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Despite over a century of observations, the obligate insect parasites within the order Entomophthorales remain poorly characterized at the genetic level. In this manuscript, we present a genome for a laboratory-tractable Entomophthora muscae isolate that infects fruit flies. Our E. muscae assembly is 1.03 Gb, consists of 7810 contigs and contains 81.3% complete fungal BUSCOs. Using a comparative approach with recent datasets from entomophthoralean fungi, we show that giant genomes are the norm within Entomophthoraceae owing to extensive, but not recent, Ty3 retrotransposon activity. In addition, we find that E. muscae and its closest allies possess genes that are likely homologs to the blue-light sensor white-collar 1, a Neurospora crassa gene that has a well-established role in maintaining circadian rhythms. We uncover evidence that E. muscae diverged from other entomophthoralean fungi by expansion of existing families, rather than loss of particular domains, and possesses a potentially unique suite of secreted catabolic enzymes, consistent with E. muscae’s species-specific, biotrophic lifestyle. Finally, we offer a head-to-head comparison of morphological and molecular data for species within the E. muscae species complex that support the need for taxonomic revision within this group. Altogether, we provide a genetic and molecular foundation that we hope will provide a platform for the continued study of the unique biology of entomophthoralean fungi.

Symbiosis can facilitate the development of specialized organs in the host body to maintain relationships with beneficial microorganisms. To understand the developmental and genetic mechanisms by which such organs develop, it is critical to first investigate the morphology and developmental timing of these structures during the onset of host development. We utilized micro-computed tomography (μCT) to describe the morphology and development of mycangia, a specialized organ, in the Asian ambrosia beetle species Euwallacea validus which maintains a mutualistic relationship with the Ascomycete fungus, Fusarium oligoseptatum. We scanned animals in larval, pupal and adult life stages and identified that mycangia develop during the late pupal stage. Here we reconcile preliminary evidence and provide additional morphological data for a second paired set of structures, including the superior, medial mycangia and an inferior, lateral pair of pouch-like structures, in both late-stage pupae and adult female beetles. Furthermore, we report the possible development of rudimentary, or partially developed pairs of medial mycangia in adult male beetles which has never been reported for any male Xyleborini. Our results illustrate the validity of μCT in observing soft tissues and the complex nature of mycangia morphology and development.

Abstract Mutualistic interactions between organisms often mediate the innovation of traits essential to maintain the relationship. Yet our understanding of these interactions has been stymied due to various hurdles in studying the genetics of non-model animals. To understand the genetic mechanisms by which such traits develop, we examined the function of genes breathless (btl), trachealess (trh), and doublesex in the development of a novel fungus-carrying organ (mycangium) that facilitates an obligate relationship between fungus-farming ambrosia beetles and specific fungal partners. Gene knockdown by RNA interference and subsequent micro-computed tomography visualization suggest btl and trh are required for initiation of mycangia and that tubulogenesis may have been co-opted for early mycangial development.