Food or sex—males and females in a sex role reversed pipefish have different interests

In a sex role reversed pipefish, Syngnathus typhle, we found that basic life history allocations were directly influenced by sexual selection. We investigated time allocation to foraging and mating, respectively, in a choice experiment, giving males and females, of small or large body size, a choice between food and a potential partner. We found that males were more interested in foraging than mating, i.e., were more frequently observed in front of the food than in front of the partner, whereas females were more interested in the potential partner. This reflects sexual selection operating differently on the two sexes, as males and females are relatively similar in other life history traits, such as growth, mortality, age of maturity, dispersal, and parental expenditure. Moreover, large individuals allocated more time to mating activities, small to feeding. Individuals more interested in mating compared to food were subsequently more critical when given a choice between a large (high-quality) and a small (low-quality) partner, whereas individuals more interested in food were not selective. These findings are consistent with our predictions: sex-role reversed males can be relatively sure of achieving one or more matings, and should allocate more time to feeding and, hence, to parental investment, growth and/or future reproduction. Females, on the other hand, have more uncertain mating prospects and should allocate time to imminent reproductive activities, thereby foregoing other life history traits such as growth and future egg production. By this, they also sacrifice future fecundity and attractiveness.     

Frequency and timing of extrapair fertilisation in the polyandrous red phalarope (Phalaropus fulicarius)

In sequentially polyandrous bird species, where females mate with different males in succession during a single breeding season, sperm stored by females can occasionally lead to extrapair fertilisations (EPFs) in clutches cared for by the second and subsequent males. Thus, we predicted that in red phalaropes (Phalaropus fulicarius) – a sex-role-reversed, sequentially polyandrous, arctic breeding shorebird – EPFs would occur more frequently in clutches laid later in the breeding season. We used multilocus DNA profiling to examine the frequency and timing of EPFs in a population of red phalaropes breeding in the Canadian high arctic. Using a technique to determine parentage without maternal DNA, we inferred that 6 of 70 chicks in 18 broods resulted from EPFs – one extrapair chick in each of 6 broods. These results were supported by a further analysis using microsatellite DNA. As predicted, broods containing EPFs hatched from clutches laid significantly later in the season than did broods containing no EPFs. The difference in median hatch dates between broods with and without EPFs was 9.0 days, or 38% of the entire egg-laying period in that season. For the whole breeding season, we estimated that 6.5% of chicks were sired by extrapair males, which is similar to extrapair paternity estimates for other sex-role-reversed birds, but relatively low compared to the majority of socially monogamous species studied so far. Received: 24 August 1998 / Received in revised form: 18 January 1999 / Accepted: 24 January 1999     

Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and competition

Mammalian life histories suggest that maternal body condition and social dominance (a measure of resource-holding potential) influence the physical and social development of offspring, and thereby their reproductive success. Predictably, a mother should produce that sex of offspring which contributes most to her fitness (as measured by the number of her grandchildren) and that she is best able to raise within the constraints imposed by her condition, social rank, and environment. Such combined effects were investigated by monitoring variations in body condition (weight) and behavior of female toque macaques, Macaca sinica of Sri Lanka, in a changing forest environment over 18 years. Maternal rank, by itself, had no influence on offspring sex, but did affect maternal body condition. The combined effects of rank and condition indicated the following: mothers in robust condition bore more sons, whereas those in moderate condition bore more daughters, but both effects were expressed most strongly among mothers of high rank. Where the consequences of low rank were felt most acutely, as shown by poor condition, mothers underproduced daughters. Environmental quality directly influenced rank and condition interactions, and thus sex ratios. These relationships, and data from other mammals suggest an empirically and theoretically consistent pattern of sex allocation in mammals. New predictions integrate effects, proposed by Trivers and Willard, that are rooted in male mate competition, which is universal among polygynous mammals, with those of local resource competition (and/or female reproductive competition), which are not universal and differ in intensity between the socioecologies and local environments of different species. Received: 30 May 1998 / Accepted after revision: 29 August 1998     

Does the African social spider Stegodyphus dumicola control the sex of individual offspring?

