Experimental assessment of ecological and phenotypic factors affecting male mating success and polyandry in northern watersnakes, Nerodia sipedon

To resolve conflicting field observations regarding the action of sexual selection, we used breeding experiments and paternity analysis of the 927 resulting offspring to assess how male size, condition, tail length, genetic similarity to the female, and variation in operational sex ratio (OSR) affected male reproductive success and the incidence of polyandry in northern watersnakes (Nerodia sipedon). Only size affected male mating success. Large males were more successful, but only when male size varied substantially and competition among males was intense (i.e., male-biased OSR). The conditional nature of the size advantage may explain why studies of free-living watersnakes have produced inconsistent results regarding the relationship between male size and mating success. Size differences between males did not affect the proportion of offspring each male sired within multiply sired litters. We found positive size-assortative mating, but only when the OSR was female biased, suggesting that smaller males had improved access to females when competition among males was reduced, but that competition with larger males still restricted mating opportunities of small males to less preferred, smaller females. Most litters (58%) were multiply sired and larger females were more likely to produce multiply sired litters, similar to free-living watersnakes. There was no association between the incidence of multiple paternity and OSR, however, suggesting that polyandry is not simply a function of opportunity, with females passively waiting for males to court them.     

Male-male interference competition decreases spawning rate in the European bitterling (<Emphasis Type="Italic">Rhodeus sericeus</Emphasis>)

We investigated the consequences of male-male interference competition associated with alternative male mating tactics in a freshwater fish, the European bitterling (Rhodeus sericeus). Male bitterling defend territories around living mussels and attract females to lay their eggs in the gill cavities of mussels. We experimentally manipulated spawning-site abundance and male density at two spatial scales. We showed that the total number of eggs spawned by females was constrained by the number of mussels available for oviposition. The effect was mediated by behavioral interactions among competing males because of variation in the Operational Sex Ratio (OSR) in close proximity to a mussel and not by a direct limitation in mussel capacity to accommodate the eggs. Both total and local male densities affected spawning behavior, and interacted in their effect on female spawning rate. Territorial male aggression caused courtship interruptions that prolonged the time until successful spawning and increased with male density. However, territoriality broke down at the highest male density, with a consequent stabilizing effect on spawning rate.Communicated by J. Krause     

Operational sex ratios and behavioural sex differences in a pipefish population

In the pipefish Syngnathus typhle, only males brood embryos in specially developed brood pouches, supplying oxygen and nutrients. Laboratory studies have shown that this elaborate paternal care has led to sex-role reversal in this species: males limit female reproductive rate, females are the primary competitors for mates and males exercise greater selectivity in accepting mates. In the first field study of this pipefish, we describe mating behaviour in the wild and test the hypothesis that temporal variations in the operational sex ratio (OSR) determine sex differences in mating behaviour. Our study comprised two reproductive seasons of two sequential mating periods each, the latter separated by a lengthy interval of male brooding. During mating periods, females displayed to all males without wandering and males moved about searching for females, without reacting to all females. The OSR was least female-biased (or even male-biased) at the onset of the breeding season, when most pipefish were simultaneously available to mate, but became strikingly female-biased as males' pouches were filled. The OSR remained substantially female-biased during the second mating period, because few males became available to remate at any one time. As hypothesised, female-biased OSRs resulted in more female-female meetings. As well, females were above the eelgrass more often than brooding males, thus exposing themselves to conspecifics and/ or predators. In the second year, males arrived earlier than females on the breeding site and male pregnancies were shorter, because of higher water temperatures, so rematings occurred earlier. Males met more often during that year than the previous one, but male competitive interactions were still not observed. The field results support laboratory studies and demonstrate that behaviours associated with female-female competition are more prominent when the OSR is more female-biased. Correspondence to: A. Vincent     

Operational sex ratios and sperm limitation in populations of Drosophila pachea

Males of the cactophilic fruitfly, Drosophila pachea, produce relatively few but very large sperm, and partition their limited gamete numbers among successive mates. The present study found that males take 10 days longer than females, post-eclosion, to become sexually mature. The pattern of testes development suggests that the need to produce testes long enough to manufacture the giant sperm is the cause of the delayed male maturity. These findings generate the prediction that the operational sex ratio (OSR) of populations will be female-biased. The size, sex ratio, and OSR of natural populations were examined. In general, local populations tended to be small and sex ratios tended to be slightly male-biased. However, as predicted, the OSR of populations, at least in one season, tended to be female-biased, with an average of 2.3 receptive females for each sexually active male. Results of laboratory experiments to determine the relationship between female remating frequency and fitness, and between population OSR and productivity, suggest that natural populations with female-biased OSRs are sperm-limited. The origin and maintenance of sperm gigantism and the unusual sperm-partitioning behavior of males are discussed with respect to population structure.     

