The effect of nest aggregation on the reproductive behaviour of the peacock blenny Salaria pavo

The effect of nest aggregation in courtship behaviour was tested experimentally in an ecologically constrained, sex-role reversed population of the peacock blenny Salaria pavo . Mixed sex groups of eight males and eight females were tested in experimental tanks, containing eight potential nests either aggregated or dispersed. In the aggregated treatment, males spent more time inside their nests and monopolized other potential nests, causing a female-biased operational sex ratio (OSR). In the aggregated treatment, females also expressed more courtship behaviour. The results in general support the prediction that the aggregation of nests promotes male monopolization of potential nests, resulting in fewer nest-holding males and therefore a female-biased OSR that leads to the reversal of sex roles.     

Monogamy and sex role reversal in the pipefish Corythoichthys haematopterus

We observed the mating pattern and social behaviour of the pipefish Corythoichthys haematopterus in temperate waters of Japan during three successive breeding seasons. Males cared for a clutch in their brood pouch for 9-19 days until hatching and had several broods in the season with nonbrooding intervals of only 1 or 2 days. The population sex ratio was female biased and some females were always excluded from reproduction. Although males were sometimes courted by unmated females together with their regular partners, they always mated with the latter. The pair bond was maintained until the next season if both members survived. When males lost their partners, they remated with neighbouring unmated females within a few days. In contrast, widowed females remained unmated for a long time. Females had larger home ranges and were more active in courtship displays than males. This pipefish provides the first example of sex role reversal among monogamous syngnathid fish. We suggest that mate guarding by females is a primary proximate factor for maintenance of monogamy in this fish. Copyright 2001 The Association for the Study of Animal Behaviour.     

Adaptive sex ratio variation in pre-industrial human (Homo sapiens) populations?

Sex allocation theory predicts that in a population with a biased operational sex ratio (OSR), parents will increase their fitness by adjusting the sex ratio of their progeny towards the rarer sex, until OSR has reached a level where the overproduction of either sex no longer increases a parent''s probability of having grandchildren. Furthermore, in a monogamous mating system, a biased OSR is expected to lead to lowered mean fecundity among individuals of the more abundant sex. We studied the influence of OSR on the sex ratio of newborns and on the population birth rate using an extensive data set (n = 14,420 births) from pre-industrial (1775-1850) Finland. The overall effect of current OSR on sex ratio at birth was significant, and in the majority of the 21 parishes included in this study, more sons were produced when males were rarer than females. This suggests that humans adjusted the sex ratio of their offspring in response to the local OSR to maximize the reproductive success of their progeny. Birth rate and, presumably, also population growth rate increased when the sex ratio (males:females) among reproductive age classes approached equality. However, the strength of these patterns varied across the parishes, suggesting that factors other than OSR (e.g. socioeconomic or environmental factors may also have influenced the sex ratio at birth and the birth rate.     

Genetic monogamy despite social promiscuity in the pot-bellied seahorse (Hippocampus abdominalis)

Sexual selection theory predicts a positive correlation between relative parental investment and mate choice. In syngnathid fishes (seahorses and pipefish), males brood offspring in specialized brooding structures. While female-female mating competition has been demonstrated in some pipefishes, all seahorses (genus Hippocampus) studied to date have been found to have conventional sex roles with greater male-male competition for access to mates despite possessing the most complex brood structures in the family. Although multiple mating is common in pipefish, seahorses are again exceptional, exhibiting strict genetic monogamy. Both demographic and behavioural explanations have been offered to explain the lack of multiple mating in seahorse species, but these hypotheses have not yet been explicitly addressed. We investigated mating systems and brood parentage of the pot-bellied seahorse, Hippocampus abdominalis, a temperate-water species that is socially promiscuous with conventional sex roles in laboratory populations. We observed promiscuous courtship behaviour and sex-role reversal in high density, female-biased field populations of H. abdominalis. We hypothesize that sex roles are plastic in H. abdominalis, depending on local population density and sex ratio. Despite promiscuous courtship behaviour, all assayed male seahorses were genetically monogamous in both laboratory and wild populations. Physiological limitations associated with embryo incubation may explain the absence of multiple mating in seahorses and may have played an important role in the development of the unique reproductive behaviour typical in these species.     

