Sex allocation of three solitary ectoparasitic wasp species on bean weevil larvae: Sex ratio change with host quality and local mate competition

Sex ratio manipulation by ovipositing females was surveyed in 3 solitary ectoparastic wasp species,Dinarmus basalis (Pteromalidae),Anisopteromalus calanrae (Pteromalidae), andHeterospilus prosopidis (Braconidae), that parasitize azuki bean weevil (Callosobruchus chinensis (L) (Coleoptera: Buruchidae)) larvae within azuki beans (Vigna angularis). 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 ageclasses 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.     

Putting your sons in the right place: the spatial distribution of fig wasp offspring inside figs

Abstract. 1. Pollinating fig wasps (Hymenoptera, Agaonidae) display sex ratio adjustment, producing less female‐biased combined sex ratios as the number of ovipositing females (foundresses) inside a fig increases. Because males have low mobility, the oviposition sites (galled ovules) chosen by each foundress are likely to have consequences for the mating structure of wasp populations within the figs. 2. In this study, the spatial location of male and female progeny of the pollinating fig wasp Liporrhopalum tentacularis developing within figs of its host plant Ficus montana was examined to investigate two questions: (i) are male and/or female wasp offspring clustered together or interspersed? and (ii) is their distribution affected by whether one or two foundresses are present? Microsatellite markers were used to identify the progeny of different foundresses in dual‐foundress figs. 3. More offspring developed in the central part of the figs, compared with the ostiolar and basal parts, irrespective of foundress number. Neither male nor female wasp offspring were clustered within a fig. 4. The sons of the second foundress to enter a fig were positioned at similar minimum distances to both sibling and non‐sibling females, whereas the sons of the first foundress were closer to their sibling females than to non‐sibling females. If male wasps mate predominantly with females in adjacent galls, then the positioning of sons by the second foundresses is beneficial for them both in terms of reduced sibling mating and because they are provided with ready access to the female progeny of the first foundress.     

The effect of interspecific mating on sex ratios in the twospotted spider mite and the Banks grass mite (Acarina: Tetranychidae)

Mixed populations of the twospotted spider mite (TSM),Tetranychus urticae (Koch), and the Banks grass mite (BGM),Oligonychus pratensis (Banks), occur on corn and sorghum plants in late summer in the Great Plains. Interspecific matings between these arrhenotokous species occur readily in the laboratory but yield no female offspring. The effect of interspecific mating on female: male sex ratios was measured by examining the F₁ progeny of females that mated with both heterospecific and conspecific males in no-choice situations. TSM females that mated first with BGM males and then with TSM males produced a smaller percentage of female offspring than TSM females that mated only with TSM males (43.1±5.8 and 78.9±2.8% females, respectively). Similarly, BGM females mated with heterospecific males and then with conspecific males produced fewer female offspring than females mated only with BGM males (55.7±5.2 and 77.5±2.5%, respectively). Lower female: male sex ratios were produced also by BGM females that mated with TSM males after first mating with conspecifics (62.4±3.4%). In mixed populations containing males of both species, females also produced lower female: male sex ratios, but these ratios were not as low as expected based on mating propensities and progeny sex ratios observed in no-choice tests. These data suggest that interspecific mating may substantially reduce female fitness in both mite species by reducing the output of female offspring, but in mixed populations this effect is mitigated by unidentified behavioral mechanisms.     

Reproductive performance of <Emphasis Type="Italic">Nesolynx thymus</Emphasis> (Hymenoptera: Eulophidae) as influenced by host (<Emphasis Type="Italic">Musca domestica</Emphasis>) size

An investigation was conducted to understand the influence of host size on the reproductive performance of Nesolynx thymus, an ecto-pupal parasitoid of the uzi fly, Exorista bombycis, inflicting 10–20% loss to silkworm crops in the southern silk producing states of India. Two day-old adults of N. thymus were allowed to parasitize pupae of M. domestica, categorized into big and small at a parasitoid-host ratio of 1:20. After parasitoid adult eclosion, data on parasitization rate, developmental duration, male, female and total adult recovery per pupa and per female, sex ratio, adult size and adult longevity were recorded. The performance of first generation adults as influenced by host size was also recorded by allowing the first generation adults to parasitize three day-old pupae of E. bombycis. The parameters female and total progeny production per female, sex ratio, longevity, body length and wing span of males, females, head width of male, and abdomen length of female increased significantly with host size. No impact of host size was observed on performance of first generation adults.     

