More highly female-biased sex ratio in the fig wasp,Blastophaga nipponica Grandi (Agaonidae)

The sex ratio of the pollinator fig wasp,Blastophaga nipponica Grandi (Agaonidae), was examined in an experiment manipulating the number of foundresses. The sex ratio ofB. nipponica was conditional on the number of foundresses and corresponded to the qualitative prediction of the local mate competition (LMC) theory that the proportion of males increases as foundress number increases. However, the sex ratio ofB. nipponica was consistently more female-biased than predicted by extended LMC theories that incorporated effects of inbreeding, and these deviations were statistically significant. Plausible factors that would make predictions more female-biased are discussed.     

母代雌蜂数、进果时间及非传粉小蜂对传粉榕小蜂后代数量及性比的影响

【目的】对性比的研究有助于我们理解自然界生物的选择压力及其所产生的原因和结果,榕树和榕小蜂之间的互惠共生关系以及生物学和生态学特性使其成为研究性比和局域配偶竞争模型（local mate competition）的理想材料。本研究旨在探明榕小蜂性比调节和进化机制。【方法】对分布于西双版纳地区的鸡嗉子榕Ficus semicordata进行了人工控制性放蜂实验。测定了母代雌蜂数量及其进果时间间隔、非传粉小蜂Sycoscapter trifemmensis数量对传粉榕小蜂Ceratosolen gravelyi后代数量（成蜂数量）和性比的影响,并分析了小蜂后代数量和性比的相关性。【结果】在榕果发育期一致的前提下,随着母代雌蜂数量的增加,每头雌蜂的平均后代数量明显下降(P<0.001),后代性比显著升高(P<0.001),后代数量和性比呈显著负相关(P<0.05);随着雌蜂进果间隔的延长,后代数量亦呈现下降趋势,且性比增大,放2头雌蜂和3头雌蜂的处理呈同样趋势,但差异均不显著(P=0.87; P=0.49),小蜂后代数量与性比无显著相关性(P=0.86)。此外,非传粉小蜂数量与传粉小蜂后代数量呈显著负相关(P<0.001),与传粉小蜂性比呈正相关(P<0.001),小蜂后代数量和性比同样呈现显著负相关(P<0.001)。【结论】本实验模拟了自然界中榕 蜂的相互作用,所得结果有助于我们理解自然状态下榕小蜂性比调节模式和机制,以及榕 蜂互利共生系统的进化机制。     

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.     

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。     

Development of 17 microsatellite markers for Ceratosolen constrictus, the pollinating fig wasp of Ficus fistulosa

The obligate mutualism between figs (Ficus) and fig pollinating wasps (Agaonidae) is regarded as a classic example of mutualism. Seventeen polymorphic microsatellite loci were developed for Ceratosolen constrictus, the pollinating wasp of the dioecious fig Ficus fistulosa. The number of alleles per locus ranged from two to 15 and the observed and expected heterozygosities ranged from 0.040 to 0.846 and from 0.040 to 0.916, respectively. These microsatellite loci offer a powerful tool for evolutionary and population genetic studies in C. constrictus, and gene flow of F. fistulosa.     

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.     

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.     

Offspring allocation in externally ovipositing fig wasps with varying clutch size and sex ratio

The simultaneous optimization of clutch size and sex ratio isa tricky problem. Unless parameters such as host size or fecundityexist to pin down the optimal clutch size, this problem remainselusive to analytical analysis. This is because the fitnesslandscape with respect to clutch size and sex ratio does nothave one single evolutionarily stable peak toward which thepopulation can evolve. To solve this problem, I used a computeremulation to optimize both clutch size and sex ratio using externallyovipositing fig wasps as a model taxon. The simulation approachallows the use of integer numbers of eggs rather than assumingthat females can produce any sex ratio between 0 and 1. Whenfemales have no information about the patches on which theyoviposit, they produce either large clutches with a strong femalebias or clutches of a single male egg. When females have completeknowledge of their oviposition site, a set of conditional substrategiesis evolutionarily stable. Again, these substrategies are eitherlarge clutches with a female bias or dutches consisting of asingle male egg. This dichotomous oviposition pattern resultsin unrelated males sharing a fig, a condition conducive to theevolution of fatal fighting. Selection on female ovipositionstrategies may therefore be an important driving force behindhigh levels of fighting observed between male fig wasps.     

