Mating system of Bracon hebetor (Hymenoptera: Braconidae)

Abstract.

• 1 We report on the mating system of a field population of the parasitic wasp, Bracon hebetor, on a corn pile infested by the Indian meal moth, Plodia interpunctella. We demonstrate that the mating system is based upon male scramble competition polygyny with male aggregations on high places on the corn.
• 2 The sex ratio among adults was greater than 80% males on the surface of the corn, whereas below the surface the sex ratio was less than 45%. Males actively courted females on the surface, but there were no aggressive interactions among males during courtship or mating.
• 3 Approximately 20% of the females found on the surface of the corn had no sperm in their spermathecae, regardless of age, but the numbers of unmated females decreased later during the day.
• 4 In laboratory studies we showed that females from this population oviposit a female biassed sex ratio, and that only 14% of females were mated before dispersing from their place of emergence.
• 5 Thus sib-mating is unlikely in this gregarious parasitoid. This outcrossing mating system probably arose because of severe inbreeding depression that B.hebetor suffers via a sex locus: diploids that are heterozygous at the sex locus develop into females, but homozygous diploids are male and are generally inviable. The female biassed sex ratio may have evolved in B. hebetor in response to males being the more expensive sex, females dispersing more frequently from the population than males, or a fraction of females remaining unmated in the population.

     

Insects and incest: Sib‐mating tolerance in natural populations of a parasitoid wasp

Sib‐mating avoidance is a pervasive behaviour that is expected to evolve in species subject to inbreeding depression. Although laboratory studies provide elegant demonstrations, small‐scaled bioassays minimize the costs of mate finding and choice, and thus may produce spurious findings. We therefore combined laboratory experiments with field observations to examine the existence of inbreeding avoidance using the parasitoid wasp Venturia canescens. In the laboratory, our approach consisted of mate‐choice experiments to assess kin discrimination in population cages with competitive interactions. A higher mating probability after sib rejections suggested that females could discriminate their sibs; however, in contrast to previous findings, sib‐mating avoidance was not observed. To compare our laboratory results to field data, we captured 241 individuals from two populations. Females laid eggs in the lab, and 226 daughters were obtained. All individuals were genotyped at 18 microsatellite loci, which allowed inference of the genotype of each female's mate and subsequently the relatedness within each mating pair. We found that the observed rate of sib‐mating did not differ from the probability that sibs encountered one another at random in the field, which is consistent with an absence of sib‐mating avoidance. In addition, we detected a weak but significant male‐biased dispersal, which could reduce encounters between sibs. We also found weak fitness costs associated with sib‐mating. As such, the sex‐biased dispersal that we found is probably sufficient to mitigate these costs. These results imply that kin discrimination has probably evolved for purposes other than mate choice, such as superparasitism avoidance.     

Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus

Sexual conflicts due to divergent male and female interests in reproduction are common in parasitic Hymenoptera. The majority of parasitoid females are monandrous, whereas males are able to mate repeatedly. Thus, accepting only a single mate might be costly when females mate with a sperm‐depleted male, which may not transfer a sufficient amount of sperm. In the present study, we investigated the reproductive performance in the parasitoid Lariophagus distinguendus Först. (Hymenoptera: Pteromalidae) and studied whether mating with experimentally sperm‐depleted males increases the tendency of females to remate. Males were able to mate with up to 17 females offered in rapid succession within a 10‐h test period. The resulting female offspring, as an indirect measure of sperm transfer, remained constant during the first six matings and then decreased successively with increasing number of copulations by the males. Experimentally sperm‐depleted males continued to mate even if they transferred only small amounts or no sperm at all. Unlike males, the majority of females mated only once during a 192‐h test period. A second copulation was observed only in a few cases (maximum 16%). The frequency of remating was not influenced by the mating status of the first male the females had copulated with, suggesting that these events are not controlled by sperm deficiency of the females. Furthermore, we investigated male courtship behaviour towards mated females. Male courtship intensity towards mated females decreased with increasing time. However, females that had mated with an experimentally sperm‐depleted male did not elicit stronger or longer‐lasting behavioural responses in courting males than those that had mated with a virgin male. As the observed behaviours in L. distinguendus are known to be elicited by a courtship pheromone, these results suggest that females no longer invest in pheromone biosynthesis after mating (as indicated by ceasing behavioural responses of courting males), irrespective of whether they have received a sufficient amount of sperm or not. We discuss the results with respect to a possible mating strategy of sperm‐depleted males.     

