Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio

We studied the effect of relative parental investment on potential reproductive rates (PRRs) to explain sex differences in selectivity and competition in the dart-poison frog Dendrobates pumilio. We recorded the reproductive behavior of this species in a Costa Rican lowland rainforest for almost 6 months. Females spent more time on parental care than males, and `time out' estimates suggest that PRRs of males are much higher than than those of females, rendering females the limiting sex in the mating process. Males defended territories that provide suitable calling sites, space for courtship and oviposition, and prevent interference by competitors. Male mating success was highly variable, from 0 to 12 matings, and was significantly correlated with calling activity and average perch height, but was independent of body size and weight. Estimates of opportunity for sexual selection and variation in male mating success are given. The mating system is polygamous: males and females mated several times with different mates. Females were more selective than males and may sample males between matings. The discrepancy in PRRs between the sexes due to differences in parental investment and the prolonged breeding season is sufficient to explain the observed mating pattern i.e., selective females, high variance in male mating success, and the considerable opportunity for sexual selection. Received: 9 June 1998 / Received in revised form: 27 March 1999 / Accepted: 3 April 1999     

A test of the "dear enemy effect" in the strawberry dart-poison frog (<Emphasis Type="Italic">Dendrobates pumilio</Emphasis>)

Some territorial animals exhibit a form of social recognition, commonly termed the "dear enemy effect", in which territory residents display lower levels of aggression toward familiar neighbors compared to unfamiliar individuals who are non-territorial "floaters". Despite the widespread occurrence of territorial social systems and use of acoustic signals for communication in anuran amphibians, only two previous studies have demonstrated vocally mediated dear enemy behavior in a territorial frog. In this study, I conducted neighbor-stranger discrimination playback experiments in a third species of territorial frog, the strawberry dart-poison frog, Dendrobates pumilio (Anura, Dendrobatidae). In the first experiment (n=24), I broadcast the calls of a subject's nearest neighbor and the calls of an unfamiliar individual from the approximate midpoint between the subject's and the neighbor's territories. Although males responded to the stimuli, they did not exhibit differential responses to the calls of neighbors and strangers. In a second experiment (n=22), I broadcast the calls of a neighbor and a stranger to subjects through a speaker located in the approximate center of the neighbor's territory. Males also responded to the playback, although less intensely than in the first experiment, but no discrimination between the calls of neighbors and strangers was found. Thus, territorial males of the strawberry dart-poison frog appear not to discriminate behaviorally between the advertisement calls of neighbors and strangers. Several proximate and ultimate-level hypotheses for this lack of vocally mediated neighbor-stranger discrimination are discussed.Communicated by T. Czeschlik     

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     

Independent effects of male and female density on sexual harassment, female fitness, and male competition for mates in the western mosquitofish Gambusia affinis

Operational sex ratio (the ratio of sexually active males to fertilizable females) has a major influence on male competition for mates and male–female interactions. The contributions of male and female density per se to mating system dynamics, however, are rarely examined, and the fitness consequences are often inferred rather than quantified. Male mosquitofish (Gambusia affinis) compete aggressively and frequently harass females for copulations, a behavior thought to reduce female fitness. Female fitness can also be reduced by increases in female density, which may affect food availability, cannibalism rates, and chemical interactions between females. I manipulated male and female densities of G. affinis to measure their effects on male–male aggression, male harassment toward females, and female fitness. I found that males chased rivals more often and attempted fewer copulations when female density decreased, but surprisingly male density had no significant effect on the frequency of these male behaviors. In contrast, males’ agonistic displays toward other males increased with male density, but display behavior was unaffected by female density. These results suggest that male and female density do not always contribute equally or at all to the patterns of behavior we observe. Female fitness declined as female density increased, the opposite pattern expected if male harassment is costly to females. This suggests that a strong, negative effect of female density overwhelmed any potential costs of male harassment. Sources of female density dependence and the consequences of changes in male and female density to patterns of male behavior are discussed.     