The reproductive strategy of the gregarious parasitoid,Pteromalus puparum (Hymenoptera: Pteromalidae)

Summary Host size of Pteromalus puparum, a gregarious pupal parasitoid, shows a wide inter- and intraspecific variation. Experiments were made to study the regulation of the number and sex ratio of progeny per host by the parasitoid. The parasitoid could discriminate inter- and intraspecific size differences of the host and regulate the number of eggs according to the host size when a single female attacked the host. The sex ratio of progeny (proportion males) was about 0.1. The number of progeny laid by the female agreed with the energetically most efficient number og eggs in order to maximize total weight of progeny per host but not with the reproductively most efficient number of eggs to maximize the total fecundity of the progeny. The parasitoid laid smaller number of eggs in a half buried host, but the number was much larger than a half of those in a fully exposed host. When more than one female attacked a single host, the number and sex ratio of progeny per host increased with the number of females attacking the host, but the number of progeny per female decreased. The change of the sex ratio agreed with the prediction of the local mate competition model.     

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.     

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.     

Life tables and intrinsic rate of natural increase ofPediobius furvus [Hym.: Eulophidae] onChilo partellus [Lep.: Pyralidae]

In the present studies, life table data and intrinsic rate of natural increase (r_m) of the eulophid pupal parasitoid,P. furvus (Gahan) were obtained fromChilo partellus (Swinhoe) at a constant temperature of 26.7±0.6°C, 52.3±2.7% RH in the laboratory. Development of immature stages took 19.1±0.3 days; adult females lived for 7.9±3.3 (range, 2–13) days and produced a mean of 91.9±22.4 progeny per female, with a sex ratio of 1:2.9 (♂:♀). The intrinsic rate of natural increase (rm) was 0.2558/female/day; the net reproductive rate (R₀), 237.25; the capacity for increase (r_c) of 0.252; and the finite rate of increase (λ) of 1.29/female/day; thus, each female contributed 231.42 individuals to the population in a mean generation time of 21.38 days.      

Delayed pollination,stigma length,sex expression,and progeny sex ratio in spinach,Spinacea oleracea (Chenopodiaceae)

Delayed outcrossed pollination of female spinach plants (Spinacea oleracea L.) resulted in increased stigma length and a male-biased progeny sex ratio. One group of females was outcrossed 10–14 d after anthesis, a second group was never outcrossed, and a third group, the control, consisted of females that were outcrossed as soon as stigmas appeared. Stigma length was significantly greater for plants in the delayed and never outcrossed groups compared to the control. Furthermore, stigmas of virgin flowers grew until they were either pollinated or the plants produced anthers. Plants that were never outcrossed produced their own anthers and self pollinated. The resulting progeny were all female. The sons of the delayed outcrossed group produced more stamens, on average, than sons of the control group. The observed male-biased sex ratio among the progeny of delayed outcrossed plants could be due to gametic selection. To test for this, plants were held virgin until their stigmas reached a length of at least 3 mm. These stigmas were then pollinated either distally or proximally. No significant difference was found between the progeny sex ratios of these two treatments. However, both sex ratios were more male biased than progeny of plants pollinated the day of anthesis (control group of the first experiment). We conclude that maternal factors, rather than gametophytic selection, may be responsible for the male-biased sex ratio observed in the first experiment.     

Diadegma mollipla parasitizing Plutella xylostella: host instar preference and suitability

