Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Sex investment ratios in eusocial Hymenoptera support inclusive fitness theory

Inclusive fitness theory predicts that sex investment ratios in eusocial Hymenoptera are a function of the relatedness asymmetry (relative relatedness to females and males) of the individuals controlling sex allocation. In monogynous ants (with one queen per colony), assuming worker control, the theory therefore predicts female‐biased sex investment ratios, as found in natural populations. Recently, E.O. Wilson and M.A. Nowak criticized this explanation and presented an alternative hypothesis. The Wilson–Nowak sex ratio hypothesis proposes that, in monogynous ants, there is selection for a 1 : 1 numerical sex ratio to avoid males remaining unmated, which, given queens exceed males in size, results in a female‐biased sex investment ratio. The hypothesis also asserts that, contrary to inclusive fitness theory, queens not workers control sex allocation and queen–worker conflict over sex allocation is absent. Here, I argue that the Wilson–Nowak sex ratio hypothesis is flawed because it contradicts Fisher's sex ratio theory, which shows that selection on sex ratio does not maximize the number of mated offspring and that the sex ratio proposed by the hypothesis is not an equilibrium for the queen. In addition, the hypothesis is not supported by empirical evidence, as it fails to explain ‘split’ (bimodal) sex ratios or data showing queen and worker control and ongoing queen–worker conflict. By contrast, these phenomena match predictions of inclusive fitness theory. Hence, the Wilson–Nowak sex ratio hypothesis fails both as an alternative hypothesis for sex investment ratios in eusocial Hymenoptera and as a critique of inclusive fitness theory.     

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.     

To mate or not to mate,and subsequent host search by a haplodiploid female parasitoid wasp

Mated females of haplodiploid species can vary the sex ratio of their offspring, but virgin or sperm‐depleted females can produce only males. Depending on the costs and benefits, the theory of constrained sex allocation states that female haplodiploids may vary in their propensity to mate, with important implications for the populations’ sex ratio. Unmated female parasitoid wasps Alabagrus texanus (Braconidae) have been observed to reject matings with males, even under highly confined spatial conditions. We performed field trials to determine whether unmated female A. texanus would mate. We then compared the preferences of the resulting unmated (constrained) and mated (unconstrained) female wasps for shelters constructed and occupied by their hosts, fern moth caterpillars Herpetogramma theseusalis (Crambidae) on fern fronds. We presented the wasps with pairs of shelters collected from the field that differed in size, as well as freshness, fern species, and presence or absence of caterpillars. Unconstrained females searched small shelters more frequently than did constrained females and tended to favor senesced (old) shelters over fresher ones. They did not differ in choice between shelters on marsh and sensitive ferns or between shelters containing caterpillars and empty shelters. The preference for small shelters by the unconstrained wasps may enhance their rate of contacting favorable hosts, but the foraging regime of the constrained females should expose them to caterpillars at sites infrequently searched by the unconstrained females.     

Evolution of pseudo-arrhenotoky

In arrhenotokous arthropods, males arise from unfertilized eggs. Hence, by controlling the fertilization process mothers can adjust the sex ratio in their offspring. In pseudo-arrhenotokous phytoseiid mites, however, males are haploid, but arise from fertilized eggs. The haploid state is achieved through elimination of the paternal chromosome set during embryonic development. It is shown in this paper that phytoseiid females can control the sex ratio in their offspring and that this control seems as flexible as in arrhenotokous arthropods. As predicted by current evolutionary theory of sex allocation, sex ratios approached half males/half females under random mating, whereas a female bias was observed under sib-mating. The importance of these results for understanding the adaptive significance of pseudo-arrhenotoky is discussed. It is suggested that arrhenotoky is selected for when there is a substantial risk to the females of remaining unmated. When this risk of becoming a wall-flower is low, pseudo-arrhenotoky may evolve because it retains the possibility to reinstal lost genetic information in the maternally derived chromosome by using the paternal chromosome as a template for DNA-repair. The retention of the diploid state in males during embryonic development may thus have certain advantages. It is argued that pseudo-arrhenotoky may be an adaptive genetic system under certain conditions, and not an unstable system that readily reverts to diploidy or evolves towards arrhenotoky or thelytoky.     

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.     

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.     