Offspring sex ratio in relation to female size in southern elephant seals,Mirounga leonina

Southern elephant seals Mirounga leonina display extreme sexual dimorphism. In addition females show great variation in size and stored resources at parturition. Therefore they present an excellent opportunity for examination of responses of sex ratio to resource availability. We studied the relationships between the size of southern elephant seal females at parturition and the size and sex of their pups at South Georgia over four breeding seasons. We found a large individual variation in maternal post-partum mass (range 296–977 kg, n=151). Larger mothers gave birth to larger pups, irrespective of the sex of their pup. Male pups were on average 14% larger than females at birth and consequently more costly to bring to parturition. Our results suggest that female southern elephant seals must weigh more than 300 kg if they are to breed at all, and more than 380 kg if they are to give birth to a male pup. Above this threshold the proportion of males among offspring rapidly increases with maternal mass, and stabilizes at a level not significantly different from parity. These results show that smaller females of southern elephant seals vary offspring sex ratio in a way that is consistent with theories on adaptive offspring sex ratio. A smaller mother with a male foetus may benefit from terminating her pregnancy and allocating the resources she saves to her own growth. She could then give birth to and raise a larger pup in the subsequent season.     

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.     

Adult sex ratio affects divorce rate in the monogamous endoparasite Schistosoma mansoni

“Divorce” (mate switching) rate is known to vary largely both between and within socially monogamous species. Although the adult sex ratio can have an important influence on mating patterns, very few studies have investigated the influence of sex ratio on divorce rate in monogamous species, and even less so from an experimental point of view. In addition, most studies on the causes and consequences of divorce have been performed on vertebrate species, whereas data for invertebrate monogamous species remain scarce. Schistosoma mansoni is a monogamous endoparasite with a complex life cycle characterized by asexual reproduction in the intermediate host and sexual reproduction in the definitive host. In the wild, populations of S. mansoni inside their definitive hosts are characterized by a male-biased sex ratio. We studied the influence of experimentally varying the adult sex ratio on divorce rate in S mansoni, using controlled infections of hosts with clonal populations. The more male-biased the sex ratio was, the more the divorce rate increased, whereas no such effect was observed under a female-biased sex ratio. In this study and for the first time, we showed, by handling the sex ratio, that the divorce rate increases in adult male-biased sex ratio conditions in a monogamous species.     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

Effects of food availability on dispersal and cub sex ratio in the Mednyi Arctic fox

Since the Pleistocene, Arctic foxes, Alopex lagopus, on Mednyi Island in the North Pacific have been isolated in a small area with rich food resources and no other terrestrial carnivores. This situation provides an unusually simple system within which the effect of food dispersion on demography and social organisation was examined. We studied the composition, location and dispersal of 67 Arctic fox groups and mapped their major food resources (seabird colonies) during 1994–2000 on Mednyi. We compared our observations with the predictions of models of sex-ratio determination. Our observations are most consistent with the predictions of Julliard's (2000) model, where mothers are expected to produce more offspring of the most dispersing sex in low-quality habitats, and more offspring of the most philopatric sex in high-quality habitats. The polygynous foxes on Mednyi Island lived where the principal food resources were patchily distributed (present on 11% of the shoreline), and cub survival to dispersal age or reproductive adult was higher in rich (25/45) than in poor (24/79) home ranges. Furthermore, dispersal was strongly sex-biased: most females (60%) remained on their natal ranges, whereas very few males (9%) did so. Significantly more female than male cubs (54 compared with 24) emerged from dens in resource rich ranges, whereas the sex ratio on poor ranges was approximately equal (51 females and 56 males). While our observations are also to some extent consistent with the local resource enhancement (LRE) hypothesis (which predicts a bias towards the sex most likely to cooperate with parents), this does not account for the observed spatial variability.     

