Host‐searching responses to herbivory‐associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores. 2. However, mated and virgin females of haplodiploid parasitoids might not necessarily respond to such chemical cues in the same way. Since virgin females can produce only sons, they might refrain from searching for hosts to invest eggs until copulation, in order to produce both sexes. 3. Here, we investigated differential host‐searching behaviours shown by mated and virgin females in the solitary parasitoid wasp, Cotesia vestalis, in response to herbivory‐associated chemical information from cruciferous plants infested by their host larvae, Plutella xylostella. 4. Mated females showed a significantly higher flight preference for host‐infested plants over intact plants, while no preference was observed with virgin females. Mated females also showed more intensive antennal searching and ovipositor probing behaviours to leaf squares with wounds caused by hosts than did virgin females. Furthermore, mated females stayed longer in host patches with higher parasitism rates than virgin females. 5. These results indicate that mating status of C. vestalis females clearly influences their host‐searching behaviour in response to herbivory‐associated chemical information and patch exploitation. Female parasitoids seem to forage for hosts depending on their own physiological condition in a tritrophic system.     

Breeding Strategies in Females of the Parasitoid Wasp Spalangia endius: Effects of Mating Status and Size

Does the mating status or body size of a female parasitoid wasp affect her host size choice or propensity to burrow? In Spalangia endius, using smaller hosts appears to reduce a female's cost of parasitization but not her son's fitness. However, virgin females, which produce only sons, did not preferentially parasitize smaller hosts. Mated females also showed no host size preference. Mated females burrowed more than virgins in the presence of hosts, although not in their absence. Burrowing may reduce a mated female's harassment from males, and not burrowing may increase a virgin female's chance of mating because males avoid burrowing. Mating did not increase female longevity. Greater female size increased the offspring production of mated females burrowing for hosts but not in the absence of burrowing and not in virgin females. A female's size had no significant effect on whether her first drill attempt was on a large or a small host or on the duration of her successful drills.     

Reproductive strategies of the larval parasitoid Microplitis croceipes

Mate choice may have important consequences for offspring sex ratio and fitness of haplodiploid insects. Mate preference of females of the solitary larval parasitoid Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) for virgin and mated males, and vice versa, and the reproductive consequences (i.e., the sex ratio expressed as the proportion of male offspring) were examined in choice and non‐choice experiments. In addition, the effect of repeated rapid and daily copulation of an individual male on the sex ratio of offspring of the female mates was assessed. Males preferred virgins over mated females, whereas females copulated with a male irrespective of his mating status. In both the rapid and daily copulation assay, females copulating with a male that had copulated five times or more produced a higher sex ratio than females that had copulated with a virgin male. Females that copulated with virgin males once or twice produced a significantly and considerably lower sex ratio than females that first copulated with a sperm‐depleted male followed by a virgin male. This indicates that copulating with a sperm‐depleted male has costs and limits acquisition by the female of sperm from virgin males.     

Mating or ovipositing? A crucial decision in the life history of the cabbage aphid parasitoid Diaeretiella rapae (M’Intosh)

1. The reproductive fitness of a parasitoid depends on its mating and ovipositing success. Virgin haplodiploid females can reproduce, but produce only males, and may diminish fitness by producing more male offspring than required. Therefore, females must decide on whether to mate or oviposit first. 2. This study was conducted to assess the mating versus ovipositing decision and its impact on the reproductive fitness of Diaeretiella rapae (Hymenoptera: Aphididae), an endoparasitoid of the cabbage aphid Brevicoryne brassicae (Hemiptera: Aphididae). 3. When newly emerged females were given a choice between mating and ovipositing, about 62% of D. rapae females preferred to mate before ovipositing. Those females who oviposited before mating parasitised only 10% of the available aphids. After mating, females superparasitised their hosts with fertilised eggs, which resulted in a highly female‐biased sex ratio in the offspring. 4. Mating success was very high (91%) in the presence of hosts (cabbage aphid nymphs) compared with that in the absence of aphids. However, mating success was not influenced by the quality (size) of the hosts present in the mating arena, despite a parasitoid preference for larger hosts during oviposition. The time between pairing and mating was also shorter in the presence of host aphids. The mean number of aphids parasitised and the parasitism rate were significantly greater after mating.     

