Egg load is a cue for offspring sex ratio adjustment in a fig‐pollinating wasp with male‐eggs‐first sex allocation

Fig‐pollinating wasps (Agaonidae) only reproduce within fig tree inflorescences (figs). Agaonid offspring sex ratios are usually female‐biased and often concur with local mate competition theory (LMC). LMC predicts less female‐bias when several foundresses reproduce in a fig due to reduced relatedness among intra‐sexually competing male offspring. Clutch size, the offspring produced by each foundress, is a strong predictor of agaonid sex ratios and correlates negatively with foundress number. However, clutch size variation can result from several processes including egg load (eggs within a foundress), competition among foundresses and oviposition site limitation, each of which can be used as a sex allocation cue. We introduced into individual Ficus racemosa figs single Ceratosolen fusciceps foundresses and allowed each to oviposit from zero to five hours thus variably reducing their eggs‐loads and then introduced each wasp individually into a second fig. Offspring sex ratio (proportion males) in second figs correlated negatively with clutch size, with males produced even in very small clutches. Ceratosolen fusciceps lay mainly male eggs first and then female eggs. Our results demonstrate that foundresses do not generally lay or attempt to lay a ‘fixed’ number of males, but do ‘reset to zero’ their sex allocation strategy on entering a second fig. With decreasing clutch size, gall failure increased, probably due to reduced pollen. We conclude that C. fusciceps foundresses can use their own egg loads as a cue to facultatively adjust their offspring sex ratios and that foundresses may also produce more ‘insurance’ males when they can predict increasing rates of offspring mortality.     

Putting your eggs in several baskets: oviposition in a wasp that walks between several figs

The interaction between figs (Ficus spp., Moraceae) and their pollinator fig wasps (Hymenoptera: Agaonidae) is an obligate mutualism, but females of dioecious fig trees exploit fig wasps without providing rewards. Figs are closed inflorescences that typically trap pollinator females after entry, but some fig wasp species can re‐emerge (although wingless) and subsequently oviposit in and pollinate further figs. Using glasshouse populations, we examined the sex ratios and clutches laid by single foundresses of Kradibia tentacularis (Grandi) in their first and subsequent male figs of Ficus montana Blume, and how the probability of emergence and entering a second fig varied between seasons. A maximum of four figs were entered by any one foundress. Wingless foundresses were able to locate and enter figs up to 60 cm from the first fig they entered, but the probability of entry declined sharply with distance from that fig. The foundresses that re‐emerged produced slightly higher adult offspring totals than those that failed to re‐emerge. Clutch sizes of a single foundress in its first fig equalled those in all the subsequent figs combined, with clutch size per fig decreasing when more figs were entered. Smaller clutches had less female‐biased sex ratios. Figs were more numerous in summer than in winter, but the proportion of figs entered by only wingless foundresses remained unchanged. Movement between figs increases pollinator reproductive success in male figs, thereby encouraging foundresses that encounter a female tree to also move between and pollinate several female figs.     

Putting your sons in the right place: the spatial distribution of fig wasp offspring inside figs

Abstract. 1. Pollinating fig wasps (Hymenoptera, Agaonidae) display sex ratio adjustment, producing less female‐biased combined sex ratios as the number of ovipositing females (foundresses) inside a fig increases. Because males have low mobility, the oviposition sites (galled ovules) chosen by each foundress are likely to have consequences for the mating structure of wasp populations within the figs. 2. In this study, the spatial location of male and female progeny of the pollinating fig wasp Liporrhopalum tentacularis developing within figs of its host plant Ficus montana was examined to investigate two questions: (i) are male and/or female wasp offspring clustered together or interspersed? and (ii) is their distribution affected by whether one or two foundresses are present? Microsatellite markers were used to identify the progeny of different foundresses in dual‐foundress figs. 3. More offspring developed in the central part of the figs, compared with the ostiolar and basal parts, irrespective of foundress number. Neither male nor female wasp offspring were clustered within a fig. 4. The sons of the second foundress to enter a fig were positioned at similar minimum distances to both sibling and non‐sibling females, whereas the sons of the first foundress were closer to their sibling females than to non‐sibling females. If male wasps mate predominantly with females in adjacent galls, then the positioning of sons by the second foundresses is beneficial for them both in terms of reduced sibling mating and because they are provided with ready access to the female progeny of the first foundress.     

