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

item KASSON, MATTHEW - Virginia Polytechnic Institution & State University
item O`Donnell, Kerry
item Rooney, Alejandro - Alex
item Sink, Stacy
item PLOETZ, RANDY - University Of Florida
item PLOETZ, JILL - University Of Florida
item KONKOL, JOSHUA - University Of Florida
item CARRILLO, DANIEL - University Of Florida
item FREEMAN, STANLEY - Volcani Center (ARO)
item MENDEL, ZVI - Volcani Center (ARO)

Submitted to: Fungal Genetics and Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/11/2013
Publication Date: 7/1/2013
Citation: Kasson, M.T., O'Donnell, K., Rooney, A.P., Sink, S.L., Ploetz, R.C., Ploetz, J.N., Konkol, J.L., Carrillo, D., Freeman, S., Mendel, Z., et al. 2013. An inordinate fondness for Fusarium: Phylogenetic diversity of fusaria cultivated by ambrosia beetles in the genus Euwallacea on avocado and other plant hosts. Fungal Genetics and Biology. 56(2013):147-157.

Interpretive Summary: In this research, we discovered that at least eight closely related pathogenic fungi are being cultivated for food by invasive wood boring beetles in the genus Euwallacea, an exotic ambrosium beetle native to Asia. These beetles and the Fusarium symbionts that they farm currently pose a significant threat to avocado production worldwide. In addition, these mutually obligate symbionts are economically destructive pests of cacao, rubber tree, tea in Asia, and literally hundreds of urban landscape trees in Los Angles and surrounding counties in southern California. Knowledge gained from DNA typing the fungi has paved the way for developing robust molecular diagnostic assays urgently needed to prevent further introductions of these exotic pests into the United States. This information will allow plant pathologists, insect biologists, and quarantine officers to develop robust methods for the early detection and identification of these economically destructive plant pathogens.

Technical Abstract: Ambrosia beetle fungiculture represents one of the most ecologically and evolutionarily successful symbioses, as evidenced by the spectacular adaptive radiation that gave rise to at least 3,500 extant Xyleborini. 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 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 cephalic 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 ~21.2 Mya, which coincides with the hypothesized adaptive radiation of the Xyleborini. Two strongly supported clades within the AFC (Clade 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 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 two 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.