The Sexually Antagonistic Genes of Drosophila melanogaster

Innocenti, Paolo; Morrow, Edward H.

doi:10.1371/journal.pbio.1000335

Cited by 311 publications

(457 citation statements)

References 38 publications

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“…These results differ notably from studies by Chippindale et al (2001) and from Innocenti and Morrow (2010), using the LH M population of D. melanogaster, who found a negative intersexual correlation for fitness (for example, r MF ¼ À0.52, from Innocenti and Morrow (2010)). The extent of intralocus sexual conflict may, therefore, vary considerably between populations, and the very high levels of sexually antagonistic variation segregating in the LH M population may not be a general feature of D. melanogaster populations.…”

Section: Comparison To Previous Studiescontrasting

confidence: 99%

Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females

Mallet

Chippindale

2010

Heredity

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Stronger selection on males has the potential to lower the deleterious mutation load of females, reducing the cost of sex. However, few studies have directly quantified the strength of selection for both sexes. As the magnitude of inbreeding depression (ID) is related to the strength of selection, we measured the cost of inbreeding for both males and females in a laboratory population of Drosophila melanogaster. Using a novel technique for inbreeding, we found significant ID for both juvenile viability and adult fitness in both sexes. The genetic variation responsible for this depression in fitness appeared to be recessive for adult fitness (h ¼ 0.11) and partially additive for juvenile viability (h ¼ 0.29). ID was identical across the sexes in terms of juvenile viability but was significantly more deleterious for males than females as adults, even though female X-chromosome homogamety should predispose them to a higher inbreeding load. We estimated the strength of selection on adult males to be 1.24 greater than on adult females, and this appears to be a consequence of selection arising from competition for mates. Combined with the generally positive intersexual genetic correlation for inbred lines, our results suggest that the mutation load of sexual females could be meaningfully reduced by stronger selection acting on males.

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Section: Comparison To Previous Studiescontrasting

confidence: 99%

Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females

Mallet

Chippindale

2010

Heredity

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“…As a consequence, the degree of SA genetic variation in well-adapted populations may be large relative to genetic variation for overall viability. Strong sexual selection on males could thus act to increase the frequencies of alleles that have deleterious effects when expressed in females, thereby limiting further adaptation (Brooks 2000;Chippindale and Rice 2001;Pischedda et al 2006;Prasad et al 2007;Bilde et al 2009;Innocenti and Morrow 2010;Berg and Maklakov 2012;Plesnar-Bielak et al 2014). However, we currently lack direct quantifications of population-level effects of SA genetic variation.…”

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

126

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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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“…However, while different female genotypes associate with differences in sperm competition outcomes, little is known about the specific genes or gene variants that underlie the differences in the female side of sperm competition. Gene expression analyses in singly mated (Lawniczak and Begun 2004;McGraw et al 2004McGraw et al , 2008McGraw et al , 2009Kapelnikov et al 2008) and doubly mated (Innocenti and Morrow 2010) females found numerous genes regulated by mating. These mating-regulated genes may include some that are important for sperm competition.…”

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confidence: 99%

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

2013

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Sperm competition arises as a result of complex interactions among male and female factors. While the roles of some male factors are known, little is known of the molecules or mechanisms that underlie the female contribution to sperm competition. The genetic tools available for Drosophila allow us to identify, in an unbiased manner, candidate female genes that are critical for mediating sperm competition outcomes. We first screened for differences in female sperm storage and use patterns by characterizing the natural variation in sperm competition in a set of 39 lines from the sequenced Drosophila Genetic Reference Panel (DGRP) of wild-derived inbred lines. We found extensive female variation in sperm competition outcomes. To generate a list of candidate female genes for functional studies, we performed a genome-wide association mapping, utilizing the common single-nucleotide polymorphisms (SNPs) segregating in the DGRP lines. Surprisingly, SNPs within ion channel genes and other genes with roles in the nervous system were among the top associated SNPs. Knockdown studies of three candidate genes (para, Rab2, and Rim) in sensory neurons innervating the female reproductive tract indicate that some of these candidate female genes may affect sperm competition by modulating the neural input of these sensory neurons to the female reproductive tract. More extensive functional studies are needed to elucidate the exact role of all these candidate female genes in sperm competition. Nevertheless, the female nervous system appears to have a previously unappreciated role in sperm competition. Our results indicate that the study of female control of sperm competition should not be limited to female reproductive tract-specific genes, but should focus also on diverse biological pathways. I N many organisms, sperm competition is an important source of reproductive variation and is critical to the reproductive success of both males and females. Sperm competition occurs when a female mates with and stores sperm from multiple males. Multiple mating creates a situation in which the males' sperm "compete" for successful fertilizations. While the ultimate outcome of a sperm competition depends on a complex interaction between male and female factors, the sexes often have different interests. Males are essentially in competition with other males, and while natural selection drives males to become better competitors with each other, it may result in males damaging the female through toxicity of seminal proteins (Wigby and Chapman 2004;Mueller et al. 2007). On the other hand, females benefit from simply being able to produce the most and highest-fitness offspring, and this may entail a specific response to male-produced molecules that influence sperm competition. The sexual conflict that arises from these different evolutionary goals of males and females implies that the genetic response to selection on sperm competition may be totally distinct in males and females. It remains largely unknown what genes drive this sexual antagon...

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The Sexually Antagonistic Genes of Drosophila melanogaster

Abstract: An association between sex-specific fitness and gene expression in the fruit fly provides an estimate of number, identity and function of sexually antagonistic genes in this species.

Cited by 311 publications

References 38 publications

Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females

Inbreeding reveals stronger net selection on Drosophila melanogaster males: implications for mutation load and the fitness of sexual females

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

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

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