Sexual selection and sperm competition in primates: What are male genitalia good for?

One hundred twenty-five years ago, in The Descent of Man and Selection in Relation to Sex,¹ Charles Darwin proposed the theory of sexual selection, as distinct from natural selection, to explain why, in some species, males have such magnificent ornaments and, in other species, such impressive weapons. He suggested two processes, which we now term female choice and male-male competition: either females choose particularly ornate males or, alternatively, relatively passive females accept the winner of fights among males. By now, knowledge of species in which the females are more brightly colored or aggressive than males has led to a more general formulation of the principle of sexual selection, in which, instead of “females”, we write “the sex with the lower potential reproductive rate”, and, instead of “male”, “the sex with the higher potential reproductive rate”.²     

The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy-sperm?

The good-sperm and sexy-sperm (GS-SS) hypotheses predict that female multiple mating (polyandry) can fuel sexual selection for heritable male traits that promote success in sperm competition. A major prediction generated by these models, therefore, is that polyandry will benefit females indirectly via their sons' enhanced fertilization success. Furthermore, like classic 'good genes' and 'sexy son' models for the evolution of female preferences, GS-SS processes predict a genetic correlation between genes for female mating frequency (analogous to the female preference) and those for traits influencing fertilization success (the sexually selected traits). We examine the premise for these predictions by exploring the genetic basis of traits thought to influence fertilization success and female mating frequency. We also highlight recent debates that stress the possible genetic constraints to evolution of traits influencing fertilization success via GS-SS processes, including sex-linked inheritance, nonadditive effects, interacting parental genotypes, and trade-offs between integrated ejaculate components. Despite these possible constraints, the available data suggest that male traits involved in sperm competition typically exhibit substantial additive genetic variance and rapid evolutionary responses to selection. Nevertheless, the limited data on the genetic variation in female mating frequency implicate strong genetic maternal effects, including X-linkage, which is inconsistent with GS-SS processes. Although the relative paucity of studies on the genetic basis of polyandry does not allow us to draw firm conclusions about the evolutionary origins of this trait, the emerging pattern of sex linkage in genes for polyandry is more consistent with an evolutionary history of antagonistic selection over mating frequency. We advocate further development of GS-SS theory to take account of the complex evolutionary dynamics imposed by sexual conflict over mating frequency.     

Gall insects and selection on plant vigor: can susceptibility compromise success in competition?

Gall insects select vigorously growing plants and plant parts when initiating gall formation. Vigor is associated with rapid growth rate, and in turn, rapid growth confers competitiveness. Are there conditions under which the cost of vigor, in the form of increased susceptibility to attack, outweighs the benefit of competitive success? I present a simulation model to explore the interaction between susceptibility and competition on the selective advantage of increased growth rate. Assuming size-symmetric competition, the model shows that in general, vigor is favored (benefit > cost) at low to intermediate gall loads. At very high plant densities, however, plants with high gall loads may lose standing in the competitive size hierarchy from which they cannot recover. The details of this result, however, change somewhat when competition is size-asymmetric, that is, when a larger focal plant suppresses smaller neighbors, but smaller neighbors cannot exert a reciprocal effect on the focal. At low densities, the pattern of selection on growth rate is qualitatively similar to the size-symmetric case. At higher plant densities, however, fast-growing genotypes can suppress slow ones so much during the preattack phase that even at the highest gall loads they maintain their standing in the competitive hierarchy. Thus, heavy gall insect attack on vigorous plants can impose selection against high intrinsic growth rates under strong symmetric competition, but not strong asymmetric competition. While life history traits can evolve as a correlated response to selection on defensive traits that reduce susceptibility, this model reveals that susceptibility can evolve as a correlated response to selection on basic life history traits.     

Maternal investment and male reproductive success in angiosperms: parent-offspring conflict or sexual selection?