Sex allocation in black-capped chickadees Poecile atricapilla

Optimal sex allocation for individuals can be predicted from a number of different hypotheses. Fisherian models of sex allocation predict equal investment in males and females up to the end of parental care and predict brood compositions based on the relative costs of producing males and females. The Trivers-Willard hypothesis predicts that individual females should alter the sex ratio of their broods based on their own condition if it has a differential impact on the lifetime reproductive success of their sons and daughters. The Charnov model of sex allocation predicts that females should alter sex allocation based on paternal attributes that may differentially benefit sons versus daughters. Because females are the heterogametic sex in birds, many recent studies have focussed on primary sex ratio biases. In black-capped chickadees Poecile atricapilla , males are larger than females suggesting they may be more costly to raise than females. Female condition affects competitive ability in contests for mates, and thus may be related to variance in fecundity. Females prefer high-ranking males as both social and extrapair partners. These observations suggest that females might vary the sex ratio of their broods based on the predictions of any of the above models. Here, we report on the results of PCR based sex determination of 1093 nestlings in 175 broods sampled from 1992 to 2001. Population-wide, we found a mean brood sex ratio of 0.525±0.016, with no significant deviation from a predicted binomial distribution. We found no effect of clutch size, female condition, hatch date, parental rank or paternity. Our results reject the idea that female black-capped chickadees systematically vary sex allocation in their broods.     

Constrained oviposition and female-biased sex allocation in a parasitic wasp

 In haplodiploid organisms such as parasitic wasps, substantial oviposition by females without sperm is predicted to cause mated females to bias their offspring sex ratios towards daughters. The effect of the production of sons by unmated and sperm-depleted (constrained) females on sex allocation by mated females was studied in two populations of the parasitic wasp Bracon hebetor over 3 years. B. hebetor females who depleted their sperm reserves from prior matings rarely remated and became constrained to produce only sons. Constrained females readily oviposited and produced clutches similar in size to those produced by mated females. Although the fraction of constrained females in the population varied considerably between sites and sampling dates, it was usually high enough to favor the production of female-biased sex ratios by mated females. Mated females consistently produced female-biased sex ratios. However, we found no evidence that the sex ratios produced by mated females from the field shifted in relation to the proportion of constrained females in the population. Females held with males or held in isolation also produced female-biased sex ratios. These findings suggest that, in B. hebetor, mated females produce sex ratios that reflect the average fraction of constrained females over evolutionary time. Received: 21 June 1996 / Accepted: 27 August 1996     

繁殖盛期雄性普通东方小蛙的个体大小不影响交配成功率

通过比较抱对和非抱对普通东方小蛙(Crinia signifera) 的吻尾干骨长(体长) 和检测个体较大或状态较好的雄体是否为成功繁殖个体, 检测雌蛙体长与交配成功的雄蛙的体长和相对状态(体重/体长) 之间是否存在线形关系, 评估交配与个体大小之间的关系。在实验室内, 令未交配雌体选择随机选出的雄体, 观测雌体是否与最大的雄体交配; 将抱对的蛙暴露于其它雄蛙, 观测其它较大或较小的雄蛙是否取代已抱对的雄蛙。结果表明: 抱对雄蛙和雌蛙的个体大小无显著的关系, 成功交配的雄蛙并不比未交配的雄蛙大, 其它雄蛙不能取代已抱对的雄蛙。在这一C. signifera种群中, 繁殖盛期雄性个体的大小似乎不影响交配成功率, 在此期间即便存在配偶选择, 亦决定于与雄性个体大小无关的其它因素。在更长的繁殖期内, 雄性个体大小则与交配成功率有关, 这是该种的典型特征。     

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 infanticide by adult male barn swallows

Since 1980, we have documented three definite and five suspected instances of sexually selected infanticide by unmated males in the monogamous barn swallow, Hirundo rustica. This is the first report of this type of infanticide by males in any bird species, or by either sex in any monogamous species. In our population, infanticide appears to be an adaptation serving two functions. It speeds the reproductive cycle of victimized females so that males can breed with them sooner than if they had been permitted to raise their young. In addition, it may enable unmated males to acquire females by causing them to desert their mates.     

Evolutionarily stable oviposition and sex ratio in parasitoid wasps with single‐sex broods

Abstract 1. The flexibility of hymenopteran sex ratios is well documented, particularly in structured populations featuring sib mating. 2. Using game theoretic models, the present study examines species producing single‐sex broods in which sib mating is unlikely, and focuses on the role of population density in determining evolutionarily stable oviposition strategies. 3. Since only mated females can produce offspring of both sexes while unmated females produce only male offspring, mated females are under selection to produce more females overall to balance the primary sex ratio. 4. As the proportion of all females that are mated should increase with density, offspring sex ratio of mated females is strongly linked to density at low to moderate densities. The present study shows that when density becomes low enough for fewer than half of all females to have mated, then female offspring generate higher fitness. 5. In this low density situation, females may gain a fitness benefit from waiting at their emergence site or from using other costly means to find and mate with males before ovipositing. 6. The predicted correspondence between females waiting at the emergence site and fewer than half of females in the population containing sperm, can be tested empirically, as can the somewhat counter‐intuitive prediction that greater access to males should yield a more male‐biased sex ratio in the offspring of mated females. 7. The present study also indicates how measuring the variance in giving up times by females waiting for males at low density, can provide insight into mechanisms determining waiting times.     