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.     

Molecular markers reveal reproductive strategies of non‐pollinating fig wasps

1. Fig wasps have proved extremely useful study organisms for testing how reproductive decisions evolve in response to population structure. In particular, they provide textbook examples of how natural selection can favour female‐biased offspring sex ratios, lethal combat for mates and dimorphic mating strategies. 2. However, previous work has been challenged, because supposedly single species have been discovered to be a number of cryptic species. Consequently, new studies are required to determine population structure and reproductive decisions of individuals unambiguously assigned to species. 3. Microsatellites were used to determine species identity and reproductive patterns in three non‐pollinating Sycoscapter species associated with the same fig species. Foundress number was typically one to five and most figs contained more than one Sycoscapter species. Foundresses produced very small clutches of about one to four offspring, but one foundress may lay eggs in several figs. 4. Overall, the data were a poor match to theoretical predictions of solitary male clutches and gregarious clutches with n ? 1 females. However, sex ratios were male‐biased in solitary clutches and female‐biased in gregarious ones. 5. At the brood level (all wasps in a fig), a decrease in sex ratio with increasing brood size was only significant in one species, and sex ratio was unrelated to foundress number. In addition, figs with more foundresses contain more wasp offspring. 6. Finally, 10–22% of females developed in patches without males. As males are wingless, these females disperse unmated and are constrained to produce only sons from unfertilised eggs.     

Genetic structure of natural Nasonia vitripennis populations: validating assumptions of sex-ratio theory

The parasitic wasp Nasonia vitripennis has been used extensively in sex allocation research. Although laboratory experiments have largely confirmed predictions of local mate competition (LMC) theory, the underlying assumptions of LMC models have hardly been explored in nature. We genotyped over 3500 individuals from two distant locations (in the Netherlands and Germany) at four polymorphic microsatellite loci to validate key assumptions of LMC theory, in terms of both the original models and more recent extensions to them. We estimated the number of females contributing eggs to patches of hosts and the clutch sizes as well as sex ratios produced by individual foundresses. In addition, we evaluated the level of inbreeding and population differentiation. Foundress numbers ranged from 1 to 7 (average 3.0 ± 0.46 SE). Foundresses were randomly distributed across the patches and across hosts within patches, with few parasitizing more than one patch. Of the hosts, 40% were parasitized by more than one foundress. Clutch sizes of individual foundresses (average 9.99 ± 0.51 SE) varied considerably between hosts. The time period during which offspring continued to emerge from a patch or host correlated strongly with foundress number, indicating that sequential rather than simultaneous parasitism is the more common. Genetic differentiation at the regional level between Germany and the Netherlands, as estimated by Slatkin's private allele method (0.11) and Hedrick's corrected G' _LT (0.23), indicates significant substructuring between regions. The level of population inbreeding for the two localities ( F _IL = 0.168) fitted the expectation based on the average foundress number per patch.     

STABILIZING SELECTION AND VARIANCE IN FIG WASP SEX RATIOS

Theory predicts that the phenotypic variance observed in a trait subject to stabilizing selection should be negatively correlated with the trait's impact on fitness. However, this relationship has rarely been tested directly. The offspring sex ratios produced by pollinating fig wasp foundresses upon entrance to a fruit and oviposition alone (single foundress sex ratios) are subject to stabilizing selection because too many males reduce the total number of dispersing females and too few males will result in unmated females or complete loss of the brood. Furthermore, we argue that the impact on fitness of, and therefore the intensity of stabilizing intensity on, single foundress sex ratios are correlated to how frequently a species produces single foundress broods in nature. Specifically, the intensity of stabilizing selection will be greater in species that encounter single foundress broods more frequently, both because the trait is expressed more often and because fitness shows a greater sensitivity to variation (narrower fitness profile) when that trait is expressed. Across 16 species of Panamanian pollinating fig wasps, the phenotypic variance in single foundress sex ratios was negatively correlated with the frequency with which that species encounters single foundress broods in nature. In addition, a formal comparative analysis based upon a molecular phylogeny of the wasps gave results that were the same as when species were used as independent data points.     

Can the extremely female‐biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model?

