Mechanisms of sperm competition: Linking physiology and behavioural ecology

Sperm competition has received a great deal of attention from behavioural ecologists because it is the ultimate form of male-male competition, and may also be important for female choice. It is becoming clear that the adaptive value of the behavioural strategies of males and females will not be fully understood until we have a better understanding of the physiological mechanisms that come into play after copulation. We now have enough information to compare the underlying mechanisms in birds and mammals and to relate these to the way in which sperm competition operates in both groups. To integrate this knowledge, the boundaries between behavioural ecology and physiology will have to be crossed in what promises to be a most fruitful enterprise.     

Bayesian sperm competition estimates

We introduce a Bayesian method for estimating parameters for a model of multiple mating and sperm displacement from genotype counts of brood-structured data. The model is initially targeted for Drosophila melanogaster, but is easily adapted to other organisms. The method is appropriate for use with field studies where the number of mates and the genotypes of the mates cannot be controlled, but where unlinked markers have been collected for a set of females and a sample of their offspring. Advantages over previous approaches include full use of multilocus information and the ability to cope appropriately with missing data and ambiguities about which alleles are maternally vs. paternally inherited. The advantages of including X-linked markers are also demonstrated.     

Gamete evolution and sperm numbers: sperm competition versus sperm limitation

Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization (N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization (F) and increasing sperm numbers (x) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups.     

Evolution of sperm size in nematodes: sperm competition favours larger sperm

In the free-living rhabditid nematode Caenorhabditis elegans, sperm size is a determinant of sperm competitiveness. Larger sperm crawl faster and physically displace smaller sperm to take fertilization priority, but not without a cost: larger sperm are produced at a slower rate. Here, we investigate the evolution of sperm size in the family Rhabditidae by comparing sperm among 19 species, seven of which are hermaphroditic (self-fertile hermaphrodites and males), the rest being gonochoristic (females and males). We found that sperm size differed significantly with reproductive mode: males of gonochoristic species had significantly larger sperm than did males of the hermaphroditic species. Because males compose 50% of the populations of gonochoristic species but are rare in hermaphroditic species, the risk of male-male sperm competition is greater in gonochoristic species. Larger sperm have thus evolved in species with a greater risk of sperm competition. Our results support recent studies contending that sperm size may increase in response to sperm competition.     

Tactic-specific success in sperm competition

Sperm competition is a major force in sexual selection, but its implications for mating-system and life-history evolution are only beginning to be understood. The well-known sneak-guard model predicts that sneaks will win in sperm competition. We now provide empirical confirmation of this prediction. Bluegill sunfish (Lepomis macrochirus) have both sneak (cuckolder) and guard (parental) males. Guards make nests, court females and provide solitary parental care for the embryos. Sneaks include small cuckolders, which are termed 'sneakers', that dart in and out of nests in order to ejaculate between the spawning pair and larger cuckolders, which are termed 'satellites', that mimic females in order to ejaculate between the spawning pair. Using field behavioural data, genetic data and new mathematical models for paternity analyses, we show, for the first time to the authors' knowledge, that sneaks fertilize more eggs than guards during sperm competition. In addition, we show that sneakers are superior to satellites in sperm competition and, thus, that even among sneaks there are tactic-specific differences in competitive success.     

Snail sperm production characteristics vary with sperm competition risk

Sperm competition is widespread and influences both male investment in spermatogenic tissue and ejaculate characteristics. Sperm competition models assume trade-offs between sperm size and number, although such trade-offs may be difficult to detect. This study examines the effects of sperm competition risk on the sperm production characteristics of the freshwater snail Viviparus ater. In this prosobranch, females mate frequently and store sperm, generating sperm competition. Males produce two sperm morphs, fertile eupyrene sperm and non-fertilizing oligopyrene sperm. Non-fertilizing sperm may play a role in sperm competition and therefore, like fertilizing sperm, the number produced could vary relative to sperm competition risk. In addition, trade-offs between sperm number and sperm size may be expected. We manipulated the sex ratio of sexually mature snails and found the presence of rivals affected the ratio of oligopyrene/eupyrene sperm males produced. In experimental and natural populations, the number of oligopyrene sperm produced, but not the number of eupyrene sperm, was significantly higher when the sex ratio was male biased. Testis mass did not vary between experimental treatments. We also found a negative relationship between the number and size of oligopyrene sperm produced, which is consistent with evolutionary models of sperm competition, and is, to our knowledge, the first intraspecific demonstration of a trade-off between these traits.     

