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.     

Variable host quality, life-history invariants, and the reproductive strategy of a parasitoid wasp that produces single sex clutches

The parasitic wasp Achrysocharoides zwoelferi (Hymenoptera, Eulophidae) produces clutches consisting of only one sex. Moreover,male clutch size is invariably one while female clutches arein the range one to four. We designed field experiments todetermine the effect of host quality on clutch composition.We found that solitary male and solitary female clutches werereared from the same size mines, and that larger mines tendedto produce gregarious female clutches. A higher proportionof male clutches were placed in older hosts, despite theirlarge size. Variation in body size, both between and withinclutches, was measured in order to test the predictions of models that take into account the constraint that clutch size is aninteger trait, something of potential importance when absoluteclutch size is low. Our data supported several predictionsof these models, including the trade-off-invariant rule foroptimal offspring size developed by Charnov and Downhower.However, while most invertebrate clutch size models assume equal resource share among members of the same clutch, we found anincrease in inequality in larger clutches.     

Fitness consequences of ovicide in a parasitoid wasp

Ovicide, superparasitism and host rejection are alternative reproductive tactics facing female parasitoid wasps encountering an already-parasitized host. Superparasitism is simply the addition of an egg or a clutch of eggs by the secondary parasitoid, but under ovicide the primary clutch is removed or destroyed. Host rejection occurs if the wasp leaves without laying a clutch. The ectoparasitoid Laelius pedatus (Say) (Hymenoptera: Bethylidae) performs ovicide in this situation. Clutch manipulation experiments show that secondary clutches suffer high mortality in competition with primary clutches, which increases with increasing time delay between clutches. Primary clutches however suffer little in competition with secondary clutches, even if there is minimal time delay between clutches. These data suggest that the offspring of ovicidal females are substantially fitter than the offspring of superparasitizing females. Handling time and clutch size do not differ significantly between first (sole) parasitoids and second (ovicidal) parasitoids. The same is true for offspring survival and development time. However, offspring of second females are slightly smaller. This suggests that parasitized and unparasitized hosts are resources of similar quality when ovicide is performed. These data strongly support the predictions of evolutionary models of ovicide. They may also give some insight into the taxonomic distribution of ovicide in parasitoids.     

How two different host species influence the performance of a gregarious parasitoid: host size is not equal to host quality

1. Hyssopus pallidus Askew (Hymenoptera, Eulophidae) is a gregarious ectoparasitoid of the two tortricid moths species Cydia molesta Busck and C. pomonella L. (Lepidoptera, Tortricidae). It paralyses and parasitizes different larval instars of both species inside the apple fruit, which leads to the death of the caterpillar. 2. We assessed the influence of host species characteristics and host food on the performance of the parasitoid female in terms of clutch size decisions and fitness of the F(1) generation. 3. A comparison of clutch size revealed that female parasitoids deposited similar numbers of eggs on the comparatively smaller C. molesta hosts as on the larger C. pomonella hosts. The number of parasitoid offspring produced per weight unit of host larva was significantly higher in C. molesta than in C. pomonella, which is contrary to the general prediction that smaller hosts yield less parasitoid offspring. However, the sex ratio was not influenced by host species that differed considerably in size. 4. Despite the fact that less host resources were available per parasitoid larva feeding on C. molesta caterpillars, the mean weight of emerging female wasps was higher in the parasitoids reared on C. molesta. Furthermore, longevity of these female wasps was neither influenced by host species nor by the food their host had consumed. In addition we did not find a positive relationship between adult female weight and longevity. 5. Parasitoid females proved to be able to assess accurately the nutritional quality of an encountered host and adjust clutch size accordingly. These findings indicate that host size is not equal to host quality. Thus host size is not the only parameter to explain the nutritional quality of a given host and to predict fitness gain in the subsequent generation.     

