Stable female-biased sex allocation in Anisopteromalus calandrae under varying intraspecific competition: implications for augmentative biological control

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

The aim of this study was to test the predictions of local mate competition (LMC), host quality (HQ) and operational sex ratio (OSR) models, using a non-arrhenotokous parasitic mite, Hemisarcoptes coccophagus (Astigmata: Hemisarcoptidae). The life-history pattern of this mite meets the assumptions of these sex allocation models. Mating group size (LMC model), HQ and OSR affected the sex allocation of H. coccophagus females. Only young mite females adjusted the sex ratio of their progenies according to the predictions of LMC and HQ models; the sex allocation of old females was contrary to these predictions. We explain these patterns by the dynamic nature of the mite's population structure. When parents are young, their population distribution is patchy and progeny matings are local; hence sex allocation is in accordance with LMC theory. When parents become older, their populations shift towards panmixis; factors which had operated previously no longer exist. Consequently, females adjust the sex ratio of late progenies so that it can compensate for the earlier sex allocation, in order to make their total sex ratio unbiased, as expected in panmictic populations. Our data, expressed as the cumulative sex ratio, support this hypothesis.

Primary sex ratio adjustment by ant queens in response to local mate competition

As an important domain of evolutionary ecology, sex allocation theory well explains the evolution of investment into female versus male offspring. Local mate competition (LMC) is a good predictor of sex allocation, where the optimal sex ratio becomes less female-biased and asymptotically approaches 0.5 as the number of foundresses increases. Parasitoid wasps, with haplodiploid sex determination, offer excellent opportunities to test how organisms manipulate their offspring sex ratio in response to environmental variation, and many species have been proved to allocate sex according to predictions under LMC. When hosts are spatially clustered, as in gregarious species, the mating systems of quasi-gregarious parasitoids meet the essential assumptions (female mating before dispersal) of LMC. However, inconsistent with predictions, in the quasi-gregarious species Anastatus disparis (Hymenoptera: Eupelmidae), a strongly female-biased eclosion sex ratio (0.156 ± 0.018 to 0.185 ± 0.016) was observed as the number of females laying eggs in a patch increased. Superparasitism, in which 44.7% of parasitized hosts contained more than one egg but only one adult emerged from each host, was common in A. disparis. However, the egg sex ratio was determined by microsatellites and likely fit the predictions of LMC theory. Male-biased offspring mortality arising from superparasitism during development likely contributes to the shift from the primary sex ratio predicted under LMC to the observed female-biased eclosion sex ratio. Inconsistent with results in gregarious parasitoids, the role of superparasitism in driving sex ratio shifts in quasi-gregarious parasitoids should be incorporated into LMC-based predictions of sex ratios.

Local mate competition (LMC) has been postulated to be the primary factor of female-biased sex allocation. In animals such as aphids that exhibit seasonal alternations of clonal and sexual reproduction, there is a high possibility of intra-clonal mating and LMC. This possibility is more plausible for more fecund clones, but outbreeding is predicted for less fecund clones. We hypothesize that clones that are more fecund will gain higher fitness returns by reducing investment in males because of more intense LMC among clonal males. We tested this hypothesis by elucidating the clonal sex allocation patterns of the galling aphid Kaltenbachiella japonica, in which inbreeding and LMC appear to be common. Winged mothers that emerge from a gall, belonging to the same clone, produced males and sexual females asexually on a branch, without dispersing to other trees. The heavier the gall, the more winged mothers were produced from the gall. Individual mothers produced a constant number of males and a variable number of females. The clonal sex allocation to males was 39.8 %, on average, and decreased with increasing gall weight. This result showed that clones that were more fecund exhibited more female-biased sex allocation and thus supported our hypothesis. Furthermore, our results corroborated Stubblefield and Seger’s hypothesis for sex allocation in patch structure rather than Yamaguchi’s constant male hypothesis. We conclude that K. japonica clones are able to adjust their sex allocation patterns adaptively depending on the quality of resources in the galls.

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.