Effects of age and repeated mating on male sperm supply and paternity in a parasitoid wasp

Post-copulatory paternity biases after female multiple mating are major constraints on both male and female reproductive systems. The outcome of paternity in certain situations is only controlled directly by male sperm stock. This was tested experimentally in the parasitoid wasp Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), in which sperm stocks are small (several hundred) and the fertilizing efficiency of stored sperm is high (the ratio of sperm stored/fertilized eggs is about 0.75). Sperm in seminal vesicles and paternity of males of different status (virgin young, virgin old, or young previously mated) were measured after female single and double mating. The amount of sperm in the seminal vesicle differed according to male status (increasing from previously mated males to old males), but there was no difference in sperm stored by females after a single mating. In double mating experiments with two males of different status, paternity increased linearly with the relative amount of sperm in seminal vesicles. Paternity distribution conforms to 'a fair raffle' of sperm from both donors following complete mixing of sperm prior to fertilization. Thus, in a female multiple mating context, male fitness depends principally on their sperm stock, which in turn depends on life history parameters, such as age and previous mating.     

Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp

Most parasitoid female wasps can distinguish between unparasitized and parasitized hosts and use this information to optimize their progeny and sex allocation. In this study, we explored the impact of mating on oviposition behaviour (parasitism and self‐ and conspecific superparasitism) on both unparasitized and already parasitized hosts in the solitary parasitoid wasp Eupelmus vuilleti (Crw.) (Hymenoptera: Eupelmidae). Virgin and mated females had the same oviposition behaviour and laid eggs preferentially on unparasitized hosts. The sex ratio (as the proportion of females) of eggs laid by mated females in parasitism and conspecific superparasitism was 0.67 ± 0.04 and 0.57 ± 0.09, respectively. Likewise, females laid more eggs in conspecific superparasitism than self‐superparasitism under our experimental conditions. These experiments demonstrate that E. vuilleti females can (i) discriminate between unparasitized and parasitized hosts and adapt the number of eggs they lay accordingly, and (ii) probably discriminate self from conspecific superparasitized hosts. Finally, mating does not appear to influence the host discrimination capacity, the ovarian function, or the oviposition behaviour.     

Purification and characterization of insecticidal toxins from venom glands of the parasitic wasp, Bracon hebetor

The potency of venom from Bracon hebetor against lepidopterous larvae has been known for over 40 years, but previous attempts to purify and characterize individual protein toxins have been largely unsuccessful. Three protein toxins were purified from venom of this small parasitic wasp and the amino acid sequences of 22–31 consecutive residues at the amino-terminus were determined. These relatively large toxins (apparent molecular mass 73 kDa) were labile under many isolation techniques, but anion-exchange chromatography allowed purification with retention of biological activity. Two purified toxins were quite insecticidal (LD₅₀ < 0.3μg/g) when injected into six species of lepidopterous larvae. On a molar basis, one toxin (Brh-I) has the highest known biocidal activity against Heliothis virescens (LD₅₀ = 2 pmol/g).     

Evidence for acoustic communication in the parasitoid wasp Glyptapanteles flavicoxis

Females of the parasitoid wasp Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae) deposit sex pheromone on substrate that elicits attraction and wing fanning in conspecific males. We tested the hypothesis that wing fanning sound induces a behavioral response from females which, in turn, affects the males’ orientation toward them. Females exposed to playback of the males’ wing fanning sound engaged in short flights, with sound characteristics different from those of the males’ wing fanning sound. In two‐choice bioassays, playback of the females’ flight sound attracted significantly more males than a silent control stimulus, and in combination with pheromone‐containing body extract of females it attracted more males than female body extract alone. Our data support the conclusion that the males’ wing fanning induces sound and visual reply signals from females that help males orient toward them.     

Environmental and genetic determinants of ovicide in parasitic wasp Bracon hebetor

Superparasitism occurs when a parasitoid lays a second clutchof eggs on a host previously parasitised by herself or a conspecific.Ovicide refers to a parasitoid destroying an existing clutchof eggs on a parasitized host before laying a second clutch.We investigated environmental and genetic determinants of ovicidein the parasitic wasp Bracon hebstor. Characterization of egglayingbehavior revealed that B. hebetor commits ovicide during thehost examination phase of oviposition. The temporal costs ofovicide were found to be relatively small for females that experiencedlow rates of host encounter, whereas the costs of ovicide increasedfor females that experienced a high rate of host encounter.Individual wasps committed ovicide on conspecifically parasitizedhosts more frequently than on self-parasitized hosts. Manipulationexperiments suggested that B. hebetor females learn about theirenvironment while foraging and commit ovicide on the basis ofthe travel time between successive hosts. Significant differenceswere also found in ovicidal behavior among laboratory and fieldpopulations of B. hebetor. The implications of our results forclutch size theory and the evolution of ovicide are discussed.     