Oviposition decisions (i.e., host selection and sex allocation) of female parasitoids are expected to correspond with host quality, as their offspring fitness is dependent on the amount and quality of resources provided by a single host. The host size model assumes that host quality is a linear function of host size, with larger hosts believed to contain a greater quantity of resources, and thus be more profitable than smaller hosts. We tested this assertion in the laboratory on a solitary larval–pupal parasitoid Diadegma mollipla (Holmgren) (Hymenoptera: Ichneumonidae) developing on three instars (second–fourth) of one of its hosts, the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). In a no‐choice test, parasitism levels and sex ratio (i.e., proportion of female progeny) were significantly high in hosts attacked in the second instar followed by third then fourth instars. However, the few parasitoids that completed a generation from the fourth instars did so significantly faster than conspecifics that started development in the other two instars. In direct observations, however, the parasitoids (i) randomly attacked the various host instars, (ii) spent a similar period examining the various host instars with their ovipositors, (iii) subdued all three host instars with about the same effort, and (iv) no statistical differences were observed in the attack rates on the three host instars. In a choice test, the females parasitized significantly more third instars followed by second then fourth instars. However, total parasitism in this experiment was 43% lower compared to parasitism of only second instars in the no‐choice test. No significant differences were detected in progeny sex ratios. In both choice and no‐choice tests, significantly more fourth instars died during the course of the experiments than second instars, while third instars were intermediate. The higher parasitism of third than second instars in the choice test indicates that the females perceived larger hosts as higher quality than smaller hosts, despite their lower suitability for larval development.     

Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio

1. Parasitic Hymenoptera reproduce by arrhenotokous parthenogenesis, and females of these species are able to control their progeny sex ratios. In structured populations of parasitic Hymenoptera, primary sex ratios are often highly biased toward females. However, sex ratio can be adjusted to the quality of encountered patches or hosts or be modified by differential developmental mortality.
2. In this paper, the effects were evaluated of the quality of encountered hosts and developmental mortality on the sex ratio in Anaphes victus , a solitary egg parasitoid whose first instar larvae present a sexual dimorphism and where superparasitism is regulated by larval fights between first instar larvae.
3. The results showed that a female-biased sex ratio is allocated to unparasitized hosts. In the presence of parasitized hosts, the second (superparasitizing) female produced a significantly higher sex ratio than the first female but the tertiary sex ratio (sex ratio at emergence) was not significantly different from the sex ratio produced with unparasitized hosts. The increase in the primary sex ratio produced by the second female was mostly compensated by the higher mortality of male larvae.     

Effects of host age and host availability on developmental period,adult size,sex ratio,longevity and fecundity inLariophagus distinguendus Förster (Hymenoptera: Pteromalidae)

The effects of host age on parasitoid reproductive capacity are studied using the pteromalid parasitoid Lariophagus distinguendusFörster and its bruchid hosts, Callosobruchus chinensis (L.) and C. maculatus (F.). A series of experiments were performed to investigate relationships between age and size of host parasitized and the developmental period of pre-imaginal progeny, sex ratio, female size, longevity, fecundity and oviposition rate. There was no effect of host size on preimaginal parasitoid developmental period. Sex ratio varied from less than 5% females from young (small) hosts to 60% females from mature (large) hosts. Adult size, female longevity, fecundity, and oviposition rate were also positively related to host age. Females provided mature hosts lived longer than those provided either young hosts or no hosts, possibly because of an increased ability to host-feed from the larger hosts. The implications of these findings to parasitoid population reproductive capacity and host-parasitoid synchrony are discussed.     

Variably male-biased sex ratio in a marine bird with females larger than males

When the costs of rearing males and females differ progeny sex ratios are expected to be biased toward the less expensive sex. Blue-footed booby (Sula nebouxii) females are larger and roughly 32% heavier than males, thus presumably more costly to rear. We recorded hatching and fledging sex ratios in 1989, and fledging sex ratios during the next 5 years. In 1989, the sample of 751 chicks showed male bias at hatching (56%) and at fledging (57% at ˜90 days). Fledging sex ratios during the five subsequent reproductive seasons were at unity (1 year) or male-biased, varying from 56% to 70%. Male bias was greater during years when mean sea surface temperature was warmer and food was presumably in short supply. During two warm-water years (only) fledging sex ratio varied with hatching date. Proportions of male fledglings increased with date from 0.48 to 0.73 in 1994, and from 0.33 to 0.79 in 1995. Similar results were obtained when the analysis was repeated using only broods with no nestling mortality, suggesting that the overall increase in the proportion of males over the season was the result of sex ratio adjustments at hatching. The male-biased sex ratio, and the increased male bias during poor breeding conditions supports the idea that daughters may be more costly than sons, and that their relative cost increases in poor conditions. Received: 3 February 1998 / Accepted: 12 September 1998     

