Matthew J. G. Gage

Sperm competition, male prudence and sperm-limited females

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.

Spermatozoal Traits and Sperm Competition in Atlantic Salmon: Relative Sperm Velocity Is the Primary Determinant of Fertilization Success

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 males 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.

Associations between Body Size, Mating Pattern, Testis Size and Sperm Lengths across Butterflies

This paper investigates mechanisms of sperm competition by comparing reproductive characteristics across 74 butterfly species. Testis size scales with body size and, after controlling for this allometry, relative testis size increases with risk of sperm competition, as defined by female mating frequency. Both eupyrene (fertilizing) and apyrene (non-fertile) sperm lengths correlate positively with body size. After controlling for body size, relative eupyrene sperm lengths are greater in species where males experience higher risks of sperm competition. These results suggest that sperm competition in butterflies selects for increased investment in spermatogenesis, and specifically longer fertilizing sperm. Because longer sperm may be faster and more powerful, eupyrene sperm may therefore compete energetically, and are not selected to be minimally sized to maximize numbers for a purely raffle-based sperm competition mode. Apyrene sperm lengths are not affected directly by risk of encountering rival sperm. Instead, apyrene sperm show closer associations with body size which, if female tract morphometry correlates with body size, is consistent with the hypothesis that apyrene sperm retard female sexual receptivity by moving while in storage.

Sperm competition games: individual assessment of sperm competition intensity by group spawners

A distinction is made between sperm competition risk (where there is typically a low probability of competition between two ejaculates) and sperm competition intensity (where typically two or more ejaculates compete). The relation between sperm competition intensity and sperm expenditure can be radically different across species from that within a species. Across species, the average ejaculate expenditure will increase with the average intensity of sperm competition. But within a species, the reverse trend is generally predicted for greater than two males competing for the same set of eggs. These effects are demonstrated with three sperm competition game models. They are devised mainly for externally fertilizing group-spawning species such as many fish, in which males group around a female and ejaculate when the female sheds her eggs. Fertilization is assumed to be instantaneous and each male gains a proportion of the eggs equal to his sperm number divided by the total sperm. In the first model, males cannot assess the number of competitors, and their ejaculate effort is shaped by the average number of males for the species or locally isolated deme. The proportion of reproductive effort expended on the ejaculate is predicted to increase as ( N — 1) / N, where N = the mean number of competing males present at a spawning. Thus if N is large, ejaculate expenditure dominates reproductive effort. In the second model, males can estimate whether there are more or less than average numbers of competitors present at a spawning, and in the third model, males can assess the number of competitors exactly. As in the first model, these models confirm that the mean ejaculate effort should increase with the mean number of competitors for the species. However, they predict that males should decrease their sperm expenditure as the estimated number of competitors present at a given spawning increases above two. These conclusions do not apply to sperm competition risk: there is thus no conflict with earlier models based on risk.

Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella

Despite being variable, reproductive environments may be predictable. Because of this variability, individuals may maximize fitness through phenotypic plasticity. Here, I describe how males of the moth Plodia interpunctella are sensitive to population density during larval development (controlling for confounding effects of diet), and tailor a strategy which best suits the predicted reproductive environment. Such a strategy may be adaptive for this semelparous species, where all resources for reproduction are accrued during larval development and adults have a brief reproductive stage. Population density influences female mating pattern: at high densities, females mate more frequently, thus generating greater risks of sperm competition. Males reared at higher densities take longer to develop, despite achieving the same body mass. Adults from high densities have relatively larger abdomens and testes, produce greater numbers of sperm and live for shorter periods. At lower densities development time is reduced, and adult males have relatively larger heads and thoraxes, relatively smaller testes, ejaculate fewer sperm and live for longer periods. These results suggest that developing male P. interpunctella detect signals which reflect larval population structure, and hence eventual mating pattern. Males at low densities anticipate rare mate encounter and low risks of sperm competition, and therefore appear to invest in competence for migration and mate-searching. Males at higher densities anticipate frequent mate encounter and high risks of sperm competition, and therefore appear to invest in competence for mating and sperm competition. Such flexible male responses represent a ‘reaction norm’ where male strategies vary as a continuous function of the predicted reproductive environment’s signal.

Experimental Evidence for the Evolution of Numerous, Tiny Sperm via Sperm Competition

Sperm competition, when sperm from different males compete to fertilize a females ova, is a widespread and fundamental force in the evolution of animal reproduction. 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. 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. However, our study does not explain why G. bimaculatus sperm length persists naturally at approximately 1 mm; we discuss possibilities for this sperm size maintenance.

