Mating system and sex allocation in the gregarious parasitoid Cotesia glomerata

The gregarious parasitoid Cotesia glomerata (L.) is often presumed to possess the characteristic attributes of a species that manifests local mate competition (LMC), as it commonly produces female-biased broods. However, our field surveys of sex ratio and laboratory observations of adult behaviour showed that this species is subject to partial local mate competition caused by natal dispersal. On average, 30% of males left their natal patch before mating, with the proportion of dispersing males increasing with an increase in the patch's sex ratio (i.e. proportion of males). Over 50% of females left their natal patch before mating, and only 27.5% of females mated with males emerging from the same natal patch. Although females showed no preference between males that were and were not their siblings, broods from females that mated with siblings had a significantly higher mean brood sex ratio (0.56) than broods from females that mated with nonsiblings (0.39). Furthermore, brood sex ratios increased as inbreeding was intensified over four generations. A field population of this wasp had a mean brood sex ratio of 0.35 over 3 years, which conformed well to the evolutionarily stable strategy sex ratio (r=0.34) predicted by Taylor's partial sibmating model for haplodiploid species. These results suggest that the sex allocation strategy of C. glomerata is based on both partial local mate competition in males and inbreeding avoidance in females. In turn, this mating system plays a role in the evolution of natal dispersal behaviour in this species.Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Mating Strategies in Solitary Aphid Parasitoids: Effect of Patch Residence Time and Ant Attendance

Mate finding and dispersal from the natal patch in parasitoid Hymenoptera are influenced by the availability of host resources and interactions with other organisms. We compared the mating behavior of three solitary aphid parasitoids, Aphidius ervi Haliday, Lysiphlebus hirticornis Mackauer and Pauesia pini (Haliday) (Hymenoptera: Braconidae: Aphidiinae) that differ in host resource exploitation and ant mutualism. In L. hirticornis, which is obligately ant-attended, the residence time on the natal patch was approximately 4 h compared with less than 2 h in the facultatively ant-attended P. pini; the sexes did not differ in residence time. Females of A. ervi, which is not attended by ants, stayed for slightly more than 2 h on the natal patch while their male siblings remained for only 1 h. In L. hirticornis, 90% of all siblings in a clutch mated on the natal patch but only 13% in A. ervi and 42% in P. pini did so. Off-patch matings (23%) were observed only in A. ervi. Males and females of L. hirticornis were 12-times more likely to mate on the natal patch when aphids and ants were present than when either of the latter species was removed; and patch residence time declined from approximately 4 h to approximately 2.5 h in the absence of either aphids or ants. We propose that, in aphidiine wasps and perhaps other quasigregarious parasitoids, mating behavior is influenced by the availability of resources on the natal patch and the presence or absence of trophobiotic ants. Partial sib mating is expected in species producing large clutches and having a long patch residence time.     

Partial local mate competition in the wasp Trichogramma euproctidis: the role of emergence sex ratio on female mating behaviour

1. Parasitic wasps with structured populations are generally assumed to follow the local mate competition (LMC) model: females lay only the minimal number of sons necessary to inseminate all daughters in the emergence patch, and increase this number when faced with additional broods from unrelated females. After emergence, daughters mate with local males before dispersing for host location and oviposition. The main predictions from the model have been verified for many species. 2. Conflicting evidence exists on the status of the egg parasitoids Trichogramma regarding their on‐patch versus off‐patch mating. Although the life‐history traits of several species indicate that mating must occur on the emergence patch, recent data suggest that mating could occur outside the natal patch. 3. In this study, we measured the level of off‐patch mating in the egg parasitoid Trichogramma euproctidis using two isofemale lines in a greenhouse experiment. The impact of the sex ratio on the level of off‐patch mating was also tested. 4. The overall off‐patch mating proportion was 40.5% with a range between 0 and 85.7%, and was influenced by the sex ratio on the emergence patch: the more males available at emergence, the less off‐patch mating occurring. 5. The mating structure of this species can be described as partial LMC.     

Evidence for Strategic Sex Allocation in the Guppy (Poecilia reticulata): Brood Sex Ratio and Size Predict Subsequent Adult Male Mating Success

Sex allocation theory predicts that females should produce more sons when the reproductive success of sons is expected to be high, whereas they should produce more daughters, not daughters when the reproductive success of sons is expected to be low. The guppy (Poecilia reticulata) is a live‐bearing fish, and female guppies are known to produce broods with biased sex ratios. In this study, we examined the relationship between brood sex ratio and reproductive success of sons and daughters, to determine whether female guppies benefit from producing broods with biased sex ratios. We found that sons in male‐biased broods had greater mating success at maturity than sons in female‐biased broods when brood sizes were larger. On the other hand, the reproductive output of daughters was not significantly affected by brood sizes and sex ratios. Our results suggest that female guppies benefit from producing large, male‐biased brood when the reproductive success of sons is expected to be high.     

