How the larval integumentary system contributes to success
The integumentary system of the bot fly larvae acts as a primary defense against the host immune system. Development of a thick pro- and epicuticle, insoluble epicuticle, and negatively charged outer cuticular layer may help larvae to mask immunogenic cuticular components from their host and avoid triggering inflammatory responses in the host’s tissues as they migrate to their development sites [1, 2, 3]. Mouth hooks and spines, which are heavily sclerotized compared to the rest of the larval cuticle, are adaptively shaped to facilitate larval attachment to, movement within, and feeding on the host’s body [4, 5]. The morphology and distribution of these structures vary among species and larval instars, contributing to the specialization on particular host animals and tissues that these insects exhibit [1, 5]. This specialization allows bot fly larvae to exploit niches that are inaccessible to many other dipterans, reducing interspecific competitive pressures. The ability to develop within a living host provides a source of nutrients to the developing larva and shields it from unfavorable environmental conditions outside the host body. By acquiring sufficient reserves of resources, particularly water and fat, the larva maximizes its chance of successfully metamorphosizing and entering the adult reproductive stage [6].
Drawbacks of host specificity
Specialization on a single host or limited range of related host organisms may limit the protection provided by the larval cuticle if larvae enter an atypical host species. For example, Oestrus ovis survival is greatly reduced in goats compared to sheep, indicating that their ability to evade the immune response is highly species dependent [7]. Larvae may be introduced to unsuitable hosts either through sub-optimal oviposition choice by adult females or, in the case of cuterebrines that hatch on vegetation, lack of appropriate hosts in the vicinity [4]. Specialization may also intensify intraspecific competition among bot fly larvae, as an excessively high parasite burden could reduce host fitness to the extent that the host dies, killing the parasites with it [4]. Additionally, in rodents and lagomorphs, heavier infestation of Cuterebra (New World skin bots) has been reported in some Old World hosts exposed to parasitism, perhaps indicating that coevolved hosts are developing some resistance to bot flies, although the prevalence and potential mechanisms of host resistance are uncertain [8].
Facultative rather than obligatory myiasis represents an alternative strategy that could address the shortcomings of reliance on the availability of a particular host species, the need to establish dynamic-equilibrium with the host’s immune system to avoid both immune responses and killing the host, and the detrimental effects of high parasite burden, which limit the population density of bot flies. Facultative myiasis-causing species are able to exploit either dead or living tissue, allowing them to continue developing even if infestation leads to the host’s death [4]. Calliphoridea (bottle flies, blow flies, screwworms), Sarcophagidae (flesh flies), and Psychodidae (moth flies, drain flies) contain species that engage in facultative myiasis, often invading wounds opportunistically while also being able to use feces or carrion as substrates for development [4]. As generalists that exploit readily available organic waste, these flies are more easily able to expand into new environments and can complete more generations annually, enhancing their capacity to develop novel adaptations to host defenses [1].
http://specialcollections.nal.usda.gov/screwworm/index.
References:
[1] Cowell, D.D., et al. Oestrid Flies : Biology, Host-Parasite Relationships, Impact and Management, CABI, 2006. ProQuest Ebook Central, https://ebookcentral.proquest.com/lib/osu/detail.action?docID=289452.
[2] Colwell, D. D. (1991). Ultrastructure of the Integument of First-Instar Hypoderma lineatum and H. bovis (Diptera: Oestridae). Journal of Medical Entomology, 28(1), 86–94. https://doi.org/10.1093/jmedent/28.1.86
[3] Innocenti, L., Lucchesi, P., & Giorgi, F. (1997). Integument ultrastructure of Oestrus ovis (L.) (Diptera: Oestridae) larvae: Host immune response to various cuticular components. International Journal for Parasitology, 27(5), 495–506. https://doi.org/10.1016/S0020-7519(96)00186-5.
[4] Scholl, P. J., Colwell, D. D., & Cepeda-Palacios, R. (2019). Myiasis (Muscoidea, Oestroidea). In Medical and Veterinary Entomology (3rd ed., pp. 383–419). Academic Press. https://doi.org/10.1016/B978-0-12-814043-7.00019-4.
[5] Li, X. Y., Pape, T., Colwell, D., Dewhurst, C., & Zhang, D. (2021). Three-dimensional characterization of first instar horse and rhinoceros stomach bot fly larvae (Oestridae: Gasterophilinae: Gasterophilus, Gyrostigma): Novel morphology and evolutionary implications. Zoological Journal of the Linnean Society, 193, 939–952. https://doi.org/10.1093/zoolinnean/zlaa164.
[6] Cepeda-Palacios, R., Angulo Valadez, C. E., Scholl, J. P., Ramirez-Orduna, R., Jacquiet, P. P., & Dorchies, P. (2011). Ecobiology of the sheep nose bot fly (Oestrus ovis L.): A review. Revue de Médecine Vétérinaire, 162(11), 503–507. https://doi.org/hal-02651191f.
[7] Otranto, D. (2001). The immunology of myiasis: Parasite survival and host defense strategies. Trends in Parasitology, 17(4), 176–182. https://doi.org/10.1016/S1471-4922(00)01943-7.
[8] Slansky, F. (2007). Insect/Mammal Associations: Effects of Cuterebrid Bot Fly Parasites on Their Hosts. Annual Review of Entomology, 52, 17–36. https://doi.org/10.1146/annurev.ento.51.110104.151017.
