Host Susceptibility Modulates Escovopsis Pathogenic Potential in the Fungiculture of Higher Attine Ants

Abstract

Health and disease emerge from intricate interactions between genotypes, phenotypes, and environmental features. The outcomes of such interactions are context-dependent, existing as a dynamic continuum ranging from benefits to damage. In host-microbial interactions, both the host and environmental conditions modulate the pathogenic potential of a microorganism. Microbial interactions are the core of the agricultural systems of ants in the subtribe Attina, which cultivate basidiomycete fungi for food. The fungiculture environment harbors a diverse microbial community, including fungi in the genus Escovopsis that has been studied as damage-causing agent. Here, we consider the ant colony as a host and investigate to what extent its health impacts the dynamics and outcomes of host-Escovopsis interactions. We found that different ant fungal cultivars vary in susceptibility to the same Escovopsis strains in plate-assays interactions. In subcolony-Escovopsis interactions, while healthy subcolonies gradually recover from infection with different concentrations of Escovopsis conidia, insecticide-treated subcolonies evidenced traits of infection and died within 7 days. The opportunistic nature of Escovopsis infections indicates that diseases in attine fungiculture are a consequence of host susceptibility, rather than the effect of a single microbial agent. By addressing the host susceptibility as a major modulator of Escovopsis pathogenesis, our findings expand the understanding of disease dynamics within attine colonies.

Distinct and enhanced hygienic responses of a leaf‐cutting ant toward repeated fungi exposures

“…Interactions among Escovopsis strains cohabiting the same host may result in competition, inhibiting each other in the system (Christopher et al, 2021b ). Nevertheless, some associations are dynamic and can shift on the parasitism–mutualism continuum in response to environmental changes and/or the host susceptibility (Brown et al, 2012 ; Jiménez‐Gómez et al, 2021 ; Leung & Poulin, 2008 ; Mendonça et al, 2021 ). The capacity of Escovopsis to cause disease at the system‐level, and therefore trigger higher sanitization, may depend on the health and susceptibility condition of the superorganism, that is, the ants, the fungal cultivar, and the symbiotic community (Jiménez‐Gómez et al, 2021 ; Mendonça et al, 2021 ).…”

“…Nevertheless, some associations are dynamic and can shift on the parasitism–mutualism continuum in response to environmental changes and/or the host susceptibility (Brown et al, 2012 ; Jiménez‐Gómez et al, 2021 ; Leung & Poulin, 2008 ; Mendonça et al, 2021 ). The capacity of Escovopsis to cause disease at the system‐level, and therefore trigger higher sanitization, may depend on the health and susceptibility condition of the superorganism, that is, the ants, the fungal cultivar, and the symbiotic community (Jiménez‐Gómez et al, 2021 ; Mendonça et al, 2021 ). Even so, we cannot exclude the chance that ants applied other prophylactic behaviors that were not measured in our study, such as metapleural gland grooming and the further discharge of infrabuccal pellets (Fernández‐Marín et al, 2013 , 2015 ; Yek et al, 2012 ).…”

Fungi inhabiting attine ant colonies: reassessment of the genus Escovopsis and description of Luteomyces and Sympodiorosea gens. nov.

“…Finally, several studies provided evidence that some Escovopsis species act as specialized mycoparasite (Currie et al 1999a , 2003 ; Currie 2001 ; Gerardo et al 2004 ; Little and Currie 2007 ; de Man et al 2016 ). However, a recent study showed that Escovopsis species may act as an opportunistic fungus in attine ant colonies depending on host susceptibility (Jiménez-Gómez et al 2021 ). Either way, the parasitic mechanisms of the Escovopsis species that have a parasitic behaviour are still poorly understood, and the hypothesis of specialized mycoparasite for the genus was also raised considering Sympodiorosea spp., L. trichodermoides and the clades C and D (Fig.…”

Actinomycetes associated with hymenopteran insects: a promising source of bioactive natural products

“…Fungi from the genus Escovopsis have specialized in infecting attine ant fungal cultivars and represent the most significant threats to the ants’ food resources ( Figure 1 ; Meirelles et al, 2014 ; Jiménez-Gómez et al, 2021 ; Montoya et al, 2021 ). The fungal garden parasites have attained a level of specialization that is suggestive of co-evolution alongside the ants and their fungal cultivars ( Mueller et al, 2018 ; Douglas, 2022 ).…”

“…At the same time, compounds derived from hymenopteran-actinomycete defensive mutualisms can display remarkable pathogen specificity. Dentigerumycin, for example, selectively inhibits Escovopsis pathogens of attine ants while causing no harm to the mutualistic fungus of the ants ( Oh et al, 2009 ; Jiménez-Gómez et al, 2021 ). Finally, actinomycete associations with hymenopterans may select for compounds with low toxicity toward animal cells ( Chevrette et al, 2019 ).…”