Offspring sex ratio produced by female guppies in the wild correlates with sexual ornaments of their sons

The attractiveness hypothesis predicts that females produce broods with male-biased sex ratios when they mate with attractive males. This hypothesis presumes that sons in broods with male-biased sex ratios sired by attractive males have high reproductive success, whereas the reproductive success of daughters is relatively constant, regardless of the attractiveness of their sires. However, there is little direct evidence for this assumption. We have examined the relationships between offspring sex ratios and (1) sexual ornamentation of sons and (2) body size of daughters in broods from wild female guppies Poecilia reticulata. Wild pregnant females were collected and allowed to give birth in the laboratory. Body size and sexual ornamentation of offspring were measured at maturity. Our analysis revealed a significant positive correlation between offspring sex ratios (the proportion of sons per brood) and the total length as well as the area of orange spots of sons, two attributes that influence female mating preferences in guppies. The sex ratio was not associated with the body size of daughters. These results suggest that by performing adaptive sex allocation according to the expected reproductive success of sons and daughters, female guppies can enhance the overall fitness of their offspring.     

Local Mating,Dispersal and Sex Ratio in a Gregarious Parasitoid Wasp

Parasitoid sex ratios can be greatly influenced by mating and dispersal behaviour. Many sex ratio models assume that mating is strictly local (only mated females disperse from the natal patch) and that a single male is sufficient to inseminate all females in a brood. Bethylids (aculeate parasitoids) have been used to test predictions of these models, but less attention has been paid to testing their underlying assumptions. We investigated the timing of eclosion, mating and dispersal in mixed-sex and single-sex broods of the bethylid wasp Goniozus nephantidis. In mixed-sex broods, almost all females mate before dispersal and a single male is sufficient to inseminate virtually all females, even when brood sizes are large. Males disperse from both mixed-sex and all-male broods, but males in all-male broods disperse more slowly. Virgin females disperse from all-female broods, which are common. Virgin females can produce a brood, mate with their own sons and subsequently produce mixed-sex broods, but their success rate is very low. Virgin females could potentially circumvent sex allocation constraints by superparasitizing mixed-sex broods, but when presented with hosts bearing mixed-sex broods they destroy all members of the initial brood before ovipositing. Because of the high prevalence of single-sex broods and dispersal of both sexes, the mating structure of G. nephantidis is unlikely to conform to the assumption of strict local mating.     

Hatching sex ratio and sex specific chick mortality in common terns Sterna hirundo

Bias in sex ratios at hatching and sex specific post hatching mortality in size dimorphic species has been frequently detected, and is usually skewed towards the production and survival of the smaller sex. Since common terns Sterna hirundo show a limited sexual size dimorphism, with males being only about 1–6% larger than females in a few measurements, we would expect to find small or no differences in production and survival of sons and daughters. To test this prediction, we carried out a 2-year observational study on sex ratio variation in common terns at hatching and on sex specific post hatching mortality. Sons and daughters hatched from eggs of similar volume. Post hatching mortality was heavily influenced by hatching sequence. In addition, we detected a sex specific mortality bias towards sons. Overall, hatching sex ratio and sex specific mortality resulted in fledging sex ratios 8% biased towards females. Thus, other reasons than body size may be influencing the costs of rearing sons. Son mortality was not homogeneous between brood sizes, but greater for two-chick broods. Since adults rearing two-chick broods were younger, lighter and bred consistently later than those rearing three-chick broods, it is suggested that lower capacity of two-chick brood parents adversely affected offspring survival of sons. Though not significantly, two-chick broods tended to be female biased at hatching, perhaps to counteract the greater male-biased nestling mortality. Thus, population bias in secondary sex ratio is not limited to strongly size dimorphic species, but species with a slight sexual size dimorphism can also show sex ratio bias through a combination of differential production and mortality of sons and daughters.     

