Flexibility in the ambrosia symbiosis of Xyleborus bispinatus

Authors: MENOCAL, OCTAVIO - University Of Florida; CRUZ, LUISA - University Of Florida; Kendra, Paul; BERTO, MARIELLE - University Of Florida; CARRILLO, DANIEL - University Of Florida

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/6/2023
Publication Date: 3/2/2023
Citation: Menocal, O., Cruz, L.F., Kendra, P.E., Berto, M., Carrillo, D. 2023. Flexibility in the ambrosia symbiosis of Xyleborus bispinatus. Frontiers in Microbiology. 14:1110474. https://doi.org/10.3389/fmicb.2023.1110474.
DOI: https://doi.org/10.3389/fmicb.2023.1110474

Interpretive Summary: Ambrosia beetles in their native environment maintain stable relationships with a specific assemblage of symbiotic fungi. However, when exotic ambrosia beetles invade new regions, there may be lateral transfer of fungal symbionts to endemic beetle species. This is the case with the laurel wilt pathogen, originally found only in the redbay ambrosia beetle from southeast Asia, but now isolated from multiple US endemic species, including Xyleborus bispinatus in Florida avocado groves. Although recovered from X. bispinatus, it is not known if the laurel wilt fungus (1) serves as a nutritional symbiont for X. bispinatus or (2) persists through multiple generations. It also is unknown if X. bispinatus can utilize the symbionts of tea shot-hole borer which cause Fusarium dieback of avocado. Therefore, scientists from the University of Florida (Homestead) and USDA-ARS (Miami) conducted research to determine the functional roles of several symbiotic fungal species. Results indicated that X. bispinatus can survive, reproduce, and maintain long-term mutualism with foreign fungal symbionts under laboratory conditions. Females fed the laurel wilt fungus produced fewer offspring; however, females fed the Fusarium dieback fungus produced significantly more offspring than females fed their typical fungal symbionts. These findings support the role of X. bispinatus as a vector of avocado pathogens and warrant further investigation of this beetle as an agricultural pest in Florida.

Technical Abstract: Ambrosia beetles maintain strict associations with specific lineages of fungi. However, anthropogenic introductions of ambrosia beetles into new ecosystems can result in the lateral transfer of their symbionts to other ambrosia beetles. We investigated the ability of a Florida endemic ambrosia beetle, Xyleborus bispinatus, to feed and establish persistent associations with two of its known symbionts (Raffaelea subfusca and Raffaelea arxii) and two other fungi (Harringtonia lauricola and Fusarium sp. nov.), which are primary symbionts of invasive ambrosia beetles. The stability of these mutualisms and their effect on the beetle’s fitness were monitored over five consecutive generations. Surface-disinfested pupae with non-developed mycangia were reared separately on one of the four fungal symbionts. Non-treated beetles (i.e., lab colony) with previously colonized mycangia were used as a control group. We experimentally demonstrated that X. bispinatus could exchange its fungal symbionts, survive, and reproduce on different fungal diets, including known fungal associates and phylogenetically distant fungi, which are plant pathogens and primary symbionts of other invasive ambrosia beetles. These changes in fungal diets resulted in persistent mutualisms, and some symbionts even increased the beetle’s reproduction. Females that developed on Fusarium sp. nov. had a significantly greater number of female offspring than non-treated beetles. Females that fed solely on Harringtonia or Raffaelea symbionts produced fewer female offspring. Even though some ambrosia beetles like X. bispinatus can partner with different ambrosia fungi, their symbiosis under natural conditions is modulated by their mycangium and possibly other environmental factors. However, exposure to symbionts of invasive beetles can result in stable partnerships with these fungi and affect the population dynamics of ambrosia beetles and their symbionts.