The significance of hotspots to lekking topi antelopes (<Emphasis Type="Italic">Damaliscus lunatus</Emphasis>)

Controversy has surrounded the question of why lek-breeding has evolved in certain ungulate species. Can the behavior be explained simply by males mapping onto a female distribution that is determined by factors unrelated to mating? Or are leks created because estrous females distinguish between males and favor males who cluster? Here I address these questions by looking at spatial distribution in lekking topi antelopes (Damaliscus lunatus). Contrary to the predictions of a model assuming male clustering in the zone of maximum female range overlap, territories were highly clustered also within this zone, and lek size correlated positively with population density. In support of models derived from the ideal free distribution of males onto female dispersion, leks were in areas with high female density during the rut. However, models not taking into account both individual variation in male quality and female mate preferences failed to explain the extreme male clumping also within high density areas, which was revealed by a strongly male-biased sex-ratio on leks. Additional support for the female preference-based model came from the finding that estrous females concentrated onto leks. Female preference for clustered males may develop if males initially follow an ideal free distribution of unequal competitors with high quality males slightly clustered at density hotspots; positive feedback between female benefits of preference for clustered males and male benefits of clustering could lead to contraction of the territorial network and lek behavior. Thus only the female preference-based model correctly predicted a negative correlation between male mating rate and resource density.     

Sex ratios,mating behavior and sexual size dimorphism of the northern water snake,Nerodia sipedon

Competition among males to mate is generally associated with male-biased size dimorphism. In this study we examine mating behavior in the northern water snake (Nerodia sipedon), a species in which males are much smaller than females despite substantial competition among males to mate. Competition among males was a consequence of a male-biased operational sex ratio due to slightly higher female mortality from a birth sex ratio of 1 : 1, and, in 1 year, more synchronous and longer mating activity by males. Approximately one-third of both males and females appeared not to mate in a given year. Larger males were generally more likely to attempt mating, but size did not explain the variance in the number of aggregations in which individual males participated. Within aggregations, males that were successful at achieving intromission were larger than unsuccessful males in 1 of 2 years. Variation in condition (mass relative to length) and relative tail length were not generally useful predictors of either mating effort or success in males. Because large size was often advantageous to males, sexual size dimorphism appeared not to be a consequence of sexual selection favoring smaller males. Because sexual dimorphism was evident at birth, and both males and females matured sexually at about 4 years, sexual dimorphism was not simply a consequence of one sex growing at the maximum rate for longer. Female fecundity increased with size, and sex differences in size-fecundity relations may underly the pattern of sexual size dimorphism. However, because multiple mating by females is common, sperm competition is likely to be important in determining male reproductive success. Therefore, allocation of energy to sperm rather than growth may also prove to be an important influence on male growth rates and sexual size dimorphism.     

Mating system,optimal number of matings,and sperm transfer in the Argentine ant Iridomyrmex humilis