Pair bond duration influences paternal provisioning and the primary sex ratio of brown thornbill broods

Parents should vary their level of investment in sons and daughters in response to the fitness costs and benefits accrued through male and female offspring. I investigated brood sex ratio biases and parental provisioning behaviour in the brown thornbill, Acanthiza pusilla, a sexually dimorphic Australian passserine. Parents delivered more food to male-biased than female-biased broods. However, factors determining parental provisioning rates differed between the sexes. Female provisioning rates were related to brood sex ratio in both natural and experimental broods with manipulated sex ratios. In contrast, male provisioning rates were not affected by brood sex ratio in either natural or experimental broods. However, males in established pairs provisioned at a higher rate than males in new pairs. Data on the sex ratio of 109 broods suggest that female brown thornbills adjust their primary sex ratio in response to pair bond duration. Females in new pairs produced broods with significantly fewer sons than females in established pairs. This pattern would be beneficial to females if the costs of rearing sons were higher for females in new than established pairs. This may be the case since females in new pairs provisioned experimental all-male broods at elevated rates. The condition of nestlings also tended to decline more in these all-male broods than in other experimental broods. This will have additional fitness consequences because nestling mass influences recruitment in thornbills. Female thornbills may therefore obtain significant fitness benefits from adjusting their brood sex ratio in response to the status of their pair bond. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Sex ratio variation among broods of great reed warblers Acrocephalus arundinaceus

The sex of 746 great reed warbler fledglings (from 175 broods) was determined by the use of single primer polymerase chain reaction. The reliability of the technique was confirmed as 104 of the fledglings were subsequently recorded as adults of known sex. The overall sex ratio did not differ from unity. Variation in sex ratios between broods was larger than expected from a binomial distribution. Female identity explained some of the variation of brood sex ratio indicating that certain females consistently produced sex ratios that departed from the average value in the population. The theory of sex allocation predicts that parents should adjust the sex ratio of their brood to the relative value of sons and daughters and this may vary in relation to the quality of the parents or to the time of breeding. In the great reed warbler, the proportion of sons was not related to time of breeding, or to any of five female variables. Of five male variables, males with early arrival date tended to produce more daughters. The sex ratio of fledglings that were a result of extra-pair fertilizations did not differ from that of legitimate fledglings. Hence, there is currently no evidence of that female great reed warblers invest in a higher proportion of sons when mated with attractive males.     

Maternal influences on brood sex ratios: an experimental study in tree swallows

When the reproductive value of sons and daughters differ, parents are expected to adjust the sex ratio of their offspring to produce more of the sex that provides greater fitness returns. The body condition of females or environmental factors, such as food abundance and mate quality, may influence these expected fitness returns. In a previous study of tree swallows (Tachycineta bicolor), we found that females produced more sons in their broods when they were in better body condition (mass corrected for size). We tested this relationship by experimentally clipping some flight feathers to reduce female body condition. As predicted, we found that females with clipped feathers had a lower proportion of sons in their broods and poorer body condition. However, female body condition alone was not a significant predictor of brood sex ratio in our experiment. We suggest that brood sex ratio is causally related to some other factor that covaries with body condition, most likely the foraging ability of females. The hypothesis that brood sex ratios are influenced by individual differences in female foraging ability is supported by a high repeatability of brood sex ratio for individual females. Thus, maternal effects may have a strong influence on the sex ratios of offspring.     

Factors influencing brood sex ratios in polyembryonic Hymenoptera

Copidosoma sp. is a polyembryonic encyrtid wasp which parasitizes isolated hosts. Most broods of this wasp are unisexual, but some contain both sexes and the secondary sex ratio of these is usually highly female biased. The overall population secondary sex ratio is female biased. Walter and Clarke (1992) argue that because the majority of individuals must mate outside the natal patch, the bias in the population secondary sex ratio contradicts predictions made by Hamilton's (1967) theory of local mate competition (LMC). We suggest that the primary sex ratio is unbiased and that Walter and Clarke's results do not cast doubt on LMC. Instead these results imply that ovipositing females make a combined clutch size and sex ratio decision influencing whether individuals developing from a particular brood will outbreed or largely inbreed; for each case the predictions of LMC theory are not violated. If this interpretation is correct, what is of interest is the basis on which this decision is made rather than the population secondary sex ratio. We show that host encounter rate influences the proportions of mixed and single sex broods laid by Copidosoma floridanum, a related polyembryonic parasitoid. Among single-sex broods the primary sex ratio is female biased, but our results are in agreement with LMC theory since offspring developing from these broods will probably mate with siblings from adjacent hosts. We consider the egg load of females to be of major influence on oviposition behaviour, and that the mating structure of parasitoid offspring, potentially differential costs of male and female broods and the natural distributions of hosts both at oviposition and eclosion, require further study.     

