Rebecca A. Boulton

Beyond sex allocation: the role of mating systems in sexual selection in parasitoid wasps.

Despite the diverse array of mating systems and life histories which characterise the parasitic Hymenoptera, sexual selection and sexual conflict in this taxon have been somewhat overlooked. For instance, parasitoid mating systems have typically been studied in terms of how mating structure affects sex allocation. In the past decade, however, some studies have sought to address sexual selection in the parasitoid wasps more explicitly and found that, despite the lack of obvious secondary sexual traits, sexual selection has the potential to shape a range of aspects of parasitoid reproductive behaviour and ecology. Moreover, various characteristics fundamental to the parasitoid way of life may provide innovative new ways to investigate different processes of sexual selection. The overall aim of this review therefore is to re‐examine parasitoid biology with sexual selection in mind, for both parasitoid biologists and also researchers interested in sexual selection and the evolution of mating systems more generally. We will consider aspects of particular relevance that have already been well studied including local mating structure, sex allocation and sperm depletion. We go on to review what we already know about sexual selection in the parasitoid wasps and highlight areas which may prove fruitful for further investigation. In particular, sperm depletion and the costs of inbreeding under chromosomal sex determination provide novel opportunities for testing the role of direct and indirect benefits for the evolution of mate choice.

The costs and benefits of multiple mating in a mostly monandrous wasp

The taxonomically widespread nature of polyandry remains a puzzle. Much of the empirical work regarding the costs and benefits of multiple mating to females has, for obvious reasons, relied on species that are already highly polyandrous. However, this makes it difficult to separate the processes that maintain the current level of polyandry from the processes that facilitate its expression and initiated its evolution. Here we consider the costs and benefits of polyandry in Nasonia vitripennis, a species of parasitoid wasp that is “mostly monandrous” in the wild, but which evolves polyandry under laboratory culture conditions. In a series of six experiments, we show that females gain a direct fecundity and longevity benefit from mating multiply with virgin males. Conversely, mating multiply with previously mated males actually results in a fecundity cost. Sexual harassment may also represent a significant cost of reproduction. Harassment was, however, only costly during oviposition, resulting in reduced fecundity, longevity, and disrupted sex allocation. Our results show that ecological changes, in our case associated with differences in the local mating structure in the laboratory can alter the costs and benefits of mating and harassment and potentially lead to shifts in mating patterns.

Life Cycle and Host Specificity of the Parasitoid Conura annulifera (Hymenoptera: Chalcididae), a Potential Biological Control Agent of Philornis downsi (Diptera: Muscidae) in the Galápagos Islands

Abstract The neotropical parasitoid Conura annulifera (Walker) (Hymenoptera: Chalcididae) is known to parasitize bird-parasitic flies in the genus Philornis (Diptera: Muscidae) including P. downsi (Dodge and Aitken), a species that has invaded the Galápagos islands and is negatively impacting populations of Darwins finches. We report here some aspects of the life history, field ecology, and host specificity of C. annulifera. We collected puparia of four Philornis species in 13 bird nests during 2015 and 2016 in western mainland Ecuador and found that C. annulifera and three other parasitoid species emerged from those puparia. This is the first record of C. annulifera in Ecuador. Rearing records and dissections of parasitized puparia revealed that C. annulifera is a solitary pupal ectoparasitoid, placing its eggs in the gap between host pupa and puparium. Laboratory studies of host specificity involving P. downsi and pupae from five other dipteran, three lepidopteran, and one hymenopteran species found that C. annulifera only produced progeny when presented with P. downsi pupae. Pupae of P. downsi that had been exposed to C. annulifera also failed to emerge more often than expected by chance compared with no-parasitoid controls, suggesting that the parasitoids can cause developmental mortality through means other than successful parasitism. These studies constitute the first steps in evaluating C. annulifera as a potential biological control agent of P. downsi in the Galápagos Islands.