How do we decide that a species is sex-role reversed?

Defining sex roles has been driven by differences in mating systems at the extreme: polygyny and polyandry. Roles may reverse depending on which sex limits the reproductive rate of the other, and it is generally the female that limits the male. Males therefore compete for female mates. But in species in which the male limits the reproductive rate of the female, the female competes for male mates and assumes the masculine role. Complications arise, however, in species with typical roles when males are temporarily limiting, and females then briefly compete for and display to males. Problems also occur among tightly monogamous species with biparental care, where the mates have equal reproductive rates; both males and females compete intrasexually for mates. Despite this, monogamous species have masculine and feminine roles, typically manifested as the male dominating the female. Some monogamous species are nevertheless sex-role reversed. The pervasive behavioral mechanism characterizing the masculine role is dominance through aggression, size, or both. Attending more to behavioral mechanisms will enrich our understanding of sex-role reversal.     

Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host

Sex-role-reversed mating systems in which females compete for males and males may be choosy are usually associated with males investing more than females in offspring. We report that sex-role reversal may also be caused by selfish genetic elements which distort the sex ratio towards females. Some populations of the butterflies Acraea encedon and Acraea encedana are extremely female biased because over 90% of females are infected with a Wolbachia bacterium that is maternally inherited and kills male embryos. Many females in these populations are virgins suggesting that their reproductive success may be limited by access to males. These females form lekking swarms at landmarks in which females exhibit behaviours which we interpret as functioning to solicit matings from males. The hypothesis that female A. encedon swarm in order to mate is supported by the finding that, in release recapture experiments, mated females tend to leave the swarm while unmated females remained. This behaviour is a sex-role-reversed form of a common mating system in insects in which males form lekking swarms at landmarks and compete for females. Female lekking swarms are absent from less female-biased populations and here the butterflies are instead associated with resources in the form of the larval food plant.     

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

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

Mating system in the tarantula spider Eupalaestrus weijenberghi (Thorell, 1894): evidences of monandry and polygyny

The road tarantula Eupalaestrus weijenberghi shows a strongly female-biased sex ratio since adult females live several years while adult males live only for 2 months. In this scenario selective males could be expected. However, several factors such as the rates of reproduction of each sex, degree of sexual selectivity and synchronicity of female receptiveness determine the operational sexual ratio and mating system of the species. Our objective was to determine the mating rates and mating tactics for females and males of E. weijenberghi and their variation throughout the reproductive period. Four hundred sexual encounters among 20 females and 20 males in all possible pair-wise combinations were carried out during 29 days, a brief but intense experimental period, as it also occurs in the field. Mating success differed strongly between sexes. Females mated once: five females mated at the first attempt, eight initially rejected males and copulated in subsequent attempts. Half of the males did not copulate and the others copulated 1-3 times. Mated females actively rejected males. Results indicate a mating system with monogamous females and polygamous males. Not all the females were receptive in every reproductive season. We suggest that female monogamy drastically affects the operational sex ratio, since several females were unreceptive after a single copulation, directly diminishing the male potential reproductive rate. This is the first experimental approach to estimate tarantula mating systems, their determinants and the consequences of the strategies shown by each sex.     

Operational sex ratio in terrestrial isopods: interaction between potential rate of reproduction and Wolbachia-induced sex ratio distortion

Selfish genetic elements distorting sex ratio are known in several arthropods. By inducing a deficit of males, these sex ratio distorters may modify sexual selection by reversing the sex that competes for a mate. They also have potential to reduce the male proportion to values limiting mating possibilities and therefore limiting population size. Wolbachia endosymbionts are intracytoplasmic, vertically transmitted bacteria that convert genotypic males of terrestrial isopods (woodlice) into functional females. We have tested the impact of these feminizing symbionts on the operational sex ratio (OSR) in three woodlice species. Preliminary experiments consisted in estimating the potential rate of reproduction in males and females, and measuring the dynamics of the onset of reproduction in the wild. These parameters were then combined with population sex ratio to discriminate key factors influencing the OSR. The results suggest that the high potential rate of reproduction of males and the asynchrony in female receptivity both counterbalance female-biased sex ratios. The result is an overall balanced or slightly female-biased OSR. Male deficit can therefore not be considered as a factor strongly limiting reproduction in woodlice. Some females were nevertheless found not mated in the wild at the beginning of the reproductive season, most of them being infected by Wolbachia . This suggests that uninfected females may have an advantage as the first mate. Consequences of these findings on woodlice population dynamics are discussed.     