Sperm production and mating potential of males after a cold shock on pupae of the parasitoid wasp Dinarmus basalis (Hymenoptera: Pteromalidae)

For ectothermic species, temperature is a key environmental factor influencing several aspects of their physiology and ecology, acting particularly on reproduction. To measure the consequences of a severe thermal stress during development on male reproduction, a cold shock (1h at -18 degrees C) was tested on Dinarmus basalis pupae. D. basalis (Hymenoptera: Pteromalidae) is a parasitoid wasp in which sperm management in both male and female is of prime importance. After a cold shock, developmental success was reduced, with a quarter of cold-shocked males not emerging correctly. The stress effects were estimated at the level of sperm stock in seminal vesicles of males at different ages and on the ability of 2-day-old males to access females in single and multiple mating and in male-male competition. Cold-shocked males had a reduced sperm stock compared to control males and this difference persisted with age. The rate of sperm production was similar in both groups. The consequences of a cold shock on male reproductive ability were perceptible in multiple mating and male-male competition but not in single mating. Cold-shocked males were at a disadvantage, inseminating fewer females and copulating less frequently. Finally, male pupae of D. basalis were able to withstand severe temperature stresses and their reproductive functions were partially preserved.     

Constrained oviposition and female-biased sex allocation in a parasitic wasp

 In haplodiploid organisms such as parasitic wasps, substantial oviposition by females without sperm is predicted to cause mated females to bias their offspring sex ratios towards daughters. The effect of the production of sons by unmated and sperm-depleted (constrained) females on sex allocation by mated females was studied in two populations of the parasitic wasp Bracon hebetor over 3 years. B. hebetor females who depleted their sperm reserves from prior matings rarely remated and became constrained to produce only sons. Constrained females readily oviposited and produced clutches similar in size to those produced by mated females. Although the fraction of constrained females in the population varied considerably between sites and sampling dates, it was usually high enough to favor the production of female-biased sex ratios by mated females. Mated females consistently produced female-biased sex ratios. However, we found no evidence that the sex ratios produced by mated females from the field shifted in relation to the proportion of constrained females in the population. Females held with males or held in isolation also produced female-biased sex ratios. These findings suggest that, in B. hebetor, mated females produce sex ratios that reflect the average fraction of constrained females over evolutionary time. Received: 21 June 1996 / Accepted: 27 August 1996     

Learning provides mating opportunities for males of a parasitoid wasp

The ability of insects to learn locations of future resources has rarely been studied. Here, we show that males of the solitary parasitoid wasp Pimpla disparis Viereck (Hymenoptera: Ichneumonidae) learn locations of future mates. Male P. disparis reportedly arrest on parasitized pupae of wax moth, Galleria mellonella L. (Lepidoptera: Pyralidae), and gypsy moth, Lymantria dispar L. (Lepidoptera: Erebidae), when mate emergence is imminent. We tested the hypothesis that male P. disparis identify, memorize, and revisit the location(s) of parasitized host pupae as a strategy to attain mates. We colour‐coded P. disparis males in the field and noticed that they revisit parasitized moth pupae on consecutive days, and arrest on those pupae with a near‐emergence P. disparis parasitoid. In a laboratory experiment with two large corrugated cardboard cylinders (CCCs) as surrogate trees, each CCC bearing two parasitized moth pupae with a near‐emergence P. disparis parasitoid or two pupae not parasitized, males on day 1 of the experiment visited parasitized pupae more often than pupae not parasitized. On day 2, when each CCC had been replaced and now carried pupae that were not parasitized, males returned to the same CCC, or the same micro‐location on that CCC, which on day 1 had carried parasitized pupae. Field and laboratory data combined indicate that male P. disparis learn the location of future mates. With female P. disparis being haplodiploid and capable of reproducing without mating experience, the onus to find a mate is on males. They accomplish this by detecting parasitized pupae, learning their location, revisiting them frequently, and then arresting on them when the prospective mate nears emergence, taking a 50% chance that it is indeed a female.     