Summary In ants, because males have a finite sperm supply and females mate only at the beginning of their reproductive lives, it is possible to infer which is the limiting sex from a few parameters: the amount of sperm produced by males, the amount of sperm stored by females, and the numerical sex ratio. In the Argentine ant Iridomyrmex humilis mating takes place in the nest. Laboratory experiments and field data showed that the numerical sex ratio is heavily male-biased (10.1:1) and that the maximum number of sperm a female can store is similar to the number of sperm a male possesses. Thus females are the limiting sex in this species. In a set of mating experiments, one queen was presented with 1–20 males. The highest proportion of successful matings occurred when females were presented with two males. There was a significant negative correlation between the amount of sperm queens stored and the number of males present in the mating arena. This relationship most likely resulted from male interference during the copulation process. When several males were present in the arena, the mating pair was frequently disturbed by other males trying to copulate. Newly mated queens collected from the field stored 172,000 ± 76,000 sperm, a quantity most similar to that measured in laboratory mating experiments with a ratio of 5 or 10 males per queen. Because the operational sex ratio in I. humilis is highly male-biased, male interference may also decrease the amount of sperm queens store in the field. In many ants, fewer sperm stored by queens should decrease their reproductive success because they would run out of sperm earlier in their reproductive lifetimes. However, comparison of the amount of sperm present in young and old I. humilis queens collected in the field suggests that most use only a small proportion of their sperm supply during their lifetimes. Males mate once and discharge all their sperm during a single mating. Females may mate with several males but dissection of these males indicated that in most cases only one of them had empty seminal vesicles thus suggesting that a single male is responsible for most of the sperm transfer. Thus caution should be exercised in inferring multiple inseminations, as is frequently done in eusocial insects, from the observation of multiple copulations. Correspondence to: L. Keller     

Reproductive success of male bank voles (<Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>): the effect of operational sex ratio and body size

The operational sex ratio (OSR) may influence the intensity of competition for mates and mate choice and is therefore thought to be a major factor predicting the intensity and direction of sexual selection. We studied the opportunity for sexual selection, i.e., the variance in male reproductive success and the direction and intensity of sexual selection on male body mass in bank vole (Clethrionomys glareolus) enclosure populations with experimentally manipulated sex ratios. The opportunity for sexual selection was high among male-biased OSRs and decreased towards female-biased OSRs. Paradoxically, selection for large male body mass was strongest in female-biased OSRs and also considerable at intermediate OSRs, whereas at male-biased OSRs, only a weak relationship between male size and reproductive success was found. Litters in male-biased OSRs were more likely to be sired by multiple males than litters in female-biased OSRs. Our results suggest that the intensity and direction of sexual selection in males differs among different OSRs. Although the direction of sexual selection on male body mass was opposite than predicted, large body mass can be favored by sexual selection. Naturally varying OSRs may therefore contribute to maintain variation in male sexually selected traits.     

Variance in female quality, operational sex ratio and male mate choice in a bushcricket

Male bushcrickets, Kawanaphila nartee, exercise mate choice when nutrients are limited. Male mate choice is associated with a female-biased operational sex ratio (OSR) that arises from an increased relative paternal investment under nutrient limitation. However, increased male choosiness could be attributable to the fact that females vary more in fecundity, and consequently in mate quality, when nutrient limited. Our objective was to experimentally partition the influences of OSR (male or female bias) and variance in mate quality (high or low) and to assess their relative influence on the intensity of mate choice by male bushcrickets. Female quality was manipulated by controlled feeding regimes that directly affected female fecundity. We found that males and females engaged in sexual interactions sooner under a male-biased than a female-biased OSR. Males were more likely to reject females on their first encounter when variance in female quality was high. However, the effect of quality variance on the total number of rejections during a 4-h observation period was dependent on the perceived OSR. A male's prior experience of variance in female quality did not influence male choosiness. Our observed rates of mate rejection conformed well with those predicted from recent theoretical models of sexual differences in choosiness. In conclusion, our results show that the opportunity for selection via male mate choice is influenced by an interaction between OSR and the variance in mate quality that arises within nutrient-limited populations of females. Received: 5 January 1998 / Accepted after revision: 25 October 1998     

Dispersal: an alternative mating tactic conditional on sex ratio and body size

Summary Small male milkweed beetles are less successful at obtaining mates than are larger males. Larger males usually win fights and prevent smaller males from obtaining mates and from choosing larger more fecund females as mates. When sex ratios are male-biased, smaller males are particularly likely to experience these mating disadvantages. It follows that smaller males should be especially responsive to their local competitive environment and behave so as to minimize the mating disadvantages of their smaller size. This paper tests the hypothesis that smaller males disperse from host plant patches with male-biased sex ratios and remain in patches with female-biased sex ratios more readily than larger males.Results show both larger and smaller males disperse from patches with male-biased sex ratios more frequently than from patches with femalebiased sex ratios. As predicted, however, small males are more likely to disperse from patches with male-biased sex ratios and remain in patches with female-biased sex ratios than are larger males.The data also show that smaller males dispersing from patches with male-biased sex ratios obtain more matings than non-dispersing males.For milkweed beetles, moving between patches can be viewed as an alternative mating tactic conditional on male body size and local sex ratio.     

