The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

The opportunity to be misled in studies of sexual selection

It is a challenge to measure sexual selection because both stochastic events (chance) and deterministic factors (selection) generate variation in individuals' reproductive success. Most researchers realize that random events ('noise') make it difficult to detect a relationship between a trait and mating success (i.e. the presence of sexual selection). There is, however, less appreciation of the dangers that arise if stochastic events vary systematically. Systematic variation makes variance-based approaches to measuring the role of selection problematic. This is why measuring the opportunity for sexual selection (I(s) and I(mates)) is so vulnerable to misinterpretation. Although I(s) does not measure actual sexual selection (because it includes stochastic variation in mating/fertilization success) it is often implicitly assumed that it will be correlated with the actual strength of sexual selection. The hidden assumption is that random noise is randomly distributed across populations, species or the sexes. Here we present a simple numerical example showing why this practice is worrisome. Specifically, we show that chance variation in mating success is higher when there are fewer potential mates per individual of the focal sex [i.e. when the operational sex ratio (OSR), is more biased]. This will lead to the OSR covarying with I(s) even when the strength of sexual selection is unaffected by the OSR. This can generate false confidence in identifying factors that determine variation in the strength of sexual selection. We emphasize that in nature, even when sexual selection is strong, chance variation in mating success is still inevitable because the number of mates per individual is a discrete number. We hope that our worked example will clarify a recent debate about how best to measure sexual selection.     

Sex-limited expression of ornamental feathers in birds

Extravagant secondary sexual characters show sexual size dimorphismin some species but are completely sex limited in others. Sexualornamentation has been hypothesized to benefit mainly malesthrough sexual selection, but the costs of secondary sexualcharacters initially would be experienced by both sexes. Theevolution of sexual size dimorphism of ornaments and, eventually,the complete sex-limited expression of these characters, willdepend on the effects of sexual and natural selection on thetwo sexes. A phylogenetic analysis controlling for similaritiesdue to common ancestry of 60 independent evolutionary originsof feather ornamentation in birds was used to investigate ecologicalfactors correlated with sexual size dimorphism and sex-limitedexpression of secondary sexual characters. When the size ofan ornament is large relative to body size, the trait willbe particularly costly for females, resulting in selectionfor increased sexual size dimorphism of the ornament. Indeed,sexual size dimorphism of ornaments was positively relatedto the relative size of male ornaments but was unrelated torelative size of female ornaments. Species with polygynousand lekking mating systems with little or no male parentalcare (in particular nest building and incubation) demonstratedsex-limited expression of ornaments as compared to monogamousspecies. Species with no food provisioning of offspring by themale showed a trend for increased sexual size dimorphism ofornaments. Therefore, large natural selection costs duringreproduction imposed by the expression of secondary sexualcharacters are related to the evolution of sexual size dimorphismof ornaments and eventually their complete loss from females.     

Points of view: Why male cannibalism won't cause a female-biased OSR -- a comment on Smith and Wootton's paper

Reviews in Fish Biology and Fisheries -     

Points of view: Cannibalism and OSR -- a response to Kvarnemo

Reviews in Fish Biology and Fisheries -     

Female pheromonal chorusing in an arctiid moth, Utetheisa ornatrix

We report an unusual case of communal sexual display in thearctiid moth Utetheisa ornatrix that we designate "female pheromonalchorusing." As in most moths, female U. ornatrix release a long-distancesexual advertisement pheromone during a nightly activity period.We arranged U. ornatrix females in 2 types of signaling conditions:grouped and solitary. When the females were grouped with neighboringsignaling females (grouped), they initiated pheromone releasesooner, continued release with less interruption and over alonger total period, and performed the release with faster abdominalpumping than observed in isolated females (solitary). This differsfrom the usual form of sexual communication in moths: female(chemical) signalers, male receivers, and a general lack ofinteraction among females. At mating, male U. ornatrix transfera large spermatophore that may enhance female reproductive successand which represents either mating effort or paternal investment.This action results in an extended postmating male refractoryperiod leading to a female-biased operational sex ratio. Weargue that this biased sex ratio generates intrasexual competitionamong females, to which they respond by elevating signalingeffort such that the likelihood of at least matching their neighbors'signals is increased. In the field, U. ornatrix are clusteredaround patches of host plants, and we also explore the possibilitythat pheromonal chorusing is driven by cooperation among groupsof related—or nonrelated—females.     