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

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

Decoupling of reproductive rates and parental expenditure in a polyandrous butterfly

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

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

Operational sex ratio (OSR), the ratio of sexually active males to fertilizable females in a population, plays a central role in the theory of mating systems by predicting that the intensity of male–male competition and the degree of sexual selection increases as the OSR becomes increasingly male biased. At high values of OSR, however, resource defence theory predicts the breakdown of territoriality and a shift towards scramble competition with a decrease in sexual selection. The direction that correlations between OSR and resource competition and variance in mating success will take depends on the biology of the species of interest. We investigated the effects of male population density and male‐biased operational sex ratio on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus . This species spawns inside living unioneid mussels. Large males defended territories, were aggressive towards conspecifics under equal sex ratios and monopolized pair spawnings with females. The mating tactic, however, changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. This change in male behaviour from pair to group spawning has two ramifications for sexual selection. The intensity of sexual selection and variance in male mating success decrease, and the form of sexual competition changes from resource‐ to sperm competition. Thus, the use of alternative mating tactics renders the OSR unable to predict the direction of resource competition and variance in male mating success at high densities.     

Parental investment, sexual selection and sex ratios

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

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.     

Simultaneous polygyny of the gobiid fish Asterropteryx semipunctata in relation to mate availability

Nesting males of Asterropteryx semipunctata conducted spawning behavior with 2–6 females simultaneously. We carried out field observations on a rocky reef in Kagoshima, Japan, to examine the hypotheses that large males will show multi-female spawning behavior because of their mating advantage, and that simultaneous multi-female spawning will occur when the operational sex ratio (OSR; the ratio of receptive males to receptive females) becomes female-biased. Contrary to our prediction, neither the total number of multi-female spawnings during a spawning season nor mean number of spawning females at a time were correlated with nesting male sizes. This indicates that larger males often did not conduct multi-female spawnings. As predicted, the incidence of multi-female spawning followed the change in the OSR over time—as the OSR in the study area became biased toward females, the incidence of multi-female spawnings gradually increased. Our results suggest that mate availability affects mating patterns in A. semipunctata.     

Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

Sexually selected females in the monogamous Western Australian seahorse

Studies of sexual selection in monogamous species have hitherto focused on sexual selection among males. Here, we provide empirical documentation that sexual selection can also act strongly on females in a natural population with a monogamous mating system. In our field-based genetic study of the monogamous Western Australian seahorse, Hippocampus subelongatus, sexual selection differentials and gradients show that females are under stronger sexual selection than males: mated females are larger than unmated ones, whereas mated and unmated males do not differ in size. In addition, the opportunity for sexual selection (variance in mating success divided by its mean squared) for females is almost three times that for males. These results, which seem to be generated by a combination of a male preference for larger females and a female-biased adult sex ratio, indicate that substantial sexual selection on females is a potentially important but under-appreciated evolutionary phenomenon in monogamous species.     

Harvesting of males delays female breeding in a socially monogamous mammal; the beaver

Human exploitation may skew adult sex ratios in vertebrate populations to the extent that males become limiting for normal reproduction. In polygynous ungulates, females delay breeding in heavily harvested populations, but effects are often fairly small. We would expect a stronger effect of male harvesting in species with a monogamous mating system, but no such study has been performed. We analysed the effect of harvesting males on the timing of reproduction in the obligate monogamous beaver (Castor fiber). We found a negative impact of harvesting of adult males on the timing of parturition in female beavers. The proportion of normal breeders sank from over 80%, when no males had been shot in the territories of pregnant females, to under 20%, when three males had been shot. Harvesting of males in monogamous mammals can apparently affect their normal reproductive cycle.     

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

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