It is possible to interpret components of seed development in angiosperms from the perspective of parent-offspring conflict (a special case of kin selection) or sexual selection. Available parent-offspring conflict models predict the evolution of traits determining the outcome of competition among related individuals soliciting maternal resources. In such models, ‘selfishness’ may spread even if it reduces female fecundity and thus population mean fitness may decline. These models are limited, however, because most of them do not simultaneously consider selection among maternal genotypes varying in the tendency to respond to their offspring. Available sexual selection models, in contrast, do consider the joint evolution of polygenic male traits (influencing viability, mating success and fecundity) and female preferences (influencing the mating success of different male phenotypes). These models have shown that male traits may evolve that are non-optimal with respect to viability. Only one recent sexual selection model explicitly incorporates direct fecundity selection upon females; this model concludes that fecundity will be maximized at equilibrium. Hence population mean fitness may decline due to reduced male viability but not due to diminished female fecundity. Available sexual selection models, however, are limited because they do not consider the effects of interactions among relatives. The assumptions and qualitative results of the two types of models are compared and discussed in the context of seed development. Differential allocation of maternal resources among genetically distinct developing seeds may be viewed from the perspective of either. Because the results of the available models of parent-offspring conflict and sexual selection are not wholly consistent and because data confirming the genetic basis of maternal patterns of investment or differential male reproductive success are scant, it is not clear which set of conclusions is most appropriate to apply to plants. To achieve the generality towards which mathematical approaches aspire, new models concerning the evolution of traits influencing resource allocation in plants must incorporate the components of both parent-offspring conflict and sexual selection.     

How does competition affect the transmission of information?

The use of social information is a prerequisite to the evolution of culture. In humans, social learning allows individuals to aggregate adaptive information and increase the complexity of technology at a level unparalleled in the animal kingdom. However, the potential to use social information is related to the availability of this type of information. Although most cultural evolution experiments assume that social learners are free to use social information, there are many examples of information withholding, particularly in ethnographic studies. In this experiment, we used a computer-based cultural game in which players were faced with a complex task and had the possibility to trade a specific part of their knowledge within their groups. The dynamics of information transmission were studied when competition was within- or exclusively between-groups. Our results show that between-group competition improved the transmission of information, increasing the amount and the quality of information. Further, informational access costs did not prevent social learners from performing better than individual learners, even when between-group competition was absent. Interestingly, between-group competition did not entirely eliminate access costs and did not improve the performance of players as compared with within-group competition. These results suggest that the field of cultural evolution would benefit from a better understanding of the factors that underlie the production and the sharing of information.     

Understanding reversals in the relative strength of sexual selection on males and females: a role for sperm competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.     

Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory?

Sperm competition theory predicts that sperm traits influencing male fertilizing ability will evolve adaptively. However, it has been suggested that some sperm traits may be at least partly encoded by mitochondrial genes. If true, this may constrain the adaptive evolution of such traits because mitochondrial DNA (mtDNA) is maternally inherited and there is thus no selection on mtDNA in males. Phenotypic variation in such traits may nevertheless be high because mutations in mtDNA that have deleterious effects on male traits, but neutral or beneficial effects in females, may be maintained by random processes or selection in females. We used backcrossing to create introgression lines of seed beetles (Callosobruchus maculatus), carrying orthogonal combinations of distinct lineages of cytoplasmic and nuclear genes, and then assayed sperm viability and sperm length in all lines. We found sizeable cytoplasmic effects on both sperm traits and our analyses also suggested that the cytoplasmic effects varied across nuclear genetic backgrounds. We discuss some potential implications of these findings for sperm competition theory.     

Prior residence effect determines success of male–male territorial competition in a color polymorphic poison frog

Male–male competition shapes resource distributions and reproductive success among individuals, and can drive trait evolution when phenotypes differ in competitive abilities and/or strategies. Divergence of populations, regardless of the cause, is often accompanied by divergence in male competitive ability, and such asymmetries can play an important role in mediating the interactions and evolutionary trajectory of the nascent lineages. Here, we designed a field experiment to examine the importance of color, a divergent trait, in determining territorial contest outcomes in the poison frog Oophaga pumilio. Males of different O. pumilio color morphs differ in aggression level, suggesting a potential dominance hierarchy between these divergent phenotypes. In a contact zone between red and blue-color morphs, we first removed territorial males from their calling sites, and examined whether certain color morph(s) were better at establishing in these now-vacant territories. We then staged a territorial contest by simultaneously releasing the original and the new occupant to their point of capture. Surprisingly, we found no significant effect of color on acquiring territories or winning staged contests. However, the original occupants won against the new occupant in 84% of the staged contests, revealing a strong prior residence effect. This suggests that asymmetries that stem from prior residency override coloration in predicting contest outcomes of male–male territorial contests in wild O. pumilio. Thus, contradicting our hypothesis, male–male territorial competition alone seems unlikely to exert selection on coloration in this contact zone.     

