Operational sex ratio and resource defence as predictors of the mating system in European bitterling

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.     

The influence of operational sex ratio on the intensity of competition for mates

The evolution and maintenance of secondary sexual characteristics and behavior are heavily influenced by the variance in mating success among individuals in a population. The operational sex ratio (OSR) is often used as a predictor of the intensity of competition for mates, as it describes the relative number of males and females who are ready to mate. We investigate changes in aggression, courtship, mate guarding, and sperm release as a function of changes in the OSR using meta-analytic techniques. As the OSR becomes increasingly biased, aggression increases as competitors attempt to defend mates, but this aggression begins to decrease at an OSR of 1.99, presumably due to the increased costs of competition as rivals become more numerous. Sperm release follows a similar but not significant trend. By contrast, courtship rate decreases as the OSR becomes increasingly biased, whereas mate guarding and copulation duration increase. Overall, predictable behavioral changes occur in response to OSR, although the nature of the change is dependent on the type of mating behavior. These results suggest considerable flexibility of mating system structure within species, which can be predicted by OSR and likely results in variation in the strength of sexual selection.     

Operational sex ratio in newts: field responses and characterization of a constituent chemical cue

Operational sex ratio (OSR) has been traditionally thought ofas a force imposing competition for mates rather than also acue used to regulate the intrasexual competition individualsencounter. To assess whether eastern red-spotted newts, Notophthalmusviridescens, could appropriately compare OSRs, we quantifiedfield responses to traps containing four males, a sexually receptivefemale, four males plus a female, or nothing as a control. Earlyin the breeding season, males from two populations chose competitivemating opportunities over no mating opportunity at all, butgenerally preferred less competitive mating prospects. Laterin the breeding season, as the OSR of newt populations becomesmore male biased, males accordingly increased their acceptanceof intrasexual competition. Females avoided groups of four males,and for both sexes, avoidance of male-biased courting groupsincreased their probability of amplexus courtship. We then isolatedan approximately 33-kD protein from male cloacal glands thatwas used by males to compare OSRs. To our knowledge, this proteinrepresents the first isolated and characterized component ofan olfactory cue used to evaluate OSR. These results supporttwo important principles regarding mating systems: (1) OSR cansomewhat paradoxically be both the source imposing competitionfor mates and the source used to reduce it, and (2) analogousto the sex in short supply often being "choosy" selecting mates,the sex in excess (here, males) appears to be choosy about itsacceptance of intrasexual competition.     

Operational sex ratio affects nest tending and aggression in male flagfish Jordanella floridae Goode & Bean

Operational sex ratio (OSR, the ratio of sexually active males to fertilizable females at a given time and location) affected male behaviour in the flagfish Jordanella floridae . When OSR was male biased, males spent (1) more time at their nests and (2) more time fanning prior to receiving eggs. Pre-mating fanning has previously been correlated with male mating success and is hypothesized to be used in female choice in this population. Thus, these results suggest that on average, male flagfish invest more time in behaviour associated with female choice when there are relatively more male competitors. The OSR also affected the frequency of male aggression, and specifically male aggression towards females was more frequent at female-biased OSR treatments. The observed patterns were dependent upon the direction of OSR bias ( i.e. unbiased, male biased and female biased), and in some cases the intensity of the OSR bias affected the patterns of behaviour. These findings suggest that experimentally detecting effects of OSR is sensitive to the specific OSR values considered, and highlight the importance of considering a range of OSR values in future studies.     

Mate choice, operational sex ratio, and social promiscuity in a wild population of the long-snouted seahorse Hippocampus guttulatus

Mate competition and mate choice are not mutually exclusivebehaviors. Both behaviors may drive sexual selection in oneor both sexes of a population. One of several factors affectingwhich behavior is exhibited by which sex is the operationalsex ratio (OSR) in the study population. The present study combinesbehavioral observations in the field with controlled experimentsin aquaria to investigate social interactions and mate choicein both male and female long-snouted seahorses Hippocampus guttulatusin the context of the population OSR. Compared with the morereadily studied pipefishes, data on OSR and mate choice in seahorsesare scarce in the published literature. Our field data providenovel evidence of social promiscuity, size-assortative mating,and an OSR that varies from being unbiased early and midseasonto male biased at the end of the breeding season. Our mate choiceexperiments revealed intersexual differences in mate preferencewith males significantly preferring larger females to familiarones. Taken together, our field and experimental results suggestthat mate choice rather than intrasexual competition could drivesexual selection in seahorses.     

Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly

Current theory postulates that the operational sex ratio (OSR)determines the relative degree of mating competition in thetwo sexes and is in turn influenced by a sexual difference inthe potential reproductive rate (PRR) denned as 1/time out,where time out is the time an individual must spend recoveringfrom a bout of mating activity and/or caring for offspring.In bushcricket mating systems where males provide females witha nuptial gift, relative energy expenditure in offspring influencesthe PRR of males and females and underlies a diet-mediated shiftin the OSR. Here we investigated if there is a similar positiverelationship between relative parental nutrient expenditurein offspring and PRR in the polyandrous butterfly Pieris napi,where female fecundity is strongly dependent on male nuptialgifts at mating. By varying the amount of nutrients femalesreceive at mating and relating this to number of offspring produced,we show that male P. napi have, on average, a nutrient expenditurein offspring equaling that of females. In spite of this, themale reproductive rate is 8–13 times higher than thatof females. Hence the relative degree of parental expenditurein offspring is largely decoupled from the degree of matingcompetition in P. napi. Two alternative explanations are advancedto account for the difference between the butterfly and thebushcricket mating systems.     

Patterns of Aggression and Operational Sex Ratio Within Alternative Male Phenotypes in Atlantic Salmon

The intensity of male–male aggression during mating is predicted to increase with the operational sex ratio (OSR) (the ratio of sexually active males to females). We observed aggressive behaviour in relation to OSR within alternative phenotypes (large anadromous males and small ‘sneaker’ mature male parr) of Atlantic salmon, Salmo salar, as they competed for access to anadromous females in large outdoor arenas immediately prior to spawning events as well as throughout the spawning season. Anadromous males were primarily aggressive outside of spawning events, and their aggression increased with OSR over a narrow range of 0.08–4. By contrast, mature male parr were aggressive just prior to spawning, with a decrease in aggression over a broad range of OSRs from 1 to 7.4. Similarly, literature data for three other salmonid species indicated a decrease in aggression with increasing OSRs over a range of 1–6.33. These observations suggest that there is considerable variability in competitive behaviour, even within alternative phenotypes. Because our data are derived from repeated observations on the same individuals of different genetic origin, further confirmation of these findings is desirable. Nevertheless, our study underscores the importance of measuring competitive behaviour and OSR at ecologically relevant spatial and temporal scales, both of which may differ between alternative maturation phenotypes.     

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog ( Rana dalmatina ). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 191–200.     

The effect of size and sex ratio experiences on reproductive competition in Nicrophorus vespilloides burying beetles in the wild

Male parents face a choice: should they invest more in caring for offspring or in attempting to mate with other females? The most profitable course depends on the intensity of competition for mates, which is likely to vary with the population sex ratio. However, the balance of pay‐offs may vary among individual males depending on their competitive prowess or attractiveness. We tested the prediction that sex ratio and size of the resource holding male provide cues regarding the level of mating competition prior to breeding and therefore influence the duration of a male's biparental caring in association with a female. Male burying beetles, Nicrophorus vespilloides were reared, post‐eclosion, in groups that differed in sex ratio. Experimental males were subsequently translocated to the wild, provided with a breeding resource (carcass) and filmed. We found no evidence that sex ratio cues prior to breeding affected future parental care behaviour but males that experienced male‐biased sex ratios took longer to attract wild mating partners. Smaller males attracted a higher proportion of females than did larger males, securing significantly more monogamous breeding associations as a result. Smaller males thus avoided competitive male–male encounters more often than larger males. This has potential benefits for their female partners who avoid both intrasexual competition and direct costs of higher mating frequency associated with competing males.     

Male-biased sex ratio increases female egg laying and fitness in the housefly, Musca domestica

A biased operational sex ratio (OSR) can have multiple, confounding effects on reproductive fitness. A biased OSR can increase harassment and mating activity directed towards potential mates but may also increase the ability of potential mates to choose a good partner if lower quality mates are screened out through competitive interactions. Additionally, a biased OSR may affect reproductive fitness through changes in male ejaculate content or in female reproductive response. We quantified how a male-biased OSR (1:1, 2:1, or 5:1 male to female) affected the size of a female??s first egg clutch and her offspring??s survivorship in the housefly, Musca domestica. A male-biased OSR increased female fitness: females laid more eggs in their first clutch, had increased offspring survivorship at a 2:1 versus 1:1 OSR, and had equivalent fitness with a 5:1 male to female OSR. Courtship activity increased when the OSR was male-biased but was not a significant predictor of female fitness. Trials where females chose their mates versus trials where a random male was chosen for them had equivalent first clutch sizes and offspring survivorship. These results suggest that there are cryptic effects from a male-biased OSR on female fitness that are most likely driven by pre-copulatory social environment.     

