Frequent mating reduces male mating rate but not offspring quality or quantity in a neriid fly

Macartney, Erin L.; Bonduriansky, Russell; Crean, Angela J.

doi:10.1007/s10682-020-10076-8

Cited by 6 publications

(10 citation statements)

References 49 publications

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“…This could be because they have fewer resources available to invest into mating (review Torres-Vila and Jennions 2005). This result is consistent with other studies where experimental elevation of mating effort leads to a subsequent decline in sexually selected male behaviors (e.g., King and Fischer 2010;Wang et al 2016;Koppik et al 2018;Macartney et al 2020, but see: Hughes et al 2000Iglesias-Carrasco et al 2019a;Thonhauser et al 2019). Given the effect of mating history on sexual behavior in G. holbrooki and the fact that age and mating history are tightly correlated, our finding bolsters our recommendation that it is necessary to control for male mating history when testing for age effects on sexually selected male traits.…”

Section: Male Mating Behaviorsupporting

confidence: 93%

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success

et al. 2021

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Many studies ask whether young or older males are better at acquiring mates. Even so, how age affects reproductive success is still poorly understood because male age and mating history are confounded in most studies: older males usually have more mating experience. To what extent does mating history rather than age explain variation in male mating success? And how do mating history and male age determine paternity when there is also postcopulatory sexual selection? Here, we experimentally manipulated the mating history of old and young males in the eastern mosquitofish (Gambusia holbrooki). We then recorded male mating behavior and share of paternity (1259 offspring from 232 potential sires) when they competed for mates and fertilizations.Old males, and males with no mating experience, spent significantly more time approaching females, and attempting to mate, than did young males and those with greater mating experience. Male age and mating history interacted to affect paternity: old males benefited from having previous mating experience, but young males did not. Our results highlight that the age-related changes in male reproductive traits and in paternity that have been described in many taxa may be partly attributable to male mating history and not simply to age itself.

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Section: Male Mating Behaviorsupporting

confidence: 93%

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success

et al. 2021

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“…Whether it really pays males to forgo mating opportunities to pursue fewer, higher investment matings (e.g. Macartney, Bonduriansky & Crean, 2020) will depend on the frequency of mating opportunities, the per-mating benefit of transferring more SP, and the distribution of male quality within populations, and represents fertile ground for theory.…”

Section: (B) Spr's Sensitivity To Sp Can Evolve Without Disrupting Sp...mentioning

confidence: 99%

The evolution of sex peptide: sexual conflict, cooperation, and coevolution

Hopkins

Perry

2022

Biological Reviews

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A central paradigm in evolutionary biology is that the fundamental divergence in the fitness interests of the sexes ('sexual conflict') can lead to both the evolution of sex-specific traits that reduce fitness for individuals of the opposite sex, and sexually antagonistic coevolution between the sexes. However, clear examples of traits that evolved in this waywhere a single trait in one sex demonstrably depresses the fitness of members of the opposite sex, resulting in antagonistic coevolutionare rare. The Drosophila seminal protein 'sex peptide' (SP) is perhaps the most widely cited example of a trait that appears to harm females while benefitting males. Transferred in the ejaculate by males during mating, SP triggers profound and wide-ranging changes in female behaviour and physiology. Early studies reported that the transfer of SP enhances male fitness while depressing female fitness, providing the foundations for the widespread view that SP has evolved to manipulate females for male benefit. Here, we argue that this view is (i) a simplification of a wider body of contradictory empirical research, (ii) narrow with respect to theory describing the origin and maintenance of sexually selected traits, and (iii) hard to reconcile with what we know of the evolutionary history of SP's effects on females. We begin by charting the history of thought regarding SP, both at proximate (its production, function, and mechanism of action) and ultimate (its fitness consequences and evolutionary history) levels, reviewing how studies of SP were central to the development of the field of sexual conflict. We describe a prevailing paradigm for SP's evolution: that SP originated and continues to evolve to manipulate females for male benefit. In contrast to this view, we argue on three grounds that the weight of evidence does not support the view that receipt of SP decreases female fitness: (i) results from studies of SP's impact on female fitness are mixed and more often neutral or positive, with fitness costs emerging only under nutritional extremes; (ii) whether costs from SP are appreciable in wild-living populations remains untested; and (iii) recently described confounds in genetic manipulations of SP raise the possibility that measures of the costs and benefits of SP have been distorted. Beyond SP's fitness effects, comparative and genetic data are also difficult to square with the idea that females suffer fitness costs from SP. Instead, these datafrom functional and evolutionary genetics and the neural circuitry of female responses to SPsuggest an evolutionary history involving the evolution of a dedicated SP-sensing apparatus in the female reproductive tract that is likely to have evolved because it benefits females, rather than harms them. We end by exploring theory and evidence that SP benefits females by functioning as a signal of male quality or of sperm receipt and storage (or both). The expanded view of the evolution of SP that we outline recognises the context-dependent and fluctuating roles played by both cooperativ...