How does the magnitude of genetic variation affect ecological and reproductive character displacement?

While previous studies on character displacement tended to focus on trait divergence and convergence as a result of long-term evolution, recent studies suggest that character displacement can be a special case of evolutionary rescue, where rapid evolution prevents species extinction by weakening interspecific competition. Here we analyzed a simple model to examine how the magnitude of genetic variation affects evolutionary rescue via ecological and reproductive character displacement that weakens interspecific competition in exploitation of shared resources (i.e., resource competition) and in the mating process caused by incomplete species recognition (i.e., reproductive interference), respectively. We found that slow trait divergence due to small genetic variance results in species extinction in reproductive character displacement but not in ecological character displacement. This is because one species becomes rare in slow character displacement, and this causes deterministic extinction due to minority disadvantage of reproductive interference. On the other hand, there is no deterministic extinction in the process of ecological character displacement. Furthermore, species extinction becomes less likely in the case of positive covariance between ecological and reproductive traits as divergence of the ecological trait (e.g., root depths) increases the divergence speed of the reproductive trait (e.g., flower colors) and vice versa. It will be interesting to compare intraspecific genetic (co)variance of ecological and reproductive traits in future studies for understanding how ecological and reproductive character displacement occur without extinction.     

Ejaculate evolution in external fertilizers: Influenced by sperm competition or sperm limitation?

The evolution of sperm quality and quantity is shaped by various selective processes, with sperm competition generally considered the primary selective agent. Particularly in external fertilizers, however, sperm limitation through gamete dispersal can also influence gamete investments, but empirical data examining this effect are limited. Here, we studied the relative importance of sperm competition and the spawning conditions in explaining the macroevolutionary patterns of sperm size and number within two taxa with external fertilization but differences in their reproductive biology. In frogs, sperm swim slowly but for up to hours as they penetrate the gelatinous egg coating, whereas fish sperm typically swim fast, are very short‐lived (seconds to minutes), and often face a relatively higher risk of being moved away from the ova by currents. Our phylogenetic models and path analyses revealed different trajectories of ejaculate evolution in these two taxa. Sperm size and number responded primarily to variation in sperm competition in the anurans, but more strongly to egg number and water turbulence in the fishes. Whereas the results across anurans align with the general expectation that sexual selection is the main driver of ejaculate evolution, our findings across the fishes suggest that sperm limitation has been underappreciated.     

How does fertility of the substrate affect intraspecific competition? Evidence and synthesis from self-thinning

When dense populations of even-aged plant monocultures are subject to intense competition, mortality can occur in a process known as self-thinning, in which changes in biomass are accompanied by decreases in density. On a plot of log biomass versus log density, self-thinning populations show a linear relationship called the self-thinning line. Variations in the fertility level of the substrate are known to affect self-thinning in a number of ways. Populations from substrates with different fertility levels have been observed to self-thin along the same line, or along different lines. A review of several experiments using the one species grown at different fertility levels was undertaken to look for any mechanisms that might account for the different patterns observed. It was postulated that the critical difference between whether populations followed a common or different line was the way in which competition developed in the stands as biomass accumulated. For the common-line pattern, data on the canopy volume required to support a given biomass showed that biomass packing did not differ between fertility levels, supporting the model of a common competitive mechanism operating at all fertility levels. When different lines were observed, the development of competition differed as plants increased in size and biomass accumulated at each fertility level. Over the upper range of fertility levels, biomass packing values per plant increased as fertility declined and the position of self-thinning lines followed predictions from biomass packing data. At the low end of the fertility scale, biomass packing values still decreased with fertility level, but the position of self-thinning lines was not linked to the biomass packing of individual plants: root interactions were presumed to dominate competition and the trajectory of self-thinning lines.     

Does competition for nests affect genetic monogamy in Cory's shearwater Calonectris diomedea?

