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.     

Prolonged mate guarding and sperm competition in the weevil Diaprepes abbreviatus (L.)

The hypothesis that prolonged copulatory mate guarding coexistswith last male sperm precedence was tested for the sugarcanerootstalk borer weevil, Diaprepes abbreviatus (L.) (Coleoptera:Curculionidae). Male D. abbreviatus showed a long copulatoryguarding. Both males and females were less likely to rematewhen prolonged guarding occurred compared with terminating copulationearly. Guarding was generally terminated by the struggling behaviorof the female. Mating experiments using normal and sterile (X-rayirradiated) males revealed a similar value of last-male spermprecedence for both irradiated and normal males. The P₂ valuesof normal and sterile males were similar when all ovipositedeggs were counted over 30 days. These data made it possibleto calculate the expected gain to a male from prolonged guardingcompared with leaving a female early and seeking out an additionalmate. We show that guarding has the higher fitness. Eggs weredeposited in clutches in which normal fertilized eggs were groupedtogether and were attached to a group of sterile eggs. This,together with identifying the form of the cul-de-sac typespermatheca,allowed us to suggest a unique repositioning process, whichhas not been described elsewhere, as the likely mechanism bywhich last-male sperm precedence was achieved.     

Sperm competition and the evolution of sperm design in mammals

Background  

The influence of sperm competition upon sperm size has been a controversial issue during the last 20 years which remains unresolved for mammals. The hypothesis that, when ejaculates compete with rival males, an increase in sperm size would make sperm more competitive because it would increase sperm swimming speed, has generated contradictory results from both theoretical and empirical studies. In addition, the debate has extended to which sperm components should increase in size: the midpiece to accommodate more mitochondria and produce more energy to fuel motility, or the principal piece to generate greater propulsion forces.     

The evolution of sperm-allocation strategies and the degree of sperm competition

The prevailing viewpoint in the study of sperm competition is that male sperm-allocation strategies evolve in response to the degree of sperm competition an ejaculate can expect to experience within a given mating. If males cannot assess the degree of sperm competition their ejaculate will face and/or they are unable to facultatively adjust sperm investment in response to perceived levels of competition, high sperm allocation (per mating) is predicted to evolve in the context of high sperm competition. An implicit assumption of the framework used to derive this result is that the degree of sperm competition is unaffected by changes in sperm-allocation strategies. We present theory based on an alternative perspective, in which the degree of sperm competition and the sperm-allocation strategy are coupled traits that coevolve together. Our rationale is that the pattern of sperm allocation in the population will, in part, determine the level of sperm competition by affecting the number of ejaculates per female in the population. In this setting, evolution in sperm-allocation strategies is driven by changes in underlying environmental parameters that influence both the degree of sperm competition and sperm allocation. This change in perspective leads to predictions that are qualitatively different from those of previous theory.     

Experimental evidence for the evolution of numerous,tiny sperm via sperm competition

Sperm competition, when sperm from different males compete to fertilize a female's 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.     

Sperm competition and the evolution of the sperm hook in house mice

Sperm morphology varies considerably both between and within species. The sperm of many muroid rodents bear an apical hook at the proximal end of the head. The curvature of the sperm hook varies greatly across species, however the adaptive significance of the sperm hook is currently not known. In wood mice the apical hooks intertwine to form sperm ‘trains’, which exhibit faster swimming velocities than single cells. Thus, it has been suggested that if sperm ‘trains’ were advantageous in a competitive situation, then the apical sperm hook might be an evolutionary product of selection via sperm competition. A comparative study of rodent species provided support for the hypothesis, and showed that species with higher levels of sperm competition had more reflected sperm hooks. Here, we tested this hypothesis at the intraspecific level. We quantified sperm hook morphology from seven house mouse populations, and found that interpopulation variation in hook curvature was not explained by variation in sperm competition risk. Furthermore, observations of ejaculated sperm revealed that sperm groups are not a common characteristic of mouse ejaculates. We suggest that selection for sperm attachment to the oviduct epithelium, and thus better retainment of sperm fertilizing potential, may provide a more general explanation of the evolutionary relationship between sperm competition risk and the curvature of the sperm hook among rodents, and provide a phylogenetic comparison among rodent species that supports our hypothesis.     