Mating modifies female life history in a haplodiploid spider mite

Mating usually modifies females' resource allocation pattern, often as a result of conflicts between male and female partners. Can such a switch occur even in the absence of sexual conflicts? We addressed this issue in the haplodiploid spider mite Tetranychus urticae, whose biology and population structure considerably reduce conflicts between males and females over reproductive decisions. Comparing virgin and mated females, we tested the hypothesis that mated females modify their allocation pattern so as to maximize their probability of producing daughters. Mated females produced fewer but larger eggs, resulting in an overall similar reproductive effort but an increased probability of producing daughters, since in this species larger eggs are more likely to be fertilized and thus to become female. Moreover, mated females concentrated their reproduction early in life. Again, this might be a way to produce more daughters, since sperm is more abundant early in life. For virgins, spreading reproductive investment might be a way to save resources to extend life span, thus increasing their probability of encountering a sexual partner. Females with multiple opportunities for mating produced fewer eggs and a less female-biased sex ratio than once-mated females, raising the question of why multiple mating often occurs in this species.     

Polyandry enhances offspring viability with survival costs to mothers only when mating exclusively with virgin males in Drosophila melanogaster

A prominent hypothesis for polyandry says that male–male competitive drivers induce males to coerce already‐mated females to copulate, suggesting that females are more likely to be harassed in the presence of multiple males. This early sociobiological idea of male competitive drive seemed to explain why sperm‐storing females mate multiply. Here, we describe an experiment eliminating all opportunities for male–male behavioral competition, while varying females’ opportunities to mate or not with the same male many times, or with many other males only one time each. We limited each female subject's exposure to no more than one male per day over her entire lifespan starting at the age at which copulations usually commence. We tested a priori predictions about relative lifespan and daily components of RS of female Drosophila melanogaster in experimental social situations producing lifelong virgins, once‐mated females, lifelong monogamous, and lifelong polyandrous females, using a matched‐treatments design. Results included that (1) a single copulation enhanced female survival compared to survival of lifelong virgins, (2) multiple copulations enhanced the number of offspring for both monogamous and polyandrous females, (3) compared to females in lifelong monogamy, polyandrous females paired daily with a novel, age‐matched experienced male produced offspring of enhanced viability, and (4) female survival was unchallenged when monogamous and polyandrous females could re‐mate with age‐ and experienced‐matched males. (5) Polyandrous females daily paired with novel virgin males had significantly reduced lifespans compared to polyandrous females with novel, age‐matched, and experienced males. (6) Polyandrous mating enhanced offspring viability and thereby weakened support for the random mating hypothesis for female multiple mating. Analyzes of nonequivalence of variances revealed opportunities for within‐sex selection among females. Results support the idea that females able to avoid constraints on their behavior from simultaneous exposure to multiple males can affect both RS and survival of females and offspring.     

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.     

A survival cost to mating in a polyandrous butterfly, Colias eurytheme

Adaptations that enhance fitness in one sex may be harmful to members of the opposite sex and lead to antagonistic coevolution between the sexes. In fruit flies, for example, selection for fertilization success has rendered the male ejaculate slightly toxic to females. Here we investigated whether mating imposes a cost upon female fitness in a polyandrous pierid butterfly ( Colias eurytheme ) by comparing life history traits between once-mated females and virgins. Mated females laid relatively more eggs early in their adult life, but suffered a reduction in longevity relative to virgins held under identical experimental conditions. The effect of mating on female survivorship was statistically independent of lifetime and early life fecundity. Moreover, lifetime fecundity co-varied positively with longevity across all females, and across females within each treatment group, hence there was no phenotypic trade-off between survival and reproduction. These results suggest that the observed longevity difference between virgin and mated females represents a true cost of mating, possibly arising from a toxic side effect of the male ejaculate. However, irrespective of this cost, virgin and mated females laid an equivalent lifetime number of eggs. Female C. eurytheme are also known to use nutrients from the male ejaculate to supplement their reproductive output, hence it is presently unclear how the observed longevity cost may have influenced the evolution of lifetime mating schedules in this polyandrous species.     

