An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts

• Published in: Fungal genetics and biology Vol. 56; pp. 147 - 157
• Main Authors: Kasson, Matthew T., O’Donnell, Kerry, Rooney, Alejandro P., Sink, Stacy, Ploetz, Randy C., Ploetz, Jill N., Konkol, Joshua L., Carrillo, Daniel, Freeman, Stanley, Mendel, Zvi, Smith, Jason A., Black, Adam W., Hulcr, Jiri, Bateman, Craig, Stefkova, Kristyna, Campbell, Paul R., Geering, Andrew D.W., Dann, Elizabeth K., Eskalen, Akif, Mohotti, Keerthi, Short, Dylan P.G., Aoki, Takayuki, Fenstermacher, Kristi A., Davis, Donald D., Geiser, David M.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01-07-2013
• Subjects: adaptive radiation; Ambrosia; ambrosia beetles; Ambrosia fungi; Animal Structures - microbiology; Animals; avocados; Cluster Analysis; Divergence dating; DNA, Fungal - chemistry; DNA, Fungal - genetics; DNA, Ribosomal - chemistry; DNA, Ribosomal - genetics; DNA, Ribosomal Spacer - chemistry; DNA, Ribosomal Spacer - genetics; ecosystems; Evolution; Fusarium - classification; Fusarium - genetics; Fusarium - isolation & purification; Fusarium - physiology; Fusarium solani; genes; Genes, rRNA; Genetic Variation; hosts; interspecific hybridization; loci; Molecular Sequence Data; monophyly; Mutualism; Mycangia; Peptide Elongation Factor 1 - genetics; Persea - parasitology; Phylogeny; plant pathogens; RNA Polymerase II - genetics; RNA, Fungal - genetics; RNA, Ribosomal - genetics; Sequence Analysis, DNA; symbionts; Symbiosis; Weevils - growth & development; Weevils - microbiology; Xyleborus; Symbiosis; Evolution; Mutualism; Mycangia; Ambrosia fungi; Divergence dating
• ISSN: 1087-1845; 1096-0937
• DOI: 10.1016/j.fgb.2013.04.004

•Novel Fusarium clade associated with destructive invasive ambrosia beetles.•Ambrosia fusaria abundant in heads of female beetles, reflecting strong symbiosis.•Evolution of club-shaped conidia may reflect an adaptation for the symbiosis.•Evidence for interspecific hybridization among ambrosia beetle-associated fusaria.•Origin of Ambrosia Fusarium Clade coincides with radiation of their insect mutualists.
Ambrosia beetle fungiculture represents one of the most ecologically and evolutionarily successful symbioses, as evidenced by the 11 independent origins and 3500 species of ambrosia beetles. Here we document the evolution of a clade within Fusarium associated with ambrosia beetles in the genus Euwallacea (Coleoptera: Scolytinae). Ambrosia Fusarium Clade (AFC) symbionts are unusual in that some are plant pathogens that cause significant damage in naïve natural and cultivated ecosystems, and currently threaten avocado production in the United States, Israel and Australia. Most AFC fusaria produce unusual clavate macroconidia that serve as a putative food source for their insect mutualists. AFC symbionts were abundant in the heads of four Euwallacea spp., which suggests that they are transported within and from the natal gallery in mandibular mycangia. In a four-locus phylogenetic analysis, the AFC was resolved in a strongly supported monophyletic group within the previously described Clade 3 of the Fusarium solani species complex (FSSC). Divergence-time estimates place the origin of the AFC in the early Miocene ∼21.2Mya, which coincides with the hypothesized adaptive radiation of the Xyleborini. Two strongly supported clades within the AFC (Clades A and B) were identified that include nine species lineages associated with ambrosia beetles, eight with Euwallacea spp. and one reportedly with Xyleborus ferrugineus, and two lineages with no known beetle association. More derived lineages within the AFC showed fixation of the clavate (club-shaped) macroconidial trait, while basal lineages showed a mix of clavate and more typical fusiform macroconidia. AFC lineages consisted mostly of genetically identical individuals associated with specific insect hosts in defined geographic locations, with at least three interspecific hybridization events inferred based on discordant placement in individual gene genealogies and detection of recombinant loci. Overall, these data are consistent with a strong evolutionary trend toward obligate symbiosis coupled with secondary contact and interspecific hybridization.