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.     

Opportunities for mate choice in the fission‐performing ant Cataglyphis cursor

1. Sexual selection has been little studied in social insects. Nonetheless, because mating is generally for life, opportunities for selecting among mating partners should be exploited. 2. In some ants, males aggregate at nest entrances to mate with emerging gynes. Both males and females thus have access to multiple mates over a relatively protracted period, giving rise to opportunities for mate choice and multiple mating. 3. We provide data from field observations of the male mating biology of the ant, Cataglyphis cursor Fonscolombe. In this species, females mate with, on average, six males each at the nest entrance and found colonies with the help of workers. 4. Males were present at the field site for approximately 1 month in spring, with up to 40 males at a single nest entrance for, on average, 4.7 days. Individual males were observed to survive up to 3 days, and mate up to eight times. 5. Thus both males and females of this species have the ability to mate multiply and have a window permitting mate choice to occur. Workers actively attacked males and may take part in the mate choice process, making C. cursor an interesting model to study questions relating to sexual selection and male mating strategies.     

Female choice for heterozygous mates changes along successive matings in a lizard

Female mate choice and female multiple mating are major focuses of studies on sexual selection. In a multiple mating context, the benefits of mate choice can change along successive matings, and female choice would be expected to change accordingly. We investigated sequential female mate choice in the moderately polyandrous common lizard (Zootoca vivipara, synonym Lacerta vivipara). Along successive mating opportunities, we found that females were relatively unselective for the first mate, but accepted males of higher heterozygosity for subsequent mating, consistent with the trade-up choice hypothesis. We discuss the evidence of trade-up mate choice in squamates and generally trade-up for mate heterozygosity in order to motivate new studies to fill gaps on these questions.     

Directional selection on body size but no apparent survival cost to being large in wild New Zealand giraffe weevils

When an individual's reproductive success relies on winning fights to secure mating opportunities, bearing larger weapons is advantageous. However, sexual selection can be extremely complex, and over an animal's life the opportunity to mate is influenced by numerous factors. We studied a wild population of giraffe weevils (Lasiorhynchus barbicornis) that exhibit enormous intra and intersexual size variation. Males bear an elongated rostrum used as a weapon in fights for mating opportunities. However, small males also employ sneaking behavior as an alternative reproductive tactic. We investigated sexual selection on size by tracking individual males and females daily over two 30‐day periods to measure long‐term mating success. We also assessed how survival and recapture probabilities vary with sex and size to determine whether there might be a survival cost associated with size. We found evidence for directional selection on size through higher mating success, but no apparent survival trade‐off. Instead, larger individuals mate more often and have a higher survival probability, suggesting an accumulation of benefits to bigger individuals. Furthermore, we found evidence of size assortative mating where males appear to selectively mate with bigger females. Larger and more competitive males secure matings with larger females more frequently than smaller males, which may further increase their fitness.     

The scale‐of‐choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples

The mode in which sexual organisms choose mates is a key evolutionary process, as it can have a profound impact on fitness and speciation. One way to study mate choice in the wild is by measuring trait correlation between mates. Positive assortative mating is inferred when individuals of a mating pair display traits that are more similar than those expected under random mating while negative assortative mating is the opposite. A recent review of 1134 trait correlations found that positive estimates of assortative mating were more frequent and larger in magnitude than negative estimates. Here, we describe the scale‐of‐choice effect (SCE), which occurs when mate choice exists at a smaller scale than that of the investigator's sampling, while simultaneously the trait is heterogeneously distributed at the true scale‐of‐choice. We demonstrate the SCE by Monte Carlo simulations and estimate it in two organisms showing positive (Littorina saxatilis) and negative (L. fabalis) assortative mating. Our results show that both positive and negative estimates are biased by the SCE by different magnitudes, typically toward positive values. Therefore, the low frequency of negative assortative mating observed in the literature may be due to the SCE's impact on correlation estimates, which demands new experimental evaluation.     