Parasitoids use herbivore-induced information to adapt patch exploitation behaviour

Abstract.  1. Optimal foraging models ultimately predict that female parasitoids should exploit rich host patches for longer than poorer ones. At the proximate level, mechanistic models and experimental studies show that parasitoids use both chemicals produced by their hosts and direct encounters with their hosts to estimate patch quality. Although it has been extensively studied in the context of host location, the use of herbivore-induced plant response by insect parasitoids has never been considered in the context of patch time allocation.
2. In this study, the respective roles of herbivore-induced plant response and direct contact with hosts on the foraging behaviour of Lysiphlebus testaceipes females on an aphid patch were quantified. For this, the level of herbivore-induced plant response and the number of aphids on the leaf bearing the patch were manipulated independently. Different levels of plant response were obtained by varying the duration of infestation on another leaf.
3. Parasitoid residence time and number of attacks increased with both the level of plant response and the number of aphids.
4. These results suggest that L. testaceipes females use the combination of herbivore-induced response of plants and direct encounters with hosts to assess patch quality and adjust their patch use behaviour.     

The evolutionary dynamics of adaptive virginity,sex‐allocation,and altruistic helping in haplodiploid animals

In haplodiploids, females can produce sons from unfertilized eggs without mating. However, virgin reproduction is usually considered to be a result of a failure to mate, rather than an adaptation. Here, we build an analytical model for evolution of virgin reproduction, sex‐allocation, and altruistic female helping in haplodiploid taxa. We show that when mating is costly (e.g., when mating increases predation risk), virginity can evolve as an adaptive female reproductive strategy. Furthermore, adaptive virginity results in strongly divergent sex‐ratios in mated and virgin queen nests (“split sex ratios”), which promotes the evolution of altruistic helping by daughters in mated queen nests. However, when helpers evolve to be efficient and increase nest production significantly, virgin reproduction is selected against. Our results suggest that adaptive virginity could have been an important stepping stone on the pathway to eusociality in haplodiploids. We further show that virginity can be an adaptive reproductive strategy also in primitively social haplodiploids if workers bias the sex ratio toward females. By remaining virgin, queens are free to produce sons, the more valuable sex in a female‐biased population. Our work brings a new dimension to the studies linking reproductive strategies with social evolution.     

Impact of mating on Anagyrus kamali Moursi (Hym., Encyrtidae) lifetime fecundity, reproductive longevity, progeny emergence and sex ratio

Abstract: The solitary endoparasitoid Anagyrus kamali Moursi (Hym., Encyrtidae) and the Hibiscus mealybug Maconellicoccus hirsutus Green (Hom., Pseudococcidae), were used as a parasite/host model to test the effect of mating on several fitness parameters, i.e. longevity, lifetime fecundity, progeny emergence and sex ratio. At 27 ± 2°C, 8 h light : 16 h dark, mating significantly affected the survival of male parasitoids. Virgin males lived longer (32.2 ± 9.51 days) than mated males (23.9 ± 7.52 days). Female longevity (40.7 ± 16.3 days for virgins and 36.2 ± 10.7 days for mated females) was not affected by mating. The lifetime fecundity of female parasitoids and their oviposition period was not significantly affected by mating. However, the number of hosts parasitized was greater for mated wasps (7.54 ± 4.85 hosts parasitized/day) compared with virgin ones (5.12 ± 2.19 hosts parasitized/day). This resulted in greater progeny production from mated A. kamali females. The progeny of virgin females consisted only of males, whereas the mated ones had a more female‐biased sex ratio. The lowest sex ratio (0.41 M/F ± 0.123) was attained when females had free access to males and were multi‐mated.     

