Postcopulatory fertilization bias as a form of cryptic sexual selection

Males and females share most of their genetic material yet often experience very different selection pressures. Some traits that are adaptive when expressed in males may therefore be maladaptive when expressed in females. Recent studies demonstrating negative correlations in fitness between parents and their opposite-sex progeny suggest that natural selection may favor a reduction in trait correlations between the sexes to partially mitigate intralocus sexual conflict. We studied sex-specific forms of selection acting in Anolis lizards in the Greater Antilles, a group for which the importance of natural selection has been well documented in species-level diversification, but for which less is known about sexual selection. Using the brown anole (Anolis sagrei), we measured fitness-related variation in morphology (body size), and variation in two traits reflecting whole animal physiological condition: running endurance and immune function. Correlations between body size and physiological traits were opposite between males and females and the form of natural selection acting on physiological traits significantly differed between the sexes. Moreover, physiological traits in progeny were correlated with the body-size of their sires, but correlations were null or even negative between parents and their opposite-sex progeny. Although results based on phenotypic and genetic correlations, as well as the action of natural selection, suggest the potential for intralocus sexual conflict, females used sire body size as a cue to sort sperm for the production of either sons or daughters. Our results suggest that intralocus sexual conflict may be at least partly resolved through post-copulatory sperm choice in A. sagrei.     

Postcopulatory sexual selection is associated with accelerated evolution of sperm morphology

Rapid diversification of sexual traits is frequently attributed to sexual selection, though explicit tests of this hypothesis remain limited. Spermatozoa exhibit remarkable variability in size and shape, and studies report a correlation between sperm morphology (sperm length and shape) and sperm competition risk or female reproductive tract morphology. However, whether postcopulatory processes (e.g., sperm competition and cryptic female choice) influence the speed of evolutionary diversification in sperm form is unknown. Using passerine birds, we quantified evolutionary rates of sperm length divergence among lineages (i.e., species pairs) and determined whether these rates varied with the level of sperm competition (estimated as relative testes mass). We found that relative testes mass was significantly and positively associated with more rapid phenotypic divergence in sperm midpiece and flagellum lengths, as well as total sperm length. In contrast, there was no association between relative testes mass and rates of evolutionary divergence in sperm head size, and models suggested that head length is evolutionarily constrained. Our results are the first to show an association between the strength of sperm competition and the speed of sperm evolution, and suggest that postcopulatory sexual selection promotes rapid evolutionary diversification of sperm morphology.     

Postcopulatory sexual selection reduces genetic diversity in experimental populations of Caenorhabditis elegans

Postcopulatory sexual selection affects the evolution of numerous features ranging from mating behavior to seminal fluid toxicity to the size of gametes. In an earlier study of the effect of sperm competition risk on sperm size evolution, experimental populations of the nematode Caenorhabditis elegans were maintained either by outcrossing (sperm competition present) or by selfing (no sperm competition), and after 60 generations, significantly larger sperm had evolved in the outcrossing populations. To determine the effects of this selection on population genetic variation, we assessed genetic diversity in a large number of loci using random amplification of polymorphic DNA-PCR. Nearly 80% of the alleles present in parental strain populations persisted in the 6 experimental populations after the 60 generations and, despite a 2.2-fold difference in expected heterozygosity, the resulting levels of genetic variation were equivalent between the outcrossing and selfing experimental populations. By inference, we conclude that genetic hitchhiking due to sexual selection in the experimental populations dramatically reduced genetic diversity. We use the levels of variation in the selfing populations as a control for the effects of drift, and estimate the strength of sexual selection to be strong in obligatorily outcrossing populations. Although sequential hermaphrodites like C. elegans probably experience little sexual selection in nature, these data suggest that sexual selection can profoundly affect diversity in outcrossing taxa.     

