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

Tim Connallon, Genevieve Matthews

Research output: Contribution to journalArticleResearchpeer-review

Abstract

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 (rfm W ) 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 rfm W 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 rfm W , 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 rfm W provides an unreliable signal of sexually antagonistic selection for two reasons. First, rfm W 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 (rfm W < 0) 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 rfm W will be conservative and underestimate its true scope. In light of these theoretical results, we revisit current data on rfm W and sex-specific selection and find that they are consistent with the theory.
Original languageEnglish
Pages (from-to)254-262
Number of pages9
JournalEvolution Letters
Volume3
Issue number3
DOIs
Publication statusPublished - 2019

Keywords

  • Additive genetic variance
  • genetic constraint
  • sexual antagonism
  • sexual conflict

Cite this

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title = "Cross‐sex genetic correlations for fitness and fitness components: Connecting theoretical predictions to empirical patterns",
abstract = "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 (rfm W ) 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 rfm W 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 rfm W , 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 rfm W provides an unreliable signal of sexually antagonistic selection for two reasons. First, rfm W 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 (rfm W < 0) 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 rfm W will be conservative and underestimate its true scope. In light of these theoretical results, we revisit current data on rfm W and sex-specific selection and find that they are consistent with the theory.",
keywords = "Additive genetic variance, genetic constraint, sexual antagonism, sexual conflict",
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Cross‐sex genetic correlations for fitness and fitness components: Connecting theoretical predictions to empirical patterns. / Connallon, Tim; Matthews, Genevieve.

In: Evolution Letters, Vol. 3, No. 3, 2019, p. 254-262.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Cross‐sex genetic correlations for fitness and fitness components: Connecting theoretical predictions to empirical patterns

AU - Connallon, Tim

AU - Matthews, Genevieve

PY - 2019

Y1 - 2019

N2 - 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 (rfm W ) 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 rfm W 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 rfm W , 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 rfm W provides an unreliable signal of sexually antagonistic selection for two reasons. First, rfm W 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 (rfm W < 0) 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 rfm W will be conservative and underestimate its true scope. In light of these theoretical results, we revisit current data on rfm W and sex-specific selection and find that they are consistent with the theory.

AB - 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 (rfm W ) 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 rfm W 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 rfm W , 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 rfm W provides an unreliable signal of sexually antagonistic selection for two reasons. First, rfm W 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 (rfm W < 0) 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 rfm W will be conservative and underestimate its true scope. In light of these theoretical results, we revisit current data on rfm W and sex-specific selection and find that they are consistent with the theory.

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KW - sexual antagonism

KW - sexual conflict

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EP - 262

JO - Evolution Letters

JF - Evolution Letters

SN - 2056-3744

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