Lethal combat and sex ratio evolution in a parasitoid wasp

Sex allocation theory provides excellent opportunities for testinghow behavior and life histories are adjusted in response toenvironmental variation. One of the most successful areas fromthis respect is Hamilton's local mate competition theory. Aspredicted by theory, a large number of animal species have beenshown to adjust their offspring sex ratios (proportion male)conditionally, laying less female-biased sex ratios as the numberof females that lay eggs on a patch increases. However, recentstudies have shown that this predicted pattern is not followedby 2 parasitoid species in the genus Melittobia, which alwaysproduce extremely female-biased sex ratios. A possible explanationfor this is that males fight fatally and that males producedby the first female to lay eggs on a patch have a competitiveadvantage over later emerging males. This scenario would negatethe advantage of later females producing a less female-biasedsex ratio. Here we examine fatal fighting and sex ratio evolutionin another species, Melittobia acasta. We show that femalesof this species also fail to adjust their offspring sex ratioin response to the number of females laying eggs on a patch.We then show that although earlier emerging males do have anadvantage in winning fights, this advantage 1) can be reducedby an interaction with body size, with larger males more likelyto win fights and 2) only holds for a brief period around thetime at which the younger males emerge from their pupae. Thissuggests that lethal male combat cannot fully explain the lackof sex ratio shift observed in Melittobia species. We discussalternative explanations.     

Extremely female-biased sex ratio and lethal male-male combat in a parasitoid wasp, Melittobia australica (Eulophidae)

Melittobia australica (Hymenoptera: Eulophidae) is a gregariousectoparasitoid of the prepupae and pupae of solitary wasps andbees. The males never disperse from their natal patch, and matingtakes place only on the host from which they emerged. We measuredthe offspring sex ratio of M. australica with differing foundressnumbers and examined combat between emerged males. The offspringsex ratios were extremely female biased and almost independentof foundress number in all cases. The population of M. australicaused in the experiment was infected with the cytoplasmicallyinherited symbiotic bacterium Wolbachia. However, although Wolbachiais a potential sex-ratio distorter, noninfected individualsshowed the same sex ratio patterns as the Wolbachia-infectedindividuals. An arena experiment showed that younger males werealmost always killed by older males that had eclosed earlier.These results suggested that lethal male–male combat isan additional factor distorting the sex ratio toward a morefemale-biased sex ratio. This provides a new perspective oncurrent local mate competition models.     

Quantitative tests of sex ratio models in a pollinating fig wasp

Pollinating fig wasps are often used to study sex ratio evolution in structured mating populations. Theory predicts a female-biased sex ratio, becoming less female biased as female (foundress) density increases. We usedLiporrhopalum tentacularis to test two mechanisms of sex ratio control when foundresses oviposit simultaneously: (1) foundresses facultatively adjust the number of males in clutches, and (2) they produce the same number of males regardless of clutch size, which, given limited numbers of oviposition sites, would lead to increases in sex ratio with increasing density. We then examined whether foundresses can oviposit sequentially into figs. When oviposition was simultaneous, brood composition indicated facultative adjustment, although sex ratios were more female biased than predicted. Instead, foundresses appeared to adjust their sex ratio in response to both others ovipositing and their own fecundity. We also found that foundresses are able to oviposit completely sequentially, with those arriving second adjusting their sex ratio in response to the previous oviposition. Hence, pollinating wasps may fail to fit the predictions of classical sex ratio theory because the conditions under which foundresses oviposit, and their responses to changes in such conditions, are more complex than once assumed. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Sex ratio response of the parasitoid wasp Muscidifurax raptor to other females

This study examines the sex ratio response of the parasitoid wasp Muscidifurax raptor to conspecific and confamilial females in relation to two groups of functional sex ratio models, local mate competition and host quality models. In some but not all experiments, M. raptor females produced a greater proportion of sons in the presence of a conspecific female than when alone, and this sex ratio effect carried over for a day after the females were isolated from each other M. raptor females also produced a greater proportion of sons in the presence of a female of the confamilial parasitoid Spalangia cameroni than when alone (although only on the second day of exposure to S. cameroni, not on the first). M. raptor's sex ratio increase in the presence of conspecifics is consistent with local mate competition models but not with host quality models because the presence of a conspecific female did not cause there to be more, and thus potentially smaller, offspring developing per host. In contrast, the presence of a S. cameroni female did cause there to be more offspring developing per host than when a M. raptor female was alone; thus M. raptor's sex ratio increase in the presence of S. cameroni may be explained by host quality models. An alternative explanation for the sex ratio increase in response to confamilials is that only a sex ratio response to conspecifics may be adaptive, due to local mate competition; but M. raptor females may be unable to distinguish between conspecific and S. cameroni females.     