Frequency-dependent sexual selection

Sexual selection by female choice is expected to give rise to a frequency-dependent sexual advantage in favour of preferred male phenotypes: the rarer the preferred phenotypes, the more often they are chosen as mates. This 'rare-male advantage' can maintain a polymorphism when two or more phenotypes are mated preferentially: each phenotype gains an advantage when it is rarer than the others; no preferred phenotype can then be lost from the population. Expression of preference may be complete or partial. In models of complete preference, females with a preference always mate preferentially. Models of partial preference are more realistic: in these models, the probability that a female mates preferentially depends on the frequency with which she encounters the males she prefers. Two different 'encounter models' of partial preference have been derived: the O'Donald model and the Charlesworth model. The encounter models contain the complete preference model as a limiting case. In this paper, the Charlesworth model is generalized to allow for female preference of more than one male phenotype. Levels of frequency dependence can then be compared in the O'Donald and Charlesworth models. The complete preference model and both encounter models are formulated in the same genetical terms of preferences for dominant and recessive male phenotypes. Polymorphic equilibria and conditions for stability are derived for each of the three models. The models are then fitted to data of frequencies of matings observed in experiments with the two-spot ladybird. The complete preference model gives as good a fit as the encounter models to the data of these and other experiments. The O'Donald and Charlesworth encounter models are shown to produce a very similar frequency-dependent relation. Generally, as females become less choosy, they express their preference with more dependence on male frequency, whereas the resulting selection of the males becomes less frequency dependent. More choosy females are more constant in expressing their preference, producing greater frequency dependence in the selection of the males.     

Postcopulatory selection for dissimilar gametes maintains heterozygosity in the endangered North Atlantic right whale

Although small populations are expected to lose genetic diversity through genetic drift and inbreeding, a number of mechanisms exist that could minimize this genetic decline. Examples include mate choice for unrelated mates and fertilization patterns biased toward genetically dissimilar gametes. Both processes have been widely documented, but the long‐term implications have received little attention. Here, we combined over 25 years of field data with high‐resolution genetic data to assess the long‐term impacts of biased fertilization patterns in the endangered North Atlantic right whale. Offspring have higher levels of microsatellite heterozygosity than expected from this gene pool (effect size = 0.326, P < 0.011). This pattern is not due to precopulatory mate choice for genetically dissimilar mates (P < 0.600), but instead results from postcopulatory selection for gametes that are genetically dissimilar (effect size = 0.37, P < 0.003). The long‐term implication is that heterozygosity has slowly increased in calves born throughout the study period, as opposed to the slight decline that was expected. Therefore, this mechanism represents a natural means through which small populations can mitigate the loss of genetic diversity over time.     

The sexual selection continuum

The evolution of mate choice for genetic benefits has become the tale of two hypotheses: Fisher's 'run-away' and 'good genes', or viability indicators. These hypotheses are often pitted against each other as alternatives, with evidence that attractive males sire more viable offspring interpreted as support for good genes and with a negative or null relationship between mating success of sons and other components of fitness interpreted as favouring the Fisher process. Here, we build a general model of female choice for indirect benefits that captures the essence of both the 'Fisherian' and 'good-genes' models. All versions of our model point to a single process that favours female preference for males siring offspring of high reproductive value. Enhanced mating success and survival are therefore equally valid genetic benefits of mate choice, but their relative importance varies depending on female choice costs. The relationship between male attractiveness and survival may be positive or negative, depending on life-history trade-offs and mating skew. This relationship can change sign in response to increased costliness of choice or environmental change. Any form of female preference is subject to self-reinforcing evolution, and any relationship (or lack thereof) between male display and offspring survival is inevitably an indicator of offspring reproductive values. Costly female choice can be maintained with or without higher offspring survival.     

The social selection alternative to sexual selection

Social selection offers an alternative to sexual selection by reversing its logic. Social selection starts with offspring production and works back to mating, and starts with behavioural dynamics and works up to gene pool dynamics. In social selection, courtship can potentially be deduced as a negotiation, leading to an optimal allocation of tasks during offspring rearing. Ornaments facilitate this negotiation and also comprise 'admission tickets' to cliques. Mating pairs may form 'teams' based on the reciprocal sharing of pleasure. The parent-offspring relation can be managed by the parent considered as the owner of a 'family firm' whose product is offspring. The cooperation in reproductive social behaviour evolves as a mutual direct benefit through individual selection rather than as some form of altruism requiring kin or multi-level selection.     

