Discordant phylogenies suggest repeated host shifts in the Fusarium–Euwallacea ambrosia beetle mutualism

•The Fusarium–Euwallacea ambrosia beetle mutualism evolved ∼20million years ago.•Fusaria and the Euwallacea ambrosia beetles that farm them are both monophyletic.•The mutualism was shaped more by multiple host shifts than diversifying coevolution.•Several exotic Fusarium–Euwallacea mutualists threat...

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Published in:Fungal genetics and biology 2015-09, Vol.82, p.277-290
Main Authors: O’Donnell, Kerry, Sink, Stacy, Libeskind-Hadas, Ran, Hulcr, Jiri, Kasson, Matthew T., Ploetz, Randy C., Konkol, Joshua L., Ploetz, Jill N., Carrillo, Daniel, Campbell, Alina, Duncan, Rita E., Liyanage, Pradeepa N.H., Eskalen, Akif, Na, Francis, Geiser, David M., Bateman, Craig, Freeman, Stanley, Mendel, Zvi, Sharon, Michal, Aoki, Takayuki, Cossé, Allard A., Rooney, Alejandro P.
Format: Article
Language:English
Subjects:
Animals
Coleoptera
Coleoptera - classification
Coleoptera - genetics
Coleoptera - microbiology
Cophylogeny
Curculionidae
Euwallacea
Evolution, Molecular
Female
Fungiculture
Fusarium
Fusarium - classification
Fusarium - genetics
Genes, Fungal
Genes, Insect
Genetic Variation
Hybrid introgression
Molecular phylogenetics
Persea americana
Phylogenetic species
Phylogeny
Scolytinae
Symbiosis
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Summary:•The Fusarium–Euwallacea ambrosia beetle mutualism evolved ∼20million years ago.•Fusaria and the Euwallacea ambrosia beetles that farm them are both monophyletic.•The mutualism was shaped more by multiple host shifts than diversifying coevolution.•Several exotic Fusarium–Euwallacea mutualists threaten avocado production worldwide.•Evidence exists consistent with hybrid introgression between Euwallacea species. 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 ∼19–24Mya. 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 E
ISSN:1087-1845
1096-0937
DOI:10.1016/j.fgb.2014.10.014