Sex allocation theory reveals a hidden cost of neonicotinoid exposure in a parasitoid wasp

P.R.W. was funded by the University of Stirling, C.V.B. and S.M.G. were funded by Nuffield Research Placements and N.C., J.G. and D.M.S. were funded by NERC (NE/J024481/1).Sex allocation theory has proved to be one the most successful theories in evolutionary ecology. However, its role in more applied aspects of ecology has been limited. Here we show how sex allocation theory helps uncover an otherwise hidden cost of neonicotinoid exposure in the parasitoid wasp Nasonia vitripennis. Female N. vitripennis allocate the sex of their offspring in line with Local Mate Competition (LMC) theory. Neonicotinoids are an economically important class of insecticides, but their deployment remains controversial, with evidence linking them to the decline of beneficial species. We demonstrate for the first time to our knowledge, that neonicotinoids disrupt the crucial reproductive behaviour of facultative sex allocation at sub-lethal, field-relevant doses in N. vitripennis. The quantitative predictions we can make from LMC theory show that females exposed to neonicotinoids are less able to allocate sex optimally and that this failure imposes a significant fitness cost. Our work highlights that understanding the ecological consequences of neonicotinoid deployment requires not just measures of mortality or even fecundity reduction among non-target species, but also measures that capture broader fitness costs, in this case offspring sex allocation. Our work also highlights new avenues for exploring how females obtain information when allocating sex under LMC.Publisher PDFPeer reviewe

The definition of sexual selection

The work was supported by Vetenskapsrådet (2020-04992) to C.K.Sexual selection is a key component of evolutionary biology. However, from the very formulation of sexual selection by Darwin, the nature and extent of sexual selection have been controversial. Recently, such controversy has led back to the fundamental question of just what sexual selection is. This has included how we incorporate female-female reproductive competition into sexual or natural selection. In this review, we do four things. First, we examine what we want a definition to do. Second, we define sexual selection: sexual selection is any selection that arises from fitness differences associated with nonrandom success in the competition for access to gametes for fertilization. An important outcome of this is that as mates often also offer access to resources, when those resources are the targets of the competition, rather than their gametes, the process should be considered natural rather than sexual selection. We believe this definition encapsulates both much of Darwin’s original thinking about sexual selection, and much of how contemporary biologists use the concept of sexual selection. Third, we address alternative definitions, focusing in some detail on the role of female reproductive competition. Fourth, we challenge our definition with a number of scenarios, for instance where natural and sexual selection may align (as in some forms of endurance rivalry), or where differential allocation means teasing apart how fecundity and access to gametes influence fitness. In conclusion, we emphasize that whilst the ecological realities of sexual selection are likely to be complex, the definition of sexual selection is rather simple.Publisher PDFPeer reviewe

The definition of sexual selection : a response to comments on Shuker and Kvarnemo

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Образовательное учреждение: проблемы правового регулирования организационно-правовой формы

The vertebrate stress response has been shown to suppress investment in reproductive and immune function and may also lead to a reduced investment in the production of secondary sexual traits. However, it has been difficult to model roles of stress in sexual selection due to the inconsistent results seen in empirical studies testing for the effect of stress on the expression of secondary sexual traits. We conducted a phylogenetically controlled meta-analysis of published associations between physiological correlates of stress and sexual signaling in vertebrates in order to identify any consistent patterns. Our analysis included signaling in both males and females, 4 stress measures, and 4 categories of sexually selected traits (vocalizations, traits that varied in size, traits that varied in coloration, and opposite-sex preference). Across 38 studies of 26 species, there was no significant relationship between physiological correlates of stress and the expression of sexual signals. Mean effect size, however, varied significantly across the 4 types of sexually selected trait. We propose development of a model that incorporates the nuanced effects of species ecology, trait type, ecological context, and the complex nature of the physiological stress response, on the expression of sexually selected traits

Is mating failure caused by cryptic male choice in the seed bug Lygaeus simulans?

Funding: VLB was funded by a University of St Andrews PhD Apprenticeship.One yet unresolved question in the study of mating system evolution is the occurrence of mating failure, when individuals go through their lives without successfully mating. This includes the failure to produce offspring even following copulation, for instance due to insemination or fertilisation failure. Copulations are costly in a variety of ways, but also a fundamental route to fitness in sexual species, and so we should expect that engaging in copulations that generate no offspring should be strongly selected against. Nonetheless, it has become apparent that mating failure is quite common in nature. Here we consider post‐copulatory sexual selection in Lygaeus simulans seed bugs to test the hypothesis that the high levels of mating failure found in this species (approximately 40%–60%) are caused by cryptic male choice (i.e. males choosing not to inseminate a female during copulation). In our first experiment, we found that mating failure depended on female size, but not male size, with smaller females experiencing mating failure more frequently. Mechanistically this is likely to be due to copulation duration, as shorter copulations were more likely to lead to mating failure. Likewise, copulations with smaller females were shorter. In our second and third experiments, rates of mating failure decreased when pairs were allowed to repeatedly interact with the same partner over longer durations (hours through to days), implying that mating failure is not primarily caused by infertility or chronic mechanical failure. Instead, our results strongly suggest cryptic male choice as the cause of mating failure in this species.Peer reviewe