Body size, host choice and sex allocation in a spider-hunting pompilid wasp

Two important relationships in parasitoid evolutionary ecology are those between adult size and fitness and between host quality and sex ratio. Sexually differential size–fitness relationships underlie predicted sex-ratio relationships. Despite each relationship receiving considerable attention, they have seldom been studied simultaneously or using field data. Here we report the biology of Anoplius viaticus paganu s Dahlbom, a little known parasitoid of spiders, using field and laboratory data. We found that larger foraging females were able to select larger host spiders from the field, thus identifying a relatively novel component of the size–fitness relationship. Larger offspring developed from larger hosts and, in agreement with the prediction of the host quality model of sex allocation, were generally female. Data on the size–fitness relationship for males are lacking and, in common with many prior studies, we could not evaluate sexually differential size–fitness relationships as an explanation for the observed sex-ratio patterns. Nonetheless, A. v. paganu s exhibited one of the strongest relationships between host size and offspring sex ratio yet reported.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 87 , 285–296.     

The influence of female age and host size on the sex ratio of the parasitoid Opius concolor

The sex ratio of the progeny of single females parasitizing large hosts favoured the females (sex ratio=0.26); but on small hosts favoured the males (0.73). No differences in mortality of the sexes were detected. The sex ratio was independent of female age when large hosts were used. The percentage of males observed in the progeny of the first day of female oviposition was significantly greater than the mean, irrespective of the age at which female oviposition began. When females were exposed to small hosts, a greater percentage of females was observed in the progeny from the last days of oviposition.

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Résumé L'influence de la taille de l'hôteret de l'âge de la femelle sur le taux sexuel de la descendance a été étudiée sur le parasitoïde Opius concolor Szépl.Le taux sexuel de la descendance des femelles isolées est favorable aux femelles (t.s.=0,26) quand elles ont à leur disposition des hôtes de grande taille, tandis qu'avec des hôtes petits le taux sexuel est favorable aux mâles (t.s.=0.73). On n'a pas détecté de mortalité différentielle des sexes.Les pourcentage de mâles obtenu le premier jour de ponte des femelles sur les hôtes de grande taille est significativement différent de la moyenne, indépendamment de l'âge de la femelle à ce moment. Cependant, sur des hôtes petits, bien que restant favorable aux mâles dans l'ensemble, une plus grande proportion de femelles à partir des premiers jours de ponte a pu être observée.

     

Constrained sex allocation in a parasitoid due to variation in male quality

The theory of constrained sex allocation posits that when a fraction of females in a haplodiploid population go unmated and thus produce only male offspring, mated females will evolve to lay a female-biased sex ratio. I examined evidence for constrained sex ratio evolution in the parasitic hymenopteran Uscana semifumipennis. Mated females in the laboratory produced more female-biased sex ratios than the sex ratio of adults hatching from field-collected eggs, consistent with constrained sex allocation theory. However, the male with whom a female mated affected her offspring sex ratio, even when sperm was successfully transferred, suggesting that constrained sex ratios can occur even in populations where all females succeed in mating. A positive relationship between sex ratio and fecundity indicates that females may become sperm-limited. Variation among males occurred even at low fecundity, however, suggesting that other factors may also be involved. Further, a quantitative genetic experiment found significant additive genetic variance in the population for the sex ratio of offspring produced by females. This has only rarely been demonstrated in a natural population of parasitoids, but is a necessary condition for sex ratio evolution. Finally, matings with larger males produced more female-biased offspring sex-ratios, suggesting positive selection on male size. Because the great majority of parasitic hymenoptera are monandrous, the finding of natural variation among males in their capacity to fertilize offspring, even after mating successfully, suggests that females may often be constrained in the sex allocation by inadequate number or quality of sperm transferred.     