SEX RATIO AND DENSITY AFFECT SEXUAL SELECTION IN A SEX‐ROLE REVERSED FISH

Understanding how demographic processes influence mating systems is important to decode ecological influences on sexual selection in nature. We manipulated sex ratio and density in experimental populations of the sex‐role reversed pipefish Syngnathus typhle. We quantified sexual selection using the Bateman gradient (), the opportunity for selection (I), and sexual selection (I_s), and the maximum standardized sexual selection differential (). We also measured selection on body length using standardized selection differentials (s′) and mating differentials (m′), and tested whether the observed I and I_s differ from values obtained by simulating random mating. We found that I, I_s, and , but not , were higher for females under female than male bias and the opposite for males, but density did not affect these measures. However, higher density decreased sexual selection (m′ but not s′) on female length, but selection on body length was not affected by sex ratio. Finally, I_s but not I was higher than expected from random mating, and only for females under female bias. This study demonstrates that both sex ratio and density affect sexual selection and that disentangling interrelated demographic processes is essential to a more complete understanding of mating behavior and the evolution of mating systems.     

Males,but not females,perform strategic mate searching movements between host plants in a leaf beetle with scramble competition polygyny

Mate searching is assumed to be performed mostly by males, but when females benefit from multiple mating or are under risk of failing to mate, they may also perform mate searching. This is especially important in scramble competition polygynies, in which mate searching is the main mechanism of mate competition. Typically, more mobile individuals are expected to achieve higher mating success because mobility increases their probability of finding mates. If we assume individual movements are mainly explained by mate searching in scramble competition polygynies, we can investigate searching strategies by asking when individuals should leave their location and where they should go. We hypothesize that individuals will leave their locations when mating opportunities are scarce and will seek spatially close sites with better mating opportunities. We tested these hypotheses for males and females of Leptinotarsa undecimlineata, a leaf beetle with scramble competition polygyny in which both sexes are promiscuous. Individuals mate and feed exclusively on Solanum plants, and thus, individual movements can be described as switches between plants. Females were less likely than males to leave isolated plants, and both males and females moved preferentially to neighboring plants. Males were more likely to leave when the local number of females was low, and the number of males was high. They moved to plants with more females, a behavior consistent with a mate searching strategy. Females were more likely to move to plants with fewer males and many females, a behavior consistent with male harassment avoidance. Strategic movement is widely considered in foraging context, but seldom in a mate searching context. Considering that selection to minimize searching costs, maximize mating success, and minimize harassment may be ubiquitous in nature, we argue that strategic movements by mate searching individuals are likely to occur in many species.     

Sexual conflict in mammals: consequences for mating systems and life history

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OPERATIONAL SEX RATIO BUT NOT DENSITY AFFECTS SEXUAL SELECTION IN A FISH

The operational sex ratio (OSR) and density are considered important factors affecting the strength of sexual selection. Although there is increasing evidence that OSR and density affect the potential for sexual selection, few studies have addressed whether this is realized in phenotypic selection and how the two factors interact. We manipulated OSR (three levels) and male density (two levels) in 36 experimental breeding populations of Gobiusculus flavescens—a fish with paternal care. We measured mating competition behavior, the opportunity for selection (I), and selection on four morphological traits in males. We found sexual selection on two male traits, with the strongest selection being 20% of I. As predicted from OSR theory, increasing female scarcity caused males to become more competitive, concomitant with an increase in I and selection on morphological traits. Model simulations of I based on random mating (I_min) and maximum mate monopolization (I_max) demonstrated that the potential for sexual selection was close to its theoretical maximum across the range of OSRs. However, male density and its interaction with the OSR did not affect sexual selection. We argue that a multifaceted approach, combining mating behavior and selection analyses, can help us to understand how ecological factors affect sexual selection.     