Experimental evidence for testis size evolution via sperm competition

Sperm competition theory predicts increased spermatogenic investment with increased sperm competition risk when competition is numerical. There is ample correlational evidence for this relationship in a wide range of taxa. However, as with all correlations, this does not establish cause and effect. Nevertheless, there are no published experimental studies of the evolutionary influence of sperm competition on testis size. We report here on evolutionary responses of testis size to variation in sperm competition intensity in the yellow dung fly. Experimental flies were divided across two treatments, polyandrous or monogamous, with four replicates of each. There was a rapid evolutionary response in testis size resulting from selection via sperm competition, with larger testes found when sperm competition intensity was greatest. These results provide direct experimental evidence of evolutionary change consistent with macro‐evolutionary patterns found across a wide range of taxa.     

Mating systems, sperm competition, and the evolution of sexual dimorphism in birds

Comparative analyses suggest that a variety of factors influence the evolution of sexual dimorphism in birds. We analyzed the relative importance of social mating system and sperm competition to sexual differences in plumage and body size (mass and tail and wing length) of more than 1,000 species of birds from throughout the world. In these analyses we controlled for phylogeny and a variety of ecological and life-history variables. We used testis size (corrected for total body mass) as an index of sperm competition in each species, because testis size is correlated with levels of extrapair paternity and is available for a large number of species. In contrast to recent studies, we found strong and consistent effects of social mating system on most forms of dimorphism. Social mating system strongly influenced dimorphism in plumage, body mass, and wing length and had some effect on dimorphism in tail length. Sexual dimorphism was relatively greater in species with polygynous or lekking than monogamous mating systems. This was true when we used both species and phylogenetically independent contrasts for analysis. Relative testis size was also related positively to dimorphism in tail and wing length, but in most analyses it was a poorer predictor of plumage dimorphism than social mating system. There was no association between relative testis size and mass dimorphism. Geographic region and life history were also associated with the four types of dimorphism, although their influence varied between the different types of dimorphism. Although there is much interest in the effects of sperm competition on sexual dimorphism, we suggest that traditional explanations based on social mating systems are better predictors of dimorphism in birds.     

The intensity of pre- and post-copulatory mate guarding in relation to spermatophore transfer in the cricket Gryllus bimaculatus

While post-copulatory mate guarding has been well documented in field crickets (Orthoptera: Gryllidae), the occurrence of pre-copulatory mate guarding in this family has been largely overlooked. We examined the relationship between the intensity of two components of mate guarding (body judders and antennal whips) and the time before and after copulation. We found that when male Gryllus bimaculatus encounter a female but do not have a spermatophore ready to transfer, they engage in pre-copulatory mate guarding that is very similar to post-copulatory mate guarding. The intensity of pre-copulatory mate guarding increased up to the point at which the male was ready to transfer his spermatophore. Following copulation, the intensity of mate guarding initially remained high before declining, after which it began to increase again just before the male resumed courtship stridulation. We interpret this pattern of post-copulatory mate guarding as being consistent with both the ejaculate-protection and spermatophore-renewal hypotheses for the function of mate guarding. We found no significant relationship between mate guarding intensity and male body mass.     

A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

Sperm competition, a prevalent evolutionary process in which the spermatozoa of two or more males compete for the fertilization of the same ovum, leads to morphological and physiological adaptations, including increases in energetic metabolism that may serve to propel sperm faster but that may have negative effects on DNA integrity. Sperm DNA damage is associated with reduced rates of fertilization, embryo and fetal loss, offspring mortality, and mutations leading to genetic disease. We tested whether high levels of sperm competition affect sperm DNA integrity. We evaluated sperm DNA integrity in 18 species of rodents that differ in their levels of sperm competition using the sperm chromatin structure assay. DNA integrity was assessed upon sperm collection, in response to incubation under capacitating or non-capacitating conditions, and after exposure to physical and chemical stressors. Sperm DNA was very resistant to physical and chemical stressors, whereas incubation in non-capacitating and capacitating conditions resulted in only a small increase in sperm DNA damage. Importantly, levels of sperm competition were positively associated with sperm DNA fragmentation across rodent species. This is the first evidence showing that high levels of sperm competition lead to an important cost in the form of increased sperm DNA damage.     

