Paul J. Ode

Host-size-dependent sex ratio theory and improving mass-reared parasitoid sex ratios

Although an effective parasitoid of agromyzid leafminers, Diglyphus isaea (Walker) (Hymenoptera: Eulophidae) is an expensive biological control agent in terms of production costs. In part, these costs arise from the production of male-biased offspring sex ratios. Here, we present a mass-rearing technique that will increase the proportion of females produced and reduce the need for frequent releases in biocontrol programs. By presenting female D. isaea groups of sequentially larger leafminer hosts to attack, we are able to generate progressively more female-biased sex ratios. After three days of providing increasingly larger hosts, we were able to reduce the sex ratios produced by individual females from 57% male to 36% male; sex ratios produced by groups of females dropped from 64% male to 45% male. Several attributes of D. isaea sex allocation allow us to manipulate sex allocation behavior. First, D. isaea is a solitary idiobiont; resources available to each offspring are present at the time of attack allowing the ovipositing female to accurately assess host quality. Host size positively affects both male and female wasps. Females laid more daughters in larger hosts and more sons in smaller hosts. We show that the observed relationship between host size and offspring sex ratio is due to maternal sex allocation decisions rather than differential mortality. Furthermore, assessment of the size threshold was relative to prior host encounters rather than an absolute assessment. Our simple memory model suggests that while females are influenced most strongly by recent encounters, females also base their assessment of the host-size threshold on prior host encounters. 2002 Elsevier Science (USA). All rights reserved.

Progeny and sex allocation decisions of the polyembryonic wasp Copidosoma floridanum.

1. The reproductive biology of the polyembryonic encyrtid wasp Copidosoma floridanum was examined in a series of laboratory experiments and related to observations from field collections. Females laid one or two eggs per host, producing broods comprised of all males, all females, or both sexes (mixed). Each egg produced multiple embryos that developed into either precocious larvae that never became adult or reproductive larvae that developed into reproductive adults. 2. The age of the host-egg when it was parasitized was found to have a substantial effect on offspring clutch sizes and sex ratios. (i) The clutch sizes and overall survivorship of female and mixed broods decreased with increasing host-egg age, whereas male clutch sizes and survivorship were relatively unaffected by host-egg age. (ii) Offspring sex ratios (proportion males) of mixed broods were higher in older hosteggs. (iii) Body sizes of males and females were negatively correlated with clutch size. Larger females had higher fecundities and larger males had greater mating abilities. 3. Host-egg age also affected competitive asymmetries between males and females. In young host-eggs, female precocious larvae were much more abundant than males and were instrumental in reducing the number of males in mixed broods. In older host-eggs, the numbers of male and female precocious larvae were much lower, and were approximately equal. As a result, sex ratios of mixed broods in older host eggs were closer to equality. 4. Ovipositing females responded to host-egg age and host encounter rates when making oviposition decisions. Females laid more female eggs in younger hosts and more mixed broods in older hosts. Females laid more mixed broods when encounter rates were low and more female broods when encounter rates were high

Brood-mate avoidance in the parasitic waspBracon hebetorSay

The parasitic waspBracon hebetorsuffers severe inbreeding depression. This study examined two behavioural mechanisms that minimize mating between close relatives. First, the majority of males and females were unwilling to mate immediately upon emergence. Receptivity to mating slowly increased with age of the adult. By the time most individuals were willing to mate, the majority of wasps had dispersed from the natal site. Second, females tended to avoid mating with brood-mates when given a choice between a male that developed on the same host and one that developed on a different host. Experiments using eye-colour mutants and broods composed of relatives and non-relatives indicated that females discriminated against male brood-mates on the basis of environmental cues. Females consistently mated with brothers and non-brothers if they developed on another host, but tended to reject brothers and non-brothers from the same brood as themselves. Females maintained the ability to recognize brood-mates for at least 5 days after eclosion.

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

Abstractu2002In 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.

Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis

In the Hymenoptera, males develop as haploids from unfertilized eggs and females develop as diploids from fertilized eggs. In species with complementary sex determination (CSD), however, diploid males develop from zygotes that are homozygous at a highly polymorphic sex locus or loci. We investigated mating behavior and reproduction of diploid males of the parasitoid wasp Cotesia vestalis (C. plutellae), for which we recently demonstrated CSD. We show that the behavior of diploid males of C. vestalis is similar to that of haploid males, when measured as the proportion of males that display wing fanning, and the proportion of males that mount a female. Approximately 29% of diploid males sired daughters, showing their ability to produce viable sperm that can fertilize eggs. Females mated to diploid males produced all-male offspring more frequently (71%) than females mated to haploid males (27%). Daughter-producing females that had mated to diploid males produced more male-biased sex ratios than females mated to haploid males. All daughters of diploid males were triploid and sterile. Three triploid sons were also found among the offspring of diploid males. It has been suggested that this scenario, that is, diploid males mating with females and constraining them to the production of haploid sons, has a large negative impact on population growth rate and secondary sex ratio. Selection for adaptations to reduce diploid male production in natural populations is therefore likely to be strong. We discuss different scenarios that may reduce the sex determination load in C. vestalis.

Sex Allocation and Sexual Asymmetries in Intra-Brood Competition in the Parasitic Wasp Bracon hebetor

1. Bracon hebetor is a gregarious parasitoid with a female-biased sex ratio. While female-biased sex ratios are often indicative of local mate competition (LMC), B. hebetor outbreeds, making LMC an unlikely explanation for biased sex ratios in this species. In this study we examined an alternative hypothesis that may explain female-biased sex ratios: competitive asymmetries between larval sons and daughters. 2. We measured two types of competitive asymmetries: asymmetric density responses (differential responses to clutch size), and asymmetric composition responses (responses to change in clutch sex ratio). We measured competitive asymmetries in terms of their effects on body size, development time, survivorship, longevity, and daily and lifetime fecundity or mating ability. 3. Males and females emerged as smaller adults, developed more quickly and experienced higher rates of larval mortality when they developed in larger clutches. The effect of clutch size on body size and survivorship was similar for males and females. Increasing clutch size decreased male larval development time more than female development time, although the effect was marginal. 4. Male and female body sizes increased as within-clutch sex ratios became more male-biased, indicating that females, not males, are stronger competitors. This should lead to male-biased sex ratios, rather than the female-biased sex ratios that exist in B. hebetor. Sex ratio had no influence on developmental time or survivorship of either sex. 5. Larger males and females lived longer than smaller individuals, whether they fed on hosts or honey. Larger females had higher daily and lifetime fecundities than smaller females. Larger males copulated with more females and sired more daughters both per day and per lifetime than did smaller males. These body size effects were only detectable when hosts were abundant. At low host densities, differences between large and small wasps were absent. 6. Although we detected asymmetric composition responses in terms of body size, the effects were slight. Therefore, we conclude that competitive asymmetries are unlikely to have important effects on male and female fitness or on the sex allocation decisions of B. hebetor.