Evolution of sex ratios in social hymenoptera: Consequences of finite brood size

Evolutionarily stable sex ratios are determined for social hymenoptera under local mate competition (LMC) and when the brood size is finite. LMC is modelled by the parameterd. Of the reproductive progeny from a single foundress nest, a fractiond disperses (outbreeding), while (l-d) mate amongst themselves (sibmating). When the brood size is finite,d is taken to be the probability of an offspring dispersing, and similarly,r, the proportion of male offspring, the probability of a haploid egg being laid. Under the joint influence of these two stochastic processes, there is a nonzero probability that some females remain unmated in the nest. As a result, the optimal proportion of males (corresponding to the evolutionarily stable strategy, ESS) is higher than that obtained when the brood size is infinite. When the queen controls the sex ratio, the ESS becomes more female biased under increased inbreeding (lowerd). However, the ESS under worker control shows an unexpected pattern, including anincrease in the proportion ofmales withincreased inbreeding. This effect is traced to the complex interaction between inbreeding and local mate competition.     

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.     

The biology of the primitively eusocial Augochloropsis iris (Schrottky, 1902) (Hymenoptera, Halictidae)

Summary: This work investigated Augochloropsis iris, its annual colony cycle, brood size and survival rate, caste differentiation, and sex ratio, and is the first detailed account of a clearly eusocial species of this genus. The population studied is located in the Campos do Jordão State Park, São Paulo, Brazil. The annual colony cycle extends from August to March and consists of three phases of cell provisioning separated by two phases of inactivity, and followed by an emergence of future queens and males. Provisioning during the first phase is carried primarily out by solitary females. The daughters, after emerging from the cells, remain in the natal nests, carrying out foraging activities, while the mother engages in reproduction. New nests are initiated during each of the provisioning phases by solitary females, principally by females from the second-phase brood which, soon after emerging from the cells, leave their natal nests to found their own nests, which they provision during the third phase. The females resulting from the third-phase brood in general mate and excavate their own nests, in which they diapause, with provisioning delayed until the following August. On average, the queens are significantly larger (5%) than the workers. In general, the workers do not have developed ovaries, but all are mated. Kin selection can be accepted as the selective force responsible for worker behavior of A. iris in eusocial colonies when the queen has mated once and semisocial colonies if the queen mated only once. The percentage of males produced in the first, second and third broods and in the brood of new nests founded by solitary females active in the second and third phases was: 20.7%, 22.2%, 13.3% and 0.0% respectively. The resultant sex ratio of the third brood suggests that the third-phase workers of eusocial nests are at least in partial control of their colony's sex ratios, in cases where the queens mated only once.     

Insemination Capacity and Dispersal in Relation to Sex Allocation Decisions in Goniozus legneri (Hymenoptera: Bethylidae): Why Are There More Males in Larger Broods?

Models considering sex ratio optima under single foundress strict local mate competition predict that female bias will be reduced by stochasticity in sex allocation, developmental mortality of males and limited insemination capacity of males. In all three cases the number of males per brood is expected to increase with brood size. Sex ratio optima may also be less female biased when several mothers contribute offspring to local mating groups or if non‐local mating occurs between members of different broods; again more males are expected in larger broods. In the parasitoid wasp Goniozus legneri (Hymenoptera: Bethylidae), sex allocation has only a small stochastic component, developmental mortality is low and non‐siblings are unlikely to develop in the same brood. However, the number of males per brood increases with the size of the brood (produced by a single mother). We investigated the further possibilities of limited insemination capacity and non‐local mating using a naturalistic experimental protocol. We found that limited insemination capacity is an unlikely general explanation for the increase in number of males with brood size. All males and females dispersed from both mixed and single sex broods. Although most females in mixed sex broods mated prior to dispersal, these data suggest that non‐local mating is possible, for instance via male immigration to broods containing virgin females. This may influence sex ratio optima and account for the trend in male number.     

Seasonal variation in the reproductive strategy of the parasitic wasp Eulophus larvarum (Hymenoptera: Chalcidoidea: Eulophidae)

ABSTRACT. 1. Eulophus larvarum (L.) (Hymenoptera: Eulophidae) is a gregarious parasitoid of lepidopterous larvae feeding on broad-leaved trees. Normally there are two generations a year.
2. Sex ratio in the spring generation of larvae is female biased. The bias is probably due to local mate competition as progeny from one brood emerge from their pupae in close proximity to each other.
3. Sex ratio in the summer generation of larvae is near equality. Local mate competition is absent as individuals from the same brood become separated during the winter.
4. Variation in sex-ratio in the spring generation is consistent with a binomial model. Variation in sex ratio in the summer generation is much greater than expected from a binomial model and there is a large proportion of single-sex broods.
5. Two hypotheses are put forward to explain the summer generation pattern: virgin oviposition, and strong intersexual competition.
6. No differences in clutch size were found between the two generations.     

