Dispersal and mating structure of a parasitoid with a female-biased sex ratio: Implications for theory

Summary Species of parasitic Hymenoptera that manifest female-biased sex ratios and whose offspring mate only with the offspring of the natal patch are assumed to have evolved biased sex ratios because of Local Mate Competition (LMC). Off-patch matings, i.e. outcrossing, are inconsistent with the conditions favouring biased sex ratios because they foster a mating structure approaching panmixia. Such a mating structure favours parents who invest equally in daughters and sons, assuming the production of each sex is of equal cost.Pachycrepoideus vindemiae (Rondani) is a solitary pupal parasitoid of patchily distributed frugivorousDrosophila, whose offspring manifest a female-biased sex ratio. Thus this species appears to manifest a population structure and progeny sex ratio consistent with LMC. However, preliminary observations and subsequent greenhouse experiments suggest that the males participate in off-patch matings and that this propensity is unlikely to be an experimental artefact. FemaleP. vindemiae dispersed from patches in which either the males were lacking (12% of the emigrant females), both resident (sibling) and immigrant males were present (23% of the females), only immigrant males were present (14% of the females), or their opportunity to mate could not be determined (14% of the females). Of the 12% that emigrated from a patch lacking males, an estimated 7% mated at an oviposition site and 5% remained unmated, presumably because they arrived at an oviposition site that lacked males before they were dissected to determine whether they were inseminated. Thus the degree of bias in the sex ratios of the progeny (18% males), coupled with the suggested outcrossing potential from the experiments (26–37%), is inconsistent with the assumptions of LMC or variants of it, i.e. asynchronous brood maturation. Thus the explanation for a biased sex ratio in the offspring ofP. vindemiae remains a conundrum. More importantly,P. vindemiae does not appear to be an isolated example.     

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.     

Observations on sex ratio and behavior of males in Xyleborinus saxesenii Ratzeburg (Scolytinae, Coleoptera)

Strongly female-biased sex ratios are typical for the fungalfeeding haplodiploid Xyleborini (Scolytinae, Coleoptera), and are a result of inbreeding and local mate competition (LMC). These ambrosia beetles are hardly ever found outside of trees, and thus male frequency and behavior have not been addressed in any empirical studies to date. In fact, for most species the males remain undescribed. Data on sex ratios and male behavior could, however, provide important insights into the Xyleborini's mating system and the evolution of inbreeding and LMC in general.In this study, I used in vitro rearing methods to obtain the first observational data on sex ratio, male production, male and female dispersal, and mating behavior in a xyleborine ambrosia beetle. Females of Xyleborinus saxesenii Ratzeburg produced between 0 and 3 sons per brood, and the absence of males was relatively independent of the number of daughters to be fertilized and the maternal brood sex ratio. Both conformed to a strict LMC strategy with a relatively precise and constant number of males. If males were present they eclosed just before the first females dispersed, and stayed in the gallery until all female offspring had matured. They constantly wandered through the gallery system, presumably in search of unfertilized females, and attempted to mate with larvae, other males, and females of all ages. Copulations, however, only occurred with immature females. From galleries with males, nearly all females dispersed fertilized. Only a few left the natal gallery without being fertilized, and subsequently went on to produce large and solely male broods. If broods were male-less, dispersing females always failed to found new galleries.     

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.     

Adaptive production of fighter males: queens of the ant Cardiocondyla adjust the sex ratio under local mate competition

Hamilton's concept of local mate competition (LMC) is the standard model to explain female-biased sex ratios in solitary Hymenoptera. In social Hymenoptera, however, LMC has remained controversial, mainly because manipulation of sex allocation by workers in response to relatedness asymmetries is an additional powerful mechanism of female bias. Furthermore, the predominant mating systems in the social insects are thought to make LMC unlikely. Nevertheless, several species exist in which dispersal of males is limited and mating occurs in the nest. Some of these species, such as the ant Cardiocondyla obscurior, have evolved dimorphic males, with one morph being specialized for dispersal and the other for fighting with nest-mate males over access to females. Such life history, combining sociality and alternative reproductive tactics in males, provides a unique opportunity to test the power of LMC as a selective force leading to female-biased sex ratios in social Hymenoptera. We show that, in concordance with LMC predictions, an experimental increase in queen number leads to a shift in sex allocation in favour of non-dispersing males, but does not influence the proportion of disperser males. Furthermore, we can assign this change in sex allocation at the colony level to the queens and rule out worker manipulation.     

