Negative phenotypic and genetic associations between copulation duration and longevity in male seed beetles

Brown, Emily; Vasudev, Ram; Tregenza, Tom; Eady, Paul E.; Hosken, David J.

doi:10.1038/hdy.2009.80

Cited by 20 publications

(24 citation statements)

References 63 publications

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“…A more recent study found the opposite result, with significant dam effects on copulation duration (although they did give H 2 or h 2 estimates), but no effect of father genotype [45]. Our estimates of the heritability of mating duration are at the lower end of those generally found in other species ( h 2 = 0.58 in Onthophagus taurus [17], 0.39 in Scatophagia stercoraria [46], 0.26–0.36 in Callosobruchus maculatus [47]), although these studies investigated narrow-sense heritability, and so may not be directly comparable with our broad-sense heritability estimates.…”

Section: Discussioncontrasting

confidence: 85%

The Heritability of Mating Behaviour in a Fly and Its Plasticity in Response to the Threat of Sperm Competition

et al. 2014

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Phenotypic plasticity is a key mechanism by which animals can cope with rapidly changeable environments, but the evolutionary lability of such plasticity remains unclear. The socio-sexual environment can fluctuate very rapidly, affecting both the frequency of mating opportunities and the level of competition males may face. Males of many species show plastic behavioural responses to changes in social environment, in particular the presence of rival males. For example, Drosophila pseudoobscura males respond to rivals by extending mating duration and increasing ejaculate size. Whilst such responses are predicted to be adaptive, the extent to which the magnitude of response is heritable, and hence selectable, is unknown. We investigated this using isofemale lines of the fruit fly D. pseudoobscura, estimating heritability of mating duration in males exposed or not to a rival, and any genetic basis to the change in this trait between these environments (i.e. degree of plasticity). The two populations differed in population sex ratio, and the presence of a sex ratio distorting selfish chromosome. We find that mating duration is heritable, but no evidence of population differences. We find no significant heritability of plasticity in mating duration in one population, but borderline significant heritability of plasticity in the second. This difference between populations might be related to the presence of the sex ratio distorting selfish gene in the latter population, but this will require investigation in additional populations to draw any conclusions. We suggest that there is scope for selection to produce an evolutionary response in the plasticity of mating duration in response to rivals in D. pseudoobscura, at least in some populations.

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Section: Discussioncontrasting

confidence: 85%

The Heritability of Mating Behaviour in a Fly and Its Plasticity in Response to the Threat of Sperm Competition

et al. 2014

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“…Ejaculate size increases with copulation duration and contributes to male reproductive success because it increases female fecundity [44]. Males that are able to copulate for longer and/or produce larger ejaculates would increase their reproductive fitness but suffer a longevity cost [38]. Selection for male longevity might lead to selection on other traits, such as locomotory behaviour, metabolic rate and metabolic efficiency.…”

Section: Resultsmentioning

confidence: 99%

“…Males constantly search for mates, attempt to mount resistant females [32] and may invest up to 10 per cent of their body weight in a single copulation [37]. Reproductive effort in male seed beetles is so costly that duration of a single copulation is phenotypically and genetically correlated with reduced survival [38]. Furthermore, males have to be persistent in order to achieve matings with previously mated females [32], which is expensive in terms of energy and water.…”

Section: Resultsmentioning

confidence: 99%

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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“…[51] who found males exposed to thermal stress during development transferred fewer sperm but spent longer in copula than males reared under optimal conditions. Taken together, these studies indicate copulation duration to be negatively related to male quality in C. maculatus and could account for the negative phenotypic and genotypic association between copulation duration and longevity found in this species [47]. However, the relationship between copulation duration and ejaculate size is clearly a complex one as Edvardson & Canal [16] and van Leishout et al .…”

Section: Discussionmentioning

confidence: 93%

“…[52] report ejaculate weight to increase with increasing copulation duration, while Savalli & Fox [20] and Brown et al . [47] found no relationship. The upshot of these conflicting results is that caution should be exercised when interpreting the adaptive value of extended copulation without detailed knowledge of its relationship with sperm and ejaculate transfer.…”

Section: Discussionmentioning

confidence: 99%

Male–female interactions drive the (un)repeatability of copula duration in an insect

Eady

Brown

2017

R. Soc. open sci.

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Across the animal kingdom the duration of copulation varies enormously from a few seconds to several days. Functional explanations for this variation are largely embedded within sperm competition theory in which males modulate the duration of copula in order to optimize their fitness. However, copulation is the union of two protagonists which are likely to have separate and often conflicting reproductive interests, yet few experimental designs specifically assess the effect of male–female interactions on the duration of copulation. This can result in inexact assertions over which sex controls copulatory behaviour. Here we analyse the repeatability of copulatory behaviour in the seed beetle Callosobruchus maculatus to determine which sex exerts primary influence over copulation duration. In C. maculatus, copulation follows two distinct phases: an initial quiescent phase followed by a period of vigorous female kicking behaviour that culminates in the termination of copulation. When males or females copulated with several novel mates, copulatory behaviour was not significantly repeatable. By contrast, when males or females mated repeatedly with the same mate, copula duration was repeatable. These data suggest copulatory behaviour in C. maculatus to be largely the product of male–female interactions rather than the consistent, sex-specific modulation of copula duration of one protagonist in response to the phenotypic variation presented by the other protagonist.

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Negative phenotypic and genetic associations between copulation duration and longevity in male seed beetles

Cited by 20 publications

References 63 publications

The Heritability of Mating Behaviour in a Fly and Its Plasticity in Response to the Threat of Sperm Competition

The Heritability of Mating Behaviour in a Fly and Its Plasticity in Response to the Threat of Sperm Competition

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

Male–female interactions drive the (un)repeatability of copula duration in an insect

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