Single-sex Broods Research Articles

Recent Evolution of a Maternally Acting Sex-Determining Supergene in a Fly with Single-Sex Broods.

Sex determination is a key developmental process, yet it is remarkably variable across the tree of life. The dipteran family Sciaridae exhibits one of the most unusual sex determination systems in which mothers control offspring sex through selective elimination of paternal X chromosomes. Whereas in some members of the family females produce mixed-sex broods, others such as the dark-winged fungus gnat Bradysia coprophila are monogenic, with females producing single-sex broods. Female-producing females were previously found to be heterozygous for a large X-linked paracentric inversion (X'), which is maternally inherited and absent from male-producing females. Here, we assembled and characterized the X' sequence. As close sequence homology between the X and X' made identification of the inversion challenging, we developed a k-mer-based approach to bin genomic reads before assembly. We confirmed that the inversion spans most of the X' chromosome (∼55 Mb) and encodes ∼3,500 genes. Analysis of the divergence between the inversion and the homologous region of the X revealed that it originated very recently (<0.5 Ma). Surprisingly, we found that the X' is more complex than previously thought and is likely to have undergone multiple rearrangements that have produced regions of varying ages, resembling a supergene composed of evolutionary strata. We found functional degradation of ∼7.3% of genes within the region of recombination suppression, but no evidence of accumulation of repetitive elements. Our findings provide an indication that sex-linked inversions are driving turnover of the strange sex determination system in this family of flies.

Sibling Cannibalism in Group-Living Larvae of the Solitary Wasp, Isodontia harmandi (Hymenoptera: Sphecidae): Effects of Prey Availability and Size Discrepancy.

Sibling cannibalism has rarely been documented in the resource-based context of sibling rivalry. The solitary wasp Isodontia harmandi (Pérez) (Hymenoptera: Sphecidae) has an exceptional style of nursery 'communal brood cells', in which multiple larvae gregariously develop while relying on maternal prey provisioning. In this species there are several distinct features; e.g., cannibalism-driven brood reduction, single-sex broods, and mass provisioning. Rearing of the wasp larvae in artificial nest chambers provides the novel opportunity to study larval interactions under controlled conditions. To determine the factors that influence the occurrence of cannibalism and its timing, we conducted a rearing experiment using sib and non-sib pairs under two prey-availability treatments, and recorded the occurrence of cannibalism and the processes of larval growth and prey consumption over a 96-hr period. Cannibalism occurred more frequently in the low-prey treatment than in the high-prey treatment, and in female pairs than in male pairs. Cannibalism tended to occur earlier when the amount of prey remaining decreased rapidly. However, cannibalism did not occur only when all prey had been completely consumed, implying that it was not triggered directly by prey exhaustion. Cannibals were always larger than their victims, whose growth rates had often slowed before they were eaten. These results strongly imply that wasp larvae commit sibling cannibalism in the context of resource-based sibling rivalry, ensuring the double benefit of nutritional gains and reduced resource competition. We also investigated the possibility that wasp larvae monitor the size difference and/or body condition of brood-mates as an indicator of prey availability.

Parasitoid developmental mortality in the field: patterns, causes and consequences for sex ratio and virginity

1. Sex ratio theory predicts that developmental mortality can affect sex ratio optima under Local Mate Competition and also lead to 'virgin' broods containing only females with no sibling-mating opportunities on maturity. 2. Estimates of developmental mortality and its sex ratio effects have been laboratory based, and both models and laboratory studies have treated mortality as a phenomenon without identifying its biological causes. 3. We contribute a large set of field data on Metaphycus luteolus Timberlake (Hymenoptera: Encyrtidae), an endoparasitoid of soft scale insects (Hemiptera: Coccidae), which has sex allocation conditional on host quality and female-biased brood sex ratios. Developmental mortality within broods can be both assessed and attributed to distinct causes, including encapsulation by the host and larval-larval competition. 4. Thirty per cent of M. luteolus offspring die during development with 65% of this mortality because of encapsulation and 28% because of larval competition. The distributions of mortality overall and for each cause of mortality separately were overdispersed. 5. The probability of an individual being encapsulated increased with clutch size, while the probability of being killed by a brood mate declined with increasing clutch size and with increasing per capita availability of resources. 6. The sexual compositions of broods at emergence were influenced by both the degree and the type of mortality operating. At higher levels of mortality, single sex broods were more common and sex ratios were less precise. Overall, virginity was more prevalent than predicted and was more greatly affected by the occurrence of competition than by other sources of mortality, almost certainly because competition tended to eliminate males. 7. The reproductive and developmental biology of M. luteolus appears to be influenced by a complex interplay of maternal clutch size and sex allocation strategies, offspring-offspring developmental interactions, host defence mechanisms and postemergence mating behaviour. Despite the great sophistication of sex ratio theory, it has not yet evolved to the point where it is capable of considering all of these influences simultaneously.