Variable sex ratios and ovicide in an outbreeding parasitic wasp

Abstract Bracon hebetor Say (Hymenoptera: Braconidae) is a gregarious parasitoid of phycitine moth larvae that infest stored grain. It has been hypothesized that B. hebetor females produce proportionately more female offspring under conditions of superparasitism (when laying eggs on previously parasitized hosts) because daughters are reproductively more valuable than sons when resources are limiting and adult body sizes are reduced. This hypothesis was re-examined by measuring the effects of body size on male and female performance and by monitoring the sex ratios and clutch sizes of individual females. The results of this study provide only weak evidence that small size differentially affects the reproductive success of male and female B. hebetor . Sex ratios were more female-biased on superparasitized hosts, but the difference arose as a consequence of two aspects of oviposition behaviour. First, male eggs were laid later within ovipositional sequences, and second, females laid smaller clutches when superparasitizing. A larger sex-ratio shift towards male progeny was seen, however, in females that committed ovicide (i.e. killed some of anothers eggs by piercing them with the ovipositor). The offspring sex ratios of ovicidal females were much less female-biased because these females laid male eggs earlier in the ovipositional sequence. Ovicidal females shifted their sex ratios whether superparasitizing or ovipositing alone. None of the females killed their own eggs, even though they were observed probing among them with their ovipositors. It is hypothesized that oviposition behaviour and sex ratio in B. hebetor may be grouped into two syndromes: ovicidal and non-ovicidal. The variation in sex ratio and ovicide may be a consequence of density-dependent selection, favouring non-ovicidal behaviour when population density is low and ovicidal behaviour when the density is high and competition for larval resources is acute.

Integration of Plant Defense Traits with Biological Control of Arthropod Pests: Challenges and Opportunities

Crop plants exhibit a wide diversity of defensive traits and strategies to protect themselves from damage by herbivorous pests and disease. These defensive traits may be naturally occurring or artificially selected through crop breeding, including introduction via genetic engineering. While these traits can have obvious and direct impacts on herbivorous pests, many have profound effects on higher trophic levels, including the natural enemies of herbivores. Multi-trophic effects of host plant resistance have the potential to influence, both positively and negatively, biological control. Plant defense traits can influence both the numerical and functional responses of natural enemies; these interactions can be semiochemically, plant toxin-, plant nutrient-, and/or physically mediated. Case studies involving predators, parasitoids, and pathogens of crop pests will be presented and discussed. These diverse groups of natural enemies may respond differently to crop plant traits based on their own unique biology and the ecological niches they fill. Genetically modified crop plants that have been engineered to express transgenic products affecting herbivorous pests are an additional consideration. For the most part, transgenic plant incorporated protectant (PIP) traits are compatible with biological control due to their selective toxicity to targeted pests and relatively low non-target impacts, although transgenic crops may have indirect effects on higher trophic levels and arthropod communities mediated by lower host or prey number and/or quality. Host plant resistance and biological control are two of the key pillars of integrated pest management; their potential interactions, whether they are synergistic, complementary, or disruptive, are key in understanding and achieving sustainable and effective pest management.

Experimental Support for Multiple Locus Complementary Sex Determination in the Parasitoid Cotesia vestalis

Despite its fundamental role in development, sex determination is highly diverse among animals. Approximately 20% of all animals are haplodiploid, with haploid males and diploid females. Haplodiploid species exhibit diverse but poorly understood mechanisms of sex determination. Some hymenopteran insect species exhibit single-locus complementary sex determination (sl-CSD), where heterozygosity at a polymorphic sex locus initiates female development. Diploid males are homozygous at the sex locus and represent a genetic load because they are inviable or sterile. Inbreeding depression associated with CSD is therefore expected to select for other modes of sex determination resulting in fewer or no diploid males. Here, we investigate an alternative, heretofore hypothetical, mode of sex determination: multiple-locus CSD (ml-CSD). Under ml-CSD, diploid males are predicted to develop only from zygotes that are homozygous at all sex loci. We show that inbreeding for eight generations in the parasitoid wasp Cotesia vestalis leads to increasing proportions of diploid males, a pattern that is consistent with ml-CSD but not sl-CSD. The proportion of diploid males (0.27 ± 0.036) produced in the first generation of inbreeding (mother–son cross) suggests that two loci are likely involved. We also modeled diploid male production under CSD with three linked loci. Our data visually resemble CSD with linked loci because diploid male production in the second generation was lower than that in the first. To our knowledge, our data provide the first experimental support for ml-CSD.

Differential dispersal and female-biased sex allocation in a parasitic wasp

1. Differential dispersal of males and females from a population is predicted to result in biased sex‐allocation decisions, even in the absence of sibmating.