The Eco-Evolutionary Dynamics of Sexual Traits That Increase Mate Encounter Rates.

In anisogamous species, sexual selection is expected to be stronger in males. Bateman's principles state that the variance in (i) reproductive and (ii) mating success is greater for males, and (iii) the relationship between reproductive success and mating success (the Bateman gradient) is also stronger for males than for females. Sexual selection, based on Bateman's principles, has been demonstrated in animals and some angiosperms, but never in a seaweed. Here we focus on the oogamous haploid-diploid rhodophyte Gracilaria gracilis in which previous studies have shown evidence for non-random mating, suggesting the existence of male-male competition and female choice. We estimated mating and reproductive success using paternity analyses in a natural population where up to 92% of fertilizations occurred between partners of that population. The results show that the variance in mating success is significantly greater in males than in females and that the Bateman gradient is positive only in males. Distance to female partners also explains a minor part of the variance in male mating success. Although there is no evidence for sexual dimorphism, our study supports the hypothesis that sexual selection occurs in G. gracilis, probably on male traits, even if we cannot observe, characterize or quantify them yet.

In a recent paper Wade and Arnold (1980) provide an elegant framework for the empirical study of sexual selection. They point out that an evolutionary response to sexual selection is dependent on both the intensity of selection and the heritability of fitness. While the heritability of fitness or its components would be very difficult to measure in most field populations, the parameters necessary for an estimation of the intensity of selection can often be obtained. Their paper focuses on measures of the intensity of, or opportunity for, sexual selection on males and shows this intensity to be equal to the variance in number of mates per individual divided by the square of the mean number of mates. Though variation among individuals in mating success is an obvious requirement for the operation of sexual selection, surprisingly few studies have succeeded in documenting the extent of such individual differences in natural populations. While empirical studies of sexual selection have been quite successful in documenting those morphological or behavioral characteristics that determine mating success in a variety of species, actual measures of variance in mating success or the intensity of sexual selection in natural populations are rarer. This is particularly true when mating success is considered over the lifetime of the organism rather than a single breeding season. Considerations of variance in mating success measured over the lifetime of the study organisms must take into account both the intraand intersexual interactions commonly associated with sexual selection and any variation in survivorship during the reproductive period that is usually associated with natural selection. Because the expression of an individual's mating ability is conditional on surviving to a given mating opportunity, a long-lived individual could accrue more mates than a shorter-lived competitor simply because he experiences more opportunities for encountering mates. Thus, the intensity of both natural and sexual selection must be considered when one uses the total number of mates acquired in a lifetime as a measure of fitness. The question then arises as to whether differences between males in their ability to find and court females (mating efficiency) or differences between males in survivorship after onset of reproduction contribute more to the total variance in the fitness of males. In understanding the evolution of life-history or mating strategies it would also be important to know if there are any phenotypic or genetic correlations between these two components of variance; such correlations have been identified by Arnold and Wade (unpubl.) as cointensities or the covariance between fitnesses at sequential episodes of selection. In order to estimate variance among individuals in number of mates one must be able to recognize individuals, identify their whereabouts during the mating season or seasons, and identify mating events. These criteria are most often met in vertebrate mating systems and accurate measures of mating success have been made for several such systems (e.g., Howard, 1979; Payne, 1979; Downhower and Brown, 1980). Few studies follow individuals through more than one breeding season, however, and thus measures of variance in lifetime mating success or fitness are virtually non-existent. Studies of invertebrates rarely examine

The sexually dimorphic ornaments and songs of birds are generally thought to be the result of sexual selection. For some time, variation in dimorphism among taxa was attributed to differences in social mating patterns. However, extrapair mating provides an alternative mechanism for sexual selection in both monogamous and polygynous birds. In monogamous systems, extrapair mating typically increases variance in mating success and hence sexual selection. However, it is less clear how extrapair mating influences sexual selection in polygynous species. We measured sexual selection acting on 6 sexually dimorphic male traits in a polygynous songbird, the dickcissel (Spiza americana). We also examined patterns of association between social and extrapair mating success, between male traits and reproductive success within each mating context, and the contribution of each type of mating to overall reproductive success. Despite high variance in both mating success and male traits, we found no evidence for current sexual selection in dickcissels. Indeed, variance among males in dimorphic traits did not significantly contribute to male success in any mating context. These results add to an array of studies uncovering relatively weak sexual selection in polygynous species. It is possible that, in contrast to monogamous systems, extrapair paternity weakens sexual selection in polygynous systems. In addition, natural selection arising from high predation and interspecific brood parasitism, stochastic processes, or annual variation in selective pressures may also weaken sexual selection in this species.

