vs. positive selection similarly increases during the course of adaptation in Fisher's geometric model [e.g., because the average mutation size increases as the distance to the optimum shrinks (Sellis et al 2011);see above].…”

Section: Discussionmentioning

confidence: 99%

Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model

2014

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How common is balancing selection, and what fraction of phenotypic variance is attributable to balanced polymorphisms? Despite decades of research, answers to these questions remain elusive. Moreover, there is no clear theoretical prediction about the frequency with which balancing selection is expected to arise within a population. Here, we use an extension of Fisher's geometric model of adaptation to predict the probability of balancing selection in a population with separate sexes, wherein polymorphism is potentially maintained by two forms of balancing selection: (1) heterozygote advantage, where heterozygous individuals at a locus have higher fitness than homozygous individuals, and (2) sexually antagonistic selection (a.k.a. intralocus sexual conflict), where the fitness of each sex is maximized by different genotypes at a locus. We show that balancing selection is common under biologically plausible conditions and that sex differences in selection or sex-by-genotype effects of mutations can each increase opportunities for balancing selection. Although heterozygote advantage and sexual antagonism represent alternative mechanisms for maintaining polymorphism, they mutually exist along a balancing selection continuum that depends on population and sex-specific parameters of selection and mutation. Sexual antagonism is the dominant mode of balancing selection across most of this continuum.O NE of the primary goals of population genetics is to evaluate how processes of mutation, selection, migration, recombination, and genetic drift account for the maintenance of genetic variation in natural populations. This "great obsession" with genetic variation (Gillespie 2004, p. 154) is reflected by a massive body of theoretical and empirical research that seeks to connect empirical patterns of population and quantitative genetic variability with the specific evolutionary processes that might account for them.Balancing selection-selection that maintains genetic variation at a locus-could potentially account for an important fraction of observed quantitative genetic variability (Dobzhansky 1955;Lewontin 1974;Charlesworth and Hughes 1999). Although relatively few unambiguous cases of balancing selection have been documented to date (see Charlesworth 2006;Hedrick 2012;Johnston et al. 2013;Leffler et al. 2013), empirical methods for detecting their population genetic signatures are highly conservative and may fail to identify many (or most) instances of balancing selection within a genome (Charlesworth 2006;Charlesworth and Charlesworth 2010). Furthermore, balanced polymorphisms may plausibly account for several empirical observations that are not easily explained by alternative models of variation maintained by recurrent mutation. For example, the high genetic variance in life history and reproductive traits (Houle 1992;Pomiankowski and Moller 1995) and the presence of intermediate-frequency alleles with large phenotypic effects (Long et al. 2000) are each potentially attributable to a subset of loci that segrega...

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Section: Discussionmentioning

confidence: 99%

Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model

2014

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“…First, idiosyncrasies of the mating system, leading to differences in the extent of IeSC and associated female harm, are likely to play a decisive role in settling the outcome of sexual selection (e.g., Holland and Rice 1999;Hollis and Houle 2011;PlesnarBielak et al 2012;Chenoweth et al 2015). Second, much of the discrepancy between experiments may be rooted in differences in the genetic architecture of the studied populations and/ or the environmental conditions used in the experiments, which can affect the relative expression of, and selection on, allelic variation (Long et al 2012;Berger et al 2014a;Connallon and Clark 2014;Duffy et al 2014;Punzalan et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles

Berger

Martinossi‐Allibert

Grieshop

et al. 2016

The American Naturalist

128

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Online enhancements: appendixes, supplemental PDF. Dryad data: http://dx.doi.org/10.5061/dryad.bc94c.abstract: The evolution of male traits that inflict direct harm on females during mating interactions can result in a so-called tragedy of the commons, where selfish male strategies depress population viability. This tragedy of the commons can be magnified by intralocus sexual conflict (IaSC) whenever alleles that reduce fecundity when expressed in females spread in the population because of their benefits in males. We evaluated this prediction by detailed phenotyping of 73 isofemale lines of the seed beetle Callosobruchus maculatus. We quantified genetic variation in life history and morphology, as well as associated covariance in male and female adult reproductive success. In parallel, we created replicated artificial populations of each line and measured their productivity. Genetic constraints limited independent trait expression in the sexes, and we identified several instances of sexually antagonistic covariance between traits and fitness, signifying IaSC. Population productivity was strongly positively correlated to female adult reproductive success but uncorrelated with male reproductive success. Moreover, male (female) phenotypic optima for several traits under sexually antagonistic selection were exhibited by the genotypes with the lowest (highest) population productivity. Our study forms a direct link between individuallevel sex-specific selection and population demography and places lifehistory traits at the epicenter of these dynamics.

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“…; Punzalan et al. ; Han and Dingemanse ; Holman and Jacomb ; Martinossi‐Allibert et al. ; reviewed in Connallon and Hall ).…”

Section: Discussionmentioning

confidence: 99%

“…; Punzalan et al. ; reviewed in the Discussion), and evaluating evidence for sexually antagonistic selection and sexually antagonistic genetic variation from dioecious plant and gonochoristic animal populations.…”

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confidence: 99%

Cross-sex genetic correlations for fitness and fitness components: Connecting theoretical predictions to empirical patterns

Connallon

Matthews

2019

Evolution Letters

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Sex differences in morphology, physiology, development, and behavior are widespread, yet the sexes inherit nearly identical genomes, causing most traits to exhibit strong and positive cross‐sex genetic correlations. In contrast to most other traits, estimates of cross‐sex genetic correlations for fitness and fitness components ( ) are generally low and occasionally negative, implying that a substantial fraction of standing genetic variation for fitness might be sexually antagonistic (i.e., alleles benefitting one sex harm the other). Nevertheless, while low values of are often regarded as consequences of sexually antagonistic selection, it remains unclear exactly how selection and variation in quantitative traits interact to determine the sign and magnitude of , making it difficult to relate empirical estimates of cross‐sex genetic correlations to the evolutionary processes that might shape them. We present simple univariate and multivariate quantitative genetic models that explicitly link patterns of sex‐specific selection and trait genetic variation to the cross‐sex genetic correlation for fitness. We show that provides an unreliable signal of sexually antagonistic selection for two reasons. First, is constrained to be less than the cross‐sex genetic correlation for traits affecting fitness, regardless of the nature of selection on the traits. Second, sexually antagonistic selection is an insufficient condition for generating negative cross‐sex genetic correlations for fitness. Instead, negative fitness correlations between the sexes ( can only emerge when selection is sexually antagonistic and the strength of directional selection on each sex is strong relative to the amount of shared additive genetic variation in female and male traits. These results imply that empirical tests of sexual antagonism that are based on estimates of will be conservative and underestimate its true scope. In light of these theoretical results, we revisit current data on and sex‐specific selection and find that they are consistent with the theory.

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Comparing the intersex genetic correlation for fitness across novel environments in the fruit fly, Drosophila serrata

Cited by 60 publications

References 40 publications

Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model

Balancing Selection in Species with Separate Sexes: Insights from Fisher’s Geometric Model

Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles

Cross-sex genetic correlations for fitness and fitness components: Connecting theoretical predictions to empirical patterns

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