Effects of spontaneous mutation accumulation on sex ratio traits in a parasitoid wasp

Sex allocation theory has proved extremely successful at predicting when individuals should adjust the sex of their offspring in response to environmental conditions. However, we know rather little about the underlying genetics of sex ratio or how genetic architecture might constrain adaptive sex-ratio behavior. We examined how mutation influenced genetic variation in the sex ratios produced by the parasitoid wasp Nasonia vitripennis. In a mutation accumulation experiment, we determined the mutability of sex ratio, and compared this with the amount of genetic variation observed in natural populations. We found that the mutability (h(2)(m)) ranges from 0.001 to 0.002, similar to estimates for life-history traits in other organisms. These estimates suggest one mutation every 5-60 generations, which shift the sex ratio by approximately 0.01 (proportion males). In this and other studies, the genetic variation in N. vitripennis sex ratio ranged from 0.02 to 0.17 (broad-sense heritability, H(2)). If sex ratio is maintained by mutation-selection balance, a higher genetic variance would be expected given our mutational parameters. Instead, the observed genetic variance perhaps suggests additional selection against sex-ratio mutations with deleterious effects on other fitness traits as well as sex ratio (i.e., pleiotropy), as has been argued to be the case more generally.     

Adaptiveness of sex ratio control by the pupal parasitoid Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size

Adaptiveness of sex ratio control by the solitary parasitoid wasp Itoplectis naranyae (Hymenoptera: Ichneumonidae) in response to host size was studied, by examining whether differential effects of host size on the fitness of resulting wasps are to be found between males and females. The offspring sex ratio (male ratio) decreased with increasing host size. Larger hosts yielded larger wasps. Male larvae were less efficient in consuming larger hosts than female larvae. No significant interaction in development time was found between parasitoid sex and host size. Larger female wasps lived longer than smaller females, while longevity of male wasps did not increase with increasing wasp size. Smaller males were able to mate either with small or with large females, while larger males failed to mate with small females. Larger female wasps had a greater number of ovarioles and mature eggs at any one time than smaller females, although the number of eggs produced per host-feeding was not influenced by female wasps. Thus, the differential effect of host size on the fitness of males and females exists in I. naranyae. The basic assumption of the host-size model was therefore satisfied, demonstrating that sex ratio control by I. naranyae in response to host size is adaptive.     

Host size induced variation in progeny sex ratio of an aphid parasitoid Lysiphlebia mirzai

A study aimed at determining the effect of host size on the pattern of sex allocation by an aphid parasitoid Lysiphlebia mirzai Shuja-Uddin (Hymenoptera: Braconidae: Aphidiinae) was undertaken to test the validity of the following three hypotheses: (1) larger hosts will yield a greater proportion of daughters, (2) differential mortality of the sexes of the parasitoid during development is a function of host-size, and (3) daughters emerging from larger hosts are more fecund. The results suggested a propensity in the parasitoid to deposit fertilised (diploid) eggs in large hosts (third instar nymph) and unfertilised (haploid) eggs in small hosts (first and second instar nymphs). Unpreferred fourth instar nymphs and apterous aphid adults also received more haploid eggs despite being larger in size than the preferred third instar nymphs. However, the perception of host size by the mother was dependent on the extent of temporal variation in the host size distribution and on her previous experience of host size. Developmental period, longevity, mating potential, fecundity and progeny sex ratio of L. mirzai emerging from small versus large hosts indicated that the host size affected the fitness of the daughters more than that of sons. No differential mortality of the sexes during development of L. mirzai was observed in small versus large hosts. This shows that L. mirzai, while ovipositing in growing stages of the host, adjusts progeny sex ratio according to the host size and by doing so she tends to contribute maximally to progeny fitness without knowing about the future host quality.     

Host Age Response in the Parasitoid Wasp Spalangia cameroni (Hymenoptera: Pteromalidae)

Female Spalangia cameroni produced more offspring from younger house fly pupae, both when given a choice of host ages and when not given a choice. Host age did not affect offspring survivorship. Offspring were larger when they had developed on younger hosts and the effect was independent of offspring sex. Having previously parasitized old hosts versus young hosts did not reduce a female's production of offspring in subsequent hosts. Females distinguished between young and old hosts both in the light and in the dark. Females did not distinguish between host ages prior to physical contact with the host but could distinguish by the time they first began exploring a host by tapping it with their antennae; thus, they could distinguish before drilling into a host.     

