Pre- and postcopulatory sexual selection favor aggressive, young males in polyandrous groups of red junglefowl

McDonald, Grant C.; Spurgin, Lewis G.; Fairfield, Eleanor A.; Richardson, David S.; Pizzari, Tommaso

doi:10.1111/evo.13242

Cited by 54 publications

(96 citation statements)

References 99 publications

(222 reference statements)

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“…But pre-copulatory and post-copulatory sexual selection can favour different traits (Evans & Garcia-Gonzalez, 2016), so it is unclear whether a female preference for older males translates into greater male reproductive success, or higher female fitness. In particular, older males might produce ejaculates that are less successful under sperm competition (McDonald, Spurgin, Fairfield, Richardson, & Pizzari, 2017), or might be less fertile thereby lowering the reproductive output of monogamous females (Carazo, Molina-Vila, & Font, 2011;Dean et al, 2010). Furthermore, the accumulation of germline mutations might reduce the mean fitness of older males' offspring (Johnson & Gemmell, 2012;Johnson et al, 2018;Preston, Saint Jalme, Hingrat, Lacroix, & Sorci, 2015;Radwan, 2003a).…”

Section: Introductionmentioning

confidence: 99%

The effects of male age, sperm age and mating history on ejaculate senescence

et al. 2019

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In polyandrous species, a male’s reproductive success depends on his ability to fertilize females, which, in turn, depends on his mating ability and his ability to produce competitive ejaculates. In many species, sperm traits differ between old and young males in ways that are likely to decrease the sperm competitiveness and fertility of older males. This age–ejaculate quality relationship is attributed to male ageing (i.e., senescence). In a natural setting, male age and mating history are usually confounded: older males have usually mated and replenished their sperm supplies more often, so they have made a greater lifetime reproductive effort. In principle, the costs of reproduction, independent of any causal effect of male age, could generate an age‐related decline in ejaculate quality. To date, only a handful of studies have determined how male age, reproductive effort or their interaction affect ejaculate quality. Here, we experimentally manipulated the long‐term mating history of 209 adult male mosquitofish (Gambusia holbrooki) over 14 weeks (N = 1,118 sperm samples). Males either had direct access to females and could mate freely, or had only visual and olfactory access to females. We documented the effect of mating history, adult male age (3, 9 and 14 weeks post‐maturation) and their interaction on sperm velocity, sperm reserves and the rate of sperm replenishment. For sperm velocity, we additionally examined the effects of sperm age, because when older males mate less (or more) often than younger males there will be a correlation between mean sperm age and male age. Sexually active males produced fewer sperm and replenished their sperm at a lower rate, and their sperm had lower velocity than males prevented from mating. Though older males produced more sperm, the rate of replenishment and velocity of their sperm was lower than the sperm of younger males. We also tested for a difference in the velocity of recently replenished (<24 hr) and older sperm (i.e., post‐meiotic sperm senescence). There was no evidence that male age or mating history affects the extent of sperm senescence, but older sperm swam faster than recently produced sperm. Crucially, complex interactions are evident between male age and male mating history with respect to sperm number and the proportion of sperm that are replenished. These results suggest that male age and mating history will interact to determine the reproductive success of a male under sperm competition. They reveal a complex relationship between a male’s age and his ejaculate quality. We suggest that both mating history and sperm age should be controlled for when measuring the intrinsic rate of senescence for male reproductive traits if the goal is to isolate effects that are solely attributable to a male’s chronological age. A plain language summary is available for this article.

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Section: Introductionmentioning

confidence: 99%

The effects of male age, sperm age and mating history on ejaculate senescence

et al. 2019

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“…We would not necessarily expect to find a difference between comparisons of precopulatory success with post‐copulatory outcome, as opposed to associating post‐copulatory outcome with precopulatory success. However, most studies in other species have found that precopulatory success is a good predictor of post‐copulatory outcome (Evans, Zane, Francescato, & Pilastro, ; Hosken, Taylor, Hoyle, Higgins, & Wedell, ; Lewis & Austad, ; Polak & Simmons, ; Sbilordo & Martin, ; McDonald, Spurgin, Fairfield, Richardson, Pizzari, ), although it matters which traits are considered (Ala‐Honkola & Manier, ). Here, however, we did not find an association between sperm length and premating success, in concordance with Droge‐Young, Manier, Lüpold, Belote, and Pitnick () and Travers et al.…”

Section: Discussionmentioning

confidence: 99%

“…However, most studies in other species have found that precopulatory success is a good predictor of post-copulatory outcome (Evans, Zane, Francescato, & Pilastro, 2003;Hosken, Taylor, Hoyle, Higgins, & Wedell, 2008;Lewis & Austad, 1994;Polak & Simmons, 2009;Sbilordo & Martin, 2014;McDonald, Spurgin, Fairfield, Richardson, Pizzari, 2017), although it matters which traits are considered (Ala- . Here, however, we did not find an association between sperm length and premating success, in concordance with Droge-Young, Manier, Lüpold, Belote, and Pitnick (2012) and Travers et al (2016).…”

Section: Discussionmentioning

confidence: 99%

Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster

Zajitschek

Josway

et al. 2019

J of Evolutionary Biology

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In Drosophila, long sperm are favoured in sperm competition based on the length of the female's primary sperm storage organ, the seminal receptacle (SR). This sperm–SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm and SR lengths may be driven by Fisherian runaway selection. Here, we explore the costs and benefits of long sperm and SR genotypes, both in the sex that carries them and in the sex that does not. We measured male and female fitness in inbred lines of Drosophila melanogaster derived from four populations previously selected for long sperm, short sperm, long SRs or short SRs. We specifically asked: What are the costs and benefits of long sperm in males and long SRs in females? Furthermore, do genotypes that generate long sperm in males or long SRs in females impose a fitness cost on the opposite sex? Answers to these questions will address whether long sperm are an honest indicator of male fitness, male post‐copulatory success is associated with male precopulatory success, female choice benefits females or is costly, and intragenomic conflict could influence evolution of these traits. We found that both sexes have increased longevity in long sperm and long SR genotypes. Males, but not females, from long SR lines had higher fecundity. Our results suggest that sperm–SR coevolution is facilitated by both increased viability and indirect benefits of long sperm and SRs in both sexes.

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“…Several of these steps are mediated by components of the male ejaculate (Box 1). Decreases in male ability to elicit favourable female post-mating responses result in reduced paternity shares for older males (McDonald et al 2017.…”

Section: Senescence Of Male Post-mating Traitsmentioning

confidence: 99%

“…It can be measured as a decline in mating activity and fertilisation success with increasing age and is often due to somatic changes, like decreased hormonal levels leading to increased dysfunction or less agile courtship resulting in lost mating opportunities. To give some brief examples, in fowl Gallus gallus, older males are less aggressive, resulting in fewer matings and reduced reproductive success as aggression is one important determinant of male mating success (McDonald et al 2017). Apart from behaviour, a reduced investment in sexual ornaments, as observed in the decreased comb size in ageing fowl (Cornwallis et al 2014) or duller foot colour in the blue-footed booby Sula nebouxii (Velando et al 2011), can result in active discrimination by females.…”

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confidence: 99%

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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Pre- and postcopulatory sexual selection favor aggressive, young males in polyandrous groups of red junglefowl

Cited by 54 publications

References 99 publications

The effects of male age, sperm age and mating history on ejaculate senescence

The effects of male age, sperm age and mating history on ejaculate senescence

Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster

Male reproductive ageing: a tale of the whole ejaculate

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