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Why is polyandry such a common mating behaviour when it exposes females to a range of significant fitness costs? Here, we investigated whether polyandry protects females against reduced male fertility caused by thermal stress from heatwave conditions. Sperm production and function are vulnerable to heat, and heatwave conditions are forecast to increase as our climate warms, so we examined these effects on female reproduction and mating behaviour in the flour beetle, Tribolium castaneum, a promiscuous ectotherm model in which fertility is damaged by environmental warming. We tested whether polyandrous matings, or polyandrous sperm stores, protect females against reduced male fertility caused by heatwave conditions, and whether females flexibly adjust their remating behaviour to enable fertility rescue. We found that polyandry protected females against reduced male fertility: monogamous matings with males exposed to heatwave conditions halved female offspring production, but opportunities to mate with five of these males allowed normal female reproductive output. By contrast with this fertility improvement following polyandrous mating opportunities, there was no protective benefit for females already carrying sperm stores from multiple males, which suffered similar heatwave damage within the female tract as monogamous sperm stores. Importantly, female polyandry was flexible to male condition, with females showing greater motivation to remate with new males if their previous mate had been damaged by heatwave exposure, enabling a rapid reproductive rescue. Our results reveal that flexible polyandry enables females to rescue their fertility when male reproductive function is compromised by heatwave conditions, a phenomenon that may become more prevalent under climate change.

Because of divergent selection acting on males and females arising from different life-history strategies, polyandry can be expected to promote sexual dimorphism of investment into immune function. In previous work we have established the existence of such divergence within populations where males and females are exposed to varying degrees of polyandry. We here test whether the removal of sexual selection via enforced monogamy generates males and females that have similar levels of investment in immune function. To test this prediction experimentally, we measured differences between the sexes in a key immune measurement (phenoloxidase (PO) activity) and resistance to the microsporidian Paranosema whitei in Tribolium castaneum lines that evolved under monogamous (sexual selection absent) vs polyandrous (sexual selection present) mating systems. At generation 49, all selected lines were simultaneously assessed for PO activity and resistance to their natural parasite P. whitei after two generations of relaxed selection. We found that the polyandrous regime was associated with a clear dimorphism in immune function: females had significantly higher PO activities than males in these lines. In contrast, there was no such difference between the sexes in the lines evolving under the monogamous regime. Survival in the infection experiment did not differ between mating systems or sexes. Removing sexual selection via enforced monogamy thus seems to erase intersexual differences in immunity investment. We suggest that higher PO activities in females that have evolved under sexual selection might be driven by the increased risk of infections and/or injuries associated with exposure to multiple males.

Behavioural plasticity allows animals to attune their behaviour to rapid environmental changes. Here we focus on plasticity in male mating behaviour in response to socio-sexual conditions. We discuss existing theory, generate predictions to facilitate exploration of the benefits of plastic behaviour, and identify parameters with the highest leverage on fitness. Existing data are synthesised to assess whether plasticity occurs pre- and post-copulation, to determine the direction of changes in behaviour, and to examine if plastic behaviour is fully flexible. We find that plasticity in males is widespread and not dominated by responses that occur pre- or post-copulation. Our synthesis also highlights areas that are underexplored, such as the limited data on the ultimate fitness consequences of such plastic behaviour.

SummaryAcross many species, males exhibit plastic responses when they encounter mating rivals [1]. The ability to tailor responses to the presence of rivals allows males to increase investment in reproduction only when necessary. This is important given that reproduction imposes costs [2] that limit male reproductive capacity, particularly when sperm competition occurs [3, 4]. Fruitfly (Drosophila melanogaster) males exposed to rivals subsequently mate for longer and thus accrue fitness benefits under increased competition [5], in line with theory [6, 7]. Here, we show that male D. melanogaster detect rivals by using a suite of cues and that the resulting responses lead directly to significant fitness benefits. We used multiple techniques to systematically remove auditory, olfactory, tactile, and visual cues, first singly and then in all possible combinations. No single cue alone was sufficient to allow males to detect rivals. However, the perception of any two cues from sound, smell, or touch permitted males to detect and respond adaptively to rivals through increased offspring production. Vision was only of marginal importance in this context. The findings indicate adaptive redundancy through the use of multiple, but interchangeable, cues. We reveal the robust mechanisms by which males assess their socio-sexual environment to precisely attune responses via the expression of plastic behavior.

