Effect of host density on offspring sex ratios and behavioral interactions between females in the parasitoid waspNasonia vitripennis (Hymenoptera: Pteromalidae)

Pairs of females of the parasitoid waspNasonia vitripennis were videotaped with one or two hosts. The presence of an additional host decreased the number of interactions between females but had no measured effect on the nature of the interactions, i.e., on whether the interaction involved physical contact or occurred while one of the females was parasitizing a host. The number of hosts did not itself affect offspring sex ratios but did influence which other factors were correlated with sex ratio. When there was one host, the proportion of sons was more positively correlated with utilization of previously drilled holes than with female-female interactions, whereas when there were two hosts, the reverse was true. Parasitizing an already parasitized host appeared to affect a female's sex ratio beyond any effects of the physical presence of another female: When two hosts were present, the proportion of sons was greater from hosts parasitized by both females than from hosts parasitized by only one female. The observation that parasitizations in previously drilled holes and female-female interactions are correlated with sex ratios is consistent with previous studies; however, that these relationships are host density dependent is a new result and remains unexplained.     

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.     

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

1. Neonicotinoid insecticides are potent neurotoxins of significant economic importance. However, it is clear that their use can adversely impact beneficial insects in the environment, even at low, sub‐lethal doses. 2. It has recently been shown that the neonicotinoid imidacloprid disrupts adaptive sex allocation in the parasitoid wasp Nasonia vitripennis (Walker) by limiting their ability to respond to the presence of other females on oviposition patches. In the present study, that work was extended to explore whether sex allocation when superparasitising – laying eggs on a host that has already been parasitised – is also disrupted by imidacloprid. 3. Under superparasitism, sex allocation theory predicts that females should vary their offspring sex ratio in relation to their relative clutch size. It was found that sex allocation under superparasitism in Nasonia is disrupted in a dose‐dependent manner, with exposed females producing more daughters. 4. Importantly, imidacloprid does not appear to influence the ability of females to estimate the number of eggs already present on a host, suggesting a disassociation between the sex ratio and clutch size cues. 5. The present work highlights the fitness costs to beneficial insects of exposure to neonicotinoids, but also provides clues as to how female Nasonia use information when allocating sex.     

Reproductive strategies under multiparasitism in natural populations of the parasitoid wasp Nasonia (Hymenoptera)

Parasitoid Nasonia wasps adjust their progeny sex ratio to the presence of conspecifics to optimize their fitness. Another trait under female control is the induction of offspring diapause. We analysed progeny sex ratios and the proportion of diapausing offspring of individual Nasonia females in host patches parasitized by two species, Nasonia vitripennis and Nasonia giraulti, in North American field populations using microsatellite fingerprinting. Both Nasonia species produced similar sex ratios on hosts that were co‐parasitized by their own species as by the other species, indicating that females do not distinguish between con‐ and heterospecific clutches. The sex ratios of the diapause and adult fractions of mixed broods from single females were not correlated. We found further indications that N. vitripennis females take the emergence time of the offspring into account in their sex allocation. The reproductive strategies of Nasonia under multiparasitism are largely adaptive, but also partially constrained by information.     

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.     

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.     

Flight activity in the parasitoid waspNasonia vitripennis (Hymenoptera: Pteromalidae)

Flight activity in females of the parasitoid wasp Nasonia vitripennis(Walker) was examined by measuring still-air tethered flight. There was a large amount of variation among females in flight duration. The longest single flight (with no pauses of more than 5 s) was more than 2 h long. Mating status had a significant and large effect on flight: mated females flew twice as long as virgin females. There also was a slight but significant effect of age on flight, with 3-day-old females being less likely to fly than 1-day-old females. Flight duration was not affected by prior exposure to other females, to honey, or to a low or a high host density.     

The quantitative genetic basis of sex ratio variation in Nasonia vitripennis: a QTL study

Our understanding of how natural selection should shape sex allocation is perhaps more developed than for any other trait. However, this understanding is not matched by our knowledge of the genetic basis of sex allocation. Here, we examine the genetic basis of sex ratio variation in the parasitoid wasp Nasonia vitripennis, a species well known for its response to local mate competition (LMC). We identified a quantitative trait locus (QTL) for sex ratio on chromosome 2 and three weaker QTL on chromosomes 3 and 5. We tested predictions that genes associated with sex ratio should be pleiotropic for other traits by seeing if sex ratio QTL co-occurred with clutch size QTL. We found one clutch size QTL on chromosome 1, and six weaker QTL across chromosomes 2, 3 and 5, with some overlap to regions associated with sex ratio. The results suggest rather limited scope for pleiotropy between these traits.     

The mechanism of sex ratio adjustment in a pollinating fig wasp

Sex ratio strategies in species subject to local mate competition (LMC), and in particular their fit to quantitative theoretical predictions, provide insight into constraints upon adaptation. Pollinating fig wasps are widely used in such studies because their ecology resembles theory assumptions, but the cues used by foundresses to assess potential LMC have not previously been determined. We show that Liporrhopalum tentacularis females (foundresses) use their clutch size as a cue. First, we make use of species ecology (foundresses lay multiple clutches, with second clutches smaller than first) to show that increases in sex ratio in multi-foundress figs occur only when foundresses are oviposition site limited, i.e. that there is no direct response to foundress density. Second, we introduce a novel technique to quantify foundress oviposition sequences and show, consistent with the theoretical predictions concerning clutch size-only strategies, that they produce mainly male offspring at the start of bouts, followed by mostly females interspersed by a few males. We then discuss the implications of our findings for our understanding of the limits of the ability of natural selection to produce 'perfect' organisms, and for our understanding of when different cue use patterns evolve.     

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.     

Competition between relatives and the evolution of dispersal in a parasitoid wasp

Evolutionary theory predicts that levels of dispersal vary in response to the extent of local competition for resources and the relatedness between potential competitors. Here, we test these predictions by making use of a female dispersal dimorphism in the parasitoid wasp Melittobia australica. We show that there are two distinct female morphs, which differ in morphology, pattern of egg production, and dispersal behaviour. As predicted by theory, we found that greater competition for resources resulted in increased production of dispersing females. In contrast, we did not find support for the prediction that high relatedness between competitors increases the production of dispersing females in Melittobia. Finally, we exploit the close links between the evolutionary processes leading to selection for dispersal and for biased sex ratios to examine whether the pattern of dispersal can help distinguish between competing hypotheses for the lack of sex ratio adjustment in Melittobia.     

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.