Crowding, sex ratio and horn evolution in a South African beetle community

Sexually selected ornaments and weapons are exceptionally variable, even between closely related species. It has long been recognized that some of this diversity can be explained by differences in mating systems between species, but there remains substantial variation between species with similar mating systems. We investigated the roles of sex ratio (measured as operational sex ratio, OSR) and population density (measured as mean male crowding, a measure indicating the average number of conspecific males that an individual male animal will encounter) in determining horn presence in a community of South African dung beetles. Analysis of data from 14 species using a generalized least-squares model incorporating phylogenetic influences found that both OSR and mean crowding were significant predictors of horn presence, with hornless species tending to show female-biased sex ratios and high levels of crowding. The influence of mean crowding on horn diversity between species probably reflects the difficulty of guarding and monopolizing females when many competitors are present, meaning that males who adopt 'scramble' tactics tend to be favoured.     

How choosy should I be? The relative searching time predicts evolution of choosiness under direct sexual selection

Most theoretical research in sexual selection has focused on indirect selection. However, empirical studies have not strongly supported indirect selection. A well-established finding is that direct benefits and costs exert a strong influence on the evolution of mate choice. We present an analytical model in which unilateral mate choice evolves solely by direct sexual selection on choosiness. We show this is sufficient to generate the evolution of all possible levels of choosiness, because of the fundamental trade-off between mating rate and mating benefits. We further identify the relative searching time (RST, i.e. the proportion of lifetime devoted to searching for mates) as a predictor of the effect of any variable affecting the mating rate on the evolution of choosiness. We show that the RST: (i) allows one to make predictions about the evolution of choosiness across a wide variety of mating systems; (ii) encompasses all alternative variables proposed thus far to explain the evolution of choosiness by direct sexual selection; and (iii) can be empirically used to infer qualitative differences in choosiness.     

Sex ratio influences the motivational salience of facial attractiveness

The sex ratio of the local population influences mating-related behaviours in many species. Recent experiments show that male-biased sex ratios increase the amount of financial resources men will invest in potential mates, suggesting that sex ratios influence allocation of mating effort in humans. To investigate this issue further, we tested for effects of cues to the sex ratio of the local population on the motivational salience of attractiveness in own-sex and opposite-sex faces. We did this using an effort-based key-press task, in which the motivational salience of facial attractiveness was assessed in samples of faces in which the ratio of male to female images was manipulated. The motivational salience of attractive opposite-sex, but not own-sex, faces was greater in the own-sex-biased (high competition for mates) than in the opposite-sex-biased (low competition for mates) condition. Moreover, this effect was not modulated by participant sex. These results present new evidence that sex ratio influences human mating-related behaviours. They also present the first evidence that the perceived sex ratio of the local population may modulate allocation of mating effort in women, as well as men.     

Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

Sexual selection theory asserts that females are well adapted to sense signals indicating the quality of potential mates. One crucial male quality parameter is functional fertility (i.e. the success of ejaculates in fertilizing eggs). The phenotype-linked fertility hypothesis (PLFH) predicts that functional fertility of males is reflected by phenotypic traits that influence female mate choice. Here, we show for Nasonia vitripennis, a parasitic wasp with haplodiploid sex determination and female-biased sex ratios, that females use olfactory cues to discriminate against sperm-limited males. We found sperm limitation in newly emerged and multiply mated males (seven or more previous matings) as indicated by a higher proportion of sons in the offspring fathered by these males. Sperm limitation correlated with clearly reduced pheromone titres. In behavioural bioassays, females oriented towards higher doses of the synthetic pheromone and were attracted more often to scent marks of males with a full sperm load than to those of sperm-limited males. Our data support the PLFH and suggest that N. vitripennis females are able to decrease the risk of getting constrained to produce suboptimal offspring sex ratios by orienting towards gradients of the male sex pheromone.