对叶榕传粉小蜂性比率的调节和稳定

传粉榕小蜂呈现偏雌的性比率,单双倍体性别决定系统、局域配偶竞争和近交效应被认为是调节偏雌性比率的3个主要机制。通过研究影响对叶榕传粉小蜂性比率的因素,结果表明传粉榕小蜂的偏雌性比率随局域配偶竞争强度的降低而增加;受母代雌蜂交配次数的影响,随着母代雌蜂交配次数的增加,子代的偏雌性比率逐渐降低,这一结果首次揭示了传粉榕小蜂的交配制次数对性比率的影响,并在个体水平上定量了性比率变异与雌蜂交配频次的关系。传粉小蜂的性比率与共生的非传粉小蜂的关系,非传粉小蜂的介入直接减少了传粉小蜂的数量,甚至对传粉小蜂的种群有显著影响,结果发现非传粉小蜂对传粉小蜂雌雄性的分配比率没有显著影响,传粉榕小蜂仍能正常地进行繁殖。传粉与非传粉者小蜂之间作用关系的确定,可为进一步理解两者的稳定共生的机制提供科学证据。     

One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps

The study of chalcid wasps that live within syconia of fig trees (Moraceae, Ficus ), provides a unique opportunity to investigate the evolution of specialized communities of insects. By conducting cospeciation analyses between figs of section Galoglychia and some of their associated fig wasps, we show that, although host switches and duplication have evidently played a role in the construction of the current associations, the global picture is one of significant cospeciation throughout the evolution of these communities. Contrary to common belief, nonpollinating wasps are at least as constrained as pollinators by their host association in their diversification in this section. By adapting a randomization test in a supertree context, we further confirm that wasp phylogenies are significantly congruent with each other, and build a "wasp community" supertree that retrieves Galoglychia taxonomic subdivisions. Altogether, these results probably reflect wasp host specialization but also, to some extent, they might indicate that niche saturation within the fig prevents recurrent intrahost speciation and host switching. Finally, a comparison of ITS2 sequence divergence of cospeciating pairs of wasps suggests that the diversification of some pollinating and nonpollinating wasps of Galoglychia figs has been synchronous but that pollinating wasps exhibit a higher rate of molecular evolution.     

Kin discrimination and sex ratios in a parasitoid wasp

Sex ratio theory provides a clear and simple way to test if nonsocial haplodiploid wasps can discriminate between kin and nonkin. Specifically, if females can discriminate siblings from nonrelatives, then they are expected to produce a higher proportion of daughters if they mate with a sibling. This prediction arises because in haplodiploids, inbreeding (sib-mating) causes a mother to be relatively more related to her daughters than her sons. Here we formally model this prediction for when multiple females lay eggs in a patch, and test it with the parasitoid wasp Nasonia vitripennis. Our results show that females do not adjust their sex ratio behaviour dependent upon whether they mate with a sibling or nonrelative, in response to either direct genetic or a range of indirect environmental cues. This suggests that females of N. vitripennis cannot discriminate between kin and nonkin. The implications of our results for the understanding of sex ratio and social evolution are discussed.     

Factors affecting sequential sex allocation in the parasitoid wasp Gryon japonicum

Female wasps of the solitary egg parasitoid Gryon japonicum (Hymenoptera: Platygastridae) allocate male and female offspring in a particular sequence to successive hosts. Male eggs are typically laid in the second host, and the sex allocation sequence is reset after a certain period of time. The present study aimed to examine the underlying mechanism to hold information and reset the sequence by using eggs of Riptortus pedestris (Heteroptera: Alydidae) as hosts. After completion of initial oviposition, a female wasp was treated by cold anesthesia for 1 h, exposure to a parasitized host for 3 h, or being kept at 15°C in darkness for 24 h, and then presented with three host eggs. Cold‐anesthetized females did not reset the sex allocation sequence, indicating that cold anesthesia did not block the mechanism of holding information about oviposition order. Frequent encounters with parasitized hosts were also insufficient to reset the sequence. However, being kept in cool, dark conditions significantly affected resetting, suggesting that low temperature lengthened the time required to reset the sequence. This implies that it is probable that the mechanism to hold information and reset sex allocation sequence in G. japonicum involves metabolism.     

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.