Immune Defenses of a Beneficial Pest: the Mealworm Beetle, Tenebrio Molitor

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Immune Defenses of a Beneficial Pest: the Mealworm Beetle, Tenebrio Molitor Immune defenses of a beneficial pest: the mealworm beetle, Tenebrio molitor. Aurélien Vigneron, Charly Jehan, Thierry Rigaud, Yannick Moret To cite this version: Aurélien Vigneron, Charly Jehan, Thierry Rigaud, Yannick Moret. Immune defenses of a beneficial pest: the mealworm beetle, Tenebrio molitor.. Frontiers in Physiology, Frontiers, 2019, 10, pp.138. 10.3389/fphys.2019.00138. hal-02078389 HAL Id: hal-02078389 https://hal.archives-ouvertes.fr/hal-02078389 Submitted on 10 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEW published: 12 March 2019 doi: 10.3389/fphys.2019.00138 Immune Defenses of a Beneficial Pest: The Mealworm Beetle, Tenebrio molitor Aurélien Vigneron1*, Charly Jehan2, Thierry Rigaud2 and Yannick Moret2* 1 Department of Epidemiology of Microbial Diseases, Yale School of Public Health, New Haven, CT, United States, 2 UMR CNRS 6282 BioGéoSciences, Équipe Écologie Évolutive, Université Bourgogne-Franche Comté, Dijon, France The mealworm beetle, Tenebrio molitor, is currently considered as a pest when infesting stored grains or grain products. However, mealworms are now being promoted as a beneficial insect because their high nutrient content makes them a viable food source and because they are capable of degrading polystyrene and plastic waste. These attributes make T. molitor attractive for mass rearing, which may promote disease transmission within the insect colonies. Disease resistance is of paramount importance for both the control and the culture of mealworms, and several biotic and abiotic environmental factors Edited by: affect the success of their anti-parasitic defenses, both positively and negatively. After Arash Zibaee, University of Guilan, Iran providing a detailed description of T. molitor’s anti-parasitic defenses, we review the main Reviewed by: biotic and abiotic environmental factors that alter their presentation, and we discuss their Sengodan Karthi, implications for the purpose of controlling the development and health of this insect. Manonmaniam Sundaranar University, India Keywords: Tenebrio molitor, innate immunity, pest control, insect farming, ecoimmunology Mauro Mandrioli, University of Modena and Reggio Emilia, Italy INTRODUCTION *Correspondence: Aurélien Vigneron Insects conflict with human activities due to their ability to successfully colonize and adapt [email protected] Yannick Moret to the majority of terrestrial habitats. They are considered as pests when they damage crops [email protected] and/or parasitize livestock, which decrease food production, or when they pose a health hazard to humans or other domesticated animals. By contrast, insects are deemed beneficial Specialty section: when they perform valuable services such as pollination and pest control, or when they This article was submitted to are bred for being used in human activities. Such a distinction is rather subjective and Invertebrate Physiology, only arises in light of desired outcomes from a human perspective. In this context, the a section of the journal mealworm beetle, Tenebrio molitor, could be seen as either a pest or a beneficial insect. Frontiers in Physiology On the one hand, T. molitor has generally been considered as a pest because they consume Received: 02 November 2018 or degrade the quality of stored grains and grain products. On the other hand, mealworms Accepted: 07 February 2019 are beneficial, as their larvae are often used as pet food. They also offer a promising Published: 12 March 2019 alternative protein-rich animal feed and are recommended as a source of human nutrition. Citation: Furthermore, T. molitor larvae may be further useful due to their ability to efficiently Vigneron A, Jehan C, Rigaud T and degrade polystyrene and plastic waste (Brandon et al., 2018). For these reasons, T. molitor Moret Y (2019) Immune Defenses of a Beneficial Pest: The Mealworm is currently being considered for production at an industrial scale. Beetle, Tenebrio molitor. T. molitor is the host of a wide range of pathogens and parasites such as entomopathogenic Front. Physiol. 