Year of Award

2018

Document Type

Dissertation - Campus Access Only

Degree Type

Doctor of Philosophy (PhD)

Degree Name

Cellular, Molecular and Microbial Biology

Department or School/College

Division of Biological Sciences

Committee Chair

Scott Miller

Commitee Members

Brandon Cooper, Diana Six, Doug Emlen, Jason Stajich

Keywords

Ambrosia Fungi, Evolution, Insect Farming, Mating Type, Phylogenomics

Abstract

Globally distributed bark and ambrosia beetles (Curculionidae) form diverse symbioses with fungi, primarily from the orders Ophiostomatales and Microascales (Ascomycota, Sordariomycetes). This ancient symbiosis resulted in more than 7,400 beetle species with a likely similar number of fungal associates. Ambrosia beetles represent ~3,400 species in this group and differ from bark beetles in that they farm fungi to serve as their sole food source. Perhaps owing to the beetles concealed existence and tiny size as well as the convergent symbiotic phenotype assumed by the fungi, our understanding of the fundamental biology underlying these symbioses has been slow to evolve over the last 180 years. For many years the ophiostomatoid fungal cultivars were thought to be asexual clones, specific to their beetle partner, and to belong to a single fungal genus domesticated ~50 million years ago. Additionally, there is much ambiguity regarding the role of persistent microbial associates within the system. Advances in DNA sequencing technology enabled us to address some of these questions in a broad sample of Ophiostomatales fungal cultivars.

During my thesis, I sequenced more than 720 whole genomes of ambrosia fungal cultivars to address questions pertaining to the origin and timing of their domestication, their reproductive mode, and population dynamics. With collaborators, I performed controlled transcriptomics experiments to investigate the underlying basis of phenotypes characteristic of the “ambrosial” growth phase of these fungi. These efforts corroborated independent estimates for the evolution of the farming habit in beetles, indicating that for ~100 million years they have farmed fungi as a food source. I conclude that cultivars within the genus Raffaelea are multiply derived, with novel domestication events most often carried out by established beetle farmers. My work suggests that the evolution of novel farming habits is facilitated by the co-mingling of bark beetles and previously domesticated fungal cultivars. I show that the majority of Ophiostomatales fungi have mating-type genes consistent with outcrossing (heterothallic) with a small minority being self-compatible (homothallic). I conclusively demonstrate that recombination, and thus sexual reproduction, is occurring in both heterothallic and homothallic species. Finally, I show that the ambrosia growth phenotype is induced by a beetle-associated bacterium, suggesting that this symbiosis may be a tripartite association between beetle, fungus, and bacterium.

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© Copyright 2018 Daniel Douglas Vanderpool