Abstract
Ambrosia beetles farm specialised fungi in sapwood tunnels and use pocket-like organs called mycangia to carry propagules of the fungal cultivars. Ambrosia fungi selectively grow in mycangia, which is central to the symbiosis, but the history of coevolution between fungal cultivars and mycangia is poorly understood. The fungal family Ceratocystidaceae previously included three ambrosial genera (Ambrosiella, Meredithiella, and Phialophoropsis), each farmed by one of three distantly related tribes of ambrosia beetles with unique and relatively large mycangium types. Studies on the phylogenetic relationships and evolutionary histories of these three genera were expanded with the previously unstudied ambrosia fungi associated with a fourth mycangium type, that of the tribe Scolytoplatypodini. Using ITS rDNA barcoding and a concatenated dataset of six loci (28S rDNA, 18S rDNA, tef1-α, tub, mcm7, and rpl1), a comprehensive phylogeny of the family Ceratocystidaceae was developed, including Inodoromyces interjectus gen. & sp. nov., a non-ambrosial species that is closely related to the family. Three minor morphological variants of the pronotal disk mycangium of the Scolytoplatypodini were associated with ambrosia fungi in three respective clades of Ceratocystidaceae: Wolfgangiella gen. nov., Toshionella gen. nov., and Ambrosiella remansi sp. nov. Closely-related species that are not symbionts of ambrosia beetles are accommodated by Catunica adiposa gen. & comb. nov. and Solaloca norvegica gen. & comb. nov. The divergent morphology of the ambrosial genera and their phylogenetic placement among non-ambrosial genera suggest three domestication events in the Ceratocystidaceae. Estimated divergence dates for the ambrosia fungi and mycangia suggest that Scolytoplatypodini mycangia may have been the first to acquire Ceratocystidaceae symbionts and other ambrosial fungal genera emerged shortly after the evolution of new mycangium types. There is no evidence of reversion to a non-ambrosial lifestyle in the mycangial symbionts.
Highlights
Multiple groups of wood-boring weevils, collectively known as ambrosia beetles, cultivate fungal gardens along the walls of their sapwood tunnels (‘galleries’) in a reciprocally obligate mutualism (Hulcr & Stelinski 2017)
Reciprocally-obligate fungus farming is shared with only two other lineages of in sects: the higher-attine ants (Mueller et al 2018) and the Termitomyces-farming termites (Nobre et al 2011), but ambrosia beetles are unique in their use of special fungus-carrying pockets called mycangia that allow cultivar persistence across
We successfully identified putative species of Ceratocystidaceae from 10 species of Scolytoplatypodini representing the three recognised lineages of the tribe (Jordal 2013), including four species from the African/Malagasy lineage of Scolytoplatypus (S. congonus, S. fasciatus, S. permirus, and S. rugosus), seven species from the Asian lineage of Scolytoplatypus (S. daimio, S. eutomoides, S. mikado, S. pubescens, S. raja, S. shogun, and S. tycon), and a species of Remansus (R. mutabilis) (Table 1)
Summary
Multiple groups of wood-boring weevils, collectively known as ambrosia beetles, cultivate fungal gardens along the walls of their sapwood tunnels (‘galleries’) in a reciprocally obligate mutualism (Hulcr & Stelinski 2017). The term mycangium is broadly applied to a range of sepa rately-evolved physical adaptations (usually invaginations of the exoskeleton that form pockets, cavities, or crevices) on different parts of the beetles’ bodies for the storage and transport of fungal spores (Francke-Grosmann 1963, 1967, Beaver 1989, Six 2003). The most effective and selective mycangia are ‘glandular sac mycangia’ (Six 2003) associated with active gland cells that secrete nutrients into or near the mycangium lumen (Schedl 1962, Francke-Grosmann 1963, 1967). Most mycangia are small relative to the beetles’ body size (hereafter ‘small mycangia’) and are relatively simple in structure, such as the oral /preoral pouch mycangia convergently developed by multiple ambrosia beetle lineages (Hulcr & Stelinski 2017).
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