10:138. microbes, protozoa, and tapeworms, which reduce the mealworm survival or reproductive success. doi: 10.3389/fphys.2019.00138 While some of these parasites might be used as biological insecticides to control unwanted Frontiers in Physiology | www.frontiersin.org 1 March 2019 | Volume 10 | Article 138 Vigneron et al. Modulating Mealworm Beetle Immunity population development, they might also be a source of concern involve therapeutic medication, behavioral fever, and grooming, in mass rearing facilities. Like other insects, T. molitor possesses which are particularly beneficial in dense insect populations, an arsenal of behavioral, physical, and physiological mechanisms where diseases can efficiently spread. No infection outbreak was that aim to prevent exogenic invasions or to lower the reported from mealworm mass rearing, but alternatives to antibiotic consequences of a successful infection. The efficacy of these use could be beneficial to avoid the rise of resistant pathogens. lines of defense may independently or synergistically vary Particularly, adopting therapeutic behavioral medication would according to biotic and abiotic environmental factors including be of great interest for the prevention and control of diseases temperature, food, population density, and individual past in large populations of beetles. Therapeutic medication can interaction with pathogens and parasites. Characterization of be defined “as a series of behaviors through which infected such phenotypic plasticity may provide valuable insights for hosts exploit additional species or compounds to reduce or clear the purpose of improving control or protection of the insect infections, whether mediated through defensive or nutritional populations. Here we review the prominent T. molitor anti- properties” (de Roode and Lefèvre, 2012). So far, therapeutic parasitic defense systems and the main environmental factors medication has not been reported in the mealworm beetle. affecting their presentation. The impact of the environmental Hence, further investigations are needed on this aspect of the factors is considered from the phenotypic to the population mealworm behavioral immunity. level. The processes affecting mealworm anti-parasitic defenses Third, the host may tolerate infections by limiting the negative are discussed in the context of controlling the development effects on their reproductive success. This limitation is mainly and health of the insect populations. achieved through increasing their reproductive effort but often at the expense of their longevity. For instance, mealworm beetles tolerate a high number of cysticercoids of the parasite ANTI-PARASITIC DEFENSES IN THE H. diminuta at the expense of their own fitness. Nevertheless, MEALWORM BEETLE in response to parasite infection, males produce improved spermatophores that contain superior nuptial gifts that will Behavioral Immunity be passed to their mating females. This increases female fecundity, Behavioral immunity refers to altered behaviors used by a host and therefore, a higher number of eggs are fertilized by the to avoid infection, reduce parasite growth, and/or alleviate disease male (Hurd and Ardin, 2003). Specifically, as beetle longevity symptoms. Such anti-parasitic behaviors are increasingly recognized is compromised by the parasite, infected males may gain a in insects, including T. molitor. Behavioral immunity involves reproductive benefit, before dying from the infection, by anti-parasitic behaviors categorized into three main infectious increasing the total protein content of the spermatophores they outcomes (de Roode and Lefèvre, 2012). First, behavioral immunity transfer to females during mating (Carver et al., 1999; Hurd may provide qualitative resistance by avoiding contact with and Ardin, 2003). Males that are experiencing a non-infectious parasites and pathogens. Behavioral immunity comprises spatial immune-challenge, e.g., a piece of nylon filament inserted into and temporal avoidance of potentially infected places, individuals their hemocoel, present a similar increased reproductive effort. or food, implementation of hygienic behaviors such as grooming, Indeed, the immune challenge may induce in males, the and adapted social contacts, such as mate choice based on a perception of a lower survival probability consequent to their partner’s immunocompetence. This range of behavior was reported simulated infection status, causing the insect to make a last when T. molitor were exposed to the tapeworm Hymenolepis attempt to achieve a maximized level of reproductive success. diminuta. H. diminuta is a rodent parasite that uses the mealworm Consequently, females find those artificially challenged males beetle as an intermediate host. Beetles become infected by more sexually attractive, probably due to an increased production consuming eggs of the parasite when feeding on infectious rodent of sexual pheromone consequent to the challenge (Sadd et al., feces.
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