Despite a central line of research aimed at quantifying relationships between mating success and sexually dimorphic traits (e.g., ornaments), individual variation in sexually selected traits often explains only a modest portion of the variation in mating success. Another line of research suggests that a significant portion of the variation in mating success observed in animal populations could be explained by correlational selection, where the fitness advantage of a given trait depends on other components of an individual's phenotype and/or its environment. We tested the hypothesis that interactions between multiple traits within an individual (phenotype dependence) or between an individual's phenotype and its social environment (context dependence) can select for individual differences in behaviour (i.e., personality) and social plasticity. To quantify the importance of phenotype- and context-dependent selection on mating success, we repeatedly measured the behaviour, social environment and mating success of about 300 male stream water striders, Aquarius remigis. Rather than explaining individual differences in long-term mating success, we instead quantified how the combination of a male's phenotype interacted with the immediate social context to explain variation in hour-by-hour mating decisions. We suggest that this analysis captures more of the mechanisms leading to differences in mating success. Males differed consistently in activity, aggressiveness and social plasticity. The mating advantage of these behavioural traits depended on male morphology and varied with the number of rival males in the pool, suggesting mechanisms selecting for consistent differences in behaviour and social plasticity. Accounting for phenotype and context dependence improved the amount of variation in male mating success we explained statistically by 30-274%. Our analysis of the determinants of male mating success provides important insights into the evolutionary forces that shape phenotypic variation. In particular, our results suggest that sexual selection is likely to favour individual differences in behaviour, social plasticity (i.e., individuals adjusting their behaviour), niche preference (i.e., individuals dispersing to particular social conditions) or social niche construction (i.e., individuals modifying the social environment). The true effect of sexual traits can only be understood in interaction with the individual's phenotype and environment.

Many studies of sexual selection assume that individuals have equal mating opportunities and that differences in mating success result from variation in sexual traits. However, the inability of sexual traits to explain variation in male mating success suggests that other factors moderate the strength of sexual selection. Extrapair paternity is common in vertebrates and can contribute to variation in mating success and thus serves as a model for understanding the operation of sexual selection. We developed a spatially explicit, multifactor model of all possible female-male pairings to test the hypothesis that ecological (food availability) and social (breeding density, breeding distance, and the social mate's nest stage) factors influence an individual's opportunity for extrapair paternity in a socially monogamous bird, the black-throated blue warbler, Setophaga caerulescens. A male's probability of siring extrapair young decreased with increasing distance to females, breeding density, and food availability. Males on food-poor territories were more likely to sire extrapair young, and these offspring were produced farther from the male's territory relative to males on food-abundant territories. Moreover, males sired extrapair young mostly during their social mates' incubation stage, especially males on food-abundant territories. This study demonstrates how ecological and social conditions constrain the spatial and temporal opportunities for extrapair paternity that affect variation in mating success and the strength of sexual selection in socially monogamous species.

Sexual Selection and Variance in Reproductive Success

The mechanisms of sexual selection in a lek-breeding anuran, Hyla intermedia

Males of the coreid bug, Margus obscurator (F.), were individually numbered in the field in southeastern Georgia (USA) and censused daily for the 6 weeks in spring from the initiation of mating activity until the complete decline of the adult population. Data was analyzed for the subset of males sighted at least 5 times since the relationship between number of observations and variance in mating success leveled off at five observations. Variance in male mating success exceeded that generated by null models, suggesting a phenotypic determinant of mating success. Body length was significantly positively correlated with male mating success. Longer males were more likely to retain a grasp on females which resist, by fleeing, most courting males. The intensity of sexual selection (standardized selection differential) on male size was greater in the second half of the season (0.43 versus 0.21) when both host plant abundance and the proportion of females in the population had declined. Consequently, male density and the number of intermale aggressive interactions increased. During fights, larger males were more likely to retain access to females or the flower heads on which mating occurred. The opportunity for sexual selection (= squared coefficient of variation for mating success) was also greater in the second half of the season (0.90 versus 0.20). The opportunity for sexual selection increased 2.5 times faster than the intensity of sexual selection on size between halves of the season, reflecting the greater male-bias in the operational sex ratio (proportion of males = 0.57 versus 0.49), a more patchy distribution of females and, perhaps, reflecting the operation of additional components of phenotypic selection.