Sex change is widespread among marine fishes, including many species that are fished heavily, and is thought to be of conservation concern under some circumstances. As such, an important question in conservation is whether the implementation of marine protected areas (MPAs), which is a commonly used marine conservation tool, works as effectively for sex-changers as for non-sex-changers. To address this issue, we used meta-analyses of the ratio of fish abundances inside vs. outside MPAs to determine whether sex change affects the extent to which fish densities respond to protection. When all data were considered, there were similar responses to protection irrespective of reproductive mode. However, when analyses were restricted to older reserves (at least 10 years’ protection), female-first sex-changers consistently benefited from protection. Non-sex-changers and male-first sex-changers showed more variable responses to protection and, as a result, there were no significant differences between fish with different reproductive modes in their overall response to protection. The same results were observed when the effects of fisheries status (targeted vs. not targeted) were controlled. Our results support the use of MPAs as important components of conservation and demonstrate that old reserves are most consistently beneficial to female-first sex-changing species. Finally, our results highlight the fact that some effects of protection are only detectable after several generations.

In species where there is postcopulatory competition between males in the form of sperm competition, theory predicts that males should show prudent sperm allocation. Specifically, males should adjust the number of sperm that they inseminate in response to variations in the risk and intensity of sperm competition. Some experimental evidence for nonmammalian species indicates that ejaculate expenditure can be dynamic and adjusted in accordance with sperm competition theory. However, most studies have not used within-subject experimental designs to demonstrate ejaculate adjustments by individual males, and there have been no unequivocal demonstrations of prudent sperm allocation in mammals. In the present study, copulatory ejaculates were collected from 12 male rats that each mated under two experimental conditions: alone in a cage with a female (monandrous) and (accompanied by a ‘rival’ male who observed the copulation from behind a perforated plastic screen (polyandrous). As predicted by sperm competition theory, males ejaculated significantly more sperm when copulating in the presence of a rival than when copulating alone. Furthermore, the magnitudes of these ejaculate adjustments were highly predictable and were relatively consistent across individual males.

Sperm competition occurs when sperm from more than one male compete for fertilizations. This form of post-copulatory sexual selection is recognized as a significant and widespread force in the evolution of male reproductive biology and as a key determinant of differential male reproductive success. Despite its importance, however, detailed mechanisms of sperm competition at the gamete level remain poorly understood. Here, we use natural variation in spermatozoal traits among wild Atlantic salmon (Salmo salar), a species naturally adapted to sperm competition, to examine how the relative influences of sperm (i) number, (ii) velocity, (iii) longevity, and (iv) total length determine sperm competition success. Atlantic salmon fertilize externally, and we were therefore able to conduct controlled in vitro fertilization competitions while concurrently measuring spermatozoal traits within the aqueous micro-environment to which salmon gametes are naturally adapted. Microsatellite DNA fingerprinting revealed that a male's relative sperm velocity was the primary determinant of sperm competition success. There was no significant relationship between fertilization success and either relative sperm number or total length; sperm longevity showed an inverse relationship with competition success. These relationships were consistent for two experimental repeats of the in vitro fertilization competitions. Our results therefore show, under the natural microenvironment for salmon gametes, that relative sperm velocity is a key spermatozoal component for sperm competition success. Atlantic salmon sperm can be considered to enter a competition analogous to a race in which the fastest sperm have the highest probability of success.

Sperm competition, when sperm from different males compete to fertilize a female's ova [1], is a widespread and fundamental force in the evolution of animal reproduction [2]. The earliest prediction of sperm competition theory was that sperm competition selected for the evolution of numerous, tiny sperm, and that this force maintained anisogamy [3]. Here, we empirically test this prediction directly by using selective breeding to generate controlled and independent variance in sperm size and number traits in the cricket Gryllus bimaculatus. We find that sperm size and number are male specific and vary independently and significantly. We can therefore noninvasively screen individuals and then run sperm competition experiments between males that differ specifically in sperm size and number traits. Paternity success across 77 two-male sperm competitions (each running over 30-day oviposition periods) shows that males producing both relatively small sperm and relatively numerous sperm win competitions for fertilization. Decreased sperm size and increased sperm number both independently predicted sperm precedence. Our findings provide direct experimental support for the theory that sperm competition selects for maximal numbers of miniaturized sperm [3]. However, our study does not explain why G. bimaculatus sperm length persists naturally at ∼1 mm; we discuss possibilities for this sperm size maintenance.

