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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. This is in part due to their large genome sizes and difficulty in obtaining sequenceable material. In this manuscript, we leveraged a recently-isolated, laboratory-tractable Entomophthora muscae isolate and improved long-read sequencing to obtain a largely-complete entomophthoralean genome. Our E. muscae assembly is 1.03 Gb, consists of 7,810 contigs and contains 81.3% complete fungal BUSCOs. Using a comparative approach with other available (transcriptomic and genomic) datasets from entomophthoralean fungi, we provide new insight into the biology of these understudied pathogens. We offer a head-to-head comparison of morphological and molecular data for species within the E. muscae species complex. Our findings suggest that substantial taxonomic revision is needed to define species within this group and we provide recommendations for differentiating strains and species in the context of the existing body of E. muscae scientific literature. We show that giant genomes are the norm within Entomophthoraceae owing to extensive, but not recent, Ty3 retrotransposon activity, despite the presence of machinery to defend against transposable elements(RNAi). In addition, we find that E. muscae and its closest allies are enriched for M16A peptidases and 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 find that E. muscae has an expanded group of acid-trehalases, consistent with trehalose being the primary sugar component of fly (and insect) hemolymph. 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. 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.

Fungi of the Conidiobolus group belong to the family Ancylistaceae (Entomophthorales, Entomophthoromycotina, Zoopagomycota) and include over 70 predominantly saprotrophic species in four similar and closely related genera, that were separated phylogenetically recently. Entomopathogenic fungi of the genus Batkoa are very close morphologically to the Conidiobolus species. Their thalli share similar morphology, and they produce ballistic conidia like closely related entomopathogenic Entomophthoraceae. Ballistic conidia are traditionally considered as an efficient tool in the pathogenic process and an important adaptation to the parasitic lifestyle. Our study aims to reconstruct the phylogeny of this fungal group using molecular and genomic data, ancestral lifestyle and morphological features of the conidiobolus-like group and the direction of their evolution. Based on phylogenetic analysis, some species previously in the family Conidiobolaceae are placed in the new families Capillidiaceae and Neoconidiobolaceae, which each include one genus, and the Conidiobolaceae now includes three genera. Intermediate between the conidiobolus-like groups and Entomophthoraceae, species in the distinct Batkoa clade now belong in the family Batkoaceae. Parasitism evolved several times in the Conidiobolus group and Ancestral State Reconstruction suggests that the evolution of ballistic conidia preceded the evolution of the parasitic lifestyle.

The fungal order Entomophthorales occurs worldwide, with most species infecting arthropods as pathogens. Species in this order can cause epizootics and change the behavior of infected hosts. Molecular data are available only for 20% of the known species