Abstract.  1. Extremely female-biased sex ratios are known in the social spider mite species, Stigmaeopsis longus and S. miscanthi . Whether Hamilton's local mate competition (LMC) theory can explain such sex ratios was investigated.
2. Significant changes of the progeny sex ratios in the direction predicted by the LMC model were found in both species when the foundress number changed. Therefore, LMC can partly explain the skewed sex ratios in these species.
3. When the foundress number increased, the progeny sex ratio was still female biased and significantly different from the prediction of the LMC model for haplodiploidy. Relatedness between foundresses could not fully explain the female-biased sex ratios. Therefore, these results suggest that there are factors other than LMC skewing the sex ratios of these species toward female.     

Pollinating fig wasp Ceratosolen solmsi adjusts the offspring sex ratio to other foundresses

Abstract Local mate competition theory predicts that offspring sex ratio in pollinating fig wasps is female‐biased when there is only one foundress, and increased foundress density results in increased offspring sex ratio. Information of other foundresses and clutch size have been suggested to be the main proximate explanations for sex ratio adjustment under local mate competition. Our focus was to show the mechanism of sex ratio adjustment in a pollinating fig wasp, Ceratosolen solmsi Mayr, an obligate pollinator of the functionally dioecious fig, Ficus hispida Linn., with controlled experiments in the field. First, we obtained offspring from one pollinator and offspring at different oviposition sequences, and found that offspring sex ratio decreased with clutch size, and pollinators produced most of their male offspring at the start of bouts, followed by mostly females. Second, we found that offspring sex ratio increased with foundress density, and pollinators did adjust their offspring sex ratio to other females in the oviposition patches. We suggest that when oviposition sites are not limited, pollinators will mainly adjust their offspring sex ratio to other foundresses independent of clutch size changes, whereas adjusting clutch size may be used to adjust sex ratio when oviposition sites are limited.     

Sex allocation and interactions between relatives in the bean beetle, Callosobruchus maculatus

When a small number of females contribute offspring to a discrete mating group, sex allocation (Local Mate Competition: LMC) theory predicts that females should bias their offspring sex ratio towards daughters, which avoids the fitness costs of their sons competing with each other. Conversely, when a large number of females contribute offspring to a patch, they are expected to invest equally in sons and daughters. Furthermore, sex ratios of species that regularly experience variable foundress numbers are closer to those predicted by LMC theory than species that encounter less variable foundress number scenarios. Due to their patterns of resource use, female Callosobruchus maculatus are likely to experience a broad range of foundress number scenarios. We carried out three experiments to test whether female C. maculatus adjust their sex ratios in response to foundress number and two other indicators of LMC: ovipositing on pre-parasitised patches and ovipositing with sisters. We did not find any evidence of the predicted sex ratio adjustment, but we did find evidence of kin biased behaviour.     

Brood sex ratio variance,developmental mortality and virginity in a gregarious parasitoid wasp

Females of the parasitoid wasp Goniozus nephantidis paralyse host caterpillars and lay a clutch of up to 18 eggs onto the host integument. The known biology of G. nephantidis suggests that matings occur exclusively between siblings from the same brood. This leads to the prediction that brood sex ratios should be highly female-biased and have low variance. Sex ratios are indeed female-biased, with the mean proportion of males equal to 0.093. However, while sex ratio variance is significantly less than binomial, many broods contain no males at emergence. During development 28% of G. nephantidis offspring die. Male mortality offers a potential explanation for all-female (= virgin) broods. For the clutch sizes and mortality observed, theory predicts that <10% of females will emerge from all-female broods but the empirical value is much higher. The prediction that the prevalence of virginity decreases with increasing clutch size is, however, supported. We consider alternative explanations for the observed proportion of all-female broods, but this appears to be neither an artefact of the laboratory environment nor due to incorrect assumptions about G. nephantidis life history. Although its reproductive biology has been much investigated and its sex ratio matches some theoretical predictions, we conclude that a fuller understanding of G. nephantidis sex ratio requires a deeper knowledge of its field biology.     