By scoring the chromosome number of developing embryos, we show that the sex ratio bias of the African social spider Stegodyphus dumicola Pocock is the result of an overproduction of female embryos. Only 17% of 585 embryos sexed from 14 egg sacs were male, a significant departure from a 1:1 sex ratio. We also explored the possibility of direct control of the sex of individual offspring in this species by examining the variance in the number of males per sac and the spatial distribution of male and female embryos within the sacs. We postulated that a variance in the number of males per sac lower than binomial (i.e., underdispersed or precise sex ratios) or a non-random distribution of male embryos within the sacs would suggest direct control of the sex of individual offspring. We found that the variance in the number of males per sac was indistinguishable from binomial and significantly larger than expected under exact ratios. Likewise, the spatial distribution of male embryos within three sacs examined was no more clustered than expected by chance. The sex ratio biasing mechanism in this species, therefore, apparently only allows control of the mean sex ratio but not of its variance. We present randomization and Monte Carlo methods that can be applied to test for departures from a random spatial arrangement of male and female embryos in an egg mass and for departures from binomial or exact ratios when not all members of a clutch have been sexed. Received: 21 October 1998 / Received in revised form: 23 March 1999 / Accepted: 26 April 1999     

Evidence for seasonal mate limitation in populations of an intertidal amphipod, Corophium volutator (Pallas)

Potential rates of reproduction (PRR) differ between the sexes of many animal species. Adult sex ratios together with PRR are expected to determine the operational sex ratio (OSR) defined as the ratio of fertilizable females to sexually active males at any given time. OSR is expected to determine the degree to which one sex competes for another—the limiting sex. We explored the potential for mate limitation in an intertidal amphipod, Corophium volutator (Pallas). Males have higher PRR than females, but males may be limiting because of extreme female-biased sex ratios observed in this species. Consistent with this idea, late season females were less likely to be ovigerous and had smaller size-specific clutches, both of which were associated with seasonal declines in availability of males of reproductive size. Seasonal changes in ovigery could not be explained by seasonal changes across sites in other factors (e.g., female body size or phenology of breeding). Smaller females were less likely to become ovigerous later in the season at three of four sites. Seasonal reductions in clutch size also occurred among small females expected to be reproducing for their first time. In complimentary laboratory experiments, reduced likelihood of ovigery and reduced fecundity occurred when the number of receptive females was increased relative to availability of a reproductively active male. Our results suggest male mate limitation can occur seasonally in this species and that male limitation is regionally widespread and may affect recruitment.     

Is sex-specific mass gain in Cory’s shearwaters <Emphasis Type="Italic">Calonectris diomedea</Emphasis> related to begging and steroid hormone expression?

Mass differences between the sexes of dimorphic bird species often appear early in the nestling development. But how do adults know how much to feed a chick in a sexually dimorphic species? Do chicks of the heavier sex beg more? We studied begging in Cory’s shearwaters Calonectris diomedea, a species with heavier adult and juvenile males than females. We found that begging rates and call numbers were not different between male and female chicks, but parameters of begging intensity differed between the sexes in their relationship to chick body condition. For the same body condition, males had significantly higher begging call numbers and rates. Acoustical parameters, which were analysed semi-automatically, included the lengths of call and silence intervals, the minimum, mean and maximum frequency in a call and the number of frequency peaks within a call. We found no consistent differences of acoustic begging call elements between the sexes. Male and female chicks did not differ in the levels of the steroid hormones testosterone or corticosterone in the second quarter of the nestling period, and the mechanism leading to sex-related differences in begging rates for a given body condition remains unknown.     

Mate guarding,copulation strategies and paternity in the sex-role reversed,socially polyandrous red-necked phalarope<Emphasis Type="Italic"> Phalaropus lobatus</Emphasis>

In a recent review, Westneat and Stewart (2003) compiled evidence that extra-pair paternity results from a three-player interaction in which sexual conflict is a potent force. Sequentially polyandrous species of birds appear to fit this idea well. Earlier breeding males may attempt to use sperm storage by females to obtain paternity in their mates subsequent clutches. Later-breeding males may consequently attempt to avoid sperm competition by preferring to pair with previously unmated females. Females may bias events one way or the other. We examined the applicability of these hypotheses by studying mating behavior and paternity in red-necked phalaropes (Phalaropus lobatus), a sex-role reversed, socially polyandrous shorebird. Male red-necked phalaropes guarded mates more strongly than other shorebirds. Males increased within-pair copulation attempts during their mates fertile period, and maintained or further increased attempts towards the end of laying, suggesting an attempt to fertilize the females next clutch; these attempts were usually thwarted by the female. Paired males sought extra-pair copulations with females about to re-enter the breeding pool. Multilocus DNA fingerprinting showed that 6% of clutches (4/63) each contained one chick sired by a male other than the incubator, producing a population rate of these events of 1.7% (n=226 chicks). Male mates had full paternity in all first clutches (n=25) and 15 of 16 monogamous replacement clutches. In contrast, 3 of 6 clutches of second males contained extra-pair young likely fathered by the females previous mate. Previously mated female phalaropes may employ counter-strategies that prevent later mating males from discriminating against them. The stability of this polyandrous system, in which males provide all parental care, ultimately may depend on females providing males with eggs containing primarily genes of the incubating male, and not a previous mate.Communicated by M. Webster     