Direct visualization of sperm competition and sperm storage in Drosophila.

Drosophila females engage in multiple matings [1] [2] [3] [4] even though they can store sperm in specialized organs for most of their life [5]. The existence of sperm competition in Drosophila has been inferred from the proportion of progeny sired by the second male in double-mating experiments [6] [7] [8]. Investigators have used this approach to quantify genetic variation underlying sperm competition [8] [9] [10], to elucidate its genetic basis [11], to identify the dependence of different male competitive ability on the genotype of the females with which they mate [12] and to discern the potential role of sperm competition in species isolation [13] [14]. This approach assumes that the sperm from two males stored in a female compete to fertilize the eggs. The mechanism by which sperm competition is accomplished is still unknown, however. Here, fluorescence microscopy, cytometry, and differently labeled sperm were used to analyze the fate of sperm inside the female's sperm storage organs, to quantify sperm competition, and to assess how closely paternity success corresponds to the appearance and location of the sperm. The results show that the first male's sperm is retained for a shortened period if the female remates, and that the second males that sire more progeny either induce females to store and use more of their sperm or strongly displace resident sperm.     

Mechanisms of competition among insectivorous mammals

Summary This study investigates the mechanisms of competition between congeneric pairs of insectivorous mammals in two communities in Australia and England. Direct field observations showed that physical interactions between species do not occur, whereas conspecific encounters are frequent. In field enclosures the smaller, subordinate species in each community (Antechinus stuartii: Marsupialia: Sorex minutus: Eutheria) remained alert in the presence of the dominant species (A. swainsonii, S. araneus), and moved quickly away when the latter approached. The rate of prey capture by subordinate individuals also increased immediately after removal of the dominants. Hourly removals of some individuals of the dominant species in each community over 24 h produced hourly increases in the numbers of subordinate individuals that were captured. The rapidity of these responses suggests strongly that the dominant insectivores in each community interfered with the resource use of the subordinate species. Biomass of invertebrates increased inconsistently or slowly within 3 months of removal of the dominant insectivores; hence the rapid responses by subordinate individuals in experiments were not due to simple exploitation or tracking of resource levels. The subordinate insectivores probably detected and avoided contact with dominants instantaneously using auditory or olfactory cues; reciprocal avoidance of congeneric odours was demonstrated using odour-scented traps. Insectivorous mammals may usually compete by interference (or encounter competition, sensu Schoener 1983). For dominant species within communities the cost of interference is minimal and the benefit of gaining exclusive access to resource-rich microhabitats is high. Conversely for subordinate species the benefit of temporarily exploiting the same rich microhabitats may exceed the small costs of vigilance and movement to nearby refugia.     

Sperm competition, sperm numbers and sperm quality in muroid rodents

Sperm competition favors increases in relative testes mass and production efficiency, and changes in sperm phenotype that result in faster swimming speeds. However, little is known about its effects on traits that contribute to determine the quality of a whole ejaculate (i.e., proportion of motile, viable, morphologically normal and acrosome intact sperm) and that are key determinants of fertilization success. Two competing hypotheses lead to alternative predictions: (a) sperm quantity and quality traits co-evolve under sperm competition because they play complementary roles in determining ejaculate's competitive ability, or (b) energetic constraints force trade-offs between traits depending on their relevance in providing a competitive advantage. We examined relationships between sperm competition levels, sperm quantity, and traits that determine ejaculate quality, in a comparative study of 18 rodent species using phylogenetically controlled analyses. Total sperm numbers were positively correlated to proportions of normal sperm, acrosome integrity and motile sperm; the latter three were also significantly related among themselves, suggesting no trade-offs between traits. In addition, testes mass corrected for body mass (i.e., relative testes mass), showed a strong association with sperm numbers, and positive significant associations with all sperm traits that determine ejaculate quality with the exception of live sperm. An "overall sperm quality" parameter obtained by principal component analysis (which explained 85% of the variance) was more strongly associated with relative testes mass than any individual quality trait. Overall sperm quality was as strongly associated with relative testes mass as sperm numbers. Thus, sperm quality traits improve under sperm competition in an integrated manner suggesting that a combination of all traits is what makes ejaculates more competitive. In evolutionary terms this implies that a complex network of genetic and developmental pathways underlying processes of sperm formation, maturation, transport in the female reproductive tract, and preparation for fertilization must all evolve in concert.     

