Parasitic success and venom composition evolve upon specialization of parasitoid wasps to different host species

AbstractFemale endoparasitoid wasps usually inject venom into hosts to suppress their immune response and ensure offspring development. However, the parasitoid’s ability to evolve towards increased success on a given host simultaneously with the evolution of the composition of its venom has never been demonstrated. Here, we designed an experimental evolution to address this question. We crossed two parasitoid lines of Leptopilina boulardi differing both in parasitic success on different Drosophila hosts and venom composition. F2 descendants were reared on three different Drosophila species for nine generations. We tested for evolution of parasitic success over the generations and for the capacity of parasitoids selected on a given host to succeed on another host. We also tested whether the venom composition - analyzed on the basis of the variation in intensity of the venom protein bands on SDS-PAGE 1D - evolved in response to different host species. Results showed a specialization of the parasitoids on their selection host and a rapid and differential evolution of the venom composition according to the host. Overall, data suggest a high potential for parasitoids to adapt to a new host, which may have important consequences in the field as well in the context of biological control.

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Rapid and differential evolution of the venom composition of a parasitoid wasp depending on the host strain

10.1101/796649 ◽

2019 ◽

Author(s):

Fanny Cavigliasso ◽

Hugo Mathé-Hubert ◽

Laurent Kremmer ◽

Christian Rebuf ◽

Jean-Luc Gatti ◽

...

Keyword(s):

Differential Evolution ◽

Rapid Evolution ◽

Intraspecific Variability ◽

Protein Composition ◽

Host Strain ◽

Parasitoid Wasps ◽

Evolutionary Potential ◽

Venom Protein ◽

Venom Composition ◽

Venom Proteins

AbstractParasitoid wasps rely primarily on venom to suppress the immune response and regulate the physiology of their host. Intraspecific variability of venom protein composition has been documented in some species, but its evolutionary potential is poorly understood. We performed an experimental evolution initiated with crosses of two lines of Leptopilina boulardi of different venom composition to generate variability and create new combinations of venom factors. The offspring were maintained for 10 generations on two strains of Drosophila melanogaster differing in resistance / susceptibility to the parasitoid lines. The venom composition of individuals was characterized by a semi-automatic analysis of 1D SDS-PAGE protein profiles whose accuracy was checked by Western blot analysis of well-characterized venom proteins. Results evidenced a rapid and differential evolution of the venom composition on both hosts and showed that the proteins beneficial on one host can be costly on the other. Overall, we demonstrated the capacity of rapid evolution of the venom composition in parasitoid wasps, important regulators of arthropod populations, suggesting a potential for adaptation to new hosts. Our approach also proved relevant in identifying, among the diversity of venom proteins, those possibly involved in parasitism success and whose role deserves to be deepened.Key ContributionThe venom protein composition of parasitoid wasps can evolve rapidly and differently depending on the host strain. Studying this evolution can help identify new venom proteins possibly involved in parasitism success on a given host.

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Quantifying the unquantifiable: why Hymenoptera – not Coleoptera – is the most speciose animal order

10.1101/274431 ◽

2018 ◽

Cited By ~ 4

Author(s):

Andrew A. Forbes ◽

Robin K. Bagley ◽

Marc A. Beer ◽

Alaine C. Hippee ◽

Heather A. Widmayer

Keyword(s):