An asexual strain of Lysiphlebus fabarum (Hymenoptera: Braconidae) gains fitness in superparasitised hosts,but a sexual strain pays costs

1. The fitness impacts of two levels of superparasitism were compared in a sexual and an asexual strain of Lysiphlebus fabarum (Marshall) developing in black bean aphids. 2. Asexual females were larger than sexuals, had higher eggs loads, and better adult emergence in two of three treatments, but parasitised fewer available aphids in 24 h (80% fewer when foraging alone). 3. Superparasitism resulted in wasps that were larger than those emerging from singly parasitised aphids, and asexual females had larger ovaries, without delayed development. In contrast, sexual wasps took about 2 days longer to develop in superparasitised hosts, and females had smaller ovaries with lower egg loads. 4. The growth of host aphids bearing asexual larvae was not reduced relative to healthy aphids, except when heavily superparasitised, whereas sexual larvae reduced aphid growth in all treatments. 5. Elimination of supernumerary larvae was virtually complete at 4.5 days after parasitism by sexual females, but no elimination occurred among asexual larvae. The evolution of diminished aggression in asexual larvae may be facilitated by greater genetic similarity, without necessarily leading to gregarious development, assuming the extended life of supernumeraries somehow improves survivor fitness. 6. Sons of virgin sexual females developed faster than sons of mated females, implicating parental effects that slowed development of the latter. 7. It is concluded that asexual females of this strain use superparasitism to improve host quality, and thus the fitness of their daughters, whereas females of the sexual strain prioritise offspring number.     

Male age and sexual experience affect male mating behavior in the hawthorn spider mite,Amphitetranychus viennensis

As is reported, in species with first-male sperm precedence, male age and previous sexual experience play crucial roles in male mating behavior. In the hawthorn spider mite, Amphitetranychus viennensis Zacher, previous studies showed that only females that copulated for the first time could achieve fertilization. Based on this, the effects of male age and mating history on male mate choice and male mate competition were investigated. It was confirmed that males could distinguish virgins from fertilized females but they were unable to discriminate between virgins and unfertilized females. Interestingly, the copulation duration of males mated with fertilized females was much shorter than that of males mated with virgins or unfertilized females. Additionally, for male mating choice, males of all ages and more experienced males preferred 5-day-old virgin females, whereas only less experienced males preferred 1-day-old virgin females. In male-male competition, 3-day-old males were more competitive and obtained more copulations compared with others. Copula duration was closely related to male age. Though no significant differences were observed in mating competition between virgin and mated males, copula duration of males in first copulation was the longest and gradually shortened in subsequent copulations. In all, this investigation demonstrated that male age and sexual experience affected male mate choice and male-male competition, leading to further insight into the influences of male age and sexual experience on the reproductive fitness of both sexes.

     

Host-searching and mating in an outbreeding parasitoid wasp

Abstract.

• 1 Female parasitoid wasps (Hymenoptera) must search for hosts to reproduce, but only require mates if their broods are to contain female progeny. In outbreeding species, females locate mates after dispersal from the emergence site. Unmated females may therefore face a trade-off between searching for hosts and searching for mates, if hosts and mates are spatially separated.
• 2 In the outbreeding parasitoid Bracon hebetor Say (Hymenoptera: Braconidae), males and females are spatially segregated in the field. Females are found primarily below the surface of stored corn where they search for hosts, whereas males are found on or above the surface.
• 3 Wasps placed in laboratory observation chambers designed to mimic B.hebetor's stored corn habitat distributed themselves in a manner consistent with field observations. Males remained on the surface of the grain, whereas females moved below the surface to attack hosts.
• 4 In the laboratory, female distribution was influenced by their mating status, the presence of males or hosts, and female age. Virgin females were more reluctant to move into the corn than were mated females, younger females foraged deeper than older females, and all females moved deeper into the com when males were present.
• 5 10% of all females did not mate even when males were present in the chambers, a percentage consistent with previous observations from the field. If B.hebetor faces a trade-off between host-searching and mate-searching, the trade-off seems to be part of 'split sex ratio strategies', with some females remaining constrained to producing only male offspring.

     

Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank voles Clethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those of monandrous females. This was mainly due to sons of polyandrous females producing significantly more offspring than those of monandrous females. No significant differences were found for offspring body mass or winter survival between the two treatments. Our results appear to provide evidence that bank vole females gain long-term benefits from polyandry.     