The opportunity for sexual selection: not mismeasured, just misunderstood

Evolutionary biologists have developed several indices, such as selection gradients (β) and the opportunity for sexual selection (I_s), to quantify the actual and/or potential strength of sexual selection acting in natural or experimental populations. In a recent paper, Klug et al. (J. Evol. Biol. 23 , 2010, 447) contend that selection gradients are the only legitimate metric for quantifying sexual selection. They argue that I_s and similar mating‐system‐based metrics provide unpredictable results, which may be uncorrelated with selection acting on a trait, and should therefore be abandoned. We find this view short‐sighted and argue that the choice of metric should be governed by the research question at hand. We describe insights that measures such as the opportunity for selection can provide and also argue that Klug et al. have overstated the problems with this approach while glossing over similar issues with the interpretation of selection gradients. While no metric perfectly characterizes sexual selection in all circumstances, thoughtful application of existing measures has been and continues to be informative in evolutionary studies.     

Operational sex ratio,reproductive costs,and the potential for intrasexual competition

Even though numerous metrics exist, we still appear to be far from a consensual view on the best way of measuring or predicting the potential strength of sexual selection. One of the earliest and simplest metrics devised was the operational sex ratio (OSR) (i.e. the ratio between sexually active males and females in a population), and even, if heavily criticized, the OSR can still be viewed as a valuable measure of the potential levels of intrasexual competition. Because this ratio is influenced by the time that individuals spend in the mating pool, the OSR depends on our ability to determine who is indeed ready to mate. Moreover, because the proximate effects of OSR on mate monopolization might not be immediately apparent, we should be prepared to account for its association with the conditions making selection favour traits that reduce the time needed to acquire additional mating opportunities. Using the worm pipefish as a working model, we conducted a more stringent calculation of the OSR by eliminating individuals that, although present, do not appear to be able to reproduce, as determined by an analysis of female size classes with immature or spent ovaries and male classes without pregnancy events. Accordingly, the OSR was not only capable of correctly highlighting the potential for intrasexual competition, but also was able to translate the desertion of individuals from the mating pool as the breeding season progressed into meaningful correlations with variables associated with reproductive investment and costs (i.e. gonad investment and energy reserves). As demonstrated, the predictive power of the OSR can be broader than anticipated, depending primarily on our ability to effectively discriminate which individuals are indeed ready to mate. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 477–484.     

Facultative pupal mating in Heliconius erato: Implications for mate choice,female preference,and speciation

Mating systems have broad impacts on how sexual selection and mate choice operate within a species, but studies of mating behavior in the laboratory may not reflect how these processes occur in the wild. Here, we examined the mating behavior of the neotropical butterfly Heliconius erato in the field by releasing larvae and virgin females and observing how they mated. H. erato is considered a pupal‐mating species (i.e., males mate with females as they emerge from the pupal case). However, we observed only two teneral mating events, and experimentally released virgins were almost all mated upon recapture. Our study confirms the presence of some pupal‐mating behavior in H. erato, but suggests that adult mating is likely the prevalent mating strategy in this species. These findings have important implications for the role of color pattern and female mate choice in the generation of reproductive isolation in this diverse genus.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Estimating sexual selection and sexual isolation effects from mating frequencies

Abstract.— Sexual selection (defined as the change in genotypic or phenotypic frequencies of mated versus total population frequencies) and sexual isolation (defined as the deviation from random mating in mated individuals) show different evolutionary consequences and partially confounded causes. Traditionally, the cross-product estimator has been used to quantify sexual selection, whereas a variety of indexes, such as Yule V , Yule Q, YA , joint I , and others have been used to quantify sexual isolation. Because the two types of estimators use different scales, the effects of both processes cannot be monitored simultaneously. We describe three new related statistics that quantify both sexual selection ( PSS ) and sexual isolation ( PSI ) effects for every mating pair combination in polymorphic traits, as well as measure their combined effects ( PTI = PSI X PSS ). The new statistics have the advantage of providing information on every mating pair combination, quantifying the effects of sexual selection and isolation in the same units, and detecting asymmetry in sexual isolation. The ability of the new statistics to ascertain the biological causes of sexual selection and sexual isolation are investigated under different models involving distinct marginal frequencies, mate propensity, and mate choice coefficients. We also studied the use of classical isolation indexes applied on PSI coefficients, instead of on raw data. The use of the classical indexes applied to PSI coefficients considerably reduces the statistical bias of the estimates, revealing the good estimation properties of the new statistics.     

