Escaping the evolutionary trap: Can size-related contest advantage compensate for juvenile mortality disadvantage when parasitoids develop in unnatural invasive hosts?

Highlights

• The Brown Marmorated Stink Bug is a major invasive agro-economic pest.

• Its eggs are seen as an evolutionary trap for native parasitoids, but some survive.

• Game theory suggests an escape from this trap via effects on subsequent contests.

• Evolutionary shifts could allow parasitoids to control the pest.

Abstract

The quality of hosts for a parasitoid wasp may be influenced by attributes such as host size or species, with high quality for successful development usually coincident with high quality for larger offspring. This is not always the case: for the Scelionid wasp Trissolcus basalis, oviposition in eggs of the Brown Marmorated Stink Bug, Halyomorpha halys, rather than of the normal host, the Southern Green Stink Bug, Nezara viridula, leads to lower offspring survival, but survivors can be unusually large. Adult female T. basalis engage in contests for host access. As larger contestants are typically favoured in contests between parasitoids, the larger size of surviving offspring may compensate for the mortality of others. We construct a general game-theoretic model to explore whether size advantage can sustain a maternal preference to utilize a more deadly host species. We find that size advantage alone is unlikely to sustain a shift in host preference, yet such an outcome is possible when size asymmetries act simultaneously with advantages in host possession (ownership effect). Halyomorpha halys is an invasive pest of major agro-economic importance in Europe and the Americas, and use of its eggs as hosts by native parasitoids such as T. basalis has been seen as an evolutionary trap due to their high developmental mortality. Our model suggests that the recently discovered effect of host choice on offspring size may provide an escape from the trap via effects on contest biology of T. basalis which could foster a more stable association with H. halys. An evolutionary shift in the reproductive value of H. halys could increase the efficiency of T. basalis as a biological control agent of this invasive stink bug pest.

Introduction

Juvenile parasitoid wasps develop on the resources provided by the body of a single host. The quality and quantity of the resource can be influenced by, for instance, the host’s size and by its developmental stage and these attributes may then be manifest in terms of parasitoid developmental mortality and/or the size, fecundity and longevity of surviving offspring, all of which are components of evolutionary fitness (Godfray, 1994). Many species of parasitoids can develop from several or even many species of hosts (oligophagy and polyphagy, respectively) and variation, in terms of nutritional composition, size and defences against parasitism, between host species can be a major determinant of parasitoid fitness parameters, in turn influencing host acceptance decisions by foraging adult females.

In some parasitoids, development in a given host species may negatively influence the probability of offspring survival to adulthood and yet positively influence the characteristics of those offspring that do survive. This is the case in Trissolcus basalis (Hymenoptera: Sceleonidae): oviposition into eggs of the invasive Brown Marmorated Stink Bug (Halyomorpha halys, Hemiptera: Pentatomidae) leads to far lower offspring survival (with estimates ranging from 0 to 6% (Rondoni et al., 2017, Peri et al., 2021) to 38% Balusu et al., 2019) than oviposition into eggs of its main host, the Southern Green Stink Bug (Nezara viridula, Hemiptera: Pentatomidae), 84% (Cusumano et al., 2011, Peri et al., 2021), but female offspring that survive are typically much larger (almost 25% increase in tibia length, Peri et al., 2021). There is a substantial difference in the size of the host eggs between H. halys and N. viridula, which is likely to be the key factor leading to an increase in the size of the T. basalis emerging from the invasive stink bug host. Among adult female parasitoid wasps, larger size is generally associated with higher fecundity (Hardy et al., 1992) and foraging ability (Karsai et al., 2006, Visser, 1994). One aspect of foraging is the ability to competitively acquire and subsequently defend hosts or patches of hosts against other foraging females, and female T. basalis engage in such contests (Field and Calbert, 1998). Although Field and Calbert (1999) did not find any effect of body size asymmetries between contestant parasitoids, the likely reason for this result is that they used only one species of host (eggs of the pentatomid bug Agonoscelis rutila) and in consequence the variation in T. basalis body size was not large. But when scelionid wasps emerge from hosts of two different species that differ greatly in size and quality, wasp size differences can be substantial and strongly affect contest resolution, as has been recently found by Guerra-Grenier et al. (2020) in the wasp Telenomus podisi, an egg parasitoid that belongs to the same family as T. basalis (Scelionidae). Across the parasitoid Hymenoptera, larger contestants are typically favoured in agonistic interactions between adults (Hardy et al., 2013) and such body size effects can influence reproductive decisions by foraging females in a game-theoretic manner (e.g. clutch size optima, (Mesterton-Gibbons and Hardy, 2004, Goubault et al., 2007). A further important factor influencing contest outcome in wasps such as T. basalis is prior ownership status (Field and Calbert, 1998): females that arrive first on a patch have an advantage against subsequent intruders. We consider both body size and prior ownership effects in this study.

Accordingly, we develop here a game-theoretic model to address the following general question: Can size advantage in contests among adults sustain a preference for a more deadly (in terms of offspring developmental mortality) host by foraging females? For greatest generality, and with future work in mind, we first formulate the model (in Section 2 and especially Appendix A) in terms of a five-dimensional parameter space. The parameters are: 1. The reproductive (developmental) value of the more deadly host relative to that of the natural host, $\alpha$; 2. The proportion of hosts that are of the more deadly species, $\theta$; 3. The probability that a host is never found, k; 4. The probability a large wasp outcompetes a normal wasp relative to the probability a normal wasp outcompetes a large wasp, $\lambda$; and 5. The owner advantage, defined as the increase in probability beyond $0.5$ of an owner winning a contest against an intruder of equal size, $\rho$: These five basic parameters are recorded in Table 1. Note that, in the context of these definitions, we are referring to a wasp as “large” if it emerges from a host of the more deadly invasive species (H. halys) and hence has a size advantage, and as “normal” if it emerges from a host of the native species (N. viridula).

The model thus integrates non-contest ($\alpha ,\theta ,k$) and contest-related ($\lambda ,\rho$) considerations. All five parameters are dimensionless and in principle measurable, but in most cases their measurement has yet to be addressed by empirical studies. As clarity of prediction in theoretical work decreases with the number of parameters considered, we then focus (Section 3) on the subset of the parameter space where size advantage in contests is most relevant, thus reducing the dimension of the parameter space from five to two. We subsequently revisit the higher-dimensional parameter space in Section 4 and in our concluding discussion (Section 5). Our model has a wide set of potential applications, given that species invasions are likely to occur increasingly frequently due to both international transport and global climate change (Berthon, 2015, Abram et al., 2017). The model is nonetheless of most immediate use in considering the invasion of European and American cropping systems by the Brown Marmorated Stink Bug (Rice et al., 2014, Leskey and Nielsen, 2018, Stoeckli et al., 2020) as the use of its eggs as hosts by native parasitoids such as Trissolcus basalis and Telenomus podisi has been seen as an “evolutionary trap” due to the high or complete developmental mortality of offspring (Abram et al., 2014, Bertoldi et al., 2021, Costi et al., 2020, Konopka et al., 2018, Tognon et al., 2019). An evolutionary trap arises when there exists a disconnect between cues that organisms use to make behavioral decisions and outcomes normally associated with those cues, and it can lead to a reduced survival/reproduction of the trapped species if a population falls below a critical size threshold before adaptation to a change in circumstances (Robertson and Blumstein, 2019, Schlaepfer et al., 2002, Schlaepfer et al., 2005). However, the recently discovered effects of host species on offspring size may provide an escape from the trap by providing a fitness advantage to surviving offspring via enhanced performance in contests for future hosts.