Fertilisation and sperm competition dynamics in salmon

Fishes have evolved an enormous range of mating patterns and sperm competition is important in the majority of these. Detailed mechanisms of fertilization and sperm competition dynamics at the gamete level are poorly understood. We have been using salmon models to conduct in vitro fertilization trials that: (1) allow us experimental control, (2) eliminate confounding effects from the whole organism, and (3) enable detailed measures of sperm form and function in the natural fertilization medium to which gametes are adapted. Using both Atlantic and sockeye salmon, we present results on experiments exploring: (1) the importance of relative sperm number, size, % motility, longevity, and velocity for fertilization and sperm competition success, (2) the importance of natural variation in egg size for 'fertilizability' under sperm limited conditions and (3) the influence of ovarian fluid in fertilization dynamics.     

Semen displacement as a sperm competition strategy

Using a sample of 652 college students, we examined several implications of the hypothesis that the shape of the human penis evolved to enable males to substitute their semen for those of their rivals. The incidence of double mating by females appears sufficient to make semen displacement adaptive (e.g., one in four females acknowledge infidelity, one in eight admit having sex with two or more males in a 24-hour period, and one in 12 report involvement in one or more sexual threesomes with two males). We also document several changes in post-ejaculatory behavior (e.g., reduced thrusting, penis withdrawal, loss of an erection) which may have evolved to minimize displacement of the male’s own semen. Consistent with predictions derived from a theoretical model (Gallup and Burch 2006), we discovered that most females report waiting at least 48 hours following an instance of infidelity before resuming sex with their in-pair partners.     

Sperm viability and sperm competition in insects

Sperm quality plays an important role in vertebrates in determining which male has the advantage when two or more males compete to fertilize a female's ova. In insects, however, the importance of sperm quality has never been considered, despite sperm competition being widespread and well studied in this group. We tested the hypothesis that sperm viability, measured as the proportion of live sperm, covaried with the intensity of sperm competition in insects. In a pairwise comparison of seven closely related species pairs, each comprising a monandrous and a polyandrous species (i.e., with and without sperm competition, respectively), we found that in all cases the polyandrous species had a higher proportion of live sperm in their sperm stores. The distribution of the percentage of live sperm showed considerable inter- and intraspecific variation, suggesting that, all else being equal, males will vary in their ability to fertilize ova on the basis of sperm viability alone. Our results suggest that sperm viability is one of a suite of male adaptations to sperm competition in insects.     

Sperm viability matters in insect sperm competition

Experimental studies in insects have shown how sperm competition can be a potent selective force acting on an array of male reproductive traits . However, the role of sperm quality in determining paternity in insects has been neglected, despite the fact that sperm quality has been shown to influence the outcome of sperm competition in vertebrates . A recent comparative analysis found that males of polyandrous insect species show a higher proportion of live sperm in their stores . Here, we test the hypothesis that sperm viability influences paternity at the within-species level. We use the cricket Teleogryllus oceanicus to conduct sperm competition trials involving prescreened males that differ in the viability of their sperm. We find that paternity success is determined by the proportion of live sperm in a male's ejaculate. Furthermore, we were able to predict the paternity patterns observed on the basis of the males' relative representation of viable sperm in the female's sperm-storage organ. Our findings provide the first experimental evidence for the theory that sperm competition selects for higher sperm quality in insects. Between-male variation in sperm quality needs to be considered in theoretical and experimental studies of insect sperm competition.     