Brood sex ratios of the solitary parasitoid wasp, Coccophagus atratus

Abstract.

• 1 Female eggs of Coccophagus atratus are deposited within the haemolymph of coccoid scale insects. Male eggs are deposited on to late larval and prepupal stages of parasitoids of scale insects, including conspecifics.
• 2 When presented with either one host type or a combination of both host types, female C.atratus deposit all their available eggs, assigning the appropriate sex egg to each host encountered. Brood sizes are not adjusted for different combinations of hosts.
• 3 Behavioural observations show that females do not move away from patches of hosts until all their eggs are laid, regardless of the host type.
• 4 Brood sex ratios varied with changes in the relative availability of hosts for males and hosts for females. When both host-types were present in equal numbers, male biased sex ratios resulted (mean ±SEM =0.71 ± 0.009) and when 70% of hosts provided were suitable for female eggs, mostly female-biased sex ratios resulted (mean ± SEM = 0.37±0.01).
• 5 Our results do not fit predictions based on the assumption that a sex ratio of 0.5 should be expected in C.atratus. Observed sex ratios indicate that the unusual life histories of these parasitoids need to be taken into account in explanations of their sex ratios.

     

Fitness consequences of superparasitism and mechanism of host discrimination in the stemborer parasitoid Cotesia flavipes

The fitness consequences of superparasitism and the mechanism of host discrimination in Cotesia flavipes, a larval parasitoid of concealed stemborer larvae was investigated. Naive females readily superparasitized and treated the already parasitized host as an unparasitized host by allocating the same amount of eggs as in an unparasitized host. However, there was no significant increase in the number of emerging parasitoids from superparasitized hosts due to substantial mortality of parasitoid offspring in superparasitized hosts. Furthermore, the developmental time of the parasitoids in a superparasitized host was significantly longer than in a singly parasitized host and the emerging progeny were significantly smaller (body length and head width). Naive females entered a tunnel in which the host was parasitized 4 h previously and accepted it for oviposition. Experienced females (oviposition experience in unparasitized host) refused to enter a tunnel with a host parasitized by herself or by another female. In experiments where the tunnel and/or host was manipulated it was demonstrated that the female leaves a mark in the tunnel when she parasitizes a host. The role of patch marking in C. flavipes is discussed in relation to the ecology of the parasitoid.     

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.     

Using hosts of mixed sizes to reduce male-biased sex ratio in the parasitoid wasp, Diglyphus isaea

Overproduction of males in mass rearing of parasitic Hymenoptera contributes to higher costs for biological control because only females directly kill pests. We present a technique, based on manipulating host composition, to generate less male‐biased sex ratios in parasitoid species that adjust their sex allocation in response to relative host size. Our system consisted of chrysanthemum, Dendranthema grandiflora Tzvelev var. ‘Miramar’; a leafminer, Liriomyza langei Frick (Diptera: Agromyzidae); and a commercially available parasitoid, Diglyphus isaea (Walker) (Hymenoptera: Eulophidae). We compared the offspring sex ratios of D. isaea females presented with different compositions of L. langei larvae on chrysanthemum. Presenting individual females with only large hosts increased mean sex ratio from 32 to 67% male over 2 days. However, presenting individual females with progressively larger hosts over 1 or 2 days reduced mean sex ratio from 90 to 100% male to less than 30% male. Groups of females produced sex ratios around 58% male if presented with both plants infested by only small hosts and plants infested by only large hosts. In comparison, groups of females produced sex ratios around 48% male if presented with plants infested by both small hosts and large hosts. We compared the use of both small hosts and large hosts to only large hosts for simulated mass rearing of wasps over 8 weeks. Using both small hosts and large hosts produced similar numbers of wasps as using only large hosts, but reduced mean sex ratio of weekly cohorts from 66% male to 56% male. The two techniques produced females of similar size, but using both large hosts and small hosts produced slightly smaller males than using only large hosts. The use of both small hosts and large hosts for mass rearing of D. isaea could reduce actual costs of females by 23%.     

