title: Discordant phylogenies suggest repeated host shifts in the Fusarium-Euwallacea ambrosia beetle mutualism.
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 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.
authors.affiliation: Bacterial Foodborne Pathogens and Mycology Research Unit, National Center for Agricultural Utilization Research, US Department of Agriculture, Agricultural Research Service, 1815 North University Street, Peoria, IL 61604, USA. Electronic address: kerry.odonnell@ars.usda.gov.
authors.forename: Kerry
authors.initials: K
authors.lastname: O'Donnell
authors.affiliation: Bacterial Foodborne Pathogens and Mycology Research Unit, National Center for Agricultural Utilization Research, US Department of Agriculture, Agricultural Research Service, 1815 North University Street, Peoria, IL 61604, USA.
authors.forename: Stacy
authors.initials: S
authors.lastname: Sink
authors.affiliation: Department of Computer Science, Harvey Mudd College, Claremont, CA 91711, USA.
authors.forename: Ran
authors.initials: R
authors.lastname: Libeskind-Hadas
authors.affiliation: School of Forest Resources and Conservation, University of Florida, Gainesville, FL 32611, USA.
authors.forename: Jiri
authors.initials: J
authors.lastname: Hulcr
authors.affiliation: Division of Plant and Soil Sciences, West Virginia University, Morgantown, WV 26506, USA.
authors.forename: Matthew T
authors.initials: MT
authors.lastname: Kasson
authors.affiliation: Tropical Research and Education Center, University of Florida, Homestead, FL 33031, USA.
authors.forename: Randy C
authors.initials: RC
authors.lastname: Ploetz
authors.affiliation: Tropical Research and Education Center, University of Florida, Homestead, FL 33031, USA.
authors.forename: Joshua L
authors.initials: JL
authors.lastname: Konkol
authors.affiliation: Tropical Research and Education Center, University of Florida, Homestead, FL 33031, USA.
authors.forename: Jill N
authors.initials: JN
authors.lastname: Ploetz
authors.affiliation: Tropical Research and Education Center, University of Florida, Homestead, FL 33031, USA.
authors.forename: Daniel
authors.initials: D
authors.lastname: Carrillo
authors.affiliation: Tropical Research and Education Center, University of Florida, Homestead, FL 33031, USA.
authors.forename: Alina
authors.initials: A
authors.lastname: Campbell
authors.affiliation: Tropical Research and Education Center, University of Florida, Homestead, FL 33031, USA.
authors.forename: Rita E
authors.initials: RE
authors.lastname: Duncan
authors.affiliation: Tea Research Institute of Sri Lanka, St. Coombs, Talawakelle, Sri Lanka.
authors.forename: Pradeepa N H
authors.initials: PN
authors.lastname: Liyanage
authors.affiliation: Department of Plant Pathology and Microbiology, University of California, Riverside, CA 92521, USA.
authors.forename: Akif
authors.initials: A
authors.lastname: Eskalen
authors.affiliation: Department of Plant Pathology and Microbiology, University of California, Riverside, CA 92521, USA.
authors.forename: Francis
authors.initials: F
authors.lastname: Na
authors.affiliation: Department of Plant Pathology and Environmental Microbiology, Pennsylvania State University, University Park, PA 16802, USA.
authors.forename: David M
authors.initials: DM
authors.lastname: Geiser
authors.affiliation: School of Forest Resources and Conservation, University of Florida, Gainesville, FL 32611, USA.
authors.forename: Craig
authors.initials: C
authors.lastname: Bateman
authors.affiliation: Institute of Plant Protection, ARO, The Volcani Center, Bet Dagan 50250, Israel.
authors.forename: Stanley
authors.initials: S
authors.lastname: Freeman
authors.affiliation: Institute of Plant Protection, ARO, The Volcani Center, Bet Dagan 50250, Israel.
authors.forename: Zvi
authors.initials: Z
authors.lastname: Mendel
authors.affiliation: Institute of Plant Protection, ARO, The Volcani Center, Bet Dagan 50250, Israel.
authors.forename: Michal
authors.initials: M
authors.lastname: Sharon
authors.affiliation: National Institute of Agrobiological Sciences, Genetic Resources Center, 2-1-3 Kannondai, Tsukuba, Ibaraki 305-8602, Japan.
authors.forename: Takayuki
authors.initials: T
authors.lastname: Aoki
authors.affiliation: Crop Bioprotection Research Unit, National Center for Agricultural Utilization Research, US Department of Agriculture, Agricultural Research Service, 1815 North University Street, Peoria, IL 61604, USA.
authors.forename: Allard A
authors.initials: AA
authors.lastname: Cossé
authors.affiliation: Crop Bioprotection Research Unit, National Center for Agricultural Utilization Research, US Department of Agriculture, Agricultural Research Service, 1815 North University Street, Peoria, IL 61604, USA.
authors.forename: Alejandro P
authors.initials: AP
authors.lastname: Rooney
mesh_terms: D000818:Animals; D001517:Coleoptera / Q000145:classification / Q000235:genetics* / Q000382:microbiology*; D019143:Evolution, Molecular; D005260:Female; D005670:Fusarium / Q000145:classification* / Q000235:genetics*; D005800:Genes, Fungal; D017344:Genes, Insect; D014644:Genetic Variation; D010802:Phylogeny; D013559:Symbiosis
keywords: Cophylogeny; Fungiculture; Hybrid introgression; Molecular phylogenetics; Phylogenetic species; Symbiosis