Combined effects of host quality and local mate competition on sex allocation inLariophagus distinguendus

Summary 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.     

Sex ratios under asymmetrical local mate competition in the parasitoid wasp Nasonia vitripennis

Sex ratio theory has proved remarkably useful in testing theadaptive nature of animal behavior. A particularly productivearea in this respect is Hamilton's theory of local mate competition(LMC), which has been extended in numerous directions to includegreater biological realism, allowing more detailed tests inspecific organisms. We have presented one such extension, termedasymmetrical LMC, which occurs when egg laying by females ona 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 Nasoniavitripennis responds to variation in the degree of asymmetricalLMC. Specifically, we show that females adjust their offspringsex ratios in response to (1) variation in the amount of asynchronyin emergence between broods on a patch and (2) the number andproportion of previously parasitized hosts on the patch. Ourresults provide qualitative support for the predictions of theory,suggesting new levels of complexity in the sex ratio behaviorof this much-studied organism. However, our results do not alwaysprovide quantitative support for theory, suggesting furthercomplexities that must be clarified.     

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.     

Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

Sexual selection theory asserts that females are well adapted to sense signals indicating the quality of potential mates. One crucial male quality parameter is functional fertility (i.e. the success of ejaculates in fertilizing eggs). The phenotype-linked fertility hypothesis (PLFH) predicts that functional fertility of males is reflected by phenotypic traits that influence female mate choice. Here, we show for Nasonia vitripennis, a parasitic wasp with haplodiploid sex determination and female-biased sex ratios, that females use olfactory cues to discriminate against sperm-limited males. We found sperm limitation in newly emerged and multiply mated males (seven or more previous matings) as indicated by a higher proportion of sons in the offspring fathered by these males. Sperm limitation correlated with clearly reduced pheromone titres. In behavioural bioassays, females oriented towards higher doses of the synthetic pheromone and were attracted more often to scent marks of males with a full sperm load than to those of sperm-limited males. Our data support the PLFH and suggest that N. vitripennis females are able to decrease the risk of getting constrained to produce suboptimal offspring sex ratios by orienting towards gradients of the male sex pheromone.     

Sex allocation by a mite parasitic on insects: local mate competition,host quality and operational sex ratio

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.     

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.     

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.     

Female dispersal and isolation-by-distance of Nasonia vitripennis populations in a local mate competition context

Dispersal behavior directly influences the level of inbreeding, but the effect of inbreeding avoidance on dispersal is less well studied. The parasitoid wasp Nasonia vitripennis (Walker) (Hymenoptera: Chalcidoidea: Pteromalidae) is known to mate exclusively on the natal patch, and females are the only dispersing sex. A previous study has shown that foundresses on a patch are typically unrelated, implying that females disperse for a considerable distance from their natal patch after mating. We investigated dispersal of N. vitripennis on two scales. On a local scale we used a mark-release-recapture experiment, and on the larger scale we investigated isolation by distance using a population genetic approach. We found that N. vitripennis females are long-distance dispersers, capable of covering at least 2 km in 48 h. Populations within a range of 100 km showed no substructure, but larger distances or major geographical barriers restricted gene flow and led to significant population structure. The results provide a basis for future research on dispersal of parasitoids and are discussed in the context of dispersal abilities and inbreeding avoidance in Nasonia .     

Female-biased sex ratios under local mate competition: An experimental confirmation

Summary Experimental work of Nadel and Luck (1992) on a chalcidoid wasp provides a confirmation of sex ratio theory under local mate competition.     

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.     

Host choice decisions in the polyembryonic wasp Copidosoma koehleri (Hymenoptera: Encyrtidae)

Female parasitoids often reject hosts of poor quality, where the survival and fitness of their offspring are expected to be low. In polyembryonic parasitoid wasps, a clone of genetically identical embryos develops from one egg in a host. In the wasp Copidosoma koehleri, each female clone produces one soldier larva that attacks competing clones inside the host. Aggression by soldiers is directed usually towards unrelated clones. Accordingly, it may be predicted that females will prefer nonparasitized over parasitized hosts, especially if the latter have been parasitized previously by a mated unrelated female, as a result of the reduced chances of survival for their offspring inside these hosts. In accordance with these predictions, females prefer nonparasitized hosts over self‐parasitized hosts when they are presented simultaneously. By contrast to the predictions, females prefer hosts parasitized by an unrelated conspecific over nonparasitized hosts when presented simultaneously. Females do not distinguish hosts parasitized by conspecifics from self‐parasitized hosts when presented simultaneously. They reject self‐parasitized hosts significantly more often than hosts parasitized by conspecifics when each host type is presented alone. Females faced with two previously parasitized hosts are not affected in their choice by the mating status (i.e. virgin or mated) of the previous parasitizing females. The combined results suggest that females are limited in their ability to assess the risk that their offspring will be attacked by a soldier, or that this risk is balanced by the relative advantages of ovipositing in a host parasitized by conspecifics. A possible advantage may be increased out‐breeding opportunities for the emerging offspring.     

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.     