Clutch loss affects the operational sex ratio in the strawberry poison frog Dendrobates pumilio

Both modelling and field data from three breeding seasons show that an environmental factor, clutch loss (CL), affects the operational sex ratio (OSR) and therefore male mating frequency in strawberry poison frogs. Clutch loss affects the length of reproductive cycles of both sexes: with increasing clutch losses, males spend proportionately more time than females in parental investment activities. Because of this, males spend relatively less time in the mating pool, i.e. exhibit proportionately more time-out than females in comparison to a situation with low or no clutch loss. Hence, clutch loss leads to a less male-biased OSR, coupled with a decrease in the opportunity for sexual selection. Furthermore, this study resolves an apparent paradox, the negative correlation between mating frequency and reproductive success (=number of produced tadpoles) of individual males in one breeding season. Clutch loss decouples the correlation between mating frequency and reproductive success because females re-enter the mating pool when they lose their offspring. However, clutch loss diminishes the reproductive output. Similar consequences of clutch loss on the OSR may be true for many species where both sexes reproduce frequently in one breeding season.Communicated by J. Christensen-Dalsgaard     

Operational sex ratio versus gender density as determinants of copulation duration in the walnut fly,Rhagoletis juglandis (Diptera: Tephritidae)

In laboratory and field studies of the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), we assessed the effect of operational sex ratio on copulation duration and partitioned the sex ratio effect into component effects due to male density and female density. In our first laboratory experiment, results were clearly consistent with theoretical expectation: increases in male density were associated with significant increases in copulation duration while increases in female density were associated with significant decreases in copulation duration. These component effects yielded a striking composite effect of operational sex ratio (OSR) on copulation duration in which male-biased ratios were associated with low frequencies of short copulations and female-biased ratios were associated with high frequencies of short copulations. Consistent with a priori expectations concerning costs of territorial behavior, the effect of male density on copulation duration was stronger than that of female density. There was no significant interaction between the effects of gender density on copulation duration: each gender density contributed additively to the composite OSR effect on copulation duration. In contrast to the effect of OSR, overall density had little effect. Field data corroborated these findings fully and showed additionally that OSR in the vicinity of fruit tended in nature to be male-biased. In a second laboratory experiment, we measured copulation duration for individuals exposed alternately to male-biased and female-biased ratios. Individual flies consistently copulated for longer in male-biased environments than in female-biased ones. We propose that this plasticity permits individuals to track changes in local sex ratio over space and time and respond appropriately. Received: 15 November 1995/Accepted after revision: 27 April 1996     

Dispersal and social organization in the Neotropical Grey sac-winged bat Balantiopteryx plicata

Recent evidence suggests that tropical bats may frequently depart from the predominant mammalian male-biased dispersal pattern. So far, two emballonurid bat species that are closely related to our study species (Grey sac-winged bat, Balantiopteryx plicata) have been found to exhibit exceptional female-biased dispersal that is in accordance with father–daughter inbreeding avoidance. In contrast, using a combination of long-term behavioral observations of banded bats and DNA sequencing of the mitochondrial d-loop, our results suggest that B. plicata is the first Neotropical emballonurid with female philopatry and frequent male dispersal. However, just like in the other emballonurids, the age of females at first conception fell below the tenure of males. Thus, philopatric B. plicata females might face a father–daughter inbreeding risk if mating with males from their roosts. Such risk could be circumvented if mating occurs outside the nursing roost, e.g., in male mating aggregations. In contrast to other Neotropical emballonurid bats, the Grey sac-winged bat forms colonies with a greatly male-biased sex ratio (only 5 and 21 % females). Males of such colonies showed high roost fidelity and the sex ratio did not change throughout the year and for up to many years, suggesting an important role in mating. We conclude that studying the diverse mating and dispersal patterns of Neotropical emballonurids shows great potential to enlarge our understanding on how the proposed ultimate causes (i.e., avoidance of inbreeding and local competition between kin) affect the evolution of sex-biased dispersal.     