Most bird species are socially monogamous. However, extra‐pair copulations (EPCs), resulting in extra‐pair paternity (EPP), commonly occur. EPCs should allow females to adjust social mate choice and allow males that fail to obtain a nest a chance to avoid missing a breeding season, especially when poor nest supply constrains social mate choice. Procellariiformes (albatrosses and petrels) are socially monogamous seabirds which seldom divorce, even when nest availability constrains social mate choice. In Cory's shearwater Calonectris diomedea, a burrow‐nesting petrel, two studies conducted in the Mediterranean, where competition for nests is weak, detected no EPP. EPP remains to be investigated at localities where competition for nests is much stronger, such as Vila islet, Azores archipelago, Atlantic Ocean. We conducted a genetic (microsatellites) study over two successive years on Vila, involving the breeding pairs of the same 65 nests each year and their single chick. EPPs occurred each year, the overall rate being 11.6%. Coupling genetic analyses to a 7‐year demographic survey provided additional data on pair bonds and competition for nests. Overall, cuckoldry was unrelated to divorce, nest density and inbreeding avoidance, but was more frequent when the social male was small. Nest changes were more costly for males than for females, and some apparently unpaired males attempted to dislodge social males during within‐pair copulations. These results are compatible with the existence of a link between poor nest availability and EPP and confirm that even species considered strongly monogamous can adopt flexible mating strategies.     

Correlation between male size and territory quality: consequence of male competition or predation susceptibility?

Territory characteristics correlate with male characteristics in several species. This can result from male competition for the best territories, or from males varying in their ability to pay other costs of territoriality, such as predation risk costs. In a population of threespine sticklebacks, Gasterosteus aculeatus , we found the biggest males to defend the biggest territories with a low structural complexity and a high female encounter rate. By experimentally manipulating competition intensity and habitat structure, we show that both male competition and predation exposure influenced the distribution of territories among males. Males increased the size of their territory when a neighbouring male was removed, whereas they reduced their territory when habitat complexity and cover from predators were reduced, with large males reducing their territory size less than smaller males. This suggests that large males occupy large, open territories both because of their superior competitive ability and because of their either lower predation susceptibility or higher risk-taking. Large, open territories were beneficial in mate attraction and male competition and predation exposure therefore biased mating opportunities towards large males. This suggests that cost of territoriality to males may reduce mate choice costs to females by securing that large males are encountered more often than small males, and by providing an additional cue, territory quality, which indicates which males are worth inspecting.     

Male–female relatedness and patterns of male reproductive investment in guppies

Inbreeding can cause reductions in fitness, driving the evolution of pre- and postcopulatory inbreeding avoidance mechanisms. There is now considerable evidence for such processes in females, but few studies have focused on males, particularly in the context of postcopulatory inbreeding avoidance. Here, we address this topic by exposing male guppies (Poecilia reticulata) to either full-sibling or unrelated females and determining whether they adjust investment in courtship and ejaculates. Our results revealed that males reduce their courtship but concomitantly exhibit short-term increases in ejaculate quality when paired with siblings. In conjunction with prior work reporting cryptic female preferences for unrelated sperm, our present findings reveal possible sexually antagonistic counter-adaptations that may offset postcopulatory inbreeding avoidance by females.     

Intrasexual competition in females: evidence for sexual selection?

In spite of recent interest in sexual selection in females, debate exists over whether traits that influence female-female competition are sexually selected. This review uses female-female aggressive behavior as a model behavioral trait for understanding the evolutionary mechanisms promoting intrasexual competition, focusing especially on sexual selection. I employ a broad definition of sexual selection, whereby traits that influence competition for mates are sexually selected, whereas those that directly influence fecundity or offspring survival are naturally selected. Drawing examples from across animal taxa, including humans, I examine 4 predictions about female intrasexual competition based on the abundance of resources, the availability of males, and the direct or indirect benefits those males provide. These patterns reveal a key sex difference in sexual selection: Although females may compete for the number of mates, they appear to compete more so for access to high-quality mates that provide direct and indirect (genetic) benefits. As is the case in males, intrasexual selection in females also includes competition for essential resources required for access to mates. If mate quality affects the magnitude of mating success, then restricting sexual selection to competition for quantity of mates may ignore important components of fitness in females and underestimate the role of sexual selection in shaping female phenotype. In the future, understanding sex differences in sexual selection will require further exploration of the extent of mutual intrasexual competition and the incorporation of quality of mating success into the study of sexual selection in both sexes.     