The evolution of sperm competition genes: The effect of mating system on levels of genetic variation within and between species

It is widely established that proteins involved in reproduction diverge between species more quickly than other proteins. For male sperm proteins, rapid divergence is believed to be caused by postcopulatory sexual selection and/or sexual conflict. Here, we derive the expected levels of gene diversity within populations and divergence between them for male sperm protein genes evolving by postcopulatory, prezygotic fertility competition, i.e. the function imputed for some sperm and seminal fluid genes. We find that, at the mutation‐selection equilibrium, both gene diversity within species and divergence between them are elevated relative to genes with similar selection coefficients expressed by both sexes. We show that their expected level of diversity is a function of the harmonic mean number of mates per female, which affects the strength of fertility selection stemming from male–male sperm competition. Our predictions provide a null hypothesis for distinguishing between other selective hypotheses accounting for the rapid evolution of male reproductive genes.     

On the evacuation of sperm from the spermatophore of the tick, Ornithodoros savignyi

The paper deals with the different mechanisms involved in the process of spermatophore evagination, its triggering, its intermediate steps, and the cause of the flow of spermiophores from the ectospermatophore to the endospermatophore.The methods employed involved exposure of the spermatophores to the influence of various media and different environmental conditions, as well as mass spectrometric measurements in respect of the gas formed in the spermatophore during evagination.Results showed the possibility of retardation, interruption, and/or total inhibition of the process and produced conclusive proof that the gas generated in the spermatophore and responsible for the flow of spermiophores was CO₂.     

Mechanisms of sperm competition

Sperm competition occurs when two (or more) males inseminate a single female during a reproductive cycle, but what determines which one of them will fertilize her eggs? Is it simply a lottery, or are there some more complex rules by which matings are translated into offspring? Several studies covering various animal groups have shown that mating order effects are often important in determining paternity patterns: in animals as different as insects and birds, the sperm from the last male to mate often has precedence over previously introduced sperm. Recently, behavioural ecologists and physiologists have started to examine the mechanisms by which sperm precedence is achieved. The study of sperm competition mechanisms complements the more behavioural studies, and a combination of the two approaches used on single species should prove to be particularly rewarding.     

Evolutionary modeling predicts a decrease in postcopulatory sperm viability as a response to increasing levels of sperm competition

Sperm competition has been found to have a strong influence on the evolution of many male and female reproductive traits. Theoretical models have shown that, with increasing levels of sperm competition, males are predicted to increase ejaculate investment, and there is ample empirical evidence supporting this prediction. However, most theoretical models concern sperm number, and although the predictions are likely to apply to other sperm traits that will affect the sperm competitive ability of males, substantiated predictions are difficult unless the evolution of specific traits is explicitly modeled. Here I present a novel theoretical model aiming at predicting evolutionarily stable sperm viability in relation to female mating frequency in a mating system with internal fertilization. At odds with verbal arguments, this model demonstrates that sperm viability is expected to decrease with increasing female remating rates and thus to decrease with increasing levels of sperm competition. The major reason for this is that, with increasing female remating rates, the prospects of future fertilization success will decrease, which acts to reduce the benefit of long-lived viable sperm. An additional interesting result is that, as the cost of sperm viability increases, the overall energy investment in ejaculates will decrease. These novel results should have a strong impact on future sperm competition studies and will also have implications for our understanding of the evolution of female polyandry.     

On sperm ultrastructure,spermiogenesis and the spermatophore of Heterolaophonte minuta (Copepoda,Harpacticoida)

Summary The spermatophore, mature spermatozoon and spermiogenesis of Heterolaophonte minuta have been investigated by light and electron microscopy. The spermatophore contains three different secretions which are responsible for the discharge of the contents of the spermatophore, the formation of the fertilization tube and the storage of the spermatozoa. The spermatozoon represents a type new for the Copepoda. It is a filiform cell about 25 m in length, ellipsoid in transverse section and tapered at the posterior end. The elongated nucleus contains chromatin fibrils and does not possess a nuclear envelope. Posterior to the nucleus, six mitochondria are placed one after the other. The posterior part of the spermatozoon contains parallel pseudomembranes. The gamete is not helically twisted and is without a flagellum and centrioles. The most remarkable feature of the spermatozoon is an osmiophilic cap in front of the nucleus. This cap corresponds to the acrosome of the spermatozoon. Early stages of spermiogenesis take place in the testis, where the spermatids are incorporated into accessory cells. The origin of the chromatin fibrils and the glycocalyx, as well as the breakdown of the nuclear envelope and centrioles, represent the final steps of spermiogenesis which occur in the vas deferens.