Female production within the gall and male production on leaves by individual alates of a social aphid

The social aphid Astegopteryx spinocephala forms a banana-bunch shaped gall, consisting of several subgalls, on Styrax benzoides in northern Thailand. The aphid’s life cycle is non-host alternating. Alates (sexuparae) containing both male and female embryos appear near the end of the dry season, when many sexuals and eggs are found in subgalls guarded by sterile soldiers. Our experiments revealed that these alates give birth to almost all (99%) females within the natal subgall before flying but most (73–86%) males on leaves of the host tree after flying, and that these first-instar males intrude into live subgalls for mating. The fact that some (14–27%) males are deposited in the natal subgall indicates the occurrence of both outbreeding and inbreeding, or some level of local mate competition (LMC), in this mating system. However, the primary (investment) sex ratio was estimated to be near 0.5. This suggests that factors other than LMC, a candidate for which is local resource competition, might also affect the sex ratio in A. spinocephala. Received 19 March 2007; revised 12 July 2007; accepted 13 August 2007.     

Queen number influences the timing of the sexual production in colonies of Cardiocondyla ants

Wingless males of the ant genus Cardiocondyla engage in fatal fighting for access to female sexual nestmates. Older, heavily sclerotized males are usually capable of eliminating all younger rivals, whose cuticle is still soft. In Cardiocondyla sp. A, this type of local mate competition (LMC) has turned the standard pattern of brood production of social insects upside down, in that mother queens in multi-queen colonies produce extremely long-lived sons very early in the life cycle of the colony. Here, we investigated the emergence pattern of sexuals in two species with LMC, in which males are much less long-lived. Queens of Cardiocondyla obscurior and Cardiocondyla minutior reared their first sons significantly earlier in multi-queen than in single-queen societies. In addition, first female sexuals also emerged earlier in multi-queen colonies, so that early males had mating opportunities. Hence, the timing of sexual production appears to be well predicted by evolutionary theory, in particular by local mate and queen-queen competition.     

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.     

Simultaneous failure of two sex-allocation invariants: implications for sex-ratio variation within and between populations

Local mate competition (LMC) occurs when male relatives compete for mating opportunities, and this may favour the evolution of female-biased sex allocation. LMC theory is among the most well developed and empirically supported topics in behavioural ecology, clarifies links between kin selection, group selection and game theory, and provides among the best quantitative evidence for Darwinian adaptation in the natural world. Two striking invariants arise from this body of work: the number of sons produced by each female is independent of both female fecundity and also the rate of female dispersal. Both of these invariants have stimulated a great deal of theoretical and empirical research. Here, we show that both of these invariants break down when variation in female fecundity and limited female dispersal are considered in conjunction. Specifically, limited dispersal of females following mating leads to local resource competition (LRC) between female relatives for breeding opportunities, and the daughters of high-fecundity mothers experience such LRC more strongly than do those of low-fecundity mothers. Accordingly, high-fecundity mothers are favoured to invest relatively more in sons, while low-fecundity mothers are favoured to invest relatively more in daughters, and the overall sex ratio of the population sex ratio becomes more female biased as a result.     

Partial local mate competition and the sex ratio: A study on non-pollinating fig wasps

In many species, mating takes place in temporary patches where only a small number of females produce offspring. In this situation Local Mate Competition (LMC) theory predicts that the optimal sex ratio (defined as proportion males) should become increasingly female biased as the number of females contributing offspring to a patch decreases. However, in a large number of these species, some mating is also likely to occur away from the natal patch (termed partial LMC). In this case the degree of LMC is reduced, and theory predicts a relatively less female biased sex ratio. We tested these two predictions with field data from 17 species of New World non-pollinating fig wasps representing three genera. We present a model which suggests that the average number of females ovipositing in a fruit (i.e. patch) is positively correlated with the proportion of fruit of a given tree species in which that species of wasp occurs. Across species, the overall sex ratio was positively correlated with the proportion of fruit in which that species occurs. Furthermore, the males of some species are wingless, and in these species all mating must take place before females disperse from their natal fruit. In contrast, the males of other species are winged, and in these species mating may also take place away from the natal fruit. Species with winged males had less female biased sex ratios than species with wingless males that occurred in a similar proportion of fruit. Finally, the correlation between sex ratio and the proportion of fruit in which a species occurs was also observed within species when comparing between the fruit crops of different trees. This suggests that individual females facultatively adjust the sex ratio of their offspring in response to variable LMC.     