Unequal distribution of local mating opportunities in an egg parasitoid

Abstract.  1. The Local Mate Competition (LMC) model predicts that, in gregarious and quasi-gregarious species, a lone female exploiting a host patch will lay only the minimal number of sons necessary to inseminate all daughters, but as the number of foundresses increases, the proportion of sons deposited by these females also increases.
2. For off-patch mating to occur, non-sperm-depleted males must leave the patch and find virgin females.
3. To investigate the distribution of matings among males, the sperm stock at dispersal and the time of dispersal were quantified for male Trichogramma turkestanica (Hymenoptera: Trichogrammatidae).
4. Matings were not distributed equally among males: some successful males acquired more matings than others. Because of this, a high variability in the sperm stock at dispersal was observed. While few males dispersed almost empty or almost full, the majority of males dispersed with enough sperm to be able to mate with females outside the emergence patch.
5. The mating capacity was thus higher than necessary for local mating and could be explained by an unequal distribution of mating opportunities and the occurrence of off-patch mating.     

Parasitic wasp assemblages associated with native and weedy plant species in an agricultural landscape

Abstract  The establishment and maintenance of suitable habitat on-farm or in the surrounding landscape can enhance the survival of beneficial parasitic Hymenoptera, thus improving the control of pest species. Both endemic and weedy non-crop plant species across a highly modified agricultural landscape supported species-rich and abundant parasitic wasp assemblages with diverse biology and host associations. It was also shown that isolated, recently planted, single-species stands of plants can rapidly accumulate diverse assemblages of parasitoids. Chalcidoidea was the most species-rich and abundant group, egg and larval parasitoids were the most speciose and abundant guilds, and parasitoids of herbivorous insects feeding on and inside plant tissue were the most species-rich and abundant functional groups. The hymenopteran assemblages associated with the majority of plant species were dominated by three parasitoid species: a Trichogrammatidae, a Scelionidae ( Telenomus sp.) and a Eulophidae ( Ceranisus sp.), all genera that contain many important biocontrol agents of pest Lepidoptera, Hemiptera and Thysanoptera. Results show that both native and weedy plant species may potentially provide an important reservoir of mobile parasitic wasps of benefit to crop protection.     

Investigation of sex ratio and adult longevity of Habrobracon hebetor Say in relation to some conventional and biorational insecticides

Habrobracon hebetor Say (Hymenoptera: Braconidae) is one of the most important natural enemies that has been used for biological control of lepidopteran pests, so the sub-lethal effects of imidacloprid, abamactin and Bacillus thuringiensis Berliner (Bt) on progeny sex ratio (male/total) and adult longevity of H. hebetor were examined under laboratory conditions. It was found that the progeny sex ratio changed to male bias significantly by Bt treatment. Also, the adult longevity of the wasp was affected adversely by insecticides treatment and it was longest in Bt treatment. In conclusion, the current results indicated that the sub-lethal concentration of these insecticides affected the progeny sex ratio and adult longevity and the best strategies for reduction of hazard to the H. hebetor in combination with Bt is to avoid their application before Bt spraying.     

Sperm stock and mating of males in a parasitoid wasp

Hymenoptera are haplodiploid insects, consequently sex ratio depends on female's sperm management which itself arises from the reproductive capacity of neighbouring males. To study the influence of ageing on male reproductive potential, laboratory experiments were conducted on Dinarmus basalis (Hymenoptera, Pteromalidae) males, a tropical wasp in which sperm counts are known to constrain sex ratio. Two groups of virgin males were compared: 1-day and 30-days old. Parameters recorded were sperm quantity and viability in seminal vesicles, shape of testis, mating ability in both individual and competitive situations and sperm stored by females after male multiple mating. Older males had twice as much sperm as young males, but their reproductive capacities did not differ. They were able to copulate with 20 successive virgin females in a short period. Sperm stored in spermathecae decreased with female mating order. In competition, old and young males had the same access to females. The difference between old and young males was visible at the level of reproductive tract: young males have functional testis and old males have empty non-functional testis. Spermatozoa are kept viable in male seminal vesicles for long periods. In this species, the reproductive potential of males is not altered by ageing. At the population level this may represent an adaptation for maintaining continuous reserves of sperm at the disposal of females.     

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.     

