Co-adaptations between Ceratocystidaceae ambrosia fungi and the mycangia of their associated ambrosia beetles

Abstract

<p>In a reciprocal, obligate mutualism, ambrosia beetles cultivate gardens of fungi to extract nutrients from sapwood and carve a unique niche in this traditionally nutrient-poor substrate. This mutualism is the most ancient, widespread, and diverse system of insect agriculture. The beetles carry pure cultures of fungal spores to new trees using a variety of organs called mycangia. However, the diversity and evolutionary dynamics of these fungi and of the mycangia that carry them are poorly understood. Beetles with particularly large and specialized mycangia appear to associate with ambrosia fungi in the family Ceratocystidaceae (Microascales). Based on widespread geographic and taxonomic sampling of host beetles, isolation and characterization of their fungi, and molecular phylogenetics of these fungi, the diversity of ambrosia fungi and the evolution of ambrosia symbiosis in the Ceratocystidaceae are related to the development of mycangia in their respective beetle hosts. The mycangia of Indocryphalus, Remansus, Anisandrus maiche, and Corthylus papulans are newly characterized. Phylogenetic analyses supported six new genera and seventeen new species of fungi. Four unrelated lineages of ambrosia beetles with unique mycangia were found to carry ambrosia fungi in five genera of Ceratocystidaceae. Ambrosiella is associated with mesonotal mycangia of the Xylosandrus complex (Xyleborini) and the pronotal disk mycangium of Remansus mutabilis (Scolytoplatypodini). Meredithiella gen. nov. is associated with prothoracic coil mycangia of Corthylus (Corthylina). Phialophoropsis is associated with prothoracic pleural mycangia of Trypodendron (Xyloterini). Toshionella gen. nov. is associated with pronotal disk mycangia of Asian Scolytoplatypus (Scolytoplatypodini) and the prothoracic pleural mycangia of Indocryphalus pubipennis (Xyloterini). Wolfgangiella gen. nov. is associated with pronotal disk mycangia of African Scolytoplatypus. Two unrelated symbionts, Raffaelea aff. canadensis (Ophiostomatales) and Kaarikia abrahamsonii gen. et sp. nov. (incertae sedis), are associated with oral and prothoracic basin mycangia, respectively, of Xyloterinus politus (Xyloterini). Sexual states are characterized for species of Ambrosiella and Wolfgangiella, the first report of sexual states in mycangial symbionts of ambrosia beetles. Co-adaption between fungal genera and mycangial type was evident, but not species-level co-evolution. It is proposed that there were at least three independant domestication events in the Ceartocystidaceae, the first domestication most likely with the Scolytoplatypodini.</p>