The effect of mating history on male reproductive ageing in Drosophila melanogaster

Koppik, Mareike; Ruhmann, Hanna; Fricke, Claudia

doi:10.1016/j.jinsphys.2018.10.003

Cited by 16 publications

(26 citation statements)

References 70 publications

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“…This is in line with observations that the socio-sexual environment leads males to allocate more resources into reproduction when rivals are present (Bretman et al 2011), with males held in isolation showing a slower reduction in lifespan (Leech et al 2017). In D. melanogaster, male mating history did not accelerate reproductive ageing for pre-mating traits, but caused a distinct pattern for post-mating traits (Koppik et al 2018). For these latter traits, prior mating opportunities proved beneficial in young males but neutral or negative in older males, potentially due to different reproductive investments and a trade-off between early and late reproductive efforts.…”

Section: Factors Affecting Reproductive Ageingsupporting

confidence: 89%

“…In D. pseudoobscura copulation duration roughly doubled from 2-4 to 14-19-day-old males and these older males indeed induced a higher egg-laying rate (Dhole & Pfennig 2014), indicating that more of the relevant Sfps were transferred as observed in D. bipectinata (Santhosh & Krishna 2013). Ageing D. melanogaster males, on the other hand, transfer smaller ejaculates despite longer mating durations and larger AGs (Koppik et al 2018). Hence, while copulation duration can be a good indicator of male investment, some caution is warranted.…”

Section: Ageing Of the Non-sperm Fraction Of The Ejaculatementioning

confidence: 99%

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Male reproductive ageing: a tale of the whole ejaculate

Fricke

Koppik

2019

Reproduction

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Ageing is nearly ubiquitous and encompasses all biological functions. We here focus on age-dependent changes in male reproductive capacity across a broad range of animal taxa. While there has been a long-standing focus on mating ability and overall reproductive success, we here highlight the underlying mechanisms that explain loss in fertilisation capacity in ageing males. Fertilisation is mediated by not only the presence of sperm, but also the cocktail of seminal fluid proteins that ensure sperm survival, capacitation and interaction with female physiology. Sperm ageing has received much attention in studies of male reproductive senescence; however, post-mating processes include a number of interlocked steps that together cumulate in successful fertilisation. As such we consider male ability to elicit female post mating responses such as uterine conformational changes, sperm storage and ovulation and the components within the ejaculate that mediate these post-mating processes. For the latter seminal fluid proteins are key and hence we reflect on age-dependent changes in quality of the entire ejaculate and its consequences for male reproductive capacity. While first studies accrue and highlight that changes in the non-sperm fraction can explain substantial variation in senescent male reproductive success and male ability to induce post-mating responses necessary for fertilisation many open questions still remain that warrant further investigations. One being what the potential age-dependent changes in composition are or whether there is a general decline and how this interacts with sperm to affect fertilisation success. Further, the impact females might have to ameliorate these changes will be an area of interest.

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Section: Factors Affecting Reproductive Ageingsupporting

confidence: 89%

Section: Ageing Of the Non-sperm Fraction Of The Ejaculatementioning

confidence: 99%

Male reproductive ageing: a tale of the whole ejaculate

Fricke

Koppik

2019

Reproduction

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“…1 A ). These time points span male peak reproductive performance (1w, young) and reproductively senesced states (5w, old) while ensuring that most males survive the experiment ( 13 ) ( SI Appendix , Fig. S1 ).…”

Section: Resultsmentioning

confidence: 99%

“…A recent study has shown associations between distinct seminal proteome profiles and sperm speed in aging red junglefowl males ( 10 ). In D. melanogaster , males exhibit age-related changes in the expression of some seminal fluid protein (Sfp) genes ( 11 ), and increased male age reduces fertility and other aspects of ejaculate performance, such as sperm competitiveness and inhibition of female sexual receptivity ( 11 – 13 ). However, whether these age-related seminal proteome changes translate into reduced ejaculate performance remains to be tested, and its importance relative to changes to sperm remains unknown.…”

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confidence: 99%

Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila

Sepil

Hopkins

Dean

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Declining ejaculate performance with male age is taxonomically widespread and has broad fitness consequences. Ejaculate success requires fully functional germline (sperm) and soma (seminal fluid) components. However, some aging theories predict that resources should be preferentially diverted to the germline at the expense of the soma, suggesting differential impacts of aging on sperm and seminal fluid and trade-offs between them or, more broadly, between reproduction and lifespan. While harmful effects of male age on sperm are well known, we do not know how much seminal fluid deteriorates in comparison. Moreover, given the predicted trade-offs, it remains unclear whether systemic lifespan-extending interventions could ameliorate the declining performance of the ejaculate as a whole. Here, we address these problems using Drosophila melanogaster. We demonstrate that seminal fluid deterioration contributes to male reproductive decline via mating-dependent mechanisms that include posttranslational modifications to seminal proteins and altered seminal proteome composition and transfer. Additionally, we find that sperm production declines chronologically with age, invariant to mating activity such that older multiply mated males become infertile principally via reduced sperm transfer and viability. Our data, therefore, support the idea that both germline and soma components of the ejaculate contribute to male reproductive aging but reveal a mismatch in their aging patterns. Our data do not generally support the idea that the germline is prioritized over soma, at least, within the ejaculate. Moreover, we find that lifespan-extending systemic down-regulation of insulin signaling results in improved late-life ejaculate performance, indicating simultaneous amelioration of both somatic and reproductive aging.

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“…Reductions in ejaculate quality mediated by male condition can therefore have important fitness consequences for females (Dean et al, 2010). Conversely, males transferring low quality ejaculates may stimulate weaker post-mating responses in females, reducing the potential harm to females, hence extending female lifespan and increasing female lifetime reproductive success (Koppik & Fricke, 2017; Koppik, Ruhmann, & Fricke, 2018; Ruhmann et al, 2018). Mating-induced changes in females may therefore be highly variable and dependent on both male and female characteristics that shape ejaculate composition, transfer, and storage.…”

Section: Introductionmentioning

confidence: 99%

Influences of male age, mating history and starvation on female post mating aggression and feeding inDrosophila

Bath

Buzzoni

Ralph

et al. 2020

Preprint

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Mating changes female behaviour and physiology across a wide range of taxa, with important effects for male and female fitness. These changes are often induced by components of the male ejaculate, such as sperm and seminal fluid proteins.However, males can vary significantly in their ejaculates, due to factors such as age, mating history, or nutritional status. This male variation may therefore lead to variation in the strength of responses males can stimulate in females, with alterations in fitness outcomes for both sexes.Using the fruit fly, Drosophila melanogaster, we tested whether three aspects of male condition shape an important, but understudied, post-mating response – increased female-female aggression.We found that females mated to old males fought less than females mated to young males. This effect was exacerbated in mates of old, sexually active males, but there was no effect of male starvation status on mating-induced female aggression. There was also a significant effect of age and mating history on female post-mating feeding duration.Our results add to a growing body of literature that variation in male condition can shape sexual selection through post-mating responses in females, including female-female interactions. Studying such variation may therefore be useful for understanding how the condition of sex affects the behaviour of the other.

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The effect of mating history on male reproductive ageing in Drosophila melanogaster

Cited by 16 publications

References 70 publications

Male reproductive ageing: a tale of the whole ejaculate

Male reproductive ageing: a tale of the whole ejaculate

Male reproductive aging arises via multifaceted mating-dependent sperm and seminal proteome declines, but is postponable in Drosophila

Influences of male age, mating history and starvation on female post mating aggression and feeding inDrosophila

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