Variation in reproductive output of Ficus superba despite aseasonal reproduction

Studies of Ficus reproductive phenology have focused on documenting its seasonality and dependence on meteorological factors. While there have been reports that duration of receptivity of syconia can be prolonged in response to pollinator limitation, the effect of pollination rate on the duration of phenological phases over a year has not been examined. Percentage of unpollinated syconia, number of foundresses per pollinated syconium, duration of receptivity, frequency of single-sex broods, crop size, frequency of parasitisation, persistence of ripe syconia, and mass abscission were recorded for Ficus superba at the crop level. Percentage of unpollinated syconia is significantly negatively correlated with the number of foundresses per syconium, and positively correlated with the duration of receptivity, and the persistence of ripe syconia. Despite the absence of sesonality in reproduction, the occurrences of receptive syconia and ripe syconia showed unimodal and bimodal peaks, respectively, owing to prolongment of these phases. This is attributable to meteorological factors, which are hypothesized to influence pollinator dispersal, or population dynamics, and thus pollination rate. This highlights the overlooked significance of pollinator, and possibly frugivore phenology in accounting for Ficus reproduction, and suggests that while reproduction may be aseasonal, reproductive potential may not be. Furthermore, crop size was shown to affect the number of foundresses per syconium, duration of receptivity, and persistence of ripe syconia. Possible adaptive value of producing crops of different sizes is discussed.

Tritrophic Effects of Xanthotoxin on the Polyembryonic Parasitoid Copidosoma sosares (Hymenoptera: Encyrtidae)

Plant chemistry can have deleterious effects on insect parasitoids, which include the reduction in body size, increased development time, and increased mortality. We examined the effects of xanthotoxin, a linear furanocoumarin, on the polyembryonic encyrtid wasp Copidosoma sosares, a specialist parasitoid that attacks the parsnip webworm, Depressaria pastinacella, itself a specialist on furanocoumarin-producing plants. Furanocoumarins, allelochemicals abundant in the Apiaceae and Rutaceae, are toxic to a wide range of herbivores. In this study, we reared parasitized webworms on artificial diets containing no xanthotoxin (control) or low or high concentrations of xanthotoxin. Clutch sizes of both male and female C. sosares broods were more than 20% smaller when they developed in hosts fed the diet containing high concentrations of xanthotoxin. Xanthotoxin concentration in the artificial diet had no effect on the development time of C. sosares, nor did it have an effect on the body size (length of hind tibia) of individual adult male and female C. sosares in single-sex broods. Webworms fed artificial diets containing low or high concentrations of xanthotoxin were not significantly smaller, and their development time was similar to that of webworms fed a xanthotoxin-free diet. Mortality of webworms was not affected by xanthotoxin in their artificial diet. Therefore, dietary xanthotoxin did not appear to affect C. sosares via impairment of host health. However, unmetabolized xanthotoxin was found in D. pastinacella hemolymph where C. sosares embryos develop. Hemolymph concentrations were fourfold greater in webworms fed the high-xanthotoxin-containing diet than in webworms fed the low-xanthotoxin-containing diet. We failed to detect any xanthotoxin metabolism by either C. sosares embryos or precocious larvae. Therefore, the observed tritrophic effects of xanthotoxin are likely to be due to the effects of xanthotoxin after direct contact in the hemolymph rather than to the effects of compromised host quality.

Asymmetric larval mobility and the evolutionary transition from siblicide to nonsiblicidal behavior in parasitoid wasps

The widespread evolution of gregarious development in parasitoid wasps presents a theoretical challenge because the conditions under which larval tolerance can spread in an intolerant population are very stringent (the individual fitness of larvae developing together must increase with clutch size). Recent empirical work has suggested that gregarious development can arise through the loss of larval mobility rather than through the gain of tolerant behavior. Using analytical genetic models, we explored whether decreased mobility presents a less stringent route to gregariousness than the gain of tolerance. Reduced mobility can spread under a wide range of conditions. The critical condition for the spread of immobility is much less stringent than that for larval tolerance. In contrast with previous models of tolerance, the criterion for the spread of a rare immobility allele is independent of any bias in the sex ratio and the likelihood of single sex broods. Superparasitism increases the stringency of the criterion for the spread of immobility, whereas double killing relaxes the criterion. Tolerance can subsequently replace immobility if there is any cost to the retention of fighting ability. Our results suggest that asymmetric larval mobility may explain many instances of the evolution of gregarious development. Copyright 2003.

A polymorphic effect of sexually differential production costs when one parent controls the sex ratio.

R. A. Fisher's sex ratio theory predicts that if sons and daughters cost fixed amounts of resources to raise and parents have fixed amounts to invest, then the numerical sex ratio of a panmictic population will evolve to be inversely proportional to relative cost. However, the theory assumes control by both parents. We show that allowing one parent to control the sex ratio biases it further from parity than Fisher's theory predicts. Quantitatively, the additional bias towards the cheaper sex depends only very weakly on which sex is in control. Qualitatively, however, the effect is very strong: a monomorphic, mixed-brood strategy evolves only if the more expensive sex is in control. If the controlling sex is cheaper to raise, then the sex ratio is instead achieved through a polymorphism of single-sex broods. Such polymorphisms are seldom observed in nature, generating the prediction that wherever the sexes are not equally costly, sex ratio is usually either under biparental control or under uniparental control by the more expensive sex. However, such polymorphisms do occur, and some of them may be explained by our model.