Alternative male phenotypes may be a source of novel adaptive traits and may evolve under strong sexual selection. We studied interpopulation differences in male mating behavior related to receptive female synchrony in the monandrous pupal-mating butterfly Heliconius charitonia. In the population in which female-receptive pupae were more synchronous, larger males were unable to monopolize mates; variance in male mating success was lower; strength of sexual selection was weak; and all males competed for access to female pupae using the same strategy (pupal mating). In the population where no more than one female was receptive at a time (extreme asynchrony), only large males competed for pupae, and among these, only the largest individuals successfully mated. Thus, variance in mating success was higher, and sexual selection within pupal maters was stronger. In this population, smaller males patrolled large areas as an alternative mating behavior. When unmated females were experimentally released, small male size was associated with higher mating success. We suggest that alternative patrolling behavior may have evolved under strong sexual selection as a consequence of high asynchrony in receptive female availability in some populations.

Sexual selection is thought to be a powerful diversifying force, based on large ornamental differences between sexually dimorphic species. This assumes that unornamented phenotypes represent evolution without sexual selection. If sexual selection is more powerful than other forms of selection, then two effects would be: rapid divergence of sexually selected traits and a correlation between these divergence rates and variance in mating success in the ornamented sex. I tested for these effects in grouse (Tetraonidae). For three species pairs, within and among polygynous clades, male courtship characters had significantly greater divergence than other characters. This was most pronounced for two species in Tympanuchus. In the Eurasian polygynous clade, relative courtship divergence gradually increased with nucleotide divergence, suggesting a less dramatic acceleration. Increase in relative courtship divergence was associated with mating systems having higher variance in male mating success. These results suggest that sexual selection has accelerated courtship evolution among grouse, although the microevolutionary details appear to vary among clades.

Through a series of replacement experiments with the bluehead wrasse, Thalassoma bifasciatum, we have identified male morphological characteristics that appear to be under phenotypic sexual selection. We were particularly interested in whether the various sources of sexual selection (male-male competition for unoccupied mating sites, defense of mating sites against small males, and female choice of males) were (1) independently associated with different phenotypic characteristics; (2) jointly affected the same characteristic in the same way; or (3) jointly affected the same characteristic in an antagonistic fashion. We replaced the resident large, brightly colored Terminal Phase (TP) males on a reef with the same number of TP males from other reefs. When transplanted, these males contest with each other to take over mating sites. The transplanted group of males were then scored for three components of fitness: (1) the quality of the site obtained through competition with other large males; (2) the male's ability to defend arriving females from small intruding males; and (3) changes in female visits to the site once the new male takes over. The first and second components are part of intrasexual selection; the third represents intersexual selection. We measured the opportunity for selection by partitioning variance in mating success, and measured the direct effects of sexual selection by estimating the covariance between morphology and fitness components. Opportunities for selection: Because females generally remain faithful to particular mating sites, most (54%) of the explainable variation in male mating success is due to the acquisition of a particular mating territory, which is the outcome of competition among TP males. There was less variation in mating success due to shifts in site use by females and defense of females against the intrusions of smaller males, but all components were significant. Effects of selection: Success in male-male competition among TP males, estimated by the quality of the territory acquired, was positively associated with body length and the relative length of the pectoral fin. Success in territorial defense against small males was primarily related to body length, with lesser contributions from body depth and the area of a white band on the flank. Contribution to fitness through female choice of males was positively associated with white band area. In the two instances where a character was associated with two fitness components, the direction of selection was the same. While body length was positively associated with winning intrasexual contests, it was not correlated to any behavioral measures of aggression. Similarly, the white band associated with attractiveness was not correlated with any aspect of courtship or aggression. Parasite load was uncorrelated with other morphological characters, and did not appear to affect any aspect of sexual selection. There was no evidence for stabilizing selection or significant additional contributions from second-order effects to the fitness surfaces. Fitness functions calculated using cubic splines were generally linear except for body length, which appeared sigmoid in its effect on site acquisition ability; this same feature tended to plateau in its effect on site defense. Analyses of the interactions of selection gradients with reef or experiment indicated that the effect of particular male characters on estimates of fitness was generally homogeneous in both time and space.