Female discrimination thresholds frequently exceed local male display variation: implications for mate choice dynamics and sexual selection

Among the factors that can influence female mate choice decisions is the degree to which females differentiate among similar displays: as differences decrease, females are expected to eventually stop discriminating. This discrimination threshold, in conjunction with the magnitude of male trait variation females regularly encounter while making mate choice decisions, may have important consequences for sexual selection. If local display variation is above the discrimination threshold, female preferences should translate into higher mating success for the more attractive male. But if display variation is frequently below the threshold, the resulting increased pattern of random mating may obscure the existence of female mate choice. I investigated the interplay between female discrimination and male display variation in green treefrogs (Hyla cinerea) and found that call trait differences between nearest neighbour males were frequently smaller than what females are expected to discriminate. This finding has two important consequences for our understanding of sexual selection in the wild: first, low display variation should weaken the strength of selection on male display traits, but the direction of selection should mirror the one predicted from females choice trials. Second, caution is needed when interpreting data on realized mating success in the wild: a pattern of random mating with respect to male display traits does not always mean that female preferences are weak or that conditions are too challenging for females to express their preferences. Rather, insufficient display variation can generate the same pattern.     

Sexual selection in fungi

The significance of sexual selection, the component of natural selection associated with variation in mating success, is well established for the evolution of animals and plants, but not for the evolution of fungi. Even though fungi do not have separate sexes, most filamentous fungi mate in a hermaphroditic fashion, with distinct sex roles, that is, investment in large gametes (female role) and fertilization by other small gametes (male role). Fungi compete to fertilize, analogous to ‘male‐male’ competition, whereas they can be selective when being fertilized, analogous to female choice. Mating types, which determine genetic compatibility among fungal gametes, are important for sexual selection in two respects. First, genes at the mating‐type loci regulate different aspects of mating and thus can be subject to sexual selection. Second, for sexual selection, not only the two sexes (or sex roles) but also the mating types can form the classes, the members of which compete for access to members of the other class. This is significant if mating‐type gene products are costly, thus signalling genetic quality according to Zahavi's handicap principle. We propose that sexual selection explains various fungal characteristics such as the observed high redundancy of pheromones at the B mating‐type locus of Agaricomycotina, the occurrence of multiple types of spores in Ascomycotina or the strong pheromone signalling in yeasts. Furthermore, we argue that fungi are good model systems to experimentally study fundamental aspects of sexual selection, due to their fast generation times and high diversity of life cycles and mating systems.     

Effects of a parasitic nematode on male mate choice in a livebearing fish with a coercive mating system (western mosquitofish, Gambusia affinis)

I examined the effects of the parasitic larval nematode, Eustrongylides ignotus, on male mate choice in the western mosquitofish, Gambusia affinis. I hypothesized that parasite presence influences male mate choice either directly (via reduction in male mating behavior due to presence of parasite in females) or indirectly (via reduction in male mating behavior due to reduced condition of infected females). Specifically, I tested the predictions that (1) males would mate preferentially with uninfected over infected females (scoring both mating attempts and association time with females); (2) parasitized females would be in poorer condition than non-parasitized females (measured as soluble fat stores); and (3) parasitized females would have reduced fecundity (measured as number of developing embryos). Males preferred to mate with non-parasitized over parasitized females, but showed no differences in association time between females. The nematode did not decrease female body condition, but did decrease female mass, and appeared to decrease female fecundity via reduction in broods (# embryos). Results support that parasites affect male mate choice in mosquitofish; however, the mechanisms used by males to differentiate between parasitized and non-parasitized females remain untested. This study provides the first empirical evidence of parasite affects on male mate choice in livebearing fishes, and suggest a potentially important role for parasite-mediated sexual selection in organisms that use coercive mating as the primary mechanism of obtaining mates.     

