Sperm depletion in relation to developmental nutrition and genotype in
            <i>Drosophila melanogaster</i>

Macartney, Erin L.; Zeender, Valérian; Meena, Abhishek; Nardo, Alessio N De; Bonduriansky, Russell; Lüpold, Stefan

doi:10.1111/evo.14373

Cited by 17 publications

(22 citation statements)

References 82 publications

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“…However, even if high‐quality males mate more often, they might continue to transfer more SP compared with low‐quality males, either because they store more SP or because they replenish SP more rapidly, which will tend to restore quality dependence in SP transfer. An analogous process presumably underlies the condition dependence of male reproductive potential in some Drosophila species, in which only high‐quality males can maintain the transfer of very long, costly sperm over successive matings (Lüpold et al ., 2016; see also Macartney et al ., 2021). Even in the face of noisiness in the relationship between SP transfer and male quality, females might integrate information from multiple sources to assess male quality more accurately.…”

Section: The Evolution Of Sp Functionmentioning

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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Section: The Evolution Of Sp Functionmentioning

confidence: 99%

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

Hopkins

Perry

2022

Biological Reviews

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“…To win the intense sperm competition, Drosophila males produce long spermatozoa, resulting in larger costs of sperm production. Indeed, it is found that nutrient diet during development affects the amount of sperm transferred to female in D. melanogaster (Macartney et al 2021) and that the number of sperm bundles that the male contains is positively correlated with male body size in D. hydei (Pitnick and Markow 1994a). In spider mites, females use sperm only from the rst mating if the mating is not disturbed, yet readily mate multiple times (Rodrigues et al 2020) indicating that sperm competition is present but not as strong as in fruit ies.…”

Section: Discussionmentioning

confidence: 99%

Sperm-depleted males of the two-spotted spider mite can replenish sperm in a few hours

Yokoi,

Sano,

Nagase

et al. 2023

Preprint

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In many animals, males increase their reproductive success by mating as many females as possible. The number of females a male can fertilize is often limited by male competition for access to females, sperm competition, and the cost of sperm production. Especially, recent studies have shown that sperm production is more costly than previously expected. In the two-spotted spider mite, Tetranychus urticae Koch, the number of females a male can inseminate is limited mainly by male competition for access to females. However, in the absence of rivals, males mate with so many females that they can become sperm-depleted. Mating without sperm transfer does not produce any offspring, although it takes time and energy. Therefore, a question arises why males continue to mate even after sperm depletion. In this study, we hypothesized that males continue to mate because sperm is replenished after a short period. To test the hypothesis, we investigated how long it takes for sperm replenishment after sperm depletion. We found that in 3 h, sperm can be replenished enough to inseminate a few females. As 3 h is sufficiently short not to lose the next mating opportunity, the results support the hypothesis. However, the copulation duration after sperm replenishment was significantly shorter than before sperm depletion, indicating that males continue to mate but may alter their mating behavior depending on the amount of sperm they retain.

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“…To this end, we manipulated the resources available to developing males, allowed these males to mate with a virgin female after reaching sexual maturity, and then identified ejaculate proteins from the female bursa copulatrix immediately after copulation. Although arthropod ejaculates can also be affected by adult diet [29], we manipulated larval diet as the metabolism, tissue growth and reproductive function of holometabolous insects are particularly sensitive to diet during development [30][31][32][33][34][35]. Larval diet manipulation may therefore affect a male's resource allocation to sexual traits, including costly ejaculate components at least in early adult life [36][37][38][39].…”

Section: Introductionmentioning

confidence: 99%

Genotype-by-environment interactions influence the composition of the Drosophila seminal proteome

Zeender,

Pfammatter,

Roschitzki

et al. 2023

Proc. R. Soc. B.

Self Cite

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Ejaculate proteins are key mediators of post-mating sexual selection and sexual conflict, as they can influence both male fertilization success and female reproductive physiology. However, the extent and sources of genetic variation and condition dependence of the ejaculate proteome are largely unknown. Such knowledge could reveal the targets and mechanisms of post-mating selection and inform about the relative costs and allocation of different ejaculate components, each with its own potential fitness consequences. Here, we used liquid chromatography coupled with tandem mass spectrometry to characterize the whole-ejaculate protein composition across 12 isogenic lines of Drosophila melanogaster that were reared on a high- or low-quality diet. We discovered new proteins in the transferred ejaculate and inferred their origin in the male reproductive system. We further found that the ejaculate composition was mainly determined by genotype identity and genotype-specific responses to larval diet, with no clear overall diet effect. Nutrient restriction increased proteolytic protein activity and shifted the balance between reproductive function and RNA metabolism. Our results open new avenues for exploring the intricate role of genotypes and their environment in shaping ejaculate composition, or for studying the functional dynamics and evolutionary potential of the ejaculate in its multivariate complexity.

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

Cited by 17 publications

References 82 publications

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

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

Sperm-depleted males of the two-spotted spider mite can replenish sperm in a few hours

Genotype-by-environment interactions influence the composition of the Drosophila seminal proteome

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