Phenotypic engineering of sperm-production rate confirms evolutionary predictions of sperm competition theory

Sperm have traditionally been regarded as energetically cheap and effectively limitless in supply, although evidence conflicting with this view has become increasingly abundant. For instance, males from a variety of taxa have been shown to strategically partition sperm across ejaculates in response to perceived sperm competition risk. It follows that males might also be predicted to adaptively modulate the rate at which sperm are produced. Here we show that, in the giant sperm producing fruitfly Drosophila bifurca , solitary males with infrequent access to females produce sperm at a much lower rate than males raised in association with females and other males. Our results support the prediction that males with little risk of sperm competition risk or few mating opportunities should divert resources away from gamete production.

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Predicting variation in sperm precedence

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1997.0061 ◽

1997 ◽

Vol 352 (1355) ◽

pp. 771-780 ◽

Cited By ~ 56

Author(s):

Penny A. Cook ◽

Ian F. Harvey ◽

Geoffrey A. Parker

Keyword(s):

Sperm Competition ◽

Mean Value ◽

Sperm Production ◽

Additional Information ◽

Competition Theory ◽

Risk Increase ◽

Large Numbers ◽

Theoretical Predictions ◽

Sperm Competition Risk ◽

Lepidoptera Pyralidae

Sperm competition theory predicts that males are adapted for success in sperm competition by the production of large numbers of sperm. This is supported by both inter– and intraspecific studies showing that males mating under high sperm competition risk increase investment in sperm production. Such an increase in sperm production is an advantage if sperm mix randomly or if sperm displacement occurs. When two males mate with the same female, the measurement of the proportion of eggs fertilized by the second male to mate (termed P 2 ) has been used to help elucidate sperm competition mechanisms. P 2 is usually quoted as a mean value, with little attention being paid to its variance, although P 2 estimates are notoriously variable. By predicting an expected variance for P 2 , additional information on sperm competition mechanisms may be obtained. Here we present a technique for analysing the variance in P 2 when a given mechanism of P 2 is assumed. We apply this technique to P 2 data collected from Plodia interpunctella (Lepidoptera, Pyralidae), assuming a ‘fair raffle’ mechanism of sperm competition. We compare observed distributions of P 2 with theoretical distributions generated assuming random mixing of two ejaculates drawn randomly from a population of known mean and variance in sperm numbers. Ejaculates of known size were obtained by counting the number of sperm ejaculated by males mating for the first (large ejaculate) or second (small ejaculate) time. Females either received two small or one small and one large ejaculate, and the distribution of P 2 (estimated using the sterile male technique) was compared with our theoretical predictions. The observed variance in P 2 was greater than our model prediction, thus we conclude that sperm from P. interpunctella do not mix randomly before fertilization.

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Reproductive Anatomy and Indices of Quality in Male Tree Swallows: The Potential Reproductive Role of Floaters

The Auk ◽

10.1093/auk/117.1.74 ◽

2000 ◽

Vol 117 (1) ◽

pp. 74-81 ◽

Cited By ~ 2

Author(s):

Katharina Peer ◽

Raleigh J. Robertson ◽

Bart Kempenaers

Keyword(s):

Sperm Competition ◽

Reproductive Organs ◽

General Assumption ◽

Tree Swallows ◽

Sperm Production ◽

Extrapair Paternity ◽

Competition Theory ◽

Male Tree ◽

Testes Size

Abstract Avian populations often consist of breeding residents and nonbreeding floaters. It is usually assumed that floaters are lower-quality individuals that do not reproduce, but floater tactics and potential reproductive success have rarely been examined carefully. To assess the potential reproductive role of male floaters in Tree Swallows (Tachycineta bicolor), we compared their reproductive organs and morphology with those of resident males. Tree Swallows show high levels of extrapair paternity, but two studies attempting to find the fathers of the extrapair offspring have been remarkably unsuccessful. Floater males that father extrapair young would face intense sperm competition. Theory predicts that under intense sperm competition, selection favors males that produce more sperm. Comparative studies in birds and other taxa provide evidence that the level of sperm competition influences relative testes size and sperm production. However, intraspecific adaptations to different levels of sperm competition have received far less attention. Floater Tree Swallows did not differ from resident males in any of the characters we measured, including testes size, but floaters had significantly larger cloacal protuberances. Thus, our results do not confirm the general assumption that floaters are lower-quality individuals that do not reproduce. Furthermore, floaters showed high variation in the volume of the cloacal protuberance (reflecting sperm numbers), which suggests that they engage in copulations. We conclude that floater male Tree Swallows invest heavily in sperm production (as do resident males) to exploit breeding opportunities through takeovers or extrapair copulations.