Body size preferences in the pot-bellied seahorse <Emphasis Type="Italic">Hippocampus abdominalis:</Emphasis> choosy males and indiscriminate females

Male seahorses (genus Hippocampus) provide all post-fertilization parental care, yet despite high levels of paternal investment, these species have long been thought to have conventional sex roles, with female mate choice and male–male competition. Recent studies of the pot-bellied seahorse (Hippocampus abdominalis) have shown that sex-role reversal occurs in high-density female-biased populations, indicating that male mating preferences may lead to sexual selection on females in this species. Egg size, egg number, and offspring size all correlate positively with female body size in Hippocampus, and by choosing large mating partners, male seahorses may increase their reproductive success. While male brood size is also positively correlated with body size, small H. abdominalis males can carry exceptionally large broods, suggesting that the fecundity benefits of female preference for large partners may be limited. We investigated the importance of body size in reproductive decisions of H. abdominalis, presenting focal individuals of both sexes with potential mating partners of different sizes. Mating preferences were quantified in terms of time spent courting each potential partner. Male seahorses were highly active throughout the mate-choice trials and showed a clear behavioral preference for large partners, while females showed significantly lower levels of activity and equivocal mating preferences. The strong male preferences for large females demonstrated here suggest that sexual selection may act strongly on female body size in wild populations of H. abdominalis, consistent with predictions on the importance of female body size for reproductive output in this species. An erratum to this article can be found at     

Population Consequences of Environmental Sex Reversal

Abstract:  When sex determination in a species is predominantly genetic but environmentally reversible, exposure to (anthropogenic) changes in the environment can lead to shifts in a population's sex ratio. Such scenarios may be common in many fishes and amphibians, yet their ramifications remain largely unexplored. We used a simple model to study the (short-term) population consequences of environmental sex reversal (ESR). We examined the effects on sex ratios, sex chromosome frequencies, and population growth and persistence after exposure to environmental forces with feminizing or masculinizing tendencies. When environmental feminization was strong, X chromosomes were driven to extinction. Analogously, extinction of normally male-linked genetic factors (e.g., Y chromosomes) was caused by continuous environmental masculinization. Although moderate feminization was beneficial for population growth in the absence of large viability effects, our results suggest that the consequences of ESR are generally negative in terms of population size and the persistence of sex chromosomes. Extreme sex ratios resulting from high rates of ESR also reduced effective population sizes considerably. This may limit any evolutionary response to the deleterious effects of ESR. Our findings suggest that ESR changes population growth and sex ratios in some counter-intuitive ways and can change the predominant factor in sex determination from genetic to fully environmental, often within only a few tens of generations. Populations that lose genetic sex determination may quickly go extinct if the environmental forces that cause sex reversal cease.     

Daring females,devoted males,and reversed sexual size dimorphism in the sand-dwelling spider <Emphasis Type="Italic">Allocosa brasiliensis</Emphasis> (Araneae,Lycosidae)

Sexual selection theory predicts that a higher investment in offspring will turn females into the selective sex, while males will compete for accessing and courting them. However, there are exceptions to the rule. When males present a high reproductive investment, sex roles can reverse from typical patterns, turning males into the choosy sex, while females locate males and initiate courtship. In many spiders, males are smaller than females, wandering in search of sedentary females and maximizing the number of copulations. In the present study, we present findings on the sand-dwelling wolf spider, Allocosa brasiliensis, evidencing a reversal in typical courtship roles reported for the first time in spiders. Males were bigger than females. Females located males and initiated courtship. Copulation always occurred in male burrows and took place mainly in long burrows. Males donated their burrows to the females after copulation, closing the entrance before leaving with female cooperation from inside. Males would provide females with a secure place for ovipositing, being exposed to predation and diminishing their future mating possibilities until constructing a new burrow. The cost of vacating the burrow and losing the refuge in an unpredictable habitat, such as sand dunes, would explain the courtship roles reversal in this spider species. Results turn A. brasiliensis as a promising model for discussing the determinants of sex roles and the pressures that drive their evolution and maintenance. Electronic supplementary material The online version of this article (doi: ) contains supplementary material, which is available to authorized users.     