Single-locus sex determination in the parasitoid wasp Cotesia glomerata (Hymenoptera: Braconidae)

The parasitoid Cotesia glomerata usually produces female-biased sex ratios in the field, which are presumably caused by inbreeding and local mate competition (LMC); yet, sibling mating increases the production of males, leading to the male-biased sex ratio of broods in the laboratory. Previous studies have suggested that the sex allocation strategy of C. glomerata is based on both partial LMC in males and inbreeding avoidance in females. The current study investigated the presence of single-locus complementary sex determination (sl-CSD) as a sex-determining mechanism in this species through inbreeding experiment, cytological examination and microsatellite analysis. Cytological examination detected diploid males in nine of 17 single pairs of sibling mating, thus in agreement with the proportion of matched matings predicted by the sl-CSD model. Sex ratio shifts in these matched sibling matings were consistent with the sl-CSD model with less viable diploid males. The haploid males have a single set of maternal chromosomes (n = 10), whereas diploid males possess a double set of chromosomes (2n = 20). Microsatellite analyses confirmed that diploid males produced from the matched matings inherited segregating genetic materials from both parents. Thus, this study provides the first solid evidence for the presence of sl-CSD as a sex-determining mechanism in the braconid genus Cotesia.     

Sex ratio schedules in a dynamic game: the effect of competitive asymmetry by male emergence order

Studies of sex allocation have provided some of the most successfultests of theory in behavioral and evolutionary ecology. Forinstance, local mate competition (LMC) theory has explainedvariation in sex allocation across numerous species. However,some patterns of sex ratio variation remain unexplained by existingtheory. Most existing models have ignored variation in malecompetitive ability and assumed all males have equal opportunitiesto mate within a patch. However, in some species experiencingLMC, males often fight fiercely for mates, such that male matingsuccess varies with male fighting ability. Here, we examinethe effect of competitive ability on optimal sex allocationschedules using a dynamic programming approach. This model assumesan asymmetric competitive ability derived from different mortalitiesaccording to the timing of male emergence. If the mortalityof newly emerging males is larger than that of already emergedmales, our model predicts a more female-biased sex ratio thanexpected under traditional LMC models. In addition, femalesare predicted to produce new males constantly at a low rateover the offspring emergence period. We show that our modelsuccessfully predicts the sex ratios produced by females ofthe parasitoid wasp Melittobia, a genus renowned for its vigorouslyfighting males and lower than expected sex ratios.     

Mating systems and sex ratios in the egg parasitoids, Trichogramma dendrolimi and T. papilionis (Hymenoptera: Trichogrammatidae)

Arrhenotokous parthenogenesis was confirmed in Trichogramma dendrolimi and T. papilionis. Subsequently the possible links between mating systems and biological traits of males, and sex ratios, were investigated in these two species, using Papilio xuthus eggs for their hosts. T. dendrolimi males attained 100% insemination of females in the parasitized host before egress from it. The high insemination rate was guaranteed by male precedence in emergence, lack of courtship in mating behaviour and short copulation time, combined with a long stay of emerging wasps within the host. The males were often the last to leave a host and made no mating attempts outside the host. Most but not all T. papilionis females were also inseminated in the host. The lower insemination rate of this species resulted from almost simultaneous emergence of both sexes, which prevented males from mating with inactive females. Another mating site of T. papilionis was just outside the host, which males left prior to most females. A reduced possibility of outbreeding was inferred in T. dendrolimi on the grounds that males were short-lived, frequently failed to expand their wings and died in the host. The reduced outbreeding was reflected in considerably lower sex ratios in T. dendrolimi.     

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.     

The continuous public goods game and the evolution of cooperative sex ratios

Some animals, such as Melittobia wasps and surface-living mites, have extremely female-biased sex ratios that cannot be explained by the existing local mate competition (LMC) theories. The restricted production of sons may entail cooperation among mothers, enabling the production of more daughters and avoiding severe competition among sons for insemination access. These unusual examples are characterized by the long-term cohabitation of egg-layers (foundresses) on resource patches and possible contact with oviposited eggs. By applying the logic of mutual policing, we develop a novel game theoretical model for the evolution of cooperation in sex-ratio traits. This is the first attempt to model the evolution of sex ratios based on iterated games. We assumed that foundresses have two abilities to enable mutual policing: they can monitor the sex ratio in the resource patch, and they can punish defectors that produce an overabundance of males. Numerical analysis and evolutionary simulations demonstrate that cooperative low sex ratios can evolve when the number of foundresses per patch is sufficiently small. Our model predicts a slight, but steady increase in oviposition sex ratios with an increase in the number of foundresses, which mimics the phenomenon observed in several animals with extremely female-biased sex ratios. We also discuss the relationship between our model and other models of sex-ratio evolution.     