Polyandry is context-dependent but not convenient in a mostly monandrous wasp

Research over the past two decades suggests that polyandry is almost ubiquitous in nature. In some cases, females can gain direct and indirect (genetic) fitness benefits from mating with multiple males. However, when females accept superfluous matings without gaining any clear benefit, polyandry has been interpreted as a strategy to mitigate the costs of resisting or avoiding matings, a situation known as convenience polyandry. When females mate out of ‘convenience’ the mating rate is expected to be plastic, since females should mate at a higher rate when the costs of resistance or avoidance are high, for instance when males occur in high densities and/or around resources required by females such as oviposition sites. Here we show that remating in Nasonia vitripennis , a species of wasp that is largely monandrous in the wild but that evolves polyandry under laboratory culture, is dependent upon the availability of hosts for oviposition and upon male density. We found that females mated at a higher rate when male density was high but only if a suitable oviposition substrate was available. Outwardly this seems suggestive of convenience polyandry. However, females that remated under these conditions did not gain more time to oviposit than females that resisted superfluous matings. The results of this study highlight the importance of comprehensively assessing the costs and benefits of mating before attributing the observed behaviour to convenience polyandry. Furthermore, these results add to the growing body of evidence that the ecological context under which sexual interactions occur is critical to the economics of mating.

Sex allocation and the evolution of insemination capacity under local mate competition

Local mate competition (LMC) theory has proved enormously successful in predicting sex ratios across a broad range of organisms when localised mating patches lead to mating competition amongst kin. As such, LMC is a key component of sex allocation theory. However, the mating systems that influence and promote LMC also shape other traits, as well as sex allocation. These aspects of LMC mating systems have received far less attention, including in species where LMC is common, such as parasitoid wasps. Here, we consider how LMC influences the evolution of insemination capacity in parasitoids, a key reproductive allocation decision for males that should be under both natural and sexual selection. Basic LMC theory predicts that a single female exploiting a patch should produce just enough sons to inseminate all her daughters, that is, between them these sons should have sufficient insemination capacity to inseminate their sisters. However, the insemination capacity of males is generally higher than predicted and, in order to classify parasitoid species, we propose an Index of Insemination Strategy (IIS): the ratio between the insemination capacity of males on the emergence patch and the average number of females available per male at emergence on that patch. A survey of IIS for 25 species belonging to 10 hymenopteran families showed that IIS values ranged from 0.9 to 40.9, supporting the idea that males typically have more sperm than predicted. Several factors could explain these high IIS values, including non‐local mating, temporal variation in emergence, variation in mate acquisition capacity, the intensity of sperm competition, and responses to host quality.

Do mothers prefer helpers or smaller litters? Birth sex ratio and litter size adjustment in cotton-top tamarins (Saguinus oedipus)

Sex allocation theory has been a remarkably productive field in behavioral ecology with empirical evidence regularly supporting quantitative theoretical predictions. Across mammals in general and primates in particular, however, support for the various hypotheses has been more equivocal. Population-level sex ratio biases have often been interpreted as supportive, but evidence for small-scale facultative adjustment has rarely been found. The helper repayment (HR) also named the local resource enhancement (LRE) hypothesis predicts that, in cooperatively breeding species, mothers invest more in the sex which assists with rearing future offspring and that this bias will be more pronounced in mothers who require extra assistance (i.e., due to inexperience or a lack of available alloparents). We tested these hypotheses in captive cotton-top tamarins (Saguinus oedipus) utilizing the international studbook and birth records obtained through a questionnaire from ISIS-registered institutions. Infant sex, litter size, mothers age, parity, and group composition (presence of nonreproductive subordinate males and females) were determined from these records. The HR hypothesis was supported over the entire population, which was significantly biased toward males (the “helpful” sex). We found little support for helper repayment at the individual level, as primiparous females and those in groups without alloparents did not exhibit more extreme tendencies to produce male infants. Primiparous females were, however, more likely to produce singleton litters. Singleton births were more likely to be male, which suggests that there may be an interaction between litter size adjustment and sex allocation. This may be interpreted as supportive of the HR hypothesis, but alternative explanations at both the proximate and ultimate levels are possible. These possibilities warrant further consideration when attempting to understand the ambiguous results of primate sex ratio studies so far.