MULTI‐LEVEL SEXUAL SELECTION: INDIVIDUAL AND FAMILY‐LEVEL SELECTION FOR MATING SUCCESS IN A HISTORICAL HUMAN POPULATION

Precopulatory sexual selection is the association between fitness and traits associated with mate acquisition. Although sexual selection is generally recognized to be a powerful evolutionary force, most investigations are limited to characters belonging to individuals. A broader multilevel perspective acknowledges that individual fitness can be affected by aspects of mating success that are characters of groups, such as families. Parental mating success in polygynous or polyandrous human societies may exemplify traits under group‐level sexual selection. Using fitness measures that account for age‐structure, I measure multilevel selection for mate number over 55 years in a human population with declining rates of polygyny. Sexual selection had three components: individual‐level selection for ever‐mating (whether an individual mated) and individual‐ and family‐level selection for polyandry and polygyny. Family‐ and individual‐level selection for polygyny was equally strong, three times stronger than family‐level selection for polyandry and more than an order of magnitude stronger than individual‐level selection for polyandry. However, individual‐level selection for polyandry and polygyny was more effective at explaining relative fitness variance than family‐level selection. Selection for ever‐mating was the most important source of sexual selection for fitness; variation for ever‐mating explained 23% of relative fitness variance.     

Bateman–Trivers in the 21st Century: sexual selection in a North American pitviper

Assessment of sexual selection in organisms with cryptic life histories is challenging, although accurate parentage assignments using genotypic markers, combined with behavioural observations and a method to account for open population bias, allow for robust estimation of metrics. In the present study, we employed 22 tetranucleotide microsatellite DNA loci to interpret mating and reproductive success in a population of Copperhead (Viperidae, Agkistrodon contortrix) in Connecticut, USA. We sampled DNA from 114 adults (56 males, 58 females) and 137 neonates from known mothers to quantify Bateman gradients (β_ss), as well as sex‐specific opportunities for selection (I) and sexual selection (I_s). We also estimated selection on male size [snout‐to‐vent length (SVL)], a trait important for successful combat and subsequent copulations. Estimates of male I and I_s differed significantly from those of females when estimated with four different methods and only males had a significant Bateman gradient. As predicted, male reproductive success was positively correlated with increasing SVL. These results contrast with those derived in another study investigating the same population but based solely on observational data and without correction for open population bias. We thus argue that molecular approaches to quantifying reproductive success and strength of sexual selection provide more accurate results than do behavioural observations alone. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 436–445.     

POLYGYNANDRY IN THE DUSKY PIPEFISH SYNGNATHUS FLORIDAE REVEALED BY MICROSATELLITE DNA MARKERS

In the dusky pipefish Syngnathus floridae, like other species in the family Syngnathidae, ‘pregnant’ males provide all post-zygotic care. Male pregnancy has interesting implications for sexual selection theory and the evolution of mating systems. Here, we employ microsatellite markers to describe the genetic mating system of S. floridae, compare the outcome with a previous report of genetic polyandry for the Gulf pipefish S. scovelli, and consider possible associations between the mating system and degree of sexual dimorphism in these species. Twenty-two pregnant male dusky pipefish from one locale in the northern Gulf of Mexico were analyzed genetically, together with subsamples of 42 embryos from each male's brood pouch. Adult females also were assayed. The genotypes observed in these samples document that cuckoldry by males did not occur; males often receive eggs from multiple females during the course of a pregnancy (six males had one mate each, 13 had two mates, and three had three mates); embryos from different females are segregated spatially within a male's brood pouch; and a female's clutch of eggs often is divided among more than one male. Thus, the genetic mating system of the dusky pipefish is best described as polygynandrous. The genetic results for S. floridae and S. scovelli are consistent with a simple model of sexual selection which predicts that for sex role-reversed organisms, species with greater degrees of sexual dimorphism are more highly polyandrous.