Cooperatively breeding superb fairy-wrens show no facultative manipulation of offspring sex ratio despite plausible benefits

We report a long-term study of offspring sex ratios in the cooperatively breeding superb fairy-wren Malurus cyaneus. Detailed study of this species had revealed a suite of potentially strong selection pressures on the sex ratio. First, females gain substantial fitness benefits from the presence of helpers; so females without male helpers would benefit from any strategy that increased the probability of recruiting help, such as overproduction of sons (local resource enhancement hypothesis), but large numbers of helper males compete among themselves, favouring the production of daughters (local resource competition). Second, daughters fledged early in the season have far greater chances of recruitment to the breeding population than late-fledged daughters, so mothers would benefit from production of daughters early in the breeding season (early bird hypothesis). Third, extra-group mate choice imposes strong sexual selection on males, suggesting that females mating with attractive sires could benefit from investing in sons (sexual selection hypothesis). However, the predictions from these and other sex ratio hypotheses were rejected. The only convincing evidence for manipulation of the sex ratio was a slight bias towards sons (11 sons to 10 daughters) that occurred regardless of context. This result does not support current theory.     

Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater)

Females of many socially monogamous bird species commonly engage in extra-pair copulations. Assuming that extra-pair males are more attractive than the females’ social partners and that attractiveness has a heritable component, sex allocation theory predicts facultative overproduction of sons among extra-pair offspring (EPO) as sons benefit more than daughters from inheriting their father’s attractiveness traits. Here, we present a large-scale, three-year study on sex ratio variation in a passerine bird, the coal tit (Parus ater). Molecular sexing in combination with paternity analysis revealed no evidence for a male-bias in EPO sex ratios compared to their within-pair maternal half-siblings. Our main conclusion, therefore, is that facultative sex allocation to EPO is absent in the coal tit, in accordance with findings in several other species. Either there is no net selection for a deviation from random sex ratio variation (e.g. because extra-pair mating may serve goals different from striving for ‘attractiveness genes’) or evolutionary constraints preclude the evolution of precise maternal sex ratio adjustment. It is interesting to note that, however, we found broods without EPO as well as broods without mortality to be relatively female-biased compared to broods with EPO and mortality, respectively. We were unable to identify any environmental or parental variable to co-vary with brood sex ratios. There was no significant repeatability of sex ratios in consecutive broods of individual females that would hint at some idiosyncratic maternal sex ratio adjustment. Further research is needed to resolve the biological significance of the correlation between brood sex ratios and extra-pair paternity and mortality incidence, respectively.     

Diet quality affects an attractive white plumage pattern in dark-eyed juncos (Junco hyemalis)

Sexually selected traits that act as signals of quality often display some degree of condition dependence. In birds, condition dependence of ornamental plumage is often mediated by production costs related to acquisition or allocation of dietary resources. White plumage ornaments, however, have often been assumed to be inexpensive because their production requires neither pigment nor specialized feather structure. In male dark-eyed juncos (Junco hyemalis), the size of a white patch on the tail contributes to attractiveness and mating success. Using captive males, we examined the effects of diet quality on the size and brightness of the tail-white patch. After removing four tail feathers to induce replacement, we maintained subjects on a subsistence (low-protein) or enriched (high-protein) diet while induced feathers grew. Birds that received an enriched diet grew their feathers more quickly and grew larger, brighter white patches. Feather growth rate was positively correlated with the increase in the size of the tail-white patch, a relationship that was stronger in the subsistence diet group. However, within diet treatments, faster-grown feathers were slightly duller. Taken together, these results suggest that variation in diet quality may lead to condition-dependent expression of tail white and that condition dependence may be stronger in more stressful environments. We suggest a mechanism by which increased feather growth rate may lead to an increase in the size of the tail-white patch and discuss potential trade-offs between signal size and brightness.     

Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, Megachile rotundata

Fisher's theoretical prediction of equal investment in each sex for a panmictic population (The genetical theory of natural selection. Clarendon, Oxford, 1930) can be altered by a number of factors. For example, the sex ratio theory predicts variation in equal investment in each sex when the maternal fitness gains from increased investment differ between sexes. Changing sex allocation because of changing payoffs may result from different ecological situations, such as foraging conditions. We investigated the impact of foraging travel cost on relative investment in sons vs daughters. Field studies were carried out with the central-place-foraging leafcutter bee Megachile rotundata (Fabricius), which has smaller males than females. Therefore, less investment is required to produce a viable son compared with a daughter. We found that with increased flight distance to resources, females produced a greater proportion of sons. Females also invested fewer resources in individual sons and daughters and produced fewer offspring with increased flight distance.     