Mating systems are defined by the pattern of matings among individuals in a population, including the number of mates obtained by each female and male, and the duration of pair bonds. Within all mating systems, mate choice, intra‐sexual competition, and sperm competition may lead to variation in mating success among individuals. Growing evidence indicates that quantification of the patterns and processes of mating may be critical to understanding population dynamics. Atlantic cod had been fished for hundreds of years and was one of the most important commercial fish species worldwide until the recent collapse of many populations. Despite being of theoretical interest and practical importance, little was known about this species’ reproductive behaviour. Our research employed a quantitative approach to understand causes and consequences of variation in the mating system of Atlantic cod at the individual and population levels. We incorporated both detailed behavioural studies in the laboratory and observations of cod captured in the commercial fishery. Preliminary observations indicate tremendous variation in reproductive behaviour and mating success both within and between populations. Furthermore, variation in reproductive behaviour and mating success appears to be related to the ability of males to produce sound. Knowledge of Atlantic cod spawning behaviour will likely contribute to better understanding of population dynamics and improved ability to predict the impact of fishing on cod populations.

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.

Operational sex ratio (OSR), the ratio of sexually active males to fertilizable females in a population, plays a central role in the theory of mating systems by predicting that the intensity of male–male competition and the degree of sexual selection increases as the OSR becomes increasingly male biased. At high values of OSR, however, resource defence theory predicts the breakdown of territoriality and a shift towards scramble competition with a decrease in sexual selection. The direction that correlations between OSR and resource competition and variance in mating success will take depends on the biology of the species of interest. We investigated the effects of male population density and male‐biased operational sex ratio on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus. This species spawns inside living unioneid mussels. Large males defended territories, were aggressive towards conspecifics under equal sex ratios and monopolized pair spawnings with females. The mating tactic, however, changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. This change in male behaviour from pair to group spawning has two ramifications for sexual selection. The intensity of sexual selection and variance in male mating success decrease, and the form of sexual competition changes from resource‐ to sperm competition. Thus, the use of alternative mating tactics renders the OSR unable to predict the direction of resource competition and variance in male mating success at high densities.

Mating systems and patterns of reproductive success in fishes play an important role in ecology and evolution. While information on the reproductive ecology of many anadromous salmonids (Oncorhynchus spp.) is well detailed, there is less information for nonanadromous species including the Yellowstone Cutthroat Trout (O. clarkii bouvieri), a subspecies of recreational angling importance and conservation concern. Using data from a parentage‐based tagging study, we described the genetic mating system of a migratory population of Yellowstone Cutthroat Trout, tested for evidence of sexual selection, and identified predictors of mating and reproductive success. The standardized variance in mating success (i.e., opportunity for sexual selection) was significantly greater for males relative to females, and while the relationship between mating success and reproductive success (i.e., Bateman gradient) was significantly positive for both sexes, a greater proportion of reproductive success was explained by mating success for males (r2 = 0.80) than females (r2 = 0.59). Overall, the population displayed a polygynandrous mating system, whereby both sexes experienced variation in mating success due to multiple mating, and sexual selection was variable across sexes. Tests for evidence of sexual selection indicated the interaction between mating success and total length best‐predicted relative reproductive success. We failed to detect a signal of inbreeding avoidance among breeding adults, but the group of parents that produced progeny were on average slightly less related than adults that did not produce progeny. Lastly, we estimated the effective number of breeders (Nb) and effective population size (Ne) and identified while Nb was lower than Ne, both are sufficiently high to suggest Yellowstone Cutthroat Trout in Burns Creek represent a genetically stable and diverse population.