Bumblebee sex ratios: why do bumblebees produce so many males?

Sex investment ratios in populations of bumblebees are male biased, which contradicts theoretical predictions. Male-biased investment ratios in eusocial Hymenoptera are assumed to be non-stable for both the queen and her workers. In this paper, we show that male-biased sex allocation does not necessarily decrease fitness in the bumblebee Bombus terrestris. A male-biased investment ratio can be the result of an optimal allocation of resources when resources are scarce if (i) there is a large cost difference between male and female production, (ii) there is uncertainty about the amount of resources a colony can invest, and (iii) only a proportion of the investment made in an individual can be reused. This resource allocation then leads to split sex ratios depending on the amount of resources available to a bumblebee colony: colonies under low resource conditions will show a male-biased investment ratio, whereas colonies under high resource conditions allocate more resources towards females. However, the extent to which bumblebee populations show a male-biased sex allocation cannot be explained by cost differences between male and female production alone. In a recent paper, A. F. G. Bourke argued that male-biased investment ratios in bumblebee populations are a by-product of the occurrence of protandry (males emerge before females). Here we will extend Bourke''s argument and show that within a protandrous population, both protandrous and protogynous (females emerge before males) colonies exist. The existence of protandrous and protogynous colonies results in split sex ratios in time, because protogynous colonies rely on males produced by protandrous colonies (partial protandry).     

Sex-ratio bias and clonal reproduction in the brittle star Ophiactis savignyi

Although the sex ratios of many groups conform to Fisher's (1930) prediction that parents should invest equally in daughters and sons, a number of taxa are characterized by excesses of one gender. A variety of mechanisms may lead to sex ratio biases, but in organisms that reproduce clonally as well as sexually, gender differences in the rate of cloning could drive the development of sex-ratio biases. In this study, I demonstrate that males of the clonal brittle star Ophiactis savignyi were significantly more likely to divide than females and that the magnitude of this difference was sufficient to explain the consistent and significant excess of males in natural populations. Females were significantly more likely to lose sexual reproductive capabilities following division, and this greater cost associated with division may explain why females are less likely to divide. Gender differences in mortality rates are unlikely to explain the excess of males in this species. Because of their potential influence on the operational sex ratio, gender differences in division rates may have important ecological and evolutionary implications including effects on the direction and strength of selection.     

Neither Biased Sex Ratio nor Spatial Segregation of the Sexes in the Subtropical Dioecious Tree Eurycorymbus cavaleriei (Sapindaceae)

Knowledge of sex ratio and spatial distribution of males and females of dioecious species is both of evolutionary interest and of crucial importance for biological conservation. Eurycorymbus cavaleriei, the only species in the genus Eurycorymbus (Saplndaceae), is a dioecious tree endemic to subtropical montane forest in South China. Sex ratios were investigated in 15 natural populations for the two defined ages (young and old). Spatial distribution of males and females was further studied in six large populations occurring in different habitats (fragmented and continuous). The study revealed a slight trend of malebiased sex ratio in both ages of E. cavaleriei, but sex ratio of most populations (13 out of 15) did not display statistically significant deviation from equality. All of the four significantly male-biased populations in the young class shifted to equality or even female-biased. The Ripley's K analysis of the distribution of males with respect to females suggested that individuals of the opposite sexes were more randomly distributed rather than spatially structured. These results suggest that the male-biased sex ratio in E. cavaleriei may result from the precocity of males and habitat heterogeneity. The sex ratio and the sex spatial distribution pattern are unlikely to constitute a serious threat to the survival of the species.     

