Density‐dependent prophylaxis in primary anti‐parasite barriers in the velvetbean caterpillar

Abstract

1. Organisms rely on a set of primary barriers to prevent invasion by parasites, and secondary defences to fight parasites that breach the primary barriers. However, maintaining these defences to be active and effective is costly. Thus, hosts increase investment in anti-parasite defences under situations of high risk of infection and reduce defences when the risk is reduced (the 'Density-Dependent Prophylaxis' hypothesis).2. In the present study, it was tested whether the midgut primary defences of the velvetbean caterpillar Anticarsia gemmatalis Hübner present density-dependent plasticity, and also whether these defences could be induced by a viral pathogenic challenge. The aim was to examine whether morphometry and the structure of the midgut and peritrophic matrix (PM) change in accordance with colour transition in caterpillars, and whether such changes may provide the caterpillars a more protective barrier against invasion by Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV).3. It was found that PM and the midgut epithelium of the velvetbean caterpillar change plastically according to phenotype, itself a response to changes in population density. Caterpillars reared at high densities (black phenotype) had a considerably thicker midgut epithelia and peritrophic matrices than those reared individually (green phenotype), and there was also more chitin in the PM of the former.4. This was interpreted as the first demonstration of increased investment in primary, barrier, defences against parasites, in response to increased conspecific density and an increased risk of infection. The possibility that this arises as a positive result of pleiotropy is discussed further, wherein the biochemical pathways responsible for the up-regulation of the immune system are also involved in midgut properties.

Temperature and population density: interactional effects of environmental factors on phenotypic plasticity, immune defenses, and disease resistance in an insect pest

“…Temperature may interfere directly with host movement rates (Ruf and Fiedler 2002;Cormont et al 2011), which in turn can affect the likelihood of contact between conspecifics, and thus phenotypic changes in this species. Velvetbean caterpillar, as other polyphenic species, has evolved plastic prophylactic responses to cope with the increased risk of parasite infection at crowding (Barnes and Siva-Jothy 2000;Wilson et al 2002;Silva et al 2013Silva et al , 2016, with cuticle melanization being indicative of a prophylactic responses. So, here we consider this feature being a visible evidence of the velvetbean caterpillar's movement rates.…”

“…It was shown recently that the velvetbean caterpillar Anticarsia gemmatalis (Fig. 1), when exposed to a high population density, beyond undergoing changes in its secondary defenses (i.e., encapsulation response, capsule melanization, and hemocyte numbers (Silva et al 2013), also change plastically its primary defenses, such as thickness of the midgut epithelium and thickness and chitin amount in the peritrophic matrix (Silva et al 2016). As other insect polyphenic species (e.g., Reeson et al 1998;Barnes and Siva-Jothy 2000;Wilson et al 2001), the velvetbean caterpillar becomes darker (or melanized) as a response to the local density of conspecifics, with this feature being indicative of up-regulation of primary and secondary defenses, and consequently, pathogen resistance.…”

Physical and chemical properties of primary defences in Tenebrio molitor

“…The structure and composition of the host's primary defences are important in the defence against parasites. For example, the black phenotype of the velvetbean caterpillar Anticarsia gemmatalis exposed to virus increases the thickness of the midgut epithelium, as well as both thickness and chitin content in the peritrophic matrix (Silva et al ., ), whereas protease inhibitors and cuticular lipids on the integuments of the silkworm Bombyx mori and whitefly Bemisia argentifolii (a race of Bemisia tabaci ) suppress the penetration of fungi (James et al ., ). These results support the hypothesis that the outermost cuticle of T. molitor may play an important role as a barrier against fungal pathogenesis.…”

Genomic analysis of a cypovirus isolated from the eucalyptus brown looper, Thyrinteina arnobia (Stoll, 1782) (Lepidoptera: Geometridae)

“…The high conspecific density itself may intensify the probability of a pathogen to find its host and replicate. Some gregarious living insects may evolve to counteract this improved risk by developing strategies such as density-dependent prophylaxis (Silva et al, 2016). Several studies indicate that cypoviruses can develop chronic diseases with sublethal effects (Mertens, 2004;Mertens et al, 1999) leading also to vertical transmission in some species (Graham et al, 2006).…”