Four mycangium types and four genera of ambrosia fungi suggest a complex history of fungus farming in the ambrosia beetle tribe Xyloterini

ABSTRACT

Ambrosia beetles farm fungal cultivars (ambrosia fungi) and carry propagules of the fungal mutualists in storage organs called mycangia, which occur in various body parts and vary greatly in size and complexity. The evolution of ambrosia fungi is closely tied to the evolution and development of the mycangia that carry them. The understudied ambrosia beetle tribe Xyloterini included lineages with uncharacterized ambrosia fungi and mycangia, which presented an opportunity to test whether developments of different mycangium types in a single ambrosia beetle lineage correspond with concomitant diversity in their fungal mutualists. We collected representatives of all three Xyloterini genera (Trypodendron, Indocryphalus, and Xyloterinus politus) and characterized their ambrosia fungi in pure culture and by DNA sequencing. The prothoracic mycangia of seven Trypodendron species all yielded Phialophoropsis (Microascales) ambrosia fungi, including three new species, although these relationships were not all species specific. Indocryphalus mycangia are characterized for the first time in the Asian I. pubipennis. They comprise triangular prothoracic cavities substantially smaller than those of Trypodendron and unexpectedly carry an undescribed species of Toshionella (Microascales), which are otherwise ambrosia fungi of Asian Scolytoplatypus (Scolytoplatypodini). Xyloterinus politus has two different mycangia, each with a different ambrosia fungus: Raffaelea cf. canadensis RNC5 (Ophiostomatales) in oral mycangia of both sexes and Kaarikia abrahamsonii (Sordariomycetes, genus incertae sedis with affinity for Distoseptisporaceae), a new genus and species unrelated to other known ambrosia fungi, in shallow prothoracic mycangia of females. In addition to their highly adapted mycangial mutualists, Trypodendron and X. politus harbor a surprising diversity of facultative symbionts in their galleries, including Raffaelea. A diversity of ambrosia fungi and mycangia suggest multiple ancestral cultivar captures or switches in the history of tribe Xyloterini, each associated with unique adaptations in mycangium anatomy. This further supports the theory that developments of novel mycangium types are critical events in the evolution of ambrosia beetles and their coadapted fungal mutualists.

KEYWORDS:

• Insect fungiculture
• Microascales
• mutualism
• Scolytinae
• symbiosis
• 5 new taxa
• 1 new typification

ACKNOWLEDGMENTS

The technical assistance of Cinthia Wilkinson, Rodrigo de Freitas, Yeganah Gharabigloozare, Caroline Wuest, and Ruben Garcia is greatly appreciated. We thank Mark Bunce, Scott Cameron, Robbie Doerhoff, Garret DuBois, Tom Eager, Stephen Fraedrich, Doug LeDoux, John Lundquist, Lennart van de Peppel, and Dan Vanderpool for providing galleries, beetles, or fungal cultures. Ji-Hyun Park and Sangwook Park assisted with obtaining Indocryphalus in South Korea. Lawrence Abrahamson, Keith Seifert, and Steven Cassar provided helpful unpublished material. We are grateful to the University of Kansas Ronald L. McGregor Herbarium for loaning specimens. We thank Dr. David Clark in Isabella County, Michigan, and Al Amstrutz of Benzie County, Michigan, for use of their private woodlots for collection of beetle and host wood. Jostein Gohli and Bjarte Jordal graciously provided COI sequences of Xyloterini for comparisons. Geoffrey Daniel (Swedish University of Agricultural Sciences), Gerard Verkleij (CBS), Shannon Dominick (BPI), and Cony Decock (MUCL) assisted with confirming typifications of specimens.

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Funding

Chase Mayers was supported in part by a fellowship from the Office of Biotechnology, Iowa State University. Other financial support was provided by cooperative agreements with the US Forest Service and Iowa State University. Peter Biedermann was supported by the German Research Foundation (DFG Emmy Noether Grant BI 1956/1-1). Craig Bateman was supported by a cooperative agreement with the United States Department of Agriculture Animal and Plant Health Inspection Service (USDA APHIS) (Farm Bill section 10007) and by the National Science Foundation (DEB 1556283).