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

AbstractModels 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.

Sex allocation and clutch size in parasitoid wasps that produce single-sex broods

The parasitoid wasp genusAchrysocharoides(Eulophidae) is unusual in that many of its species lay male and female eggs in single-sex clutches. The average clutch size of female broods is always greater than that of male broods, and in some species male clutch size is always one. We constructed models that predicted that severely egg-limited wasps should produce equal numbers of male and female eggs while severely host-limited wasps should produce equal numbers of male and female broods (and hence an overall female-biased sex ratio). Theory is developed to predict clutch size and sex ratio across the complete spectrum of host and egg limitation. A comparison of 19 surveys of clutch composition in seven species ofAchrysocharoidesshowed a general pattern of equal numbers of male and female broods with a female-biased sex ratio (suggesting host limitation) although with considerable heterogeneity amongst collections and with a number of cases of unexpectedly low frequencies of male broods. Using a previous estimate of the relationship between fitness and size in the field, we predicted the maximally productive (Lack) clutch size for female broods ofAchrysocharoides zwoelferito be three. Of clutches observed in nature, 95% were equal to or smaller in size than the predicted Lack clutch size. When we manipulated local host density in the field, and as predicted by our models, clutch size and the proportion of female broods ofA.zwoelferidecreased as hosts became more common, but the absolute frequency of male clutches was lower than expected.

Virginity in haplodiploid populations: a comparison of estimation methods

1. The presence of ovipositing virgin females, who are able to produce only male offspring, may have several important consequences for the evolution of reproductive strategies.2. The prevalence of virginity for five fig wasp species was estimated using three different methods: (1) the proportion of females developing in fruit that contained no conspecific males; (2) dissection of females caught on sticky traps; and (3) dissection of females that had emerged from their galled flowers into the fruit cavity.3. The estimates obtained by method 1 (females developing in single sex broods) were lower than those obtained by the other methods.4. Across species, the estimates obtained by method 1 (females developing in single sex broods) were significantly correlated with those obtained by method 2 (sticky trap caught females).5. Mating with sperm‐depleted males is unlikely to occur in these species.

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.

Single-Sex Broods and the Evolution of Nonsiblicidal Parasitoid Wasps

Obligate siblicide as observed in many parasitoid wasps may commonly be a manifestation of parent-offspring conflict over clutch size. Genetic models have revealed that very stringent conditions may be required for a nonsiblicidal allele to successfully invade a siblicidal population. The parasitoid studied here, Argochrysis armilla Bohart (Hymenoptera: Chrysididae), appears to have undergone a transition from siblicidal to nonsiblicidal behavior during its recent evolutionary history. The appearance of nonsiblicide in A. armilla is paradoxical, because factors facilitating the evolution of nonsiblicidal behavior (costs of producing the fighting apparatus, female-biased sex ratios) appear to be absent, while factors favoring siblicidal behavior (superparasitism, mobile parasitoid larvae) appear to be present. Argochrysis armilla does, however, produce a preponderance of single-sex broods. I construct genetic models to demonstrate that single-sex broods can substantially relax the conditions under which a nonsiblicidal allele can invade a siblicidal population and simultaneously make more stringent the conditions under which a siblicidal allele can invade a nonsiblicidal population. The production of single-sex broods may be common during the evolutionary transition from siblicidal to nonsiblicidal behavior and could therefore play an important role in facilitating the evolution of nonsiblicidal behavior.

Oviposition behavior and progeny allocation of the polyembryonic waspCopidosoma floridanum (Hymenoptera: Encyrtidae)

Oviposition behavior was used to determine the primary clutch size and sex ratio of the polyembryonic wasp Copidosoma floridanumAshmead (Hymenoptera: Encyrtidae) parasitizing Pseudoplusia includens(Walker) (Lepidoptera: Noctuidae). The laying of a female egg was associated with a pause in abdominal contractions during oviposition, while the laying of a male egg was associated with uninterrupted abdominal contractions. Although unmated females produced only male broods, they also displayed male and female egg oviposition movements. Wasps always laid a primary clutch of one or two eggs. For mated females if only one egg was laid, the emerging secondary clutch was all male or female, but if two eggs were laid a mixed brood of males and females was almost always produced. The secondary clutch of single sex broods was usually between 1000 and 1200 individuals, but the secondary clutch of mixed broods averaged 1143 females and 49 males. Thus, the primary sex ratio for mixed broods was 0.5 (frequency males), but the secondary sex ratio was 0.042. Manipulation of the sequence of male and female egg oviposition or of the primary clutch did not produce major alterations in the secondary clutch size or sex ratio.