Contradictory results in sex ratio studies: populations do not necessarily differ

In avian sex ratio studies, results often differ between species and between populations within species. Some researchers argued that positive results were simply statistical artefacts and that sex ratio adjustment did not exist. However, many of the proposed mechanisms of sex ratio adjustment result in costly laying gaps. In these cases, females laying large clutches may restrict the sex manipulation to the first egg of the clutch. Consequently, detectability of sex ratio adjustment on the level of the clutch can be low. Though obvious, this fact is often neglected in the literature. Using simulations, I show that the proportion of undetected sex manipulation can be surprisingly high when the manipulation is restricted to the first egg. If the sample size is 50 broods, there is 47% and 71% chance in 6- and 12-egg clutches, respectively, that sex manipulation is undetected. Even with large samples (n = 100), the figures are 15% and 46%. These data suggest that nonsignificant results for clutch sex ratios do not necessarily mean that sex is not manipulated in a portion of the brood, e.g. in first-laid eggs. Hence, whenever possible, data on laying order-specific sex manipulation should also be collected. Without such data, contradictory results on brood sex ratios should be interpreted cautiously.     

The sex in short supply for matings varies over small spatial scales in a katydid (Kawanaphilanartee, Orthoptera: Tettigoniidae)

In katydids such as Kawanaphilanartee, a female bias in the operational sex ratio (OSR) results in female competition for mates and male choice of mates. Previous work showed that the excess of sexually active females occurs when food availability is low, in part because less food increases the propensity of females to mate as they forage for the large edible spermatophores produced by males. In this study with K.nartee, a pollen-feeding species, we estimate natural variation in numbers of sexually active males and females by assessing male calling activity and the propensity of females to respond to experimental calling males. We found an excess of sexually active males at a site with many flowers and an excess of sexually active females at a site with few flowers about 900 m away. Between-site differences in gut masses of calling males were consistent with the hypothesis that pollen availability controls OSR. Finally, at a third site where flowers were at first scarce, we found that the initial excess in sexually active females changed to an excess of sexually active males after a clump of grass-trees flowered. The mean gut mass of all sampled males from this site increased after flowering. The large variation in OSR that we document for K. nartee highlights the importance of identifying the appropriate spatial and temporal scales over which OSRs are measured in studies of factors controlling sexual selection. Received: 13 May 1997 / Accepted after revision: 27 October 1997     

Preventing behavioural interactions with a male facilitates sex change in female bluebanded gobies, Lythrypnus dalli

Sex change in marine teleost fishes is commonly regulated by social factors. In species that exhibit protogynous sex change, such as the bluebanded goby Lythrypnus dalli, the most dominant female typically initiates sex change when a male is removed from the social group. Females can use visual, chemical or tactile cues to assess the presence or absence of a male. The primary goal of our study was to determine whether the olfactory and visual presence of a male versus its behavioural interactions with females were important for mediating sex change. We exposed females to three different treatments: absence of a male, presence of a male that could physically interact with her and presence of a male behind a barrier that allowed visual and olfactory interactions but prohibited physical interactions. Sex change occurred in the absence of a male but not in the presence of a male that could physically interact with the female. The presence of a male behind the barrier did not prevent sex change but affected the timing of sex change. Season appeared to affect the latency to initiate male typical courtship, with a delay at the end of the reproductive season only when the male was present behind the barrier. We discuss the seasonal results in terms of L. dalli life history and the potential benefits and costs of changing sex late in the season in the presence or absence of aggressive reinforcement by the male. Our results identify direct behavioural interactions as an important proximate mechanism in the social regulation of sex change in L. dalli.     

Birth sex ratios in sheep over nine lambing seasons: years 7–9 and the effects of ageing

The birth sex ratio of a commercial flock of Suffolk cross sheep, Ovis aries, was studied over nine consecutive lambing seasons. In all data from 2704 lambs were recorded and analysed. The overall (1985–1993) birth sex ratio was 49.96% male lambs. Ewes with single lambs produced significantly more males (53.04%) than ewes with triplets (45.54% male). A significant positive correlation was found between the flock age and the birth sex ratio (1985–1992). As the flock aged the birth sex ratio changed from female biased to male biased, remained male biased for a number of years, and then became female biased again. This pattern is evident first in single, then in twin and later in triplet births. Among like sex twins (males and females) (1985–1993) more males (53.88%) were born in the first half and more females (45.57% males) in the second half of the lambing season. The difference between the two halves is significant.     

