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ARS Home » Midwest Area » Peoria, Illinois » National Center for Agricultural Utilization Research » Mycotoxin Prevention and Applied Microbiology Research » Research » Publications at this Location » Publication #308898
Title: Discordant phylogenies suggest repeated host shifts in the Fusarium–Euwallacea ambrosia beetle mutualism

Author
item O Donnell, Kerry
item Sink, Stacy
item HULCR, JIRI - University Of Florida
item KASSON, MATTHEW - West Virginia University
item PLOETZ, JILL - University Of Florida
item ESKALEN, AKIF - University Of California
item GEISER, DAVID - Pennsylvania State University
item FREEMAN, STANLEY - Volcani Center (ARO)
item Cosse, Allard
item Rooney, Alejandro - Alex

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/27/2014
Publication Date: 11/1/2014
Citation: O'Donnell, K., Sink, S.L., Libeskind-Hadas, R., Hulcr, J., Kasson, M.T., Ploetz, R.C., Konkol, J.L., Ploetz, J.N., Carrillo, D., Campbell, A., Cosse, A.A., Rooney, A.P., et al. 2014. Discordant phylogenies suggest repeated host shifts in the Fusarium–Euwallacea ambrosia beetle mutualism. Fungal Genetics and Biology. 82:277-290.

Interpretive Summary: This research was conducted to characterize the genetic diversity of wood-boring ambrosia beetles in the genus Euwallacea and the Fusarium fungi they cultivate for food. Native to Asia, five different infestations of these economically destructive symbionts are currently present within the United States. These fungus-farming beetles currently pose a significant threat to avocado production, urban landscape trees, and forested areas worldwide. Using collections from the United States, Australia, and Sri Lanka, we DNA typed beetles and the Fusarium species they transport in special cavities by their mouth parts to assess the fidelity of this mutualism. We identified 12 ambrosia fusaria and eight Fusarium-farming Euwallacea species worldwide, based on genetic analyses of DNA sequence data from multiple genes. We discovered that five Euwallacea spp. cultivating six fusaria have been introduced inadvertently into the United States, most just within the past decade. Genetic analyses indicate that the Euwallacea beetles have switched Fusarium symbionts multiple times during their evolution. Results of the present study highlight the importance of understanding the potential for and frequency of host-switching between Euwallacea and the fusaria they cultivate for food, given that these shifts may bring together more aggressive and virulent combinations of these invasive mutualists. Results of the present study should help inform quarantine officials and agricultural scientists of each species’ genetic diversity, host range, and geographic distribution so that these economically destructive pests and pathogens can be monitored using molecular markers such as those developed in this study.

Technical Abstract: The mutualism between xyleborine beetles in the genus Euwallacea (Coleoptera: Curculionidae: Scolytinae) and members of the Ambrosia Fusarium Clade (AFC) represents one of 11 known independent evolutionary origins of fungiculture by ambrosia beetles. Female Euwallacea beetles transport fusarial symbionts in paired mandibular mycangia from their natal gallery to woody hosts where they are cultivated in galleries as a source of food. Native to Asia, several of these exotic species were introduced into the United States and Israel within the past two decades and they now threaten urban landscapes, forests, and avocado production. To assess species limits and to date the evolutionary diversification of the mutualists, we reconstructed the evolutionary histories of key representatives of the Fusarium and Euwallacea clades using maximum parsimony and maximum likelihood methods. Twelve species-level lineages, termed AF 1-12, were identified within the monophyletic AFC and seven among the Fusarium-farming Euwallacea. Bayesian diversification-time estimates placed the origin of the Euwallacea – Fusarium mutualism near the Oligocene – Miocene boundary ~19-24 Mya. Most Euwallacea spp. appear to be associated with one species of Fusarium, but two species farmed two closely related fusaria. Euwallacea sp. #2 in Miami-Dade County, Florida cultivated Fusarium spp. AF-6 and AF-8 on avocado, and Euwallacea sp. #4 farmed F. ambrosium AF-1 and Fusarium sp. AF-11 on Chinese tea in Sri Lanka. Cophylogenetic analyses indicated that the Euwallacea and Fusarium phylogenies were largely incongruent, apparently due to the beetles switching fusarial symbionts at least five times during the evolution of this mutualism. Three cospeciation events between Euwallacea and their AFC symbionts were detected, but randomization tests failed to reject the null hypothesis that the putative parallel cladogenesis could have occurred by chance. Lastly, three collections of Euwallacea sp. #2 from Miami-Dade County, Florida shared an identical cytochrome oxidase subunit 1 (CO1) allele with E. validus, suggesting introgressive hybridization between these species. Results of the present study highlight the importance of understanding the potential for and frequency of host-switching between Euwallacea and members of the AFC, given that these shifts may bring together more aggressive and virulent combinations of these invasive mutualists.