Presence of conspecifics triggers host searching behavior in an egg parasitoid wasp

Parasitoids and predators compete for host or prey species. The efficiency of obtaining prey or host items is reduced by intraspecific competition. As the optimal search behavior depends on the intensity of competition, it is important for the parasitoid or predator to obtain information on this intensity. Previous studies have shown that parasitoids can obtain information regarding competition from encounters with already parasitized hosts. They then change their host searching behavior accordingly. However, whether parasitoids obtain the information directly from observing the presence of conspecifics remains unclear. We used Tiphodytes gerriphagus (Marchal) (Hymenoptera: Scelionidae), the solitary egg parasitoid of water striders, for testing the effect of density of conspecifics on host searching behavior. Females of T. gerriphagus dive into the water to search for hosts and sometimes they dive without hosts present. Thus, we investigated whether T. gerriphagus changed underwater activities in response to the density of conspecifics in the absence of hosts. Four densities (1, 2, 4, and 8 female T. gerriphagus) were investigated. Females in competitive situations (groups of 2, 4, and 8 females) displayed host searching behavior, but the solitary females did not. This indicates that the presence of conspecifics triggers host searching behavior and that T. gerriphagus females obtain information on competition directly from conspecifics and use it for modifying their behavior.     

Substrate influences mating success and transmission of courtship vibrations for the parasitoid Cotesia marginiventris

The influences of artificial and natural rearing substrates on mating success were investigated for the parasitoid wasp Cotesia marginiventris (Cresson) (Hymenoptera: Braconidae), a candidate for augmentative biological control of various lepidopteran pests. Five rearing substrates were tested: plastic, glass, chiffon fabric, and leaves of two host plants, bean [Vigna unguiculata (L.) (Fabaceae)] and maize [Zea mays L. (Poaceae)]. Mating success was highest on chiffon, lowest on plastic and glass, and intermediate on maize and bean. The transmission characteristics of one component (buzz 1) of the courtship vibrations produced by male wing fanning were investigated using laser vibrometry. The duration of buzz 1 was longer on maize, bean, and chiffon than on plastic and glass. The fundamental frequency of buzz 1 (~300 Hz) was lowest on bean and highest on glass, and intermediate among other substrates. The relative amplitude of buzz 1 was higher on chiffon than on plastic, glass, or bean, and intermediate on maize. The relative importance of airborne sound and substrate vibration as courtship signals was also investigated with experiments that manipulated the production of courtship vibrations and the mating substrates. The amplitude of courtship vibrations on chiffon was significantly higher for winged males than for dealated males. The mating success of males was impacted by both the presence of wings and the mating substrate. These findings suggest that mating success and transmission of courtship vibrations are influenced by the rearing substrate, and that courtship vibrations are critical to mating success in C. marginiventris. Future efforts to mass rear this parasitoid and other insects should consider the potential influences of rearing substrates on mating.     

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.     

A genetic perspective on mating systems and sex ratios of parasitoid wasps

Parasitoid sex ratios are influenced by mating systems, whether complete inbreeding, partial inbreeding, complete inbreeding avoidance, or production of all-male broods by unmated females. Population genetic theory demonstrates that inbreeding is possible in haplodiploids because the purging of deleterious and lethal mutations through haploid males reduces inbreeding depression. However, this purging does not act quickly for deleterious mutations or female-limited traits (e.g., fecundity, host searching, sex ratio). The relationship between sex ratio, inbreeding, and inbreeding depression has not been explored in depth in parasitoids. The gregarious egg parasitoid, Trichogramma pretiosum Riley, collected from Riverside, CA (USA) produced a female-biased sex ratio of 0.24 (proportion of males). Six generations of sibling mating in the laboratory uncovered considerable inbreeding depression (∼ 20%) in fecundity and sex ratio. A population genetic study (based upon allozymes) showed the population was inbred (F _it = 0.246), which corresponds to 56.6% sib-mating. However, average relatedness among females emerging from the same host egg was only 0.646, which is less than expected (0.75) if ovipositing females mate randomly. This lower relatedness could arise from inbreeding avoidance, multiple mating by females, or superparasitism. A review of the literature in general shows relatively low inbreeding depression in haplodiploid species, but indicates that inbreeding depression can be as high as that found in Drosophila. Finally, mating systems and inbreeding depression are thought to evolve in concert (in plants), but similar dynamic models of the joint evolution of sex ratio, mating systems, and inbreeding depression have not been developed for parasitoid wasps. Received: November 13, 1998 /Accepted: January 8, 1999