Mating status affects female choice when females are signalers

Sexual selection in animals has been mostly studied in species in which males are signalers and females are choosers. However, in many species, females are (also) signalers. In species with non‐signaling females, virgin females are hypothesized to be less choosy than mated females, as virgins must mate to realize fitness and the number of available males is generally limited. Yet, when females signal to attract males, mate limitation can be overcome. We tested how virgin and mated females differ in their calling behavior, mating latency, and in mate choice, using the tobacco budworm Chloridea (Heliothis) virescens as an example for a species in which females are not only choosers but also signalers. We found that virgin females signaled longer than mated females, but virgin and mated signaling females were equally ready to mate, in contrast to non‐signaling females. However, we found that virgin signaling females showed weaker mate preference than mated females, which can be explained by the fact that females increase their fitness with multiple matings. Mated females may thus further increase their fitness by more stringent mate selection. We conclude that signaling is a crucial aspect to consider when studying female mate choice because signaling may affect the number of available mates to choose from.     

Impact of male mating history on the temporal sperm dynamics of Choristoneura rosaceana and C. fumiferana females

In the oblique-banded leafroller, Choristoneura rosaceana, and the spruce budworm, C. fumiferana, male reproductive performance decreases with consecutive matings. While the onset time of mating did not vary, the time spent mating was longer in mated than in virgin males. Furthermore, a decline observed in the spermatophore mass with successive matings was associated with a concomitant decline in its apyrene and eupyrene spermatozoa content. In the hours following mating, spermatozoa migrate from the spermatophore, located in the bursa copulatrix, to the spermatheca. Regardless of the male's previous mating history, the number of apyrene sperm dropped rapidly in the days following mating whereas the number of eupyrene spermatozoa declined gradually. As the temporal pattern of sperm movement was similar in all treatments, females mated with previously-mated males would suffer from sperm shortage sooner than those mated with virgins. Large C. rosaceana females stored more apyrene spermatozoa in their spermatheca than small ones, irrespective of the time after mating or male mating history, while only large females mated with once-mated males received more apyrene sperm and accessory gland secretions than small ones mated with virgin or twice-mated males. The results obtained in this study are discussed in relation with their potential impact on the reproductive success of both sexes.     

Variability and Parasitoid Foraging Efficiency: A Case Study of Pea Aphids and Aphidius ervi

When a parasitoid is searching for hosts, not all hosts are equally likely to be attacked. This variability in attack probability may affect the parasitoid functional response. Using a collection of experiments, we quantified the functional response of Aphidius ervi (Hymenoptera: Braconidae), an insect parasitoid of the pea aphid Acyrthosiphon pisum (Homoptera: Aphididae). We measured variability in the number of hosts attacked by a foraging parasitoid both among plants and within plants. At the first scale, A. ervi, searching among plants containing different numbers of aphids, showed both aphid-density-dependent and aphid-density-independent variability in the number of aphids attacked per plant. Within plants, A. ervi selectively attacked second and third instar aphids relative to other instars. Furthermore, there was variability in the susceptibility of attack among aphids independent of instar. Variability in attack rates among aphids both among and within plants decreased parasitoid foraging efficiency, with the greatest decrease caused by among-plant variability. Furthermore, the decrease in foraging efficiency was greatest when the average number of aphids per plant was low, thereby transforming a strong Type II functional response into one approaching Type I.     

Seminal fluids mediate sexual inhibition and short copula duration in mated female Queensland fruit flies

Molecules in male seminal fluid transferred to female insects during mating can have potent effects on their subsequent sexual and reproductive behaviour. Like many other tephritids, female Queensland fruit flies (Bactrocera tryoni) typically have diminished sexual receptivity after their first mating. Also, copulations of females that do remate tend to be shorter than those of virgins. We here find that virgin females injected with small doses (0.1, 0.2 or 0.5 male equivalents) of extracts from the male reproductive tract accessory tissues, which consist of male accessory glands, ejaculatory apodeme and ejaculatory duct (AG/EA/ED), have diminished receptivity and short copula duration very similar to naturally mated females. In contrast, virgin females injected with saline or with high doses of AG/EA/ED (1 or 2 male equivalents) that likely exceed the range of natural variation retain the higher levels of sexual receptivity and longer copulations of un-injected virgins. We conclude that reduced sexual receptivity and shorter copulations of mated female Q-flies are mediated by products in the male seminal fluid derived from the male reproductive tract accessory tissues.     

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.