Host Species ◽

Parasitic Wasp ◽

Parasitoid Wasps ◽

Beetle Species ◽

Insect Host ◽

Parasitic Wasps ◽

Logical Model ◽

Wasp Species

AbstractBackgroundWe challenge the oft-repeated claim that the beetles (Coleoptera) are the most species-rich order of animals. Instead, we assert that another order of insects, the Hymenoptera, are more speciose, due in large part to the massively diverse but relatively poorly known parasitoid wasps. The idea that the beetles have more species than other orders is primarily based on their respective collection histories and the relative availability of taxonomic resources, which both disfavor parasitoid wasps. Though it is unreasonable to directly compare numbers of described species in each order, the ecology of parasitic wasps – specifically, their intimate interactions with their hosts – allows for estimation of relative richness. We present a simple logical model that shows how the specialization of many parasitic wasps on their hosts suggests few scenarios in which there would be more beetle species than parasitic wasp species. We couple this model with an accounting of what we call the “genus-specific parasitoid-host ratio” from four well-studied genera of insect hosts, a metric by which to generate extremely conservative estimates of the average number of parasitic wasp species attacking a given beetle or other insect host species. Synthesis of our model with data from real host systems suggests that the Hymenoptera may have 2.5 - 3.2× more species than the Coleoptera. While there are more described species of beetles than all other animals, the Hymenoptera are almost certainly the larger order.

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Impact of Temperature on the Immune Interaction between a Parasitoid Wasp and Drosophila Host Species

Insects ◽

10.3390/insects12070647 ◽

2021 ◽

Vol 12 (7) ◽

pp. 647

Author(s):

Fanny Cavigliasso ◽

Jean-Luc Gatti ◽

Dominique Colinet ◽

Marylène Poirié

Keyword(s):

Immune Response ◽

Foreign Body ◽

Host Species ◽

Parasitoid Wasp ◽

Immune Defense ◽

Effect Of Temperature ◽

Leptopilina Boulardi ◽

Venom Composition ◽

The Impact ◽

Parasitoid Rearing

Temperature is particularly important for ectotherms, including endoparasitoid wasps that develop inside another ectotherm host. In this study, we tested the impact of three temperatures (20 °C, 25 °C and 30 °C) on the host–parasitoid immune interaction using two Drosophila host species (Drosophila melanogaster and D. yakuba) and two parasitoid lines of Leptopilina boulardi. Drosophila’s immune defense against parasitoids consists of the formation of a melanized capsule surrounding the parasitoid egg. To counteract this response, Leptopilina parasitoids rely on the injection of venom during oviposition. Here, we tested the effect of temperature on parasitic success and host encapsulation capacity in response to a parasitoid egg or other foreign body. Increased temperature either promoted or did not affect the parasitic success, depending on the parasitoid–host pairs considered. The mechanisms behind the higher success seemed to vary depending on whether the temperature primarily affected the host immune response or also affected the parasitoid counter-immune response. Next, we tested the effect of parasitoid rearing temperature on its success and venom composition. Venom composition varied strongly with temperature for both parasitoid lines, partially consistent with a change in their parasitic success. Overall, temperature may have a significant impact on the host–parasitoid immune interaction.

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Rapid and Differential Evolution of the Venom Composition of a Parasitoid Wasp Depending on the Host Strain

Toxins ◽

10.3390/toxins11110629 ◽

2019 ◽

Vol 11 (11) ◽

pp. 629 ◽

Cited By ~ 9

Author(s):

Cavigliasso ◽

Mathé-Hubert ◽

Kremmer ◽

Rebuf ◽

Gatti ◽

...

Keyword(s):

Differential Evolution ◽

Rapid Evolution ◽

Intraspecific Variability ◽

Protein Composition ◽

Parasitoid Wasp ◽

Parasitoid Wasps ◽

Evolutionary Potential ◽

Venom Protein ◽

Venom Composition ◽

Venom Proteins

Parasitoid wasps rely primarily on venom to suppress the immune response and regulate the physiology of their host. Intraspecific variability of venom protein composition has been documented in some species, but its evolutionary potential is poorly understood. We performed an experimental evolution initiated with the crosses of two lines of Leptopilina boulardi of different venom composition to generate variability and create new combinations of venom factors. The offspring were maintained for 10 generations on two strains of Drosophila melanogaster differing in resistance/susceptibility to the parental parasitoid lines. The venom composition of individuals was characterized by a semi-automatic analysis of 1D SDS-PAGE electrophoresis protein profiles whose accuracy was checked by Western blot analysis of well-characterized venom proteins. Results made evident a rapid and differential evolution of the venom composition on both hosts and showed that the proteins beneficial on one host can be costly on the other. Overall, we demonstrated the capacity of rapid evolution of the venom composition in parasitoid wasps, important regulators of arthropod populations, suggesting a potential for adaptation to new hosts. Our approach also proved relevant in identifying, among the diversity of venom proteins, those possibly involved in parasitism success and whose role deserves to be deepened.

