Selective protein self-deprivation by Mormon crickets following fungal attack

Authors: Srygley, Robert

Submitted to: Journal of Insect Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/15/2023
Publication Date: 8/19/2023
Citation: Srygley, R.B. 2023. Selective protein self-deprivation by Mormon crickets following fungal attack. Journal of Insect Physiology. 149. Article 104555. https://doi.org/10.1016/j.jinsphys.2023.104555.
DOI: https://doi.org/10.1016/j.jinsphys.2023.104555

Interpretive Summary: Mormon crickets aggregate and march in bands containing millions of insects in the western U.S. Some of these migrating Mormon crickets seek protein. In the lab, protein-restricted diets caused Mormon crickets to have lower enzymatic immunity and they were more susceptible to fungal attack. Here, we ask: Do Mormon crickets elevate phenoloxidase (PO) activity and consume protein in response to B. bassiana fungal infection? B. bassiana was applied topically (day 0), and mortality began on day 5. As predicted, PO titers were elevated as a result of fungal infection, and hemolymph protein was reduced. Surprisingly, during the first three days post-infection, infected insects reduced protein consumption while consuming carbohydrates at a similar rate to the controls. Following day 3, a general starvation of protein and carbohydrate was evident in infected insects. Because survivorship to infection was associated with the amount of protein consumed and unrelated to carbohydrate consumption, selective protein starvation by the host seems counterintuitive. Protein starvation is an unexpected benefit of fungal application. A reduction in the need for protein should reduce aggression between members of the migratory band and acts of cannibalism, which force the band to march in a single direction. Slowing the band would reduce band interference with traffic on roadways and encounters with irrigated crops. Fungal application might even result in disbanding, reducing insect density and further lowering economic impact.

Technical Abstract: Immune responses to infection result in behavioral changes that affect resource acquisition, such as general starvation and compensatory feeding to offset changes in resource allocation. Mormon crickets aggregate and march in bands containing millions of insects. Some bands are comprised of insects seeking proteins. They are also low in circulating phenoloxidase (PO) and more susceptible to fungal attack, as we have demonstrated in the lab. Here, we ask: Do Mormon crickets elevate PO and consume protein in response to infection by the pathogenic fungus Beauveria bassiana? B. bassiana was applied topically (day 0), and mortality began on day 5. Total protein, PO, and prophenoloxidase (proPO) were assayed in hemolymph on day 1 and 4. On day 1, PO titers were not different between inoculated and control insects, whereas by day 4, PO was greater in the inoculated group. proPO activity was unchanged. Circulating protein declined in inoculated insects relative to controls. As predicted, PO titers were elevated as a result of fungal infection, and hemolymph protein was reduced, but the insects did not compensate behaviorally. Indeed, during the first three days post-infection, infected insects reduced protein consumption while maintaining carbohydrate consumption similar to the controls. Following day 3, a more general reduction in protein and carbohydrate intake was evident in infected insects. Survivorship to infection was associated with the amount of protein consumed and unrelated to carbohydrate consumption. Selective protein deprivation by the host seems counterintuitive, but it might limit growth and toxin production by the invading fungus. Alternatively, the fungus might control the host diet to compromise host immunity to infection. Abrupt changes in allocation resulting from an infection can lead to changes in acquisition that are not always intuitive. Because protein acquisition drives aggression between members of the migratory band, B. bassiana application may reduce cannibalism and slow band movement.