Do female roe deer in good condition produce more sons than daughters

In polygynous roe deer Capreolus capreolus, males are only slightly heavier than females and the overall sex ratio at birth is close to unity. We studied offspring sex ratio and litter size (range 1–4, n = 74) of culled females, in utero, which provided an opportunity to examine responses of sex ratio to maternal condition. Male embryos were heavier than their sisters, and male fawns (9 months old) heavier than female fawns, suggesting a higher growth rate in males. There was no evidence for differential mortality between the sexes from birth to 9 months old. Heavier adult females produced larger embryos than lighter, or primiparous females. The overall sex ratio of embryos did not differ from unity, but adult does had more male embryos (55%) than primiparous does (32%), and the proportion of male embryos in a litter increased with the mother's body mass. Litter size also tended to increase with maternal age and body mass. We argue that this pattern reflects adaptive variation in offspring sex ratio.     

Optimal investment in sons and daughters when parents do not know the sex of their offspring

Optimal parental investment usually differs depending on the sex of the offspring. However, parents in most organisms cannot discriminate the sex of their young until those young are energetically independent. In a species with physical male–male competition, males are often larger and usually develop sexual ornaments, so male offspring are often more costly to produce. However, Onthophagus dung beetles (Coleoptera; Scarabaeidae) are highly dimorphic in secondary sexual characters, but sexually monomorphic in body size, despite strong male–male competition for mates. We demonstrate that because parents provide all resources required by their offspring before adulthood, O. atripennis exhibits no sexual size dimorphism irrespective of sexual selection pressure favoring sexual dimorphism. By constructing a graphic model with three fitness curves (for sons, daughters, and expected fitness return for parents), we demonstrate that natural selection favors parents that provide both sons and daughters with the optimal amount of investment for sons, which is far greater than that for daughters. This is because the cost of producing small sons, that are unable to compete for mates, is far greater than the cost of producing daughters that are larger than necessary. This theoretical prediction can explain sexual dimorphism without sexual size dimorphism, widely observed in species with crucial parental care such as dung beetles and leaf-rolling beetles, and may provide an insight into the enigmatic relationship between sexual size dimorphism and sexual dimorphism.     

Multiple mate choice criteria and the importance of age for male mating success in the microhylid frog, Cophixalus ornatus

We examined multiple mate choice criteria in Cophixalus ornatus, a terrestrial breeding, microhylid frog. Mate choice consisted of three stages: mate attraction (male calling), courtship (male behavior between the call site and the nest), and nest site selection by the female. For male C. ornatus, the possession of a call with low dominant frequency relative to calling neighbors increased the probability that they would attract females. Dominant frequency was negatively correlated with age independent of male mass and snout vent length. When escorting the female from the call site to their nest, males traveled along more convoluted paths than when returning to the nest alone. The convolution of the path was, therefore, considered an aspect of courtship. Females released eggs into nests with structural characteristics typical of nests constructed by older males. Thus, females increased their chances of locating an acceptable nest by preferentially approaching males with lower dominant frequencies. This study is the first to demonstrate that age, independent of mass or snout-vent length, can influence call characteristics in anurans, and it is also the first to demonstrate the importance of male age to female mate choice in an amphibian.     