Copying and sexual selection

Recent studies of a variety of polygynously mating animals indicate that females do not always choose mates independently, but instead may copy the choices of others. Copying could serve either to increase the accuracy of mate assessment or to reduce its costs. It is also likely to affect the intensity of sexual selection.     

Theories of sexual selection

Recent research on sexual selection in animals has begun to indicate that 'handicaps' and 'honest signalling' may play more important roles than hitherto thought. This review reappraises theories of sexual selection in the light of these new developments.     

Humor and sexual selection

Recently Geoffrey Miller has suggested that humor evolved through sexual selection as a signal of "creativity," which in turn implies youthfulness, intelligence, and adaptive unpredictability. Drawing upon available empirical studies, I argue that the evidence for a link between humor and creativity is weak and ambiguous. I also find only tenuous support for Miller’s assumption that the attractiveness of the "sense of humor" is to be found in the wittiness of its possessor, since those who use the phrase often seem to associate it with the affects of relatively mirthless "bonding" laughter. Humor, I conclude, may have evolved as an instrument for achieving broad social adhesiveness and for facilitating the individual’s maneuverability within the group, but that it evolved through sexual selection has yet to be convincingly demonstrated. Robert Storey teaches drama and modern fiction at Temple University. In addition to his recent work on literary representation and humor, he has published two books on the French Pierrot figure and articles on such writers as James Joyce, Alain Robbe-Grillet, and David Mamet.     

Postcopulatory inbreeding avoidance in guppies

In many species, the negative fitness effects of inbreeding have facilitated the evolution of a wide range of inbreeding avoidance mechanisms. Although avoidance mechanisms operating prior to mating are well documented, evidence for postcopulatory mechanisms of inbreeding avoidance remain scarce. Here, we examine the potential for paternity biases to favour unrelated males when their sperm compete for fertilizations though postcopulatory inbreeding avoidance mechanisms in the guppy, Poecilia reticulata. To test this possibility, we used a series of artificial inseminations to deliver an equal number of sperm from a related (either full sibling or half sibling) and unrelated male to a female while statistically controlling for differences in sperm quality between rival ejaculates. In this way, we were able to focus exclusively on postcopulatory mechanisms of inbreeding avoidance and account for differences in sperm competitiveness between rival males. Under these carefully controlled conditions, we report a significant bias in paternity towards unrelated males, although this effect was only apparent when the related male was a full sibling. We also show that sperm competition generally favours males with highly viable sperm and thus that some variance in sperm competitiveness can be attributed to difference in sperm quality. Our findings for postcopulatory inbreeding avoidance are consistent with prior work on guppies, revealing that sperm competition success declines linearly with the level of relatedness, but also that such effects are only apparent at relatedness levels of full siblings or higher. These findings reveal that postcopulatory processes alone can facilitate inbreeding avoidance.     

Fluctuating asymmetry and sexual selection

Fluctuating asymmetry occurs when an individual is unable to undergo identical development on both sides of a bilaterally symmetrical trait. Fluctuating asymmetry measures the sensitivity of development to a wide array of genetic and environmental stresses. We propose that fluctuating asymmetry is used in many signalling contexts for assessment of an individual's ability to cope with its environment. We hypothesize that fluctuating asymmetry is used in sexual selection, both in fighting and mate choice, and in competition for access to resources. Evidence is reviewed showing that the patterns of fluctuating asymmetry in secondary sexual characters differ from those seen in other morphological traits. Secondary sexual characters show much higher levels of fluctuating asymmetry. Also, there is often a negative relationship between fluctuating asymmetry and the absolute size of ornaments, whereas the relationship is typically U-shaped in other morphological traits. The common negative relationship between fluctuating asymmetry and ornament size suggests that many ornaments reliably reflect individual quality.