Sperm are produced in astronomical numbers compared with eggs, and there is good evidence that sperm competition is the force behind the evolution of many tiny sperm. However, sperm production inevitably has costs. Recent research shows that male ejaculate expenditure is dynamic in both time and space, and that males are sensitive to risks of sperm competition and can vary ejaculate size accordingly. We focus on studies showing that males assess mating status and relative fecundity of females, and reveal that modulation of ejaculate investment by males can sometimes result in sperm limitation for females.

SummaryConflicts between and within species can drive fast evolutionary change. A recent study has documented remarkably rapid counter-adaptations in the wild to an extreme sex-ratio distortion caused by a bacterial symbiont.

In their correspondence, Slate and Pemberton [1xDoes reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)?. Slate, J. and Pemberton, J. Curr. Biol. 2006; 16: 790–791Abstract | Full Text | Full Text PDF | Scopus (27)See all References[1] argue that the key interpretation of our study, namely the finding of a negative correlation between heterozygosity and sperm abnormality across wild UK rabbits [2xReduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Gage, M.J.G., Surridge, A.K., Tomkins, J.L., Green, E., Wiskin, L., Bell, D.J., and Hewitt, G.M. Curr. Biol. 2006; 16: 612–617Abstract | Full Text | Full Text PDF | PubMed | Scopus (72)See all References[2], is flawed. According to their view, the reason for this is that our analysis did not adequately deal with population stratification. Slate and Pemberton [1xDoes reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)?. Slate, J. and Pemberton, J. Curr. Biol. 2006; 16: 790–791Abstract | Full Text | Full Text PDF | Scopus (27)See all References[1] claim that demonstrations of heterozygosity–fitness correlations are only convincing when heterozygosity–fitness relationships are found across individuals within populations.Slate and Pemberton [1xDoes reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)?. Slate, J. and Pemberton, J. Curr. Biol. 2006; 16: 790–791Abstract | Full Text | Full Text PDF | Scopus (27)See all References[1] rightly point out that sampling individuals from different geographic origins could confound associations because of environmental heterogeneity at the sites. Such problems are inherent to all correlative studies in the natural environment. There is a subjective problem of defining which level of a ‘population’ will actually control for environmental heterogeneity. In our system, for instance, mobile male rabbits [3xNatal dispersal and genetic structure in a population of the European wild rabbit (Oryctolagus cuniculus). Webb, N.J., Ibrahim, K.M., Bell, D.J., and Hewitt, G.M. Mol. Ecol. 1999; 4: 239–247CrossrefSee all References[3] will be exposed to uncontrolled environmental variation even within a ‘site’.In our study [2xReduced heterozygosity depresses sperm quality in wild rabbits, Oryctolagus cuniculus. Gage, M.J.G., Surridge, A.K., Tomkins, J.L., Green, E., Wiskin, L., Bell, D.J., and Hewitt, G.M. Curr. Biol. 2006; 16: 612–617Abstract | Full Text | Full Text PDF | PubMed | Scopus (72)See all References[2], we explore some potential environmental heterogeneity: the correlation of population heterozygosity means shows that the relationship holds; moreover, there is no covariance with body mass or condition, which are possible indicators of environmental influence. The relationship we found also holds across separate ‘mainland’ or ‘island’ samples.Moreover, we applied the model suggested by Slate and Pemberton [1xDoes reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)?. Slate, J. and Pemberton, J. Curr. Biol. 2006; 16: 790–791Abstract | Full Text | Full Text PDF | Scopus (27)See all References[1] and controlled for ‘population’ by fitting it as a categorical term. Across individuals, the relationship remains significant (F = 23.3, P < 0.0001) (similar if we also include body mass, F = 15.8, P < 0.0001). However, as one of the referees observed, there are concerns about the validity of this analysis because non-random