Genetic structure of natural Nasonia vitripennis populations: validating assumptions of sex-ratio theory

The parasitic wasp Nasonia vitripennis has been used extensively in sex allocation research. Although laboratory experiments have largely confirmed predictions of local mate competition (LMC) theory, the underlying assumptions of LMC models have hardly been explored in nature. We genotyped over 3500 individuals from two distant locations (in the Netherlands and Germany) at four polymorphic microsatellite loci to validate key assumptions of LMC theory, in terms of both the original models and more recent extensions to them. We estimated the number of females contributing eggs to patches of hosts and the clutch sizes as well as sex ratios produced by individual foundresses. In addition, we evaluated the level of inbreeding and population differentiation. Foundress numbers ranged from 1 to 7 (average 3.0 ± 0.46 SE). Foundresses were randomly distributed across the patches and across hosts within patches, with few parasitizing more than one patch. Of the hosts, 40% were parasitized by more than one foundress. Clutch sizes of individual foundresses (average 9.99 ± 0.51 SE) varied considerably between hosts. The time period during which offspring continued to emerge from a patch or host correlated strongly with foundress number, indicating that sequential rather than simultaneous parasitism is the more common. Genetic differentiation at the regional level between Germany and the Netherlands, as estimated by Slatkin's private allele method (0.11) and Hedrick's corrected G' _LT (0.23), indicates significant substructuring between regions. The level of population inbreeding for the two localities ( F _IL = 0.168) fitted the expectation based on the average foundress number per patch.     

Sex ratio manipulation by the parasitoid waspSpalangia cameroni in response to host age: A test of the host-size model

Summary A sex ratio response to host resources as measured by external host dimensions has been demonstrated in many parasitoid wasps, includingSpalangia cameroni. The responses generally are in the direction predicted by sex ratio theory, specifically the host-size models. Here I show that femaleS. cameroni also respond to differences in resource availability not associated with changes in external host dimensions, and this response is in the direction predicted by host-size models. When given old and young hosts simultaneously, femaleS. cameroni oviposit a greater proportion of sons in old than in young host pupae, at least for 0-day old versus 3-day old hosts. Old hosts weigh less than young hosts but are not significantly different in external width. Thus it appears that the offspring sex ratio response may result from mothers detecting physical or chemical changes within the host which are associated with host age. No evidence is found that the manipulation in response to host age has been selected for via an effect of host age on wasp size; there was no significant effect of host age on either male of female wasp size. A second prediction of the host-size models is also supported by this study: when each female is presented with only a single host age, rather than two host ages simultaneously, host age has no effect on offspring sex ratio.     

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.     

Do female parasitoid wasps recognize and adjust sex ratios to build cooperative relationships?

Sex allocation theories provide excellent opportunities to investigate not only the extent to which individuals' behaviour is adaptive, but also how they use relevant information for their decision-making. Here, we investigated whether female parasitoid wasps recognize the sex ratios of other females and adjust their laying sex ratios accordingly. Specifically, we tested the prediction of reciprocal cooperation over sex allocation. Theory predicts more female-biased (cooperative) sex ratios than in the interest of individual benefit, when a restricted number of ovipositing females interact for a long period and their offspring mate within the natal patch. This is because the female-biased sex ratio reduces competition for mates among the male offspring of the females and increases the overall reproductive productivity of the patch. In this case, females would be expected to respond to more even (noncooperative) sex ratios by others and to retaliate by also producing a less female-biased sex ratio to avoid exploitation by defectors. However, contrary to this prediction, our experiment using a sterile male technique showed that female Melittobia australica did not change their offspring sex ratios in response to the sex ratios produced by other females. This suggests that their extremely female-biased sex ratios cannot be explained by reciprocity. A meta-analysis of studies examining sex recognition ability in parasitoid wasps also did not support the predicted pattern of relevant sex ratio adjustment, suggesting that parasitoid females do not possess this ability. Here, we discuss the conditions necessary for the evolution of reciprocity linked to recognition ability.     

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.     

To mate or not to mate,and subsequent host search by a haplodiploid female parasitoid wasp

Mated females of haplodiploid species can vary the sex ratio of their offspring, but virgin or sperm‐depleted females can produce only males. Depending on the costs and benefits, the theory of constrained sex allocation states that female haplodiploids may vary in their propensity to mate, with important implications for the populations’ sex ratio. Unmated female parasitoid wasps Alabagrus texanus (Braconidae) have been observed to reject matings with males, even under highly confined spatial conditions. We performed field trials to determine whether unmated female A. texanus would mate. We then compared the preferences of the resulting unmated (constrained) and mated (unconstrained) female wasps for shelters constructed and occupied by their hosts, fern moth caterpillars Herpetogramma theseusalis (Crambidae) on fern fronds. We presented the wasps with pairs of shelters collected from the field that differed in size, as well as freshness, fern species, and presence or absence of caterpillars. Unconstrained females searched small shelters more frequently than did constrained females and tended to favor senesced (old) shelters over fresher ones. They did not differ in choice between shelters on marsh and sensitive ferns or between shelters containing caterpillars and empty shelters. The preference for small shelters by the unconstrained wasps may enhance their rate of contacting favorable hosts, but the foraging regime of the constrained females should expose them to caterpillars at sites infrequently searched by the unconstrained females.     

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.