The genetic architecture of fitness in a seed beetle: assessing the potential for indirect genetic benefits of female choice

Bilde, Trine; Friberg, Urban; Maklakov, Alexei A.; Fry, James D.; Arnqvist, Göran

doi:10.1186/1471-2148-8-295

Cited by 48 publications

(63 citation statements)

References 94 publications

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“…In the male assays, focal males were competing with tester males for access to females from the base population, and the total number of offspring was counted as a measure of LRS. Sterile males were included to increase reproductive competition [32,36], providing a more accurate measure of focal male fitness in this protandrous system [11,28]. In the female assays, we paired focal females from selected lines with males from the base population and recorded realized fecundity as LRS [11,36].…”

Section: Resultsmentioning

confidence: 99%

“…Sterile males were included to increase reproductive competition [32,36], providing a more accurate measure of focal male fitness in this protandrous system [11,28]. In the female assays, we paired focal females from selected lines with males from the base population and recorded realized fecundity as LRS [11,36]. To compare LRS of the sexes across selection regimes in the same model, we used the variance standardization approach, which measures the change in trait value in the units of standard deviation for this trait.…”

Section: Resultsmentioning

confidence: 99%

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Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

2012

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Males and females have different routes to successful reproduction, resulting in sex differences in lifespan and age-specific allocation of reproductive effort. The trade-off between current and future reproduction is often resolved differently by males and females, and both sexes can be constrained in their ability to reach their sex-specific optima owing to intralocus sexual conflict. Such genetic antagonism may have profound implications for evolution, but its role in ageing and lifespan remains unresolved. We provide direct experimental evidence that males live longer and females live shorter than necessary to maximize their relative fitness in Callosobruchus maculatus seed beetles. Using artificial selection in a genetically heterogeneous population, we created replicate long-life lines where males lived on average 27 per cent longer than in short-life lines. As predicted by theory, subsequent assays revealed that upward selection on male lifespan decreased relative male fitness but increased relative female fitness compared with downward selection. Thus, we demonstrate that lifespan-extending genes can help one sex while harming the other. Our results show that sexual antagonism constrains adaptive life-history evolution, support a novel way of maintaining genetic variation for lifespan and argue for better integration of sex effects into applied research programmes aimed at lifespan extension.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

2012

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“…For undomesticated species, dominance is typically estimated by inbreeding or by crossing inbred lines (e.g., Hughes et al 2002;Kearsey et al 2003;Bilde et al 2008). Throughout the genome, these processes create levels of homozygosity and heterozygosity, respectively, that are unlikely to be seen in natural populations.…”

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confidence: 99%

Dominance Genetic Variance for Traits Under Directional Selection inDrosophila serrata

Sztepanacz

Blows

2015

Genetics

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In contrast to our growing understanding of patterns of additive genetic variance in single-and multi-trait combinations, the relative contribution of nonadditive genetic variance, particularly dominance variance, to multivariate phenotypes is largely unknown. While mechanisms for the evolution of dominance genetic variance have been, and to some degree remain, subject to debate, the pervasiveness of dominance is widely recognized and may play a key role in several evolutionary processes. Theoretical and empirical evidence suggests that the contribution of dominance variance to phenotypic variance may increase with the correlation between a trait and fitness; however, direct tests of this hypothesis are few. Using a multigenerational breeding design in an unmanipulated population of Drosophila serrata, we estimated additive and dominance genetic covariance matrices for multivariate wing-shape phenotypes, together with a comprehensive measure of fitness, to determine whether there is an association between directional selection and dominance variance. Fitness, a trait unequivocally under directional selection, had no detectable additive genetic variance, but significant dominance genetic variance contributing 32% of the phenotypic variance. For single and multivariate morphological traits, however, no relationship was observed between trait-fitness correlations and dominance variance. A similar proportion of additive and dominance variance was found to contribute to phenotypic variance for single traits, and double the amount of additive compared to dominance variance was found for the multivariate trait combination under directional selection. These data suggest that for many fitness components a positive association between directional selection and dominance genetic variance may not be expected.KEYWORDS genetic variance; animal model; dominance; fitness C HARACTERIZING the genetic basis of phenotypes and the form and resulting consequences of selection on these phenotypes is a major goal of evolutionary biology. Substantial effort has been devoted to estimating additive genetic variance in metric traits and fitness components (Falconer and Mackay 1996;Lynch and Walsh 1998), establishing that the majority of metric traits have additive genetic variance and a heritability in the range of 0.2-0.6 (Lynch and Walsh 1998). More recently, the necessity of examining multivariate patterns of additive genetic variance and selection has been emphasized (Walsh and Blows 2009) and shown to influence the multivariate response to selection in laboratory (e.g., McGuigan and Blows 2009;Hine et al. 2014) and natural populations (Clements et al. 2011;Morrissey et al. 2012). In particular, additive genetic variance in all single traits often does not equate to genetic variance in all multivariate trait combinations (Hine and Blows 2006;Blows 2007;Walsh and Blows 2009), and a response to selection in trait combinations with low levels of additive genetic variance may be stochastic in nature .In contrast to our growing und...

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“…By allowing gift donors to store more sperm females can gain indirect benefits, either through Fisherian processes if females produce 'sexy sons' that are more likely to provide nuptial gifts, or by elevated fitness of offspring if gift-giving males pass on genes that are superior for survivorship traits [7,8,13,19]. Pisaura mirabilis males that offer nuptial gifts may signal good hunting abilities that are inherited by their offspring and through which male offspring would further gain an advantage in attracting females.…”

Section: Discussionmentioning

confidence: 99%

“…Internal processes that result in fertilization bias can be mediated by both sexes or by interactions between male and female traits [2,3,13]. There is a wealth of studies on syn-or postcopulatory processes focusing on male traits that confer advantages in sperm competition [2,4,5].…”

Section: Introductionmentioning

confidence: 99%

Sperm storage mediated by cryptic female choice for nuptial gifts

2013

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Polyandrous females are expected to discriminate among males through postcopulatory cryptic mate choice. Yet, there is surprisingly little unequivocal evidence for female-mediated cryptic sperm choice. In species in which nuptial gifts facilitate mating, females may gain indirect benefits through preferential storage of sperm from gift-giving males if the gift signals male quality. We tested this hypothesis in the spider Pisaura mirabilis by quantifying the number of sperm stored in response to copulation with males with or without a nuptial gift, while experimentally controlling copulation duration. We further assessed the effect of gift presence and copulation duration on egg-hatching success in matings with uninterrupted copulations with giftgiving males. We show that females mated to gift-giving males stored more sperm and experienced 17% higher egg-hatching success, compared with those mated to no-gift males, despite matched copulation durations. Uninterrupted copulations resulted in both increased sperm storage and egg-hatching success. Our study confirms the prediction that the nuptial gift as a male signal is under positive sexual selection by females through cryptic sperm storage. In addition, the gift facilitates longer copulations and increased sperm transfer providing two different types of advantage to gift-giving in males.

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The genetic architecture of fitness in a seed beetle: assessing the potential for indirect genetic benefits of female choice

Cited by 48 publications

References 94 publications

Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

Dominance Genetic Variance for Traits Under Directional Selection inDrosophila serrata

Sperm storage mediated by cryptic female choice for nuptial gifts

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