Factors affecting the reproductive biology of Melittobia digitata and failure to meet the sex ratio predictions of Hamilton's local mate competition theory

Melittobia digitata Dahms (Eulophidae, Tetrastichini), a species of parasitic wasp satisfying all of Hamilton's local mate competition requisites, does not exhibit the predicted change in sex ratio with increased foundress number. A multifactorial design was used to test how age, oviposition experience, feeding experience, mating, and foundress number affect host‐acceptance, number of offspring, and sex ratio of this species developing on honey bee pupae, Apis mellifera (L.) (Apidae, Apini). All factors significantly affected the time it took for oviposition to commence. Females oviposited soonest when they were 2 days old, mated, had previous feeding and oviposition experience, and were placed on hosts with multiple foundresses. Although the age difference between 2‐ and 5‐day‐old females is small, it significantly affected reproductive behavior. Age, mating, and foundress number were found to have an effect on sex ratio, however, the foundress effect was found to be a mathematical artifact of the limited host size. After correcting for this variable, females were found to have a constant sex ratio of approximately 0.05. Several 2‐way interactions between factors were revealed: age and experience, age and foundress number, age and mating, foundress number and experience, and foundress number and mating. One 3‐way interaction was found between age, mating, and foundress number. This study demonstrates that the sex ratio of M. digitata is not altered with increased foundresses, as predicted by Hamilton , and that slight changes in preconditioning may modify reproductive behavior.     

Sex ratios under asymmetrical local mate competition: theory and a test with parasitoid wasps

Sex ratio theory allows unparalleled opportunities for testing how well animal behavior can be predicted by evolutionary theory. For example, Hamilton's theory of local mate competition (LMC) is well understood and can explain variation in sex allocation across numerous species. This allows more specific predictions to be developed and tested. Here we extend LMC theory to a situation that will be common in a range of species: asymmetrical LMC. Asymmetrical LMC occurs when females lay eggs on a patch asynchronously and male offspring do not disperse, leading to relatively weaker LMC for males emerging from later broods. Varying levels of LMC then lead to varying optimal sex ratios for females, depending on when and where they oviposit. We confirm the assumptions of our theory using the wasp Nasonia vitripennis and then test our predictions. We show that females adjust their offspring sex ratios in the directions predicted, laying different sex ratios on different hosts within a patch. Specifically, there was a less female-biased sex ratio when ovipositing on an unparasitized host if another host on the patch had previously been parasitized and a less female-biased sex ratio on parasitized hosts if females also oviposited on an unparasitized host.     

Determination of the optimal parasitoid‐to‐host ratio for efficient mass‐rearing of the parasitoid,Sclerodermus pupariae (Hymenoptera: Bethylidae)

Sclerodermus pupariae Yang et Yao (Hymenoptera: Bethylidae) is used as a potential biocontrol agent for several buprestid and cerambycid larvae. This study aimed to enhance the efficiency of mass‐rearing of this parasitoid by investigating the fitness gain of this bethylid wasp, including the proportion of successful parasitism and development, brood size, sex ratio, proportion of winged female offspring, body size and longevity of female offspring, under eight different maternal parasitoid density treatments using Thyestilla gebleri Faldermann as host in the laboratory. The results indicated that the foundress densities did not affect the parasitism or emergence rate of this parasitoid. Brood size of the parasitoids increased significantly when the number of maternal wasps ranged from one to four. However, further increases in foundress number did not affect the parasitoid brood size. The sex ratios of S. pupariae were always female‐biased. The proportions of male in the progeny colonies were <10% throughout all experimental treatments. The percentage of winged female progeny was not significantly influenced by the density of adult maternal parasitoids. Body sizes of parasitoids significantly declined with increasing maternal parasitoid densities. Although the parasitoid body size reduced when maternal wasp number was higher, it could be compromised by the relatively higher number of female offspring produced. Further, more than 70% of the parasitoids remained alive when they were stored at 12°C for four months throughout the experiments. These findings suggest that exposure of four female wasps to a single host larva would result in the highest fitness of S. pupariae. Our findings might provide a new approach to enhance the efficiency of mass‐rearing of this bethylid wasp.     

Within‐female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens

Sex allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within‐individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioural polyphenism in females, and its expression varies with seasonal changes in the environment. Between‐nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over‐represented in the earlier‐laid eggs, were in better condition than daughters, which are over‐represented in the later‐laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within‐female changes in offspring sex and not by sex‐biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.     

