Female sperm storage mediates post‐copulatory costs and benefits of ejaculate anticipatory plasticity in the guppy

Cardozo, Gabriela; Devigili, Alessandro; Antonelli, Pietro; Pilastro, Andrea

doi:10.1111/jeb.13673

Cited by 15 publications

(15 citation statements)

References 108 publications

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“…2002; Kelly and Jennions 2011; Cattelan and Pilastro 2018; Cardozo et al. 2020) also indicates that ejaculates are a limited resource, consistent with their production being costly. However, we recently showed that male G. holbrooki have a lower risk of sperm depletion and do not adjust ejaculate components in response to social status or female cues (Chung et al.…”

Section: Discussionmentioning

confidence: 91%

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

2021

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Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre‐ and postcopulatory investment on components of male fitness in a vertebrate.

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Section: Discussionmentioning

confidence: 91%

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

2021

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“…Evidence of such a trade-off has been found in many species, e.g. 53 – 55 . As recently suggested by Reinhardt and Turnell 31 , this trade-off could be mediated by sperm metabolic rate.…”

Section: Discussionmentioning

confidence: 97%

“…On one hand, high mating opportunities may allow males to release sperm frequently, thus minimizing the need for the evolution of a strategy to avoid the consequences of long sperm storage. On the other hand, since under high mating availability and sperm competition (the competition between sperm from different males 65 ) males producing more sperm usually fertilize more eggs 66 , males may have been selected for continuously producing sperm to avoid sperm limitation even at the cost of sperm quality 55 . Moreover, it is worth noting that in our study we individually isolated males during sexual rest to avoid the confunding effects of social environment, which could have made difficult the interpretation of results.…”

Section: Discussionmentioning

confidence: 99%

Male sperm storage impairs sperm quality in the zebrafish

Cattelan

Gasparini

2021

Sci Rep

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Variation in sperm traits is widely documented both at inter- and intraspecific level. However, sperm traits vary also between ejaculates of the same male, due for example, to fluctuations in female availability. Variability in the opportunities to mate can indeed have important consequences for sperm traits, as it determines how often sperm are used, and thus the rate at which they are produced and how long they are stored before the mating. While being stored within males’ bodies, sperm are subjected to ageing due to oxidative stress. Sperm storage may significantly impair sperm quality, but evidence linking male sperm storage and variation in sperm traits is still scarce. Here, we tested the effect of the duration of sperm storage on within-male variation in sperm traits in the zebrafish, Danio rerio. We found that without mating opportunities, sperm number increased as storage duration increased, indicating that sperm continue to be produced and accumulate over time within males without being discharged in another way. Long sperm storage (12 days) was associated with an overall impairment in sperm quality, namely sperm motility, sperm longevity, and sperm DNA fragmentation, indicating that sperm aged, and their quality declined during storage. Our results confirm that male sperm storage may generate substantial variation in sperm phenotype, a source of variation which is usually neglected but that should be accounted for in experimental protocols aiming to assay sperm traits or maximise fertilization success.

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“…R. Soc. B 288: 20210979 other ejaculate traits, namely sperm morphology, sperm viability and seminal fluid content, must explain the higher fertilization success of older males [46,[56][57][58]. We recommend that future studies measure a greater range of ejaculate traits when testing for the effect of age and mating history on male reproductive senescence.…”

Section: (B) Sperm Velocitymentioning

confidence: 99%

Male age alone predicts paternity success under sperm competition when effects of age and past mating effort are experimentally separated

et al. 2021

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Older males often perform poorly under post-copulatory sexual selection. It is unclear, however, whether reproductive senescence is because of male age itself or the accumulated costs of the higher lifetime mating effort that is usually associated with male age. To date, very few studies have accounted for mating history and sperm storage when testing the effect of male age on sperm traits, and none test how age and past mating history influence paternity success under sperm competition. Here, we experimentally manipulate male mating history to tease apart its effects from that of age on ejaculate traits and paternity in the mosquitofish, Gambusia holbrooki . We found that old, naive males had more sperm than old, experienced males, while the reverse was true for young males. By contrast, neither male age nor mating history affected sperm velocity. Finally, using artificial insemination to experimentally control the number of sperm per male, we found that old males sired significantly more offspring than young males independently of their mating history. Our results highlight that the general pattern of male reproductive senescence described in many taxa may often be affected by two naturally confounding factors, male mating history and sperm age, rather than male age itself.

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Female sperm storage mediates post‐copulatory costs and benefits of ejaculate anticipatory plasticity in the guppy

Cited by 15 publications

References 108 publications

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort

Male sperm storage impairs sperm quality in the zebrafish

Male age alone predicts paternity success under sperm competition when effects of age and past mating effort are experimentally separated

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