Synchronous female spawning and male mating behavior in a land-locked population of Japanese charr, Salvelinus leucomaenis japonicus

In resource-based promiscuous mating systems, synchronous spawning of females affects competition among males and variation in the reproductive success of males. We documented the mating behavior of Japanese charr (Salvelinus leucomaenis japonicus) through an annual breeding season to examine the relationship between female spawning synchrony and male mating behavior. Females spawned highly synchronously in the population studied, i.e., approximately half the spawning was finished within the first three days of the entire spawning season (11 days). The daily operational sex ratio (OSR) was nearly 1:1 through the spawning period. The number of males around a spawning female was very small (1.21+/-0.49 males per female) over the spawning ground and period, suggesting that a competitive male could effectively chase subordinate males away from a spawning female. A few males attempted to sneak near the oviposition site of females (16%; 9 of 57 breeding groups), while some males adopted sneaking tactics in the initial phase of females' spawning (24%). We did not observe any males to succeed in sneak fertilizations. We conclude that in this Japanese charr population, the synchronous spawning of females was related to the unbiased daily OSR, male aggregation around females, and consequently whether and how efficiently males engaged in sneak mating behavior.     

Temperature affects operational sex ratio and intensity of male-male competition: an experimental study of sand gobies, Pomatoschistus minutus

The operational sex ratio is intimately related to the intensityof sexual selection, but factors governing variation in theoperational sex ratio and their effects on mating competitionare still poorly understood. In this study, temperature wasfound to affect both the operational sex ratio and the intensityof male-male competitive interactions in the sand goby [Pomatoschistusminutus (Pallas)]. In an experiment with two different temperaturetreatments, the operational sex ratio became male biased inthe warm treatment (15°C) and males in that treatment interactedmore frequendy than in the cold treatment (8.5°C). Theseresults were as predicted since the potential reproductive rateof males increases faster with temperature than does the potentialreproductive rate of females. Thus, an environmental factor,water temperature, affects not only the reproductive rates ofthe sexes, but also the operational sex ratio and mating competition,and thereby the intensity of sexual selection. Operational sexratio was not found to be correlated with male behavior. Thismay suggest a direct effect of temperature or potential reproductiverates on mate competition. The mechanism behind the evolutionof such a direct relationship would, however, probably be theimpact of potential reproductive rates on operational sex ratio,which in turn direcdy affects sexual selection.     

Female egg dumping and the effect of sex ratio on male egg carrying in a coreid bug

Phyllomorpha laciniata Vill (Heteroptera, Coreidae) is uniqueamong terrestrial insects in that females glue eggs on the backsof other conspecifics. Egg carrying byP. laciniatamales haspreviously been considered as paternal care. We explored femaleoviposition with respect to previous mating experience of femalesand tested whether sex ratio affects male egg-carrying. Thehypothesis that male egg-carrying is a form of paternal carepredicts that a male should always accept eggs after matingwith a female. However, if male egg-carrying is a form of postcopulatorymate guarding rather than paternal care, egg carrying shouldincrease in the presence of other males. When two couples wereplaced together, females laid eggs on the backs of all individualsenclosed, including the backs of other females. However, whena female was accompanied by 2 males, 22 out of 26 females ovipositedon their mating partner. Thus, sexual competition rather thanpaternity alone, affects a male's eagerness to carry eggs. However,even if males sometimes carry their own eggs, females lay eggson the backs of all conspecifics they can easily acquire. Thus,egg carrying in P. laciniata is partially voluntary and partiallythe result of female egg dumping     

Mate choice and the operational sex ratio: an experimental test with robotic crabs

The operational sex ratio (OSR: sexually active males: receptive females) predicts the intensity of competition for mates. It is less clear, however, under what circumstances, the OSR predicts the strength of sexual selection – that is, the extent to which variation in mating success is attributable to traits that increase the bearer's attractiveness and/or fighting ability. To establish causality, experiments that manipulate the OSR are required. Furthermore, if it is possible to control for any OSR‐dependent changes in the chosen sex (e.g. changes in male courtship), we can directly test whether the OSR affects the behaviour of the choosing sex (e.g. female choice decisions). We conducted female mate choice experiments in the field using robotic models of male fiddler crabs (Uca mjoebergi). We used a novel design with two females tested sequentially per trial. As in nature, the choice of the first female to mate therefore affected the mates available to the next female. In general, we detected significant sexual selection due to female choice for ‘males’ with larger claws. Importantly, the strength of sexual selection did not vary across five different OSR/density treatments. However, as the OSR decreased (hence the number of available males declined), females chose the ‘males’ with the largest claws available significantly more often than expected by chance. Possible reasons for this mismatch between the expected and observed effects of the OSR on the strength of sexual selection are discussed.     