Cross‐fostering eggs reveals that female collared flycatchers adjust clutch sex ratios according to parental ability to invest in offspring

Across animal taxa, reproductive success is generally more variable and more strongly dependent upon body condition for males than for females; in such cases, parents able to produce offspring in above‐average condition are predicted to produce sons, whereas parents unable to produce offspring in good condition should produce daughters. We tested this hypothesis in the collared flycatcher (Ficedula albicollis) by cross‐fostering eggs among nests and using the condition of foster young that parents raised to fledging as a functional measure of their ability to produce fit offspring. As predicted, females raising heavier‐than‐average foster fledglings with their social mate initially produced male‐biased primary sex ratios, whereas those raising lighter‐than‐average foster fledglings produced female‐biased primary sex ratios. Females also produced male‐biased clutches when mated to males with large secondary sexual characters (wing patches), and tended to produce male‐biased clutches earlier within breeding seasons relative to females breeding later. However, females did not adjust the sex of individuals within their clutches; sex was distributed randomly with respect to egg size, laying order and paternity. Future research investigating the proximate mechanisms linking ecological contexts and the quality of offspring parents are able to produce with primary sex‐ratio variation could provide fundamental insight into the evolution of context‐dependent sex‐ratio adjustment.     

Reconstruction of fig wasp mating structure: how many mothers share a fig?

Abstract.  1. Fig wasps (Hymenoptera: Agaonidae) represent an important model system for studies of sex ratio evolution, mainly because they may adjust their sex ratios in response to the numbers of ovipositing females (foundresses) that enter a fig and their clutch size.
2. Until recently, it was assumed that all foundresses fail to re-emerge from the figs that they have entered to oviposit, but there is increasing evidence that such re-emergence may be routine. The common practice of counting the number of dead foundresses present in a fig in order to deduce the number of foundresses is therefore questionable in species where failure to re-emerge has not been confirmed.
3. In this study, the alternative approach of microsatellite markers was used to reconstruct the within-fig breeding structure of a pollinating fig wasp by genetic analysis of the offspring. Broods of Liporrhopalum tentacularis , a species where foundresses regularly re-emerge from figs, were collected from figs of Ficus montana in their natural habitat in Indonesia as well as from an experimental glasshouse population in Leeds (U.K.).
4. The estimated foundress densities in the glasshouse population were similar to those in the field and ranged from one to six foundresses per brood.
5. Nearly 40% of all broods were produced by a single foundress, indicating that mating in these broods occurs exclusively between full siblings. High levels of inbreeding are therefore common in this species.     

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.     

母体亲缘关系在杨氏榕树金小蜂后代性比调节中的作用

局域配偶竞争(local mate competition, LMC)理论问世以来在很多方面获得了发展,其中一个观点就是相互作用的繁殖母体之间的亲缘关系越近,后代性比越低,即产生更多的雌性后代。本研究以西双版纳广泛分布的钝叶榕Ficus curtipes上寄生的非传粉小蜂杨氏榕树金小蜂Diaziella yangi为研究对象,研究在同一榕果上产卵的繁殖雌蜂之间的亲缘关系对后代性比的影响。处理1：在同一榕果产卵的2头繁殖雌蜂来自蜂源1号树的同一个榕果;处理2：在同一榕果产卵的2头繁殖雌蜂来自蜂源2号树的同一个榕果,处理3：在同一榕果上产卵的2头繁殖蜂分别来自1、2号蜂源树。实验结果却显示出与理论预测值不一致。实验结果中,具有姐妹关系的2头繁殖雌蜂的2个处理的后代性比分别为0.195±0.028和0.189±0.043;亲缘关系较远的2头繁殖雌蜂的后代性比为0.240±0.030;不同处理的后代性比并没有显著差异。说明杨氏榕树金小蜂没有识别相互作用的繁殖雌蜂之间的亲缘关系以及据此调整后代性比的能力,这与其他大量研究 结果一致。     

管氏肿腿蜂母蜂产卵前合作的适合度代价

[目的]硬皮肿腿蜂Sclerodermus母蜂可合作寄生寄主,但在产卵前需不断蛰刺释放毒液以麻醉寄主.已明确合作可有效制服和寄生体型较大的寄主,但迄今对由此而付出的适合度代价尚不明确.[方法]用管氏肿腿蜂S.guani和替代寄主黄粉虫Tenebrio molitor蛹为材料,在两头已交配雌蜂(母蜂)分别合作0.5,1....