Context-dependent use of visual cues in the shell selection behaviour of the hermit crab Pagurus bernhardus

Animals avoid predator attack in different ways; some carry defensive structures to reduce predation, with the classic example being hermit crabs and their use of a mollusc shell as a portable refugium. During shell selection, various shell characteristics are investigated by the crab to determine their suitability. Here we consider the role of visual cues. Previous research suggests that some hermit crabs are more likely to initially choose a conspicuous shell but also to move to backgrounds against which they are less conspicuous, suggesting a short-term/long-term trade-off. Across experiments in which we manipulated shell and background colour, we show initially that Pagurus bernhardus prefer black shells over white but this preference was lost in the absence of visual cues. We then show that the strength of preference was dependent on background colour. We repeated this last experiment with red and yellow shells against red or yellow backgrounds to investigate whether this preference extended to chromatic hues. A preference for darker (red) shells was expressed, but preference alteration with background was not observed. P. bernhardus therefore discriminate between shells in terms of shell and background colour, and discrimination may be rooted in a preference for darker shaded shells.PostprintPeer reviewe

Can females choose to avoid mating failure in the seed bug Lygaeus simulans?

We thank the Natural Environmental Research Council (Ph.D. studentship to E.V.G.) and the Association for the Study of Animal Behaviour (Undergraduate Project Scholarship awarded to V.L.B.) for funding.It is becoming increasingly clear that copulation does not necessarily always lead to offspring production in many organisms, despite fertilization success presumably being under both strong natural and sexual selection. In the seed bug Lygaeus simulans, between 40% and 60% of copulations fail to produce offspring, with this ‘mating failure’ representing a significantly repeatable male-associated trait. Mating has been demonstrated to be costly in this species and, as such, we might expect females to minimize the chance of mating failure by displaying a preference for males with higher insemination success where possible. After assaying males for mating failure, we asked whether females preferred males with a history of successful inseminations versus unsuccessful inseminations in pairwise mate choice trials. Contrary to our expectations, females showed no preference for more successful over less successful males. Moreover, females showed no preference for larger males in the choice trials, even though larger males were significantly more likely to successfully inseminate females in the initial assay. This apparent lack of female precopulatory choice suggests that postcopulatory choice mechanisms may be key to mating failure in this species. However, this does not necessarily explain why females pay the cost of mating with males they will then reject via postcopulatory processes. More generally, our results suggest that mating failure may play a largely underappreciated role in mating systems evolution, influencing both the cost of choosiness, and the costs and benefits of polyandry.Publisher PDFPeer reviewe

Inbreeding and selection on sex ratio in the bark beetle Xylosandrus germanus

Background Local Mate Competition (LMC) theory predicts a female should produce a more female-biased sex ratio if her sons compete with each other for mates. Because it provides quantitative predictions that can be experimentally tested, LMC is a textbook example of the predictive power of evolutionary theory. A limitation of many earlier studies in the field is that the population structure and mating system of the studied species are often estimated only indirectly. Here we use microsatellites to characterize the levels of inbreeding of the bark beetle Xylosandrus germanus, a species where the level of LMC is expected to be high. Results For three populations studied, genetic variation for our genetic markers was very low, indicative of an extremely high level of inbreeding (FIS = 0.88). There was also strong linkage disequilibrium between microsatellite loci and a very strong genetic differentiation between populations. The data suggest that matings among non-siblings are very rare (3%), although sex ratios from X. germanus in both the field and the laboratory have suggested more matings between non-sibs, and so less intense LMC. Conclusions Our results confirm that caution is needed when inferring mating systems from sex ratio data, especially when a lack of biological detail means the use of overly simple forms of the model of interest

Sib-mating does not lead to facultative sex ratio adjustment in the parasitoid wasp, Nasonia vitripennis

Sex ratio theory predicts that in haplodiploid species, females should lay a relatively more female-biased offspring sex ratio when they mate with a sibling compared with when they mate with a non-relative. This is because in haplodiploids, inbreeding leads to females having greater relatedness to daughters relative to sons. This prediction has only been tested in the parasitoid waspNasonia vitripennis, where no support for this prediction was found. However, a limitation of this previous work is that it was carried out with only two females laying eggs per patch. This is a problem, because in this case the predicted difference in the offspring sex ratio is small and therefore hard to detect. We addressed this problem by utilizing a situation in which larger sex ratio differences are predicted – five females laying eggs per patch. Consistent with the previous results, we also found that the offspring sex ratio laid by a female was not influenced by whether she mated with a sibling or non-relative. Meta-analysis of all the experiments we have undertaken confirms this pattern. This failure to respond to the identity of a mating partner suggests females are unable to discriminate kin and is a relatively rare example of maladaptive sex allocation