Pathogen-mediated natural and manipulated population collapse in an invasive social insect

LeBrun, Edward G.; Jones, Melissa; Plowes, Robert M.; Gilbert, Lawrence E.

doi:10.1073/pnas.2114558119

Cited by 10 publications

(6 citation statements)

References 39 publications

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“…Pathogens have been hypothesized to cause boom‐and‐bust dynamics in introduced species, including invasive ants (LeBrun et al, 2022; Lester & Gruber, 2016; Simberloff & Gibbons, 2004). Outside their native range, many invasive ants such as the Argentine ant ( Linepithema humile ) form large, dense, cooperating unicolonial populations that comprise a great number of nests (Holway et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Can immune gene silencing via dsRNA feeding promote pathogenic viruses to control the globally invasive Argentine ant?

Felden

Dobelmann

Baty

et al. 2022

Ecological Applications

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Pest control methods that can target pest species with limited environmental impacts are a conservation and economic priority. Species-specific pest control using RNA interference is a challenging but promising avenue in developing the next generation of pest management. We investigate the feasibility of manipulating a biological invader's immune system using double-stranded RNA (dsRNA) in order to increase susceptibility to naturally occurring pathogens. We used the invasive Argentine ant as a model, targeting the immunity-associated genes Spaetzle and Dicer-1 with dsRNA. We show that feeding with Spaetzle dsRNA can result in partial target gene silencing for up to 28 days in the laboratory and 5 days in the field. Dicer-1 dsRNA only resulted in partial gene knockdown after 2 days in the laboratory. Double-stranded RNA treatments were associated with significant gene expression disruptions across immune pathways in the laboratory and to a lower extent in the field. In total, 12 viruses and four bacteria were found in these ant populations. Some changes in viral loads in dsRNA-treated groups were observed. For example, Linepithema humile Polycipivirus 2 (LhuPCV2) loads increased after 2 days of treatment with Spaetzle and Dicer-1 dsRNA treatments in the laboratory. After treatment with the dsRNA in the field, after 5 days the virus Linepithema humile toti-like virus 1 (LhuTLV1) was significantly more abundant. However, immune pathway disruption did not result in a consistent increase in microbial infections, nor did it alter ant abundance in the field. Some viruses even declined in abundance after dsRNA treatment. Our study explored the feasibility of lowering a pest's immunity as a control tool. We demonstrate that it is possible to alter immune gene expression of pest species and pathogen loads, although in our specific system the affected pathogens did not appear to influence pest abundance. We provide suggestions on future directions for dsRNA-mediated immune disruption in pest species, including potential avenues to improve dsRNA delivery as well as the Antoine Felden and Jana Dobelmann contributed equally to the study.

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Section: Introductionmentioning

confidence: 99%

Can immune gene silencing via dsRNA feeding promote pathogenic viruses to control the globally invasive Argentine ant?

Felden

Dobelmann

Baty

et al. 2022

Ecological Applications

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“…For instance, genetically differentiated populations of green peach aphids (Myzus persicae Sulzer), Mediterranean fruit ies (Ceratitis capitata Wiedemann), and mountain pine beetles (Dendroctonus ponderosae Hopkins) have all been shown to vary in their susceptibility to pesticides and stress tolerance [49][50][51]. Recently, the application of a fungus-like microsporidian pathogen was found effective at decreasing and in some instances eliminating TCA populations [52][53][54]. Further investigation is required into the effectiveness of this biopesticide on other TCA populations.…”

Section: Discussionmentioning

confidence: 99%

High-Resolution Population Genetic Structure of Tawny Crazy Ant (Nylanderia fulva Mayr: Hymenoptera: Formicidae) from the Origin in South America and Introduced Regions of the United States

Holt

Lerma

Calcaterra

et al. 2023

Preprint

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Background The tawny crazy ant (Nylanderia fulva Mayr) is native to South America and was first reported in the continental United States (US) in 1938. It was not until the 1990s in Florida and 2000s in Texas that this ant was considered a serious pest in the US. Tawny crazy ant (TCA) is currently considered an invasive pest in six US states and this ant’s invasion success is attributed in part to a unicolonial nature, multiple queens per nest, natural enemies release in the invasive range, and ability to detoxify venom from other competitor ant species. A limited number of low-density molecular markers have previously shown little genetic differentiation among TCA populations across their geographic distribution in the US. Results Using High Throughput Sequencing (HTS) we obtained high-density molecular markers (i.e., SNPs) for TCA samples. With 26,657 SNPs we identified genetic variation among TCA populations in different states across the US (i.e., Texas, Louisiana, Alabama, Mississippi, Georgia, and Florida) and in South America (i.e., Argentina, Colombia, and Peru). Conclusion Our results underscore that for recently introduced invasive species, increasing the number of molecular markers used in population genetic studies can provide greater resolution. High-resolution information on regional genetic differences can help inform pest management strategies.

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“…In males captured in 2017 and 2018, no pattern was immediately evident despite a significant difference in infection load between trap years, trap days and the interaction between the two as shown in figure 6. While the results may be statistically significant, insect pathogens, like human pathogens, are known to vary annually and seasonally (Abdel-Baki et al 2009, Herren et al 2020, LeBrun et al 2022).…”

Section: Discussionmentioning

confidence: 99%

“…While we cannot confirm the reason for the discrepancies in Nosema sp. prevalence, it has previously been observed that, in general, the low virulence of microsporidian pathogens allows for an increase in prevalence in the population over time (Biganski et al 2021, LeBrun et al 2022). A possible explanation for the difference in results may be that during the range expansion by the western bean cutworm, not all individuals were infected with the microsporidian parasite.…”

Section: Discussionmentioning

confidence: 99%

Natural occurrence and analysis of Nosema sp. infection in the adult population of western bean cutworm in Michigan

Bunn

Miller

2022

Preprint

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An understanding of population dynamics and insect biology is important for effective crop management strategies. Biotic factors such as pathogens play a large role on the fitness and dynamics of insect populations. Microsporidia are obligate intracellular parasites that infect more than 150 insect species and range from sublethal and chronic to fast acting and deadly. The western bean cutworm, Striacosta albicosta (Smith) (Lepidoptera: Noctuidae), is a pest of both corn (Zea maize L.) and dry beans (Phaseolus sp L.) that is infected by a microsporidian parasite from the genus Nosema. Unfortunately, little is known about the interactions between the Nosema sp. infecting the western bean cutworm and its prevalence and effects on the host population. This is especially true for the western bean cutworm population that has settled in the Great Lakes region over the last two decades. Using field caught samples and phase contrast microscopy, we found a 100% prevalence of infection in the adult western bean cutworm population in Michigan. No consistent trends in pathogen load were observed over the course of the western bean cutworm flight season. A weak, but statistically significant relationship was observed between male body weight and pathogen load.

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Pathogen-mediated natural and manipulated population collapse in an invasive social insect

Cited by 10 publications

References 39 publications

Can immune gene silencing via dsRNA feeding promote pathogenic viruses to control the globally invasive Argentine ant?

Can immune gene silencing via dsRNA feeding promote pathogenic viruses to control the globally invasive Argentine ant?

High-Resolution Population Genetic Structure of Tawny Crazy Ant (Nylanderia fulva Mayr: Hymenoptera: Formicidae) from the Origin in South America and Introduced Regions of the United States

Natural occurrence and analysis of Nosema sp. infection in the adult population of western bean cutworm in Michigan

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