Size‐selective fishing affects sex ratios and the opportunity for sexual selection in Alaskan sockeye salmon Oncorhynchus nerka

Selective exploitation can cause adverse ecological and evolutionary changes in wild populations and also affect sex ratios but few studies have empirically documented skewed sex ratios in exploited fishes (other than species with extreme sexual size dimorphism, SSD). To investigate the possibility of sex‐selective fishing on Alaskan sockeye salmon Oncorhynchus nerka, we assessed sex ratios in fish at two spatial scales: within each of five fishing districts and among 13 breeding populations in one of these districts. We predicted that populations’ sex ratios would vary based on the average size of fish and SSD because size affects vulnerability to fishing. At the larger scale, we found a small but significant bias in fish returning to four of the five fishing districts (average = 52% females), and in four of the five districts males were caught at significantly higher rates than females. At the finer scale there was marked variation in sex ratio on the breeding grounds, ranging from 36% to 47% males. Populations with fish of intermediate sizes experienced the greatest sex ratio biases; the greater vulnerability of males than females to fishing resulted from a combination of larger SSD and different harvest rates between the sexes associated with the fishery size‐selectivity curve shape. Skewed sex ratios may change competition and behavior on the breeding grounds, relaxing selection on male traits associated with mate choice by females or intra‐sexual competition and altering demographic and evolutionary pressures on the fish. Assessment of the size selectivity of fishing gear and the population's SSD can help to illuminate if and how exploitation can affect sex ratios. Future studies examining size‐selective fishing should also evaluate the consequences for sex ratios, as this might help explain changes in harvested population structure and sustainability.     

Sex ratio bias in the dung beetle <Emphasis Type="Italic">Onthophagus taurus</Emphasis>: adaptive allocation or sex-specific offspring mortality?

Sex allocation theory predicts that females should adjust the sex of their offspring when the fitness returns of one sex are higher than the other. However, biased sex ratios may also arise if mortality differs between the sexes. Here, we examine whether offspring sex ratio bias in the dung beetle, Onthophagus taurus, represents adaptive sex allocation by females or is due to sex-specific mortality. First, we re-analyze an existing data set to show that females produce an excess of daughters when mating to smaller, less attractive males and near equal sex ratio with large, more attractive males. We show, that this results from females adjusting larval provisions after mating to males of variable attractiveness which in turn influences the likelihood that sons die during development. Second, we conduct a manipulative experiment varying the quantity and quality of larval provisions and show that the mortality of sons increased when larval provisions were reduced. Collectively, our work demonstrates that offspring mortality is contingent on the amount of resources provisioned by females and that sons have greater nutritional demands than daughters during development, leading to higher mortality. Our results therefore demonstrate the importance of considering sex-specific offspring mortality in studies of sex ratio evolution.     

Mating system of Bracon hebetor (Hymenoptera: Braconidae)

Abstract.

• 1 We report on the mating system of a field population of the parasitic wasp, Bracon hebetor, on a corn pile infested by the Indian meal moth, Plodia interpunctella. We demonstrate that the mating system is based upon male scramble competition polygyny with male aggregations on high places on the corn.
• 2 The sex ratio among adults was greater than 80% males on the surface of the corn, whereas below the surface the sex ratio was less than 45%. Males actively courted females on the surface, but there were no aggressive interactions among males during courtship or mating.
• 3 Approximately 20% of the females found on the surface of the corn had no sperm in their spermathecae, regardless of age, but the numbers of unmated females decreased later during the day.
• 4 In laboratory studies we showed that females from this population oviposit a female biassed sex ratio, and that only 14% of females were mated before dispersing from their place of emergence.
• 5 Thus sib-mating is unlikely in this gregarious parasitoid. This outcrossing mating system probably arose because of severe inbreeding depression that B.hebetor suffers via a sex locus: diploids that are heterozygous at the sex locus develop into females, but homozygous diploids are male and are generally inviable. The female biassed sex ratio may have evolved in B. hebetor in response to males being the more expensive sex, females dispersing more frequently from the population than males, or a fraction of females remaining unmated in the population.

     

Sex ratio from germination through maturity and its reproductive consequences in the liverwort Sphaerocarpos texanus

Summary The dioecious winter ephemeral liverwort, Sphaerocarpos texanus disperses spore tetrads consisting of two males and two females. I examined the subsequent sex ratio of S. texanus at different stages in its life cycle to detect possible mechanisms affecting deviations from a 1:1 sex ratio and the effect of sex ratio on reproductive success. As S. texanus occurs in pure male, pure female and mixed sex clumps, I examined the proportions and sizes of these, the reproductive success of pure female and mixed sex clumps in the field and the sex ratio of germinating plants in a growth chamber. In both the field and the growth chamber the most abundant clump type was pure female followed by mixed sex and pure male clumps. These abundance patterns suggest that males have a lower survival rate than females before emergence and this lower survival rate continues through the gametophytic stage. This disadvantage may be due to the higher susceptibility of males to environmental conditions, to their competitive inferiority to females, and/or to differential resource allocation to the sexes within the spore tetrad. The female biased sex ratio at germination is consistent with predictions from sex ratio theory. Further my field data indicate that males may gain a survival benefit from growing in a mixed sex clump and both males and females benefit reproductively when they occur in mixed sex clumps.