Sex ratio manipulation by ovipositing females was surveyed in 3 solitary ecto- parasitic wasp species, Dinarmus basal& (Pteromalidae), Anisopteromalus calandrae (Pteromalidae), and Heterospilus prosopidis (Braconidae), that parasitize azuki bean weevil (Callosobruchus chinensis (L) (Coleoptera: Buruchidae)) larvae within azuki beans (Vigna angular&). Variables were local mate competition (LMC) and host quality (HQ). We used host age as a measure of host quality (from 9- to 16-day-old hosts), changed the number of ovipositing females to control the level of local mate competition (1 female and 10 females), and examined oviposition patterns of the wasps. The offspring sex ratios (proportion of females) of the 3 wasp species respond qualitatively same to HQ and LMC. The common qualitative tendency among the 3 species is an increase of sex ratios increase with host age. In the process of changing the sex ratio (9- 13-day-old) 3 wasp species respond only to HQ. In the hosts that end development in size (14-16-day-old) wasps respond to LMC. The response of sex ratio change to LMC in the old host age- classes are different among the 3 species. In the situation that there exists LMC (10 females) sex ratios are the same among the 3 wasps. However, the sex ratios in no LMC (single female) are heterogeneous among the 3 wasps.

While simultaneous hermaphroditism occurs in most animal phyla, theories for its adaptive significance remain untested. Sex allocation theory predicts that combined sexes are favored in sedentary and sessile organisms because localized gamete dispersal and local mate competition (LMC) among gametes promote decelerating fitness "gain curves" that relate male investment to reproductive success. Under this LMC model, males fertilize all locally available eggs at low sperm output, additional output leads to proportionally fewer fertilizations, and combined sexes with female-biased sex allocation are favored. Decelerating male gain curves have been found in hermaphroditic flowering plants, but the present paper reports the first analysis in an animal. The colonial hermaphroditic bryozoan Celleporella hyalina forms unisexual male and female zooids that can be counted to estimate absolute and relative gender allocations. I placed "sperm donor" colonies-each with different numbers of male zooids, and each homozygous for diagnostic allozyme alleles-among target maternal colonies on field mating arrays, and estimated donor fertilization success by scoring allozyme markers in target-colony progeny. Fertilization success increased with numbers of donor male zooids, but linear and not decelerating curves fit the data best. Mean sex allocation was not female biased, consistent with nondecelerating male gain. Sperm donors, moreover, did not monopolize matings as expected under high LMC, but rather shared paternity with rival colonies. Hence localized water-borne gamete dispersal alone may not yield decelerating male gain and favor the maintenance of hermaphroditism; relaxed sperm competition in low density populations might also be required. In free-spawning marine organisms, males cannot control access to fertilizations, intense sperm competition may be commonplace, and high male sex allocation may be selected to enhance siring success under competition.

Sex allocation theory offers excellent opportunities for testing how animals adjust their behaviour in response to environmental conditions. A major focus has been on instances of local mate competition (LMC), where female-biased broods are produced to maximise mating opportunities for sons. However, the predictions of LMC theory can be altered if there is both local competition for resources during development and an asymmetry between the competitive abilities of the sexes, as has been seen in animals ranging from wasps to birds. In this paper, we test the extent to which asymmetric larval competition alters the predictions of LMC theory in the parasitoid wasp Nasonia vitripennis. We found that the body size of both sexes was negatively correlated with the number of offspring developing within the host. Further, we found that when faced with high levels of competition, the body size of females, but not males, was influenced by the sex ratio of the competing offspring; females were smaller when a higher proportion of the brood was female. This asymmetric competition should favour less biased sex ratios than are predicted by standard LMC theory. We then develop a theoretical model that can be parameterised with our data, allowing us to determine the quantitative consequences of the observed level of asymmetric larval competition for sex allocation. We found that although asymmetric competition selects for less biased sex ratios, this effect is negligible compared to LMC. Furthermore, a similar conclusion is reached when we re-analyse existing data from another parasitoid species where asymmetric larval competition has been observed; Bracon hebetor. Consequently, we suspect that asymmetric larval competition will have its greatest influence on sex ratio evolution in species that have smaller clutches and where local mate competition is not an issue, such as birds and mammals.