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Fertilization dynamics of sperm from different male mating tactics in bluegill (Lepomis macrochirus)

Canadian Journal of Zoology ◽

10.1139/z05-164 ◽

2005 ◽

Vol 83 (12) ◽

pp. 1638-1642 ◽

Cited By ~ 14

Author(s):

Albrecht I Schulte-Hostedde ◽

Gary Burness

Keyword(s):

Sperm Competition ◽

Lepomis Macrochirus ◽

Fertilization Success ◽

Male Mating ◽

Motile Sperm ◽

Mating Tactics ◽

Sperm Activation ◽

Competition Theory ◽

Sperm Density ◽

Over Time

Sperm competition results in the evolution of ejaculate characteristics such as high sperm density, high motility, and fast sperm swimming speed. A fundamental assumption of sperm competition theory is that ejaculates with high motility and fast-swimming sperm have an advantage with respect to fertilization success. We tested this assumption by studying the fertilization dynamics of alternative mating tactics (cuckolders and parentals) of male bluegill (Lepomis macrochirus Rafinesque, 1819). Sneakers (cuckolders) have faster swimming sperm and a higher proportion of motile sperm immediately following sperm activation than do parentals; however, these variables decline more quickly over time in sneaker sperm than in the sperm of parental males. We used a controlled fertilization experiment to test the prediction that parental males will have higher fertilization success than sneakers late in the sperm activation cycle because of the reduced rate of decline in ejaculate quality over time. We found that as the time from sperm activation increases parental sperm fertilizes more eggs than the sperm of sneakers. Our results support the idea that fertilization success is higher when ejaculates contain a higher proportion of either motile sperm or faster swimming sperm, all else being equal. In addition, after controlling for time from sperm activation, we found a significant bias in fertilization success toward parental males, suggesting that cryptic female choice might play a role in fertilization dynamics.

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Sperm competition games: optimal sperm allocation in response to the size of competing ejaculates

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2006.3722 ◽

2006 ◽

Vol 274 (1607) ◽

pp. 209-217 ◽

Cited By ~ 13

Author(s):

Leif Engqvist ◽

Klaus Reinhold

Keyword(s):

Sperm Competition ◽

Negative Correlation ◽

Competitive Ability ◽

Sperm Storage ◽

Competition Intensity ◽

Mating Partner ◽

Storage Model ◽

Sperm Allocation ◽

Competition Theory ◽

Different Levels

Sperm competition theory predicts that when males are certain of sperm competition, they should decrease sperm investment in matings with an increasing number of competing ejaculates. How males should allocate sperm when competing with differently sized ejaculates, however, has not yet been examined. Here, we report the outcomes of two models assuming variation in males' sperm reserves and males being faced with different amounts of competing sperm. In the first ‘spawning model’, two males compete instantaneously and both are able to assess the sperm competitive ability of each other. In the second ‘sperm storage model’, males are sequentially confronted with situations involving different levels of sperm competition, for instance different amounts of sperm already stored by the female mating partner. In both of the models, we found that optimal sperm allocation will strongly depend on the size of the male's sperm reserve. Males should always invest maximally in competition with other males that are equally strong competitors. That is, for males with small sperm reserves, our model predicts a negative correlation between sperm allocation and sperm competition intensity, whereas for males with large sperm reserves, this correlation is predicted to be positive.