Operational sex ratio and density do not affect directional selection on male sexual ornaments and behavior

Demographic parameters including operational sex ratio (OSR) and population density may influence the opportunity for, and strength of sexual selection. Traditionally, male-biased OSRs and high population densities have been thought to increase the opportunity for sexual selection on male sexual traits due to increased male competition for mates. Recent experimental evidence, however, suggests that male-biased OSRs might reduce the opportunity for sexual selection due to increased sexual coercion experienced by females. How OSR, density, and any resultant changes in the opportunity for sexual selection actually affect selection on male sexual traits is unclear. In this study, we independently manipulated OSR and density in the guppy (Poecilia reticulata) without altering the number of males present. We recorded male and female behavior and used DNA microsatellite data to assign paternity to offspring and estimate male reproductive success. We then used linear selection analyses to examine the effects of OSR and density on directional sexual selection on male behavioral and morphological traits. We found that females were pursued more by males in male-biased treatments, despite no change in individual male behavior. There were no differences in sexual behavior experienced by females or performed by males in relation to density. Neither OSR nor density significantly altered the opportunity for sexual selection. Also, Although there was significant multivariate linear selection operating on males, neither OSR nor density altered the pattern of sexual selection on male traits. Our results suggest that differences in either OSR or density (independent of the number of males present) are unlikely to alter directional evolutionary change in male sexual traits.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Mating distribution and its temporal dynamics affect operational sex ratio: a simulation study

The present study investigated how variation in mating distribution in time and among males influences the operational sex ratio (OSR) with a simulation inspired by paternally caring fish. Varying (1) the potential reproductive rate of each sex, (2) the mating distribution among males, and (3) the length of male mating phase, we created different mating patterns. In each case, we searched for the adult sex ratio that resulted in an OSR of 50% (where sex-roles switch). This approach enabled a comparison with a previous model. We found that the OSR was influenced by the distribution of matings in time and among males when the male mating phase was limited by a parental phase. Furthermore, the mating dynamics were shaped by the fact that the numbers of males and females and their capacities for collateral investment affected OSR immediately from the start of the reproductive season, whereas their times-out had a delayed effect on OSR.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 551–559.     

Using potential reproductive rates to predict mating competition among individuals qualified to mate

The potential reproductive rate (PRR), which is the offspringproduction per unit time each sex would achieve if unconstrainedby mate availability, often differs between the sexes. An increasingsexual difference in PRR predicts an intensified mating competitionamong the sex with the higher PRR. The use of PRR can providedetailed predictions of when, where, and how the intensityin mating competition and hence sexual selection will vary.Previous models have focused on the "time out" from mate searchingas a major component of PRR. Here, we suggest some improvementsand clarifications: in a population where individuals haveto compete for specific resources that are prerequisites formating (e.g., nest sites), individuals unable to obtain sucha resource will not qualify to mate. We suggest how a conceptof the ratio of males and females qualified to mate, Q, canimprove previous models designed to use the sexual differencein PRR to estimate the operational sex ratio (OSR). Further,when estimating the sexual difference in PRR of a population,it is important that each sex is given free access to matingpartners. Jointly, this provides an empirical approach basedon estimates of Q and the sexual difference in PRR.     

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.     

Effects of breeding site density on competition and sexual selection in the European lobster

The availability of breeding sites has been predicted to affectthe intensity of sexual selection, including mate competition,mate choice and ultimately, variation in mating success. Wetested the hypothesis that reduced density of shelters wouldcause an increase in the intensity of sexual selection in Europeanlobsters, Homarus gammarus. However, we found little supportfor our predictions. For example, within-sex competition bymales and by females was not more intense when shelters werescarce. Indeed, females attempted to evict one another fromshelters significantly more often when shelters were common.When shelters were abundant, shelter-holding males had greatermating success than males without shelters, yet females didnot show more interest towards these males during courtshipencounters. Mate attraction was more strongly related to largemale body size when shelters were scarce. Overall, the resultssuggest that reduced shelter density does not lead to more overtwithin-sex aggression in this species. Instead, we suggest thatimpacts of breeding resource availability on sexual selectionmay depend on the range over which resources are measured, withextreme scarcity of shelters rendering overt competition uneconomical.Furthermore, females may become more selective of male traitssuch as large size, which enhance male control of breeding sitesand hence protection of females.