Sex-ratio adjustments are commonly observed in haplodiploid species. However, the underlying proximate mechanisms remain elusive. We investigated these mechanisms in Tetranychus urticae, a haplodiploid spider mite known to adjust sex ratio in response to the level of local mate competition (LMC). In this species, egg size determines fertilization probability, with larger eggs being more likely to be fertilized, and thus become female. We explored the hypothesis that sex-ratio adjustment is achieved through adjustment of egg size. By using spider mites from a large population, we found that females produced not only a higher proportion of daughters under high levels of LMC, but also larger eggs. Moreover, in populations experimentally evolving under varying levels of LMC, both the proportion of females and the egg size increased with LMC intensity. These results suggest that sex-ratio adjustment in spider mites is mediated by egg size, although the causal relationship remains to be tested.

Sex ratio theory has proved remarkably useful in testing the adaptive nature of animal behavior. A particularly productive area in this respect is Hamilton's theory of local mate competition (LMC), which has been extended in numerous directions to include greater biological realism, allowing more detailed tests in specific organisms. We have presented one such extension, termed asymmetrical LMC, which occurs when egg laying by females on a patch is asynchronous, and emerging males do not disperse, resulting in the extent of LMC on a patch varying over time. Our aim here is to test whether the parasitoid wasp Nasonia vitripennis responds to variation in the degree of asymmetrical LMC. Specifically, we show that females adjust their offspring sex ratios in response to (1) variation in the amount of asynchrony in emergence between broods on a patch and (2) the number and proportion of previously parasitized hosts on the patch. Our results provide qualitative support for the predictions of theory, suggesting new levels of complexity in the sex ratio behavior of this much-studied organism. However, our results do not always provide quantitative support for theory, suggesting further complexities that must be clarified.

Host‐size related feeding and oviposition behaviour, and allocation of progeny sex by Anisopteromalus calandrae (Howard) were tested on Sitophilus oryzae L. The parasitoid showed a host‐size‐dependent partition of feeding and oviposition behaviour, preferring small hosts for feeding, but large hosts for oviposition. Neither the mutual interference nor the host density showed any effect on the behaviour of the parasitoid. Allocation of progeny sex by the female parasitoid appeared to be based more likely on absolute than on relative host size encountered. A model for the progeny sex ratio was constructed based on: (1) ovipositional preference of the parasitoid on large hosts; (2) feeding preferentially on small hosts; and (3) host‐size‐related regulation of progeny sex ratio. The progeny sex ratio of the parasitoid predicted by the model was in close agreement with the observed value.

It is well recognized that sex allocation strategies can be influenced by sexual selection, when females adjust offspring sex ratios in response to their mates' attractiveness. Yet the reciprocal influence of strategic sex allocation on processes of sexual selection has only recently been revealed. Recent theoretical work demonstrates that sex allocation weakens selection for female preferences, leading to the decline of male traits. However, these results have been derived assuming that females have perfect knowledge of mate attractiveness and precise control over cost-free allocation. Relaxing these assumptions highlights the importance of another feedback: that adaptive sex allocation must become difficult to maintain as traits and preferences decline. When sex allocation strategies erode not only traits and preferences but also their own selective advantage, predictions can no longer be expressed as a simple linear correlation between ornament exaggeration and adaptive sex allocation. Instead, strongest sex ratio biases may be found at intermediate trait levels.

Parents may adapt their offspring sex ratio in response to their own phenotype and environmental conditions. The most significant causes for adaptive sex-ratio variation might express themselves as different distributions of fitness components between sexes along a given variable. Several causes for differential sex allocation in raptors with reversed sexual size dimorphism have been suggested. We search for correlates of fledgling sex in an extensive dataset on common buzzards Buteo buteo, a long-lived bird of prey. Larger female offspring could be more resource-demanding and starvation-prone and thus the costly sex. Prominent factors such as brood size and laying date did not predict nestling sex. Nonetheless, lifetime sex ratio (LSR, potentially indicative of individual sex allocation constraints) and overall nestling sex were explained by territory quality with more females being produced in better territories. Additionally, parental plumage morphs and the interaction of morph and prey abundance tended to explain LSR and nestling sex, indicating local adaptation of sex allocation However, in a limited census of nestling mortality, not females but males tended to die more frequently in prey-rich years. Also, although females could have potentially longer reproductive careers, a subset of our data encompassing full individual life histories showed that longevity and lifetime reproductive success were similarly distributed between the sexes. Thus, a basis for adaptive sex allocation in this population remains elusive. Overall, in common buzzards most major determinants of reproductive success appeared to have no effect on sex ratio but sex allocation may be adapted to local conditions in morph-specific patterns.

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