Why do males tolerate sneakers? Tests with the European bitterling, Rhodeus sericeus

In most species, males attack other males that attempt to gain fertilizations through sneak copulations. Here we report on a system where dominant males show a low level of aggression against sneakers at the initial stages of territory establishment. Females of the European bitterling, Rhodeus sericeus, lay their eggs in living mussels and males fertilize the eggs by releasing sperm over the mussels both before and after egg laying. When we allowed males to court females to a mussel containing no eggs at different male densities - one, two, four, or six males - the dominant male showed a low level of aggression against other males that released sperm. The dominant male became aggressive toward the other males only after eggs had been laid. This unusual pattern could be due to either some benefit of accepting sneakers or a high cost of aggression. We found support for both possibilities. The presence of several males decreased the time until a female spawned, whereas increased aggression by the dominant male against other males during a second female presentation, when the male was more territorial, interrupted courtship and increased the time until spawning. Females appeared to be attracted by both the presence of several males around a mussel and increased courtship under male competition. The bitterling mating system possibly differs from that of other species due to lack of investment in nest building and parental care, and high costs of defending the spawning site against sneakers.     

Factors affecting male yearly mating success in the common frog,Rana temporaria

Summary The mating behavior of the European common frog, Rana temporaria, was studied experimentally. Female body length was correlated with body mass as well as with fecundity. However, males showed no mating preference with regard to either female body length, body mass, or fecundity. In successive multiple matings, male readiness to re-mate as well as fertilization success did not vary among the first four matings. Further, fertilization success was not correlated with either the number of days since the previous fertilization, water volume in the experimental container, testes mass, female/male body length ratio, or female fecundity. However, there was a positive correlation between fertilization success and male fat reserve status. Sexual competition and mating patterns were studied in tanks in which operational sex ratio (OSR) and male density were manipulated, and time for sexual competition was allowed to vary. Successful take-overs and nonrandom mating (large male advantage) were observed only at a combination of a four-fold male bias in OSR and an unnaturally high male density (30–50/m²). I argue that in natural populations of Rana temporaria: (1) There is considerable intraspecific variation in the opportunity for sexual competition, (2) OSR influences mating pattern more than male density and time (duration of the prespawning period), and (3) nonrandom mating should be rare.     

Biased sperm use by polyandrous queens of the ant<Emphasis Type="Italic"> Proformica longiseta</Emphasis>

The occurrence and genetic effects of polyandry were studied in the ant Proformica longiseta using three microsatellite markers. The average queen mating frequency (QMF) estimated from the sperm dissected from the spermathecae of 61 queens was 2.4 with 69% of the queens being multiply mated. QMF estimated from worker offspring in a subsample of eight monogynous colonies was 3.5, but the effective paternity (m_e,p) was only 1.23. The difference between these values reflected unequal sperm use by the queens. Most colonies of P. longiseta were polygynous and the average relatedness among workers was 0.35. Polyandry thus added only marginally to the genetic diversity of colonies, and our results gave little support to the genetic-variability hypothesis for explaining polyandry. Diploid male load was low, as only 1% of males were diploid. A large majority (92%) of nests produced one sex only, with males produced in colonies that had higher than average worker relatedness. This contradicted the predictions derived from worker control of sex ratios. Males produced enough sperm to fill the spermathecae of several queens. Thus, the results indicated that diploid male load, sperm limitation and sex ratio conflict are also unlikely explanations of polyandry. Plausible hypotheses for polyandry include mating by convenience, as the sex ratio is male biased and the mating costs to a female can be low because the females are wingless and have no mating flight. The observed unequal sperm use furthermore points to sperm choice and sperm competition as important factors in the evolution of polyandry.     