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Imminent risk of predation reduces the relative strength of postcopulatory sexual selection in the guppy

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0076 ◽

2020 ◽

Vol 375 (1813) ◽

pp. 20200076

Author(s):

Alexandra Glavaschi ◽

Silvia Cattelan ◽

Alessandro Grapputo ◽

Andrea Pilastro

Keyword(s):

Sexual Selection ◽

Sperm Competition ◽

Repeated Measures ◽

Poecilia Reticulata ◽

Male Reproductive Success ◽

Sperm Production ◽

Postcopulatory Sexual Selection ◽

Repeated Measures Design ◽

Risk Of Predation ◽

Livebearing Fish

Fifty years of research on sperm competition has led to a very good understanding of the interspecific variation in sperm production traits. The reasons why this variation is often very large within populations have been less investigated. We suggest that the interaction between fluctuating environmental conditions and polyandry is a key phenomenon explaining such variation. We focus here on imminent predation risk (IPR). IPR impacts significantly several aspects of prey behaviour and reproduction, and it is expected to influence the operation of sexual selection before and after mating. We estimated the effect of IPR on the male opportunity for pre- and postcopulatory sexual selection in guppies ( Poecilia reticulata ), a livebearing fish where females prefer colourful males and mate multiply. We used a repeated-measures design, in which males were allowed to mate with different females either under IPR or in a predator-free condition. We found that IPR increased the total opportunity for sexual selection and reduced the relative contribution of postcopulatory sexual selection to male reproductive success. IPR is inherently variable and our results suggest that interspecific reproductive interference by predators may contribute towards maintaining the variation in sperm production within populations. This article is part of the theme issue ‘Fifty years of sperm competition'.

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Conceptual developments in sperm competition: a very brief synopsis

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0061 ◽

2020 ◽

Vol 375 (1813) ◽

pp. 20200061 ◽

Cited By ~ 2

Author(s):

Geoff A. Parker

Keyword(s):

Sexual Selection ◽

Sperm Competition ◽

Seminal Fluid ◽

Female Reproduction ◽

Internal Fertilization ◽

Seminal Fluid Proteins ◽

Competition Theory ◽

Past Half Century ◽

Mate Acquisition ◽

Gamete Competition

The past half century has seen the development of the field of post-ejaculatory sexual selection, the sequel to sexual selection for mate-acquisition (pre-ejaculatory) described by Darwin. In richness and diversity of adaptations, post-ejaculatory selection rivals that of pre-ejaculatory sexual selection. Anisogamy—and hence two sexes—likely arose by primeval gamete competition, and sperm competition remains a major force maintaining high sperm numbers. The post-ejaculatory equivalent of male–male competition for matings, sperm competition was an intense ancestral form of sexual selection, typically weakening as mobility and internal fertilization developed in many taxa, when some expenditure became diverted into pre-ejaculatory competition. Sperm competition theory has been relatively successful in explaining variation in relative testes size and sperm numbers per ejaculate and is becoming more successful in explaining variation in sperm phenotype. Sperm competition has generated many other male adaptations such as seminal fluid proteins that variously modify female reproduction towards male interests, and copulatory plugs, prolonged copulations and post-ejaculatory guarding behaviour that reduce female remating probability, many of which result in sexual conflict. This short survey of conceptual developments is intended as a broad overview, mainly as a primer for new researchers. This article is part of the theme issue ‘Fifty years of sperm competition'.

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Male crickets adjust ejaculate quality with both risk and intensity of sperm competition

Biology Letters ◽

10.1098/rsbl.2007.0328 ◽

2007 ◽

Vol 3 (5) ◽

pp. 520-522 ◽

Cited By ~ 64

Author(s):

Leigh W Simmons ◽

Amy Denholm ◽

Chantelle Jackson ◽

Esther Levy ◽

Ewa Madon

Keyword(s):

Sperm Competition ◽

High Intensity ◽

Teleogryllus Oceanicus ◽

Competition Theory ◽

Rival Male ◽

Testes Size ◽

Increasing Risk ◽

Live Sperm

Sperm competition theory predicts that males should increase their expenditure on the ejaculate with increasing risk of sperm competition, but decrease their expenditure with increasing intensity. There is accumulating evidence for sperm competition theory, based on examinations of testes size and/or the numbers of sperm ejaculated. However, recent studies suggest that ejaculate quality can also be subject to selection by sperm competition. We used experimental manipulations of the risk and intensity of sperm competition in the cricket, Teleogryllus oceanicus . We found that males produced ejaculates with a greater percentage of live sperm when they had encountered a rival male prior to mating. However, when mating with a female that presented a high intensity of sperm competition, males did not respond to risk, but produced ejaculates with a reduced percentage of live sperm. Our data suggest that males exhibit a fine-tuned hierarchy of responses to these cues of sperm competition.

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