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Potential Host Range of the Larval Endoparasitoid Cotesia vestalis (=plutellae) (Hymenoptera: Braconidae)

International Journal of Insect Science ◽

10.1177/1179543317715623 ◽

2017 ◽

Vol 9 ◽

pp. 117954331771562 ◽

Cited By ~ 3

Author(s):

Satoshi Hiroyoshi ◽

Jeffrey A Harvey ◽

Yutaka Nakamatsu ◽

Hisashi Nemoto ◽

Jun Mitsuhashi ◽

...

Keyword(s):

Host Range ◽

Host Species ◽

Diamondback Moth ◽

Growth Potential ◽

Parasitoid Wasps ◽

Cotesia Vestalis ◽

Potential Host ◽

First Instar ◽

Developmental Capacity ◽

Lepidopteran Host

Many parasitoid wasps are highly specialized in nature, attacking only one or a few species of hosts. Host range is often determined by a range of biological and ecological characteristics of the host including diet, growth potential, immunity, and phylogeny. The solitary koinobiont endoparasitoid wasp, Cotesia vestalis, mainly parasitizes diamondback moth (DBM) larvae in the field, although it has been reported that to possess a relatively wide lepidopteran host range. To better understand the biology of C vestalis as a potential biological control of hosts other than the DBM, it is necessary to determine suitability for potential hosts. In this study, the potential host range of the wasp and its developmental capacity in each host larva were examined under laboratory conditions using 27 lepidopteran species from 10 families. The wasp was able to parasitize 15 of the 27 species successfully. Some host species were not able to exclude C vestalis via their internal physiological defenses. When parasitization was unsuccessful, most hosts killed the parasitoid at the egg stage or early first-instar stage using encapsulation, but some host species disturbed the development of the parasitoid at various stages. No phylogenetic relationships were found among suitable and unsuitable hosts, revealing that host range in some endoparasitoids is not constrained by relatedness among hosts based on immunity.

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Asymmetries affecting aggressive contests between solitary parasitoids: the effect of host species

Behavioral Ecology ◽

10.1093/beheco/araa096 ◽

2020 ◽

Vol 31 (6) ◽

pp. 1391-1400 ◽

Cited By ~ 2

Author(s):

Eric Guerra-Grenier ◽

Paul K Abram ◽

Jacques Brodeur

Keyword(s):

Body Size ◽

Host Species ◽

Host Community ◽

Community Diversity ◽

Parasitoid Wasps ◽

Offspring Production ◽

Solitary Parasitoid ◽

The Difference ◽

Telenomus Podisi

Abstract Conflicts in animals are usually resolved based on asymmetries, where contest winners are often those that value a resource the most and/or those who have the greatest potential to retain it. In parasitoid wasps, contests between females determine which individual exploits hosts for offspring production. Previous studies on solitary parasitoids rarely considered the role of biotic factors generating phenotypic variation that could influence the strength of asymmetries. Some parasitoid species parasitize host species of various sizes, producing offspring that vary considerably in size and potentially fighting ability. In this study, we reared the egg endoparasitoid Telenomus podisi (Hymenoptera: Scelionidae) on two host species to measure the effect of body size on contest resolution and how it interacts with ownership and resource value (RV) asymmetries. Our results showed that ownership status best predicts the final contest outcome when similar-sized wasps fight over hosts. The frequency and outcomes of individual fights structuring contests were better explained by the difference in the number of eggs laid in the hosts by each female at a given time. When contestants varied in body size, larger intruders frequently dislodged small owners regardless of ownership and RV asymmetries. These results imply that body size is an important factor to consider in solitary parasitoid contests and that it can overshadow the effects of other asymmetries. Our study suggests that host community diversity could have a direct effect on parasitoid contests and that biotic communities, through their effects on animal phenotypes, may play an underrated role in contest resolution.

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