Control of placental protein production by retinoic acid in cultured placental cells

Summary The synthesis of human chorionic gonadotropin (HCG), the subunit of HCG (HCGα), and pregnancy-specific β₁-glycoprotein (PSβG) was studied in temperature senstive (ts), simian virus 40 (SV40)tsA mutant-transformed human first trimenster placental (SPA255-26) cells. Retinoic acid increased the production of HCG and PSβG but inhibited the production of HCGα in these cells. Passage ofSPA255-26 placental cells in medium containing retinoic acid induced a stable altered phenotype characterized by elevated levels of HCG and PSβG and a reduced level of HCGα. The retinoic acid induced phenotypic changes in these placental cells were reversible; removal of retinoic acid immediately decreased the production of HCG and PSβG while increasing the production of HCGα. The ratio of HCG to HCGα in controlSPA255-26 cells was approximately 0.1; this ratio in creased to 4.8 in cells maintained in medium containing retinoic acid. Similarly, the HCG-to-HCGα ratio increased in choriocarcinoma cells maintained in retinoic acid containing medium. Our data suggest that retinoic acid may be needed to maintain a blanced production of HCG, HCGα, and PSβG in placental cells in vitro. Retinoic acid may also play a role in modulating placental protein production during pregnancy.     

Sex determination and sex ratio in the dioecious shrub Salix viminalis L.

 Various ecological factors (e.g. herbivory, difference between males and females in colonising ability) have been invoked to explain female-biased sex ratios in populations of willow species. It was implicitly assumed that genetic factors would lead to a balanced sex ratio in the absence of ecological disturbances. In an experiment carried out in a homogeneous environment and in the absence of herbivores the progeny sex ratio of 13 crosses of basket willow (Salix viminalis L.) was observed to range from extreme female bias to extreme male bias. The observed sex ratio cannot be explained by the presence of sex chromosomes without assuming that additional loci are also involved in the sex determination. Alternatively, the sex ratios in this study can be explained by a sex determination mechanism governed by multiple independent loci. Received: 1 February 1996 / Accepted: 14 June 1996     

Effects of parental age at mating on the fecundity and progeny sex ratio of <Emphasis Type="Italic">Campoletis chlorideae</Emphasis>, an endolarval parasitoid of the pod borer, <Emphasis Type="Italic">Helicoverpa armigera</Emphasis>

Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), commonly called gram pod borer, is a serious pest of pulse crops in India and damages chickpea (Cicer arietinum L). On average a 30% crop loss is reported. One of the potential natural enemies reported for its biological control is Campoletis chlorideae Uchida (Hymenoptera: Ichneumonidae), an idiobiont parasitic wasp that attacks second instar larvae of the pod borer. Male-biased sex ratios hinder efforts to mass release parasitic Hymenoptera for biological control by making the production of females costly. Parental age at time of mating is known to affect the progeny sex ratio in some Braconidae. In this view, we examined the reproduction and survival of the parasitoid C. chlorideae in the laboratory [22 ± 4°C, 70 ± 10% R.H. and 10:14 h light:dark photoperiod]. All the nine (i.e. 3 × 3) combinations of possible mating were made for males and females, being each of different age groups (0–12, 48–60 and 96–108 h old). Second instar larvae of the pod borer were reared on chickpea and exposed to mated females of different mating age group combinations. Results revealed that (a) newly emerged females (0–12 h old) mated to aged males yielded more progeny contrasted to the older females inseminated by newly emerged males (0–12 h old). This implies that increased maternal age at mating caused greater reduction in the progeny yield than that of paternal age; (b) the progeny sex ratio was lowest (0.344 ± 0.057) (mean ± SD) when parents mated just after emergence (0–12 h old). It became more and more male biased as parents were deprived of mate and was highest (0.666 ± 0.701) for 96–108 h old parents. The analysis of variance of the data shows that mate deprived males caused greater contribution in the production of sons, resulting a male-biased progeny sex ratio. Our conclusion indicate that newly emerged parasitoids (0–12 h old) are most fecund and should be used in rearing practices in order to enhance the progeny yield, particularly with respect to daughters. Handling Editor: Torsten Meiners     