Effects of risks of sperm competition on the numbers of eupyrene and apyrene sperm ejaculated by the moth Plodia interpunctella (Lepidoptera: Pyralidae)

This study examines the effects of different risks of sperm competition upon ejaculate characteristics in the moth Plodia interpunctella. In this short-lived species, females will remate and thus generate sperm competition, while males have a limited sperm supply. We therefore predict males to have evolved prudence in ejaculate allocation and investigate the effects of (1) rival male presence, (2) female mating history and (3) female age, upon the ejaculation of eupyrene (fertilizing) and apyrene (non-fertile) sperm numbers. We found no effect of the presence of rival males upon ejaculate characteristics, and conclude, due to the mating system of P. interpunctella, that rival males do not represent a proximate risk of sperm competition. We controlled female mating history by allowing females to receive different and predictable numbers of sperm which they then store for at least 7 days. In subsequent matings (7 days later) we found that new males ejaculated significantly more eupyrene sperm to females that had previously received larger numbers of sperm. We conclude that males increase numbers of eupyrene sperm to maintain success in sperm competition with rival sperm already in storage in the female. We found no effect of female mating history upon the ejaculation of apyrene sperm. Female age, however, had a significant negative effect upon both sperm types. We discuss these results in relation to sperm competition theory and apyrene sperm function.

The evolution of sperm length in moths

Sperm form and function remain poorly understood despite being of fundamental biological importance. An instructive approach has been to examine evolutionary associations across comparable taxa between sperm characters and other, potentially selective reproductive traits. We adopt this approach here in a comparative study examining how sperm lengths are associated with male and female reproductive characters across moths. Primary data have revealed Lepidoptera to be an ideal order for examination: there is profound variation in the dimensions (but not organization) of the reproductive traits between closely related species which all share a monophyletic ancestry, for example, eupyrene sperm length varies from 110 to 12675 μm. Eupyrene (normal fertilizing) and apyrene (anucleate and non–fertile) sperm lengths are positively correlated across taxa and both sperm types show positive associations with mating pattern (as measured by the residual testis size). At fertilization, eupyrene sperm must migrate down the often elongated female spermathecal duct from storage to unite with the ovum. Across taxa, the elongation of this duct is associated with increased eupyrene sperm length, suggesting a positive female influence on sperm size since longer, more powerful sperm may be selected to migrate and/or compete successfully down greater ductal lengths. Apyrene sperm length is not associated with female reproductive tract dimensions. However, we found a positive relationship between the residual testis volume and spermathecal volume, suggesting coevolution between male investment in spermatogenesis and the extent of the female sperm storage capacity. Within males, there is a positive association between the two organs which form the ejaculate–containing spermatophore: the testes and the accessory gland. The ‘trade–up’ in investment to these components is discussed in relation to paternal investment and mating patterns.

Reduced Heterozygosity Depresses Sperm Quality in Wild Rabbits, Oryctolagus cuniculus

When close relatives are forced to reproduce, the resulting offspring inherit above average homozygosity and reduced fitness. Biologists now recognize inbreeding depression in the wild, a phenomenon that will probably increase as natural populations become depleted and fragmented. Inbreeding depression is most commonly expressed as compromised fertility and embryogenesis, but actual mechanisms remain poorly understood, especially for wild populations. Here, we examine how reduced heterozygosity influences spermatozoal and gonadal traits in wild rabbits (Oryctolagus cuniculus) sampled across the United Kingdom. By using a suite of 29 microsatellite markers (analyzed to confirm representation of individual heterozygosity across our sample), we found a significant negative relationship between heterozygosity and the production of normal sperm; the relationship was significant both between (n = 12) and within (n = 91 [total males], 42 [island], 49 [mainland]) populations. Reduced heterozygosity was also associated with decreased testis size across males (n = 112), but no relationship was seen at the population level, suggesting environmental confounds. Our results show, for a wild mammal, that inbreeding is associated with decreased sperm quality, confirming suggestions of links between inbreeding and elevated sperm abnormalities in rare felids . These findings could explain why inbreeding depression so frequently arises via compromised fertility and embryogenesis .

Sexual selection and speciation in mammals, butterflies and spiders.

Recently refined evolutionary theories propose that sexual selection and reproductive conflict could be drivers of speciation. Male and female reproductive optima invariably differ because the potential reproductive rate of males almost always exceeds that of females: females are selected to maximize mate ‘quality’, while males can increase fitness through mate ‘quantity’. A dynamic, sexually selected conflict therefore exists in which ‘competitive’ males are selected to override the preference tactics evolved by ‘choosy’ females. The wide variation across taxa in mating systems therefore generates variance in the outcome of intrasexual conflict and the strength of sexual selection: monandry constrains reproductive heterozygosity and allows female choice to select and maintain particular (preferred) genes; polyandry promotes reproductive heterozygosity and will more likely override female choice. Two different theories predict how sexual selection might influence speciation. Traditional ideas indicate that increased sexual selection (and hence conflict) generates a greater diversity of male reproductive strategies to be counteracted by female mate preferences, thus providing elevated potentials for speciation as more evolutionary avenues of male–female interaction are created. A less intuitively obvious theory proposes that increased sexual selection and conflict constrains speciation by reducing the opportunities for female mate choice under polyandry. We use a comparative approach to test these theories by investigating whether two general measures of sexual selection and the potential for sexual conflict have influenced speciation. Sexual size dimorphism (across 480 mammalian genera, 105 butterfly genera and 148 spider genera) and degree of polyandry (measured as relative testes size in mammals (72 genera) and mating frequency in female butterflies (54 genera)) showed no associations with the variance in speciosity. Our results therefore show that speciation occurs independently of sexual selection.