Bitterling as models for studies of sperm competition

The plight of the world fish stocks is all too well documented. As part of an ongoing attempt to bolster fish stocks for both commercial and conservation purposes, many fish are reared in captivity and released into the wild. It is well known that hatchery‐reared fish have low post‐release survival compared with wild fish of similar age. Part of the reason for this high mortality is that hatchery fish show deficits in virtually all aspects of their behaviour, including prey selection and predator avoidance. Much behaviour requires repeated experience so that it may become fine‐tuned to prevailing circumstances via learning during development. It has been suggested that inappropriate behaviour is encouraged when fish are reared in the unnatural surroundings of the hatchery. However, hatchery fish can be taught to recognise live, novel prey items and predators and the rate of learning is increased in the presence of a more knowledgeable conspecifics. Here we present data showing how social learning protocols can be used to dramatically increase foraging success in juvenile Atlantic salmon. We also outline related aspects of our ongoing research and discuss some of the possibilities for altering hatchery practices to maximize post‐release survival.     

Male sperm expenditure under sperm competition risk and intensity in quacking frogs

In the frog Crinia georgiana, reproductive behavior comprisesa "guarding tactic," in which males defend spawn sites and attractfemales by calling, and a "sneak tactic," in which males joinspawning pairs. The aims of the present study were to (1) relateejaculate expenditure by "guarding" and "sneak" males to theirprobability of mating with other males present (sperm-competitionrisk), and (2) determine if males adjust their ejaculate expenditureaccording to the number of males involved in a spawning (sperm-competitionintensity). Theory predicts that because sneak males alwaysmate with other males present, they will experience a highersperm-competition risk and should release larger ejaculatesrelative to that of guarding males. However, as the proportionof sneaks in a population increases so does the risk of spermcompetition to guarders, so expenditure by each tactic shouldmove toward equality. Given that the incidence of sneak behavioris high in C. georgiana, guarders and sneaks were expected toexperience similar risks of sperm competition and show similarinvestment in spermatogenesis. Comparison of testes size andejaculate size showed no difference between tactics. Modelsof sperm-competition intensity predict that males should increasetheir ejaculate size when spawning in the presence of one othermale but decrease their ejaculate size when spawning in thepresence of multiple males. Here, males maintained a constantsperm number irrespective of whether a mating involved one,two, or three males. This result suggests that male C. georgianado not facultatively adjust ejaculate investment in responseto fluctuating intensities of sperm competition.     

Mass-specific metabolic rate and sperm competition determine sperm size in marsupial mammals

Two complementary hypotheses have been proposed to explain variation in sperm size. The first proposes that post-copulatory sexual selection favors an increase in sperm size because it enhances sperm swimming speed, which is an important determinant of fertilization success in competitive contexts. The second hypothesis proposes that mass-specific metabolic rate acts as a constraint, because large animals with low mass-specific metabolic rates will not be able to process resources at the rates needed to produce large sperm. This constraint is expected to be particularly pronounced among mammals, given that this group contains some of the largest species on Earth. We tested these hypotheses among marsupials, a group in which mass-specific metabolic rates are roughly 30% lower than those of eutherian mammals of similar size, leading to the expectation that metabolic rate should be a major constraint. Our findings support both hypotheses because levels of sperm competition are associated with increases in sperm size, but low mass-specific metabolic rate constrains sperm size among large species. We also found that the relationship between sperm size and mass-specific metabolic rate is steeper among marsupials and shallower among eutherian mammals. This finding has two implications: marsupials respond to changes in mass-specific metabolic rate by modifying sperm length to a greater extent, suggesting that they are more constrained by metabolic rate. In addition, for any given mass-specific metabolic rate, marsupials produce longer sperm. We suggest that this is the consequence of marsupials diverting resources away from sperm numbers and into sperm size, due to their efficient sperm transport along the female tract and the existence of mechanisms to protect sperm.