Porcine oviduct sperm binding glycoprotein and its deleterious effect on sperm: a mechanism for negative selection of sperm?

In their journey through the oviduct some subpopulations of sperm are preserved in a reservoir, while others are negatively selected. Sperm binding glycoprotein (SBG) is a pig oviductal epithelial cell glycoprotein that produces, under capacitating conditions, acrosome alteration, p97 tyrosine-phosphorylation and reduction of the motility of sperm. In this paper, we show that SBG is accessible at the extracellular surface of the oviductal epithelial cells, supporting a sperm interaction biological role in situ. We analyze the possible dependence of the tyrosine-phosphorylation of p97 on the PKA mechanism, finding that apparently it is not PKA dependent. Also, after SBG treatment the phosphorylated proteins locate mainly at the detached periacrosomal region and at the tail of sperm; the latter may be related to SBG's motility reduction effect. The study of the time course effect of SBG on sperm as detected by chlortetracycline (CTC) staining and of its binding to sperm by immunodetection in conjunction with CTC, shows results in agreement with the hypothesis that this glycoprotein is involved in the alteration of acrosomes in a specific sperm subpopulation. The results suggest that SBG may be part of a mechanism for negative selection of sperm.     

Female aggression in red deer: Does it indicate competition for mates?

Female–female competition over mates is often considered of minor importance, particularly in polygynous species. In red deer (Cervus elaphus), female–female aggression within harems during the breeding season has not been studied to date. Herein, we examined if oestrous female red deer in harems show elevated aggression rates, compared to when they are in harems but not in oestrous, and also when they are in foraging groups outside of the breeding season. Any increased levels of aggression involving oestrous females, could indicate the potential for female–female competition for mates in this species. We found that aggressive interactions among female red deer were clearly evident. The most common forms of aggression were displacements, nose threats and kicking. Biting and ear threats occurred less frequently, and chases were rare. There were no differences in the proportion of the different aggression types in the three social contexts. More importantly, we found that the highest overall rates of aggression were for oestrous females in harems, and for females in foraging groups. The lowest rates of aggression were found in harems (when the focal female was not in oestrous). If high rates of aggression also occur when several females are simultaneously in oestrous within single harems, then it is possible that this aggression could affect either mate choice or mating order. These results suggest that female–female competition over mates could play a role in the mating behaviour of red deer.     

Avian egg colour and sexual selection: does eggshell pigmentation reflect female condition and genetic quality?

Avian egg colour has been explained as mainly serving crypsis or mimetism, although the function of certain colours (e.g. blue and green) has not yet been demonstrated. We interpret egg colour as a sexually selected signal of the laying female's genetic quality to its mate in order to induce a higher allocation of paternal care. The blue–green pigment biliverdin is an antioxidant, the deposition of which may signal antioxidant capacity whereas the deposition of the brown pigment protoporphyrin, a pro‐oxidant, may signal tolerance of oxidative stress. Egg ground colour is presumably heritable and phylogenetically labile. The hypothesis can be applied to animals with colourful eggs and paternal care.     

Why do multiple traits determine mating success? Differential use in female choice and male competition in a water boatman

Mating success is often determined by multiple traits, but why this occurs is largely unknown. Much attention has been paid to female preferences for multiple traits, but surprisingly few researchers have addressed the possibility that multiple traits are important because they serve different functions in female choice and male-male competition. Differential trait function could result from a conflict of interest between the sexes or from constraints forcing the sexes to pay attention to different traits. I show that traits determined at distinct life-history stages differ in their importance in female choice and male-male competition in a water boatman Sigara falleni. Juvenile conditions determined body and foreleg pala size and were the main determinants of mating success under female choice, whereas adult conditions determined body mass and influenced mating success when male competition was included. This differential use of condition-dependent traits under the two selection regimes appeared to arise partly from a conflict between the sexes, since the two selection forces (female choice and male competition) conflict for selection on pala size, and partly from constraints, as females appeared unable to assess adult condition.