A sex allocation cost to polyandry in a parasitoid wasp

The costs and benefits of polyandry are central to understanding the near-ubiquity of female multiple mating. Here, we present evidence of a novel cost of polyandry: disrupted sex allocation. In Nasonia vitripennis, a species that is monandrous in the wild but engages in polyandry under laboratory culture conditions, sexual harassment during oviposition results in increased production of sons under conditions that favour female-biased sex ratios. In addition, females more likely to re-mate under harassment produce the least female-biased sex ratios, and these females are unable to mitigate this cost by increasing offspring production. Our results therefore argue that polyandry does not serve to mitigate the costs of harassment (convenience polyandry) in Nasonia. Furthermore, because males benefit from female-biased offspring sex ratios, harassment of ovipositing females also creates a novel cost of that harassment for males.

An Inconvenient Truth: The Unconsidered Benefits of Convenience Polyandry

Polyandry, or multiple mating by females with different males, is commonplace. One explanation is that females engage in convenience polyandry, mating multiple times to reduce the costs of sexual harassment. Although the logic underlying convenience polyandry is clear, and harassment often seems to influence mating outcomes, it has not been subjected to as thorough theoretical or empirical attention as other explanations for polyandry. We re-examine here convenience polyandry in the light of new studies demonstrating previously unconsidered benefits of polyandry. We suggest that true convenience polyandry is likely to be a fleeting phenomenon, even though it can profoundly shape mating-system evolution via potential feedback loops between resistance to males and the costs and benefits of mating.

Differential gene expression is not required for facultative sex allocation : a transcriptome analysis of brain tissue in the parasitoid wasp Nasonia vitripennis

Whole-transcriptome technologies have been widely used in behavioural genetics to identify genes associated with the performance of a behaviour and provide clues to its mechanistic basis. Here, we consider the genetic basis of sex allocation behaviour in the parasitoid wasp Nasonia vitripennis. Female Nasonia facultatively vary their offspring sex ratio in line with Hamiltons theory of local mate competition (LMC). A single female or ‘foundress’ laying eggs on a patch will lay just enough sons to fertilize her daughters. As the number of ‘foundresses’ laying eggs on a patch increases (and LMC declines), females produce increasingly male-biased sex ratios. Phenotypic studies have revealed the cues females use to estimate the level of LMC their sons will experience, but our understanding of the genetics underlying sex allocation is limited. Here, we exposed females to three foundress number conditions, i.e. three LMC conditions, and allowed them to oviposit. mRNA was extracted from only the heads of these females to target the brain tissue. The subsequent RNA-seq experiment confirmed that differential gene expression is not associated with the response to sex allocation cues and that we must instead turn to the underlying neuroscience to reveal the underpinnings of this impressive behavioural plasticity.

Environmentally cued hatching in the bird‐parasitic nest fly Philornis downsi

Under the hypothesis of environmentally cued hatching (ECH), eggs are stimulated to hatch by cues favouring larval survival. Here we investigated whether the bird‐parasitic nest fly Philornis downsi Dodge & Aitken (Diptera: Muscidae) exhibits ECH in response to the presence of suitable hosts and environmental conditions. Philornis downsi is an invasive in the Galapagos Islands and ECH could help to explain its success in a novel habitat. We found that the presence of hosts (nesting birds) per se does not accelerate hatching time in P. downsi, but that nesting birds do produce a microclimate, in terms of temperature and/or humidity that is conducive to faster hatching and higher hatching success. Eggs that are laid under extremely dry conditions die rather than delay their hatching time. We also found that P. downsi eggs hatch more rapidly when the substrate is very wet. Furthermore, larvae that hatch rapidly survive longer under starvation conditions. We suggest that eggs hatching more rapidly can either take advantage of optimal conditions for larval growth (host presence) or escape unfavourable microclimatic conditions (as larvae are mobile).