The effect of mating behaviour on progeny sex ratio of Mastrus ridens (Hymenoptera: Ichneumonidae), a biological control agent of codling moth

Mastrus ridens (Horstmann) (Hymenoptera: Ichneumonidae) was imported into quarantine as a potential biocontrol agent for codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Mating behaviour of the parasitoid and its effect on progeny sex ratio (as a proportion of males) were studied to help sustain the laboratory culture. Both females and males were reproductively active soon after emergence. Unmated females produced only male progeny, confirming males developed from unfertilized eggs. The proportion of males in a progeny was independent of the copulation period (24–40 s) of the parents. The progeny sex ratios from three parent ratios (f:m 2:1, 1:1 and 1:2) were not significantly different. Females effectively mated only once but males mated frequently in their lifetime. The progeny sex ratios from single females with a known single mating and possible multiple matings (through exposure to two males for 18 days) were not significantly different. However, when males copulated with five virgin females in sequence over a 2 h period, the fifth female produced more males than the preceding four, presumably due to sperm depletion. Results of this study provide data on progeny sex allocation of M. ridens that help to prevent the development of a male-biased sex ratio that could threaten the maintenance of the culture over time.     

Reproductive performance of Nesolynx thymus (Hymenoptera: Eulophidae), in relation to age of Musca domestica (Diptera: Muscidae)

An investigation was undertaken to record the influence of host age on the reproductive performance of Nesolynx thymus (Hymenoptera:Eulophidae). This is an indigenous, gregarious, ecto-pupal parasitoid of certain dipteran insects, including the tachinid fly, Exorista bombycis (Louis) which is a well-known endo-larval parasitoid of the silkworm, Bombyx mori. Each gravid N. thymus female was allowed to parasitise 1–4-day-old puparia of Musca domestica L. for 2 days at a parasitoid–host ratio of 1:20. The parasitised host puparia were observed for progeny recovery, sex ratio, female longevity and fitness (adult size). In addition, reproductive performance of the parasitoid progeny was assessed by allowing its females to parasitise for 2 days, 3-day-old puparia of E. bombycis at a parasitoid–host ratio of 1:4. There was a significant negative correlation between host age and parasitisation rate, parasitoid developmental duration, sex ratio and female longevity while the correlation was positive between host age and parasitoid recovery per host puparium. Similarly, negative correlation was observed between host age and morphometric parameters (body length, head width and wing span of male and female and length and width of female abdomen) of the progeny adults. Host age did not have any impact on the reproductive performance of progeny adults when allowed to parasitise puparia of E. bombycis.     

Opposing effects of mortality factors on progeny operational sex ratio may thwart adaptive manipulation of primary sex ratio

Despite extensive research on mechanisms generating biases in sex ratios, the capacity of natural enemies to shift or further skew operational sex ratios following sex allocation and parental care remains largely unstudied in natural populations. Male cocoons of the sawfly Neodiprion abietis (Hymenoptera: Diprionidae) are consistently smaller than those of females, with very little overlap, and thus, we were able to use cocoon size to sex cocoons. We studied three consecutive cohorts of N. abietis in six forest stands to detect cocoon volume‐associated biases in the attack of predators, pathogens, and parasitoids and examine how the combined effect of natural enemies shapes the realized operational sex ratio. Neodiprion abietis mortality during the cocoon stage was sex‐biased, being 1.6 times greater for males than females. Greater net mortality in males occurred because male‐biased mortality caused by a pteromalid parasitic wasp and a baculovirus was greater and more skewed than female‐biased mortality caused by ichneumonid parasitic wasps. Variation in the susceptibility of each sex to each family of parasitoids was associated with differences in size and life histories of male and female hosts. A simulation based on the data indicated that shifts in the nature of differential mortality have different effects on the sex ratio and fitness of survivors. Because previous work has indicated that reduced host plant foliage quality induces female‐biased mortality in this species, bottom‐up and top‐down factors acting on populations can affect operational sex ratios in similar or opposite ways. Shifts in ecological conditions therefore have the potential to alter progeny fitness and produce extreme sex ratio skews, even in the absence of unbalanced sex allocation. This would limit the capacity of females to anticipate the operational sex ratio and reliably predict the reproductive success of each gender at sex allocation.