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。     

Outbreeding depression, but no inbreeding depression in haplodiploid Ambrosia beetles with regular sibling mating

In sexual reproduction the genetic similarity or dissimilarity between mates strongly affects offspring fitness. When mating partners are too closely related, increased homozygosity generally causes inbreeding depression, whereas crossing between too distantly related individuals may disrupt local adaptations or coadaptations within the genome and result in outbreeding depression. The optimal degree of inbreeding or outbreeding depends on population structure. A long history of inbreeding is expected to reduce inbreeding depression due to purging of deleterious alleles, and to promote outbreeding depression because of increased genetic variation between lineages. Ambrosia beetles (Xyleborini) are bark beetles with haplodiploid sex determination, strong local mate competition due to regular sibling mating within the natal chamber, and heavily biased sex ratios. We experimentally mated females of Xylosandrus germanus to brothers and unrelated males and measured offspring fitness. Inbred matings did not produce offspring with reduced fitness in any of the examined life-history traits. In contrast, outcrossed offspring suffered from reduced hatching rates. Reduction in inbreeding depression is usually attributed to purging of deleterious alleles, and the absence of inbreeding depression in X. germanus may represent the highest degree of purging of all examined species so far. Outbreeding depression within the same population has previously only been reported from plants. The causes and consequences of our findings are discussed with respect to mating strategies, sex ratios, and speciation in this unusual system.     

Sex allocation of parasitic wasps: local mate competition,dispersal before mating and host quality variation

We constructed a sex allocation model for parasitic wasps to explain the wide variation in their sex ratio, considering the effects of local mate competition, partial dispersal of progeny before mating, and heterogeneity in host quality among patches. We conducted an experiment to compare with the predictions of our model. We considered the following situations. First, the hosts are distributed in discrete patches: a number of female wasps visit and oviposit in each patch. Second, all the progeny do not mate within the natal patch; some of them disperse to take part in population-wide random mating. We calculated ES sex ratios in cases where there are two kinds of patches: good ones and poor ones. We examined the dependency of ES sex ratios on several parameters, i.e., 1) the probability that a daughter mates in her natal patch, 2) the ratio of the female fitness of the good patch to that of the poor patch, 3) the proportion of poor patches, and 4) the number of foundresses in a patch. The result of our experiment showed the same tendency as the calculation in case where the LMC effect is high in each patch. We briefly discuss a possible selection pressure for dispersal of progeny, with special reference to the mating structure of parasitic wasps.     

Superparasitism and sex ratio adjustment in a wasp parasitoid: results at variance with Local Mate Competition?

Anaphes nitens is a solitary parasitoid of the egg capsules of the Eucalyptus snout beetle, Gonipterus scutellatus. Some traits of its natural history suggest that Local Mate Competition (LMC) could account for sex ratio adjustment in this species. We tested whether males emerged early, a prerequisite for fully local mating, and investigated the occurrence and effect of superparasitism on adult size and pre-emergence mortality, factors that might influence sex ratio adjustment. We found in field-collected egg capsules that males emerged first. To investigate the effects of superparasitism on adult size, we compared the sizes of parasitoids that emerged early and late from egg capsules collected in the field, and from egg capsules parasitized and superparasitized in the laboratory. Superparasitism reduced parasitoid size, affecting females more strongly than males, and increased pre-emergence mortality. We estimated A. nitens sex ratio and parasitism rate in the field during 2 years in five localities and during 4 years in a sixth. Following LMC we expected an increase in sex ratio (proportion of males) with increasing parasitism rate (assumed to reflect parasitoid density). We found that sex ratio decreased from 0.38 when the parasitism rate was low (0-20%) to 0.21 when parasitism was high (80-100%). In contrast with field results, a laboratory experiment showed that: (1) at a low parasitism level sex ratio was clearly female biased (0.28+/-0.04), (2) at a high parasitism level sex ratio increased (0.40+/-0.07), (3) male larval survivorship was not lower than female survivorship, and (4) low-quality hosts (i.e. superparasitized) were allocated more males. We conclude that LMC cannot explain the sex ratio adjustment observed in the field, even at low parasitism rates, and alternative explications for highly female-biased sex ratios must be found. One such alternative is female-biased dispersal.     

Sex-ratios of the wasp Nasonia vitripennis from self-versus conspecifically-parasitized hosts: local mate competition versus host quality models

Sex ratio patterns in the parasitoid wasp Nasonia vitripennis are frequently cited in support of a major group of evolutionary sex ratio models referred to as local mate competition (LMC) models. It has been shown repeatedly that, as predicted by LMC models, females generally oviposit a greater proportion of sons in previously parasitized hosts than in unparasitized hosts. However, this sex ratio pattern is also a prediction of another group of sex ratio models, the host quality models. Here I test a prediction of LMC models that is not also a prediction of host quality models: a female should produce a greater proportion of sons when she parasitizes a host previously parasitized by a conspecific female than when she parasitizes a host previously parasitized by herself. Females made this predicted distinction between self- and conspecifically-parasitized hosts under some conditions. There was no evidence that a female recognizes a self-parasitized host when her exposure to the host is interrupted by exposure to an unparasitized host, or that a female can distinguish between hosts parasitized by sisters versus nonsisters.