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Different ambrosia beetle species can coexist in tree trunks, where their immature stages feed upon symbiotic fungi. Although most ambrosia beetles are not primary pests and their fungal symbionts are not pathogenic to the host tree, exceptional situations exist. Notably, Xyleborus glabratus carries a phytopathogenic symbiont, Raffaelea lauricola, which causes laurel wilt, a lethal disease of some Lauraceae species. Both X. glabratus and R. lauricola are natives of Asia that recently invaded much of the coastal plain of the southeastern USA. This study examined ambrosia beetles that breed in susceptible trees in Florida (USA), including avocado (Persea americana), redbay (P. borbonia) and swampbay (P. palustris). Raffaelea lauricola was recovered from six of eight ambrosia beetle species that emerged from laurel wilt-affected swampbay trees, in addition to X. glabratus. Controlled infestations with cohorts of the six species other than X. glabratus revealed that each could transmit the pathogen to healthy redbay trees and two could transmit the pathogen to healthy avocado trees; laurel wilt developed in five and one of the respective beetle 9 host interactions. These results indicate flexibility in the lateral transfer of a non-native ambrosial fungus to other ambrosia beetles, and for the first time documents the transmission of a laterally transferred phytopathogenic symbiont by new ambrosia beetle species. Additional work is needed to determine whether, or to what extent, the new beetle 9 R. lauricola combinations play a role in spreading laurel wilt.

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 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 exotic Euwallacea 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 Fusarium 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 (i.e., host shifts) 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 is a stochastic pattern. Lastly, two collections of Euwallacea sp. #2 from Miami-Dade County, Florida shared an identical cytochrome oxidase subunit 1 (CO1) allele with Euwallacea validus, suggesting introgressive hybridization between these species and/or pseudogenous nature of this marker. 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, and that these shifts may bring together more aggressive and virulent combinations of these invasive mutualists.

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