Mate choice in the yellow-shouldered widowbird: correlates of male attractiveness

Recent investigations of male ornaments in sexual selection have used experimental manipulation of tail length in three widowbird species, but only for one of these have correlates of male reproductive success been reported. I examined correlates of male attractiveness to nesting females over two breeding seasons for the polygynous yellow-shouldered widowbird, Euplectes macrourus, in order to discover which cues females may be using to select mates. The black, long-tailed ( 10 cm) males defend large territories and build nest frames, or cock's nests, which females then line and use for nesting. I examined various aspects of male morphology, five behavioral displays, territory characteristics, and the number of cock's nests that males built. Few correlates of mating success were found. The best predictor was the number of cock's nests that a male builds, though one courtship display also correlated with male mating success in 1 year, as did average grass height. Tail length did not correlate with male mating success. A partial correlation analysis confirmed that cock's nests and, in 1 year, grass height, were the primary contributers to male success. Females may choose where to nest primarily on the availability of suitable nesting sites. Long tails may be used by females seeking extra-pair copulations or in male-male competition for territories.     

Offspring sex ratio in relation to parental structural size and body condition in the long-lived wandering albatross (<Emphasis Type="Italic">Diomedea exulans</Emphasis>)

Sex ratio theory is one of the most controversial topics in evolutionary ecology. Many deviations from an equal production of males and females are reported in the literature, but few patterns appear to hold across species or populations. There is clearly a need to identify fitness effects of sex ratio variation. We studied this aspect in a population of a long-lived seabird, the wandering albatross (Diomedea exulans), using molecular sex-identification techniques. We report that parental traits affect both (1) fledgling traits in a sex-dependent way and (2) chick sex: Sons are overproduced when likely to be large at fledging and, to a lesser extent, daughters are overproduced when likely to be in good body condition at fledging. Because for the same population, a previous study reported that post-fledging survival was positively affected by size in males and by body condition in females, our results suggest that wandering albatrosses manipulate offspring sex to increase post-fledging survival.     

Search costs influence the spatial distribution,but not the level,of extra-pair mating in tree swallows

Costs of searching for a mate are an important component of models of sexual selection, yet they have rarely been examined in wild populations of vertebrates. In this paper, we report an experiment in which we handicapped female tree swallows by clipping some flight feathers. This manipulation increased the costs of flight and searching for extra-pair mates. Despite these costs, handicapped females had the same level of extra-pair mating (percentage of extra-pair young, percentage of broods with extra-pair young, and the number of extra-pair sires per brood) as control females. However, handicapped females were more likely to have young sired by extra-pair males that lived closer to her nest than control females. This change in the distribution of extra-pair mating was most likely due to female choice rather than male coercion, and it suggests that extra-pair mating has significant benefits to females. One important implication of our study is that ecological and social factors that influence search costs could affect the spatial distribution of extra-pair sires and, consequently, the intensity of sexual selection. These effects may have been overlooked in previous studies that did not identify extra-pair sires.     

Sexual selection in the northern pintail (Anas acuta): the importance of female choice versus male-male competition in the evolution of sexually-selected traits

We experimentally studied the relative importance of plumage, dominance status, and courtship behavior in determining male pairing success in the northern pintail Anas acuta and assessed whether these traits function in female choice, male-male competition or both. In an experiment (experiment IA) that eliminated the confounding effects of male-male competition and social courtship, females chose males with pure white breasts and colorful scapular feathers. When the same group of birds were free to interact (experiment 1B), male behavior was more important: females chose males that courted them intensely and were attentive to them, although preferred males again had whiter breasts and more colorful scapulars. In a second experiment (experiment 2), testing the effect of age on pairing success, females showed a significant preference for 2-year-old males over yearlings: 2-year-old males courted more and were more attentive to the female than yearlings; they were also more colorful than yearlings in a number of plumage measurements. Although males (in both experiments 1B and 2) were aggressive to one another while courting the female and dominant males were sometimes able to exclude subordinates from social courtship, contrary to expectation, we found no relationship between initial dominance rank and pairing success or dominance rank and age. In addition, dominance was not correlated with any of the morphological traits measured. Once chosen, however, subordinate males typically initiated fights with the higher-ranked male(s) and quickly achieved dominance. These results suggest that (1) females choose males based on a suite of morphological and behavioral characteristics, (2) male dominance relationships do not constrain active female choice, (3) a male's position in a dominance hierarchy is largely a result rather than a cause of female choice, and (4) female choice plays a more significant role than male-male competition in the evolution of several secondary sexual traits in male northern pintails.