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.     

Sex-specific effects of yolk-androgens on growth of nestling American kestrels

Maternally derived androgen hormones concentrate in avian egg yolks as the yolks grow on the female’s ovary, possibly forming a basis for important maternal effects in birds. In the American kestrel (Falco sparverius), experimental elevation of yolk androgens in the first-laid egg of a clutch (a-egg) to the concentrations found naturally in a clutch’s later-laid eggs reduces the growth rate of a-egg nestlings compared to controls. These findings, together with discoveries from other species that the effects of yolk androgens on growth of female nestlings may differ from their effects on growth of male nestlings, raise the hypothesis that natural changes in yolk-androgen concentrations with laying order are ultimately due to a difference between the sexes in their yolk-androgen sensitivity and between early- and late-laid eggs in their sex ratio. By re-analyzing previously published data and adding to the analysis data from previously unanalyzed blood samples used for sex determination, we investigated possible sex-specific effects of yolk-androgens in the context of a potential sex-biased laying order in free-living American kestrels. We used a multi-level, mixed model with a Gompertz function to analyze growth of nestlings hatching from a-eggs that were control-treated or in which we experimentally elevated yolk-androgen concentrations shortly after laying to the higher concentrations naturally found in later-laid eggs. We discovered that male nestlings were more susceptible than female nestlings to growth inhibition by yolk-androgen elevation but did not find a bias in sex ratio with respect to laying order. Together, these findings do not support the above hypothesis. However, they are consistent with the hypothesis that sex differences in yolk-androgen sensitivity enable mothers to economically tune reproductive effort to an individual offspring’s reproductive value, which can vary more for one sex than the other.     

Human digit ratios depend on birth order and sex of older siblings and predict maternal fecundity

In men, the length ratio of the second to fourth finger (2D:4D) is smaller, while the length of the fourth finger relative to body height (4D:H) is larger than in women. Inter- and intrasexual variations in 2D:4D and 4D:H may depend on variation in fetal androgen and oestrogen environment. As maternal physiology varies with parity and is differentially affected by gestation of either sex, offspring 2D:4D and 4D:H may change according to sex and number of older siblings and may predict subsequent maternal performance. We analysed 2D:4D and 4D:H in Caucasian university students. 2D:4D was smaller and 4D:H was larger in males than in females, but no sexual dimorphism existed in 2D:H. In males, length ratios did not vary with birth order. 2D:4D became more masculine with increasing proportion of males among older siblings, and 2D:4D and 4D:H became more feminine as the number of older sisters increased. In females, length ratios did not vary with the number of older sisters or brothers. 2D:4D was also not related to birth order, but 4D:H became more masculine with birth order. In females, residual maternal fecundity (number of maternal offspring after the participant) decreased as 4D:H became more masculine. These findings are partly consistent with those from previous studies and suggest that maternal fecundity co-varies with length ratios and thus possibly fetal hormone environment of older offspring. 2D:4D and 4D:H may therefore represent powerful tools to investigate the relationships between fetal environment, offspring phenotype and maternal life history at mechanistic and evolutionary levels.     

Size assessment via a visual signal in snapping shrimp

Snapping shrimp are highly aggressive decapod crustaceans, with large, asymmetric chelae. Body size determines the outcome of both inter- and intrasexual interactions. Both the body and chela sizes of mated pairs are correlated, but the body size correlation is significantly stronger. In competitive interactions between individuals of the same sex, larger individuals usually win. Because the size of the major chela is a function of body size in both males and females, chela size could be used to assess body size early in interactions, before engaging in more high risk behaviors. To determine whether the major chela is used in size assessment, I presented shrimp with isolated chelae. Male snapping shrimp responded aggressively to isolated chelae when they were fixed open in a display posture, and the degree of aggressive response depended on the relative size of the chela. These data provide direct experimental evidence for the use of a visual signal in size assessment. Females, in contrast, responded aggressively to both the open and closed chela, and their responses did not depend on relative size. This sex difference in response may be due to differences in the value of certain resources, such as shelters, to males and females: females may be more willing to respond aggressively regardless of the apparent size of their opponent, in order to acquire more reliable information regarding size, motivation or fighting ability. Received: 30 December 1994/Accepted after revision: 14 August 1995     

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.