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“…These results clearly demonstrate that males do not have unlimited sperm supplies, and they are indicative of significant costs related to ejaculate production (Dewsbury 1982;Pitnick 1996;Olsson et al 1997;Thomsen et al 2006;Lüpold et al 2016). That male sperm depletion was further accompanied by an increasing refractory period between successive matings could indicate that males may reduce their mating rate to conserve ejacu-late stores and/or to replenish depleted stores to some degree (also see Macartney et al 2020). However, this declining mating rate could also result from physical exhaustion or reduced motivation (Franklin et al 2012), or from more time spent assessing females to maximize fitness benefits with the increasingly limited sperm reserves (Dewsbury 1982).…”

Section: Discussionmentioning

confidence: 76%

“…That male sperm depletion was further accompanied by an increasing refractory period between successive matings could indicate that males may reduce their mating rate to conserve ejaculate stores and/or to replenish depleted stores to some degree (also see Macartney et al. 2020 ). However, this declining mating rate could also result from physical exhaustion or reduced motivation (Franklin et al.…”

Section: Discussionmentioning

confidence: 99%

“…The rate of ejaculate depletion could also shape male reproductive strategies. For example, males could be selected to adjust their mating behavior to mitigate ejaculate depletion, sacrificing mating opportunities to maintain full ejaculate transfer across successive matings (Macartney et al 2020). The rate of ejaculate depletion could depend on nutrient availability as well as genetic effects on resource allocation per mating (Hopkins et al 2019).…”

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confidence: 99%

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Sperm depletion in relation to developmental nutrition and genotype in Drosophila melanogaster

et al. 2021

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Nutrient limitation during development can restrict the ability of adults to invest in costly fitness traits, and genotypes can vary in their sensitivity to developmental nutrition. However, little is known about how genotype and nutrition affect male ability to maintain ejaculate allocation and achieve fertilization across successive matings. Using 17 isogenic lines of Drosophila melanogaster, we investigated how variation in developmental nutrition affects males' abilities to mate, transfer sperm, and sire offspring when presented with successive virgin females. We found that, with each successive mating, males required longer to initiate copulation, transferred fewer sperm, and sired fewer offspring. Males reared on a low-nutrient diet transferred fewer sperm than those reared on nutritionally superior diets, but the rate at which males depleted their sperm, as well as their reproductive performance, was largely independent of diet. Genotype and the genotype × diet interaction explained little of the variation in these male reproductive traits. Our results show that sperm depletion can occur rapidly and impose substantial fitness costs for D. melanogaster males across multiple genotypes and developmental environments.

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Frequent mating reduces male mating rate but not offspring quality or quantity in a neriid fly

Cited by 6 publications

References 49 publications

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success

Disentangling the effects of male age and mating history: Contrasting effects of mating history on precopulatory mating behavior and paternity success

The evolution of sex peptide: sexual conflict, cooperation, and coevolution

Sperm depletion in relation to developmental nutrition and genotype in Drosophila melanogaster

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