covariation exists between the independent variable (heterozygosity) and ‘population’, hence, the relationship across population means.A particular problem presented by UK rabbits is that their populations are genetically structured at extremely fine scales: sites in East Anglia separated by a few hundred metres are as different as those separated by 125 kilometres [4xFrom population structure to individual behaviour: genetic analysis of social structure in the European wild rabbit (Oryctolagus cuniculus). Surridge, A.K., Bell, D.J., and Hewitt, G.M. Biol. J. Linn. Soc. 1999; 68: 57–71CrossrefSee all References, 5xFine-scale genetic structuring in a natural population of European wild rabbits (Oryctolagus cuniculus). Surridge, A.K., Ibrahim, K.M., Bell, D.J., Webb, N.J., Rico, C., and Hewitt, G.M. Mol. Ecol. 1999; 8: 299–307Crossref | PubMed | Scopus (47)See all References, 6xPopulation structure and genetic variation of European wild rabbits (Oryctolagus cuniculus) in East Anglia. Surridge, A.K., Bell, D.J., Ibrahim, K.M., and Hewitt, G.M. Heredity. 1999; 82: 479–487Crossref | PubMedSee all References]. Such extreme differentiation means that insufficient genetic variation exists within discrete ‘populations’ to explore fitness relationships, with potential non-independence due to close relatedness.Our results clearly indicate the established importance [7xDoes heterozygosity estimate inbreeding in real populations?. Balloux, F., Amos, W., and Coulson, T. Mol. Ecol. 2004; 13: 3021–3031Crossref | PubMed | Scopus (290)See all References[7] of sampling very low heterozygosities for revealing possible fitness correlations: the relationship is heavily influenced by a small number (∼12) of strongly homozygous males (one homozygous at all 29 loci). These individuals will be rare in the wild in general, and even rarer within one discrete population that holds individuals with a high degree of heterozygosity. Without an isolation-by-distance relationship, such fine-scale structuring also means that our sampling sites contain numerous ‘populations’. As sampling was spread throughout most areas by several kilometres, we can be confident that most individuals represent single samples from different ‘populations’ by those criteria.A key consideration is what constitutes a discrete population? There are arguments for designating the UK to be a population at one level of interpretation: rabbits colonised the wild recently, in the 18th century [4xFrom population structure to individual behaviour: genetic analysis of social structure in the European wild rabbit (Oryctolagus cuniculus). Surridge, A.K., Bell, D.J., and Hewitt, G.M. Biol. J. Linn. Soc. 1999; 68: 57–71CrossrefSee all References, 8xThe European Rabbit: History and Biology of a Successful Colonizer. Thompson, H.V. and King, C.M. See all References], providing us with a natural experiment. However, we agree that we cannot eliminate all potential confounds. Although our study was founded upon evidence that heavily inbred big cats have unusually elevated sperm abnormalities [9xReproductive characteristics of male Florida panthers: comparative studies from Florida, Texas, Colorado, Latin America, and North American zoos. Barone, M.A., Roelke, M.E., Howard, J., Brown, J.L., Anderson, A.E., and Wildt, D.E. J. Mammal. 1994; 75: 150–162CrossrefSee all References[9], we cannot exclude additional interpretations, such as that proposed by Slate and Pemberton [1xDoes reduced heterozygosity depress sperm quality in wild rabbits (Oryctolagus cuniculus)?. Slate, J. and Pemberton, J. Curr. Biol. 2006; 16: 790–791Abstract | Full Text | Full Text PDF | Scopus (27)See all References[1]: abnormal sperm constrain reproductive output which leads to inbreeding. Ideally, we would match our natural environment correlations with experiments that applied tight ‘environmental’ control. However, complementary approaches are important because inbreeding depression could be influenced by both genetic and environmental variation [10xInbreeding effects in wild populations. Keller, L.F. and Waller, D.M. Trends Ecol. Evol. 2002; 17: 230–241Abstract | Full Text | Full Text PDF | Scopus (1423)See all References[10].