Combined effects of host quality and local mate competition on sex allocation inLariophagus distinguendus

Summary Many parasitoid wasps are known to adjust sex ratio in response to either local mate competition (LMC) or host quality. Nevertheless, few studies have investigated the combined effects of these two factors on sex allocation. The sex allocation pattern inLariophagus distinguendus, a parasitoid of granary weevil larvae, is contrasted to the expectations of Werren's (1984) model combining LMC and host quality. Several predictions of the model are confirmed, but others are not. Sex ratio on both large and small hosts declines with proportion of small hosts attacked in a manner consistent with the model. However, when only one host size is parasitized, sex ratio is not independent of that host size, as predicted by the model. Various possibilities for the deviation between expected and observed are discussed. A partial LMC/host quality model is developed which allows for some matings outside the natal patch, and predictions of this model conform more closely to the pattern observed inL. distinguendus. Finally, the application of parasitoid studies to basic questions in evolutionary ecology is briefly discussed.     

Spiderling sex ratio and maternal investment in the bolas spider Mastophora cornigera (Araneae,Araneidae)

Male Mastophora cornigera exit egg sacs as adults, which allowed us to determine spiderling sex ratios and patterns of maternal investment in this species. We collected 15 egg sacs produced by seven mothers, which yielded 1945 emergent spiderlings which were sexed, 1850 of which were weighed. Two emergent broods were significantly male and female biased and were unaffected by pre-emergence mortality. The weights of male and female spiderlings differed in eight broods, with males and females being heavier in four cases each. Five of these broods were derived from multiple egg sac sets produced by one mother, and in each case, the total mean male and female spiderling weights for all broods in a set were biased in the same direction as the biased brood(s) within that set. Mean emergent spiderling weight was independent of brood size and sex ratio for both males and females. Despite such independence, sex allocation in M. cornigera can favor sons, daughters, or both equally, and by numbers, by weight, or both at once. The proximate mechanisms and adaptive significance of such variability is unknown. We also review evidence for gender-biased allocations in arachnid offspring and suggested mechanisms for their applicability to M. cornigera.     

A Comparative Study of Sex Ratio and Clutch Size in Gregarious Ichneumonoid Wasps

Some convincing support for sex ratio theory comes from the cross-species relationship between sex ratio and brood size in gregarious bethylid wasps (Hymenoptera: Bethylidae), in which the proportion males declines as brood size increases as predicted under local mate competition. It is unknown how widely such relationships hold within parasitoid wasps as a whole. We assemble a dataset on sex ratio and brood size for gregarious Braconidae and Ichneumonidae. Their sex ratios deviate substantially from those of bethylids; sex ratios differ widely across species; and they are not significantly related to brood size across species. Several factors explain the heterogeneity in sex ratios including across-species differences in mating system, sex determining mechanism, and sexual asymmetries in larval competition and polyembryony leading to single-sexed broods.     

Nestling sex ratio is associated with both male and female attractiveness in rock sparrows

According to theory, in species in which male variance in reproductive success exceeds that of the females, sons are more costly to produce; females mated with high quality males or those in better condition should produce more sons. In monogamous species, however, the variance in the reproductive success of the two sexes is often similar and mate choice is often mutual, making predictions regarding sex allocation more difficult. In the rock sparrow Petronia petronia, both males and females have a sexually selected yellow patch on the breast, whose size correlates with individual body condition. We investigated whether the brood sex ratio co‐varies with the size of the yellow patch of the father and the mother in a sample of 173 broods (818 chicks) over 8 breeding seasons. While the size of the yellow patch of the mother and the father did not predict per se a deviation from the expected 1:1 sex ratio, brood sex ratios were predicted by the interaction of male and female yellow patch size. This result is surprising, as the ornament is sexually selected by both males and females as an indicator of quality in both sexes and should therefore be inherited by all offspring irrespective of their sex. It indirectly suggests that other sex‐specific traits associated with patch size (e.g. polygyny in males and fecundity in females) may explain the sex allocation bias observed in rock sparrows. Thus, female individual quality alone, as expressed through the size of the yellow patch, was not associated with the biases in sex ratios reported in this study. Our results rather suggest that sex allocation occurs in response to male attractiveness in interaction with female attractiveness. In other words, females tend to preferentially allocate towards the sex of the parent with more developed ornament within the pair.