Costs and benefits of host feeding in the parasitoid wasp Trichogramma turkestanica

Females of the parasitoid wasp Trichogramma turkestanica Meyer (Hymenoptera: Trichogrammatidae) generally host feed after ovipositing on the first egg of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) they encounter. We measured the impact of host feeding on the fecundity and longevity of females, in absence of host or food, and on the fitness of their progeny. We also determined if the frequency of host feeding is influenced by the humidity level at which T. turkestanica females developed. Host feeding increased egg production by 70% but decreased female longevity. This impact of host feeding on the longevity of females is probably due to the allocation of carbohydrates to egg production at the expense of somatic maintenance. Humidity did not influence the occurrence or duration of host feeding. The size of individuals developing in eggs on which females host fed was smaller, indicating that their fitness was affected.     

Does time until mating affect progeny sex ratio? A manipulative experiment with the parasitoid wasp Aphelinus asychis

In haplodiploid organisms, unmated or sperm depleted females are “constrained” to produce only male progeny. If such constrained females reproduce, the population sex ratio will shift toward males and unconstrained females will be selected to produce more females. Assuming that a female's own time spent constrained is an index of the population-wide level of constrained oviposition, and that constrained and unconstrained females reproduce at the same rate, the proportion of sons that females produce when unconstrained should decrease with increasing time spent constrained. Alternatively, if females cannot measure time spent constrained or if time spent constrained is not an index to the level of constrained oviposition in the population, the proportion of sons among progeny produced when unconstrained should not depend upon time spent constrained and should be female biased to an extent depending upon the average time spent constrained over evolutionary time. To test these predictions, we manipulated the amount of time spent virgin in the parasitoid wasp Aphelinus asychis Walker (Hymenoptera: Aphelinidae) and measured the number of males and females among progeny produced before and after mating. First, we found no interaction between age and age at mating in their effect on fecundity, which suggests that mating does not change fecundity. Second, we found that females mated at 8 days and 15 days produced equal sex ratios after mating but these were slightly more female biased than the sex ratios of females mated at 1 day. This observed “step response” suggests that females may perceive time from emergence to mating as a discrete rather than a continuous variable (i.e., short versus long), or that females do not perceive time per se but assess their age class (i.e., young versus old) at the time of mating.     

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.     

Parasitoid size as a function of host sex: potential for different sex allocation strategies

Parasitoid females are known to preferentially allocate female eggs to hosts with the higher resource value, usually leading to oviposition of female eggs in larger hosts and male eggs in smaller hosts. For koinobiont parasitoids, if male and female hosts are of equal size at time of oviposition, but differ in size in later developmental stages, the sex of the host could be used to indicate future resource value. Using parasitoids of the braconid genus Asobara, which are larval parasitoids of Drosophila, it is shown that parasitoids emerging from female hosts are larger than those from male hosts. Given this difference in resource value, ovipositing females should preferentially allocate female eggs to female hosts. An alternative strategy would be to decrease the difference in resource value between male and female hosts by castrating male hosts. The primary sex ratio of A. tabida in their two main host species does not differ between male and female hosts. In contrast to A. tabida, A. citri is known to partially castrate male hosts, but this does not decrease the size difference between male and female hosts. As in A. tabida, there is no difference in sex allocation to male and female hosts in A. citri. Despite the clear difference between the resource value of male and female hosts, these parasitoid species do not seem to make optimal use of this difference. They may not be able to discriminate between host sexes or, alternatively, there is a presently unknown fitness disadvantage to ovipositing in female hosts.