The effect of female arrivals on mate monopolization in the yellow dung fly

The degree of resource monopolization relates to the distribution of resources in space and time. In general, monopolization is predicted to be high when resources (food or mates) are clumped in space, dispersed in time, and predictable in space or time. Using the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae), we qualitatively tested a general model that predicts the distribution of mating success among competing males based on the temporal pattern of female arrivals relative to mating time and a ranking of males in priority of access to the resource (here by body size). In a laboratory experiment approximating the natural mating situation, a constant number of males of various sizes were allowed to compete for females. As predicted, mate monopolization decreased as the temporal clumping of female arrivals increased, mediated by either a decrease in the mean or an increase in the variance of female inter-arrival times, which were manipulated independently. Males appeared to adjust their behavior to variation in female arrivals in a manner consistent with the marginal value theory of Parker and associates: forcible take-overs of females were rarer, and copula durations shorter, when females arrived regularly at short intervals. Therefore, a complex interaction of variation in intrinsic characteristics affecting male resource holding potential, mating time and stochastic, extrinsic variables increasing temporal clumping of mates generally reduces the variance in mating success among competing males and thus ultimately the opportunity and intensity of sexual selection on traits influencing male success. This theory extends operational sex ratio theory at the mechanistic, behavioral level.     

Repeatability and heritability of sperm competition outcomes in males and females of <Emphasis Type="Italic">Tribolium castaneum</Emphasis>

Differences among males in their success in achieving fertilisations when females mate with more than one partner are now recognised as an important target of sexual selection. However, very few studies have attempted to determine whether particular males are consistently successful in sperm competition and whether success in sperm competition is a heritable trait. Additionally, the potential heritability of female traits that influence the outcome of sperm competition has received only limited attention. Using the polyandrous beetle Tribolium castaneum, we examined repeatability of male success in sperm competition by mating pairs of males carrying different visible genetic markers to a string of different females. Males showed consistency in their ability to successfully transfer sperm to females, but not in their success in sperm competition. Furthermore, when we independently compared success in sperm competition of fathers with their sons, we found no evidence for heritability of this trait. Similarly, females that exhibited high or low first male sperm precedence did not tend to have daughters that showed the same pattern. Our results suggest that we should be wary of assuming that success in sperm competition is heritable through either sex.     

Alternative reproductive tactics in the spider Meta segmentata

Summary In the spider Meta segmentata web site quality and competitive ability determine female distributions, and ultimately male mating strategy. Large, fecund females position their webs in aggregations in high quality habitats, whereas small females live alone in lower quality sites. Competition for web sites is intense. Large females have a fighting advantage, but web ownership can offset size disadvantages of about 10%. Males compete for access to female webs. The smallest males are excluded from aggregations of females but have a very high probability of mating monogamously with females in poor habitats. The largest males move about within aggregations and by mating with many females achieve the highest reproductive gains. Moderately sized males only have a low probability of mating in an aggregation, but for those that do succeed the reproductive gains are higher than for those that mate monogamously in low quality areas. On average, moderately sized males obtain reproductive gains from the high risk, high gain strategy of defending webs in aggregations that are equal to those from definding solitary females in poor areas. That 18 of 21 moderately sized males defend females in aggregations suggests that M. segmentata behaves in a riskprone fashion.     

Sex-specific effects of the local social environment on juvenile post-fledging dispersal in great tits

An individual’s decision to disperse from the natal habitat can affect its future fitness prospects. Especially in species with sex-biased dispersal, we expect the cost–benefit balance for dispersal to vary according to the social environment (e.g., local sex ratio and density). However, little is known about the social factors affecting dispersal decisions and about the temporal and spatial patterns of the dispersal process. In our study, we investigated experimentally the effects of the social environment on post-fledging dispersal of juvenile great tits by simultaneously manipulating the density and sex ratio of fledglings within forest plots. We expected young females in the post-fledging period mainly to compete for resources related to food and, as they are subordinate to males, we predicted higher female dispersal from male-biased plots. Juvenile males compete for vacant territories already in late summer and autumn; thus, we predicted increased male dispersal from high density and male-biased plots. We found that juvenile females had a higher probability to leave male-biased plots and had dispersed further from male-biased plots in the later post-fledging phase when juvenile males start to become territorial and more aggressive. Juvenile males were least likely to leave male-biased plots and had smallest dispersal distances from female-biased plots early after fledging. The results suggest that the social environment differentially affected the costs and benefits of philopatry for male and female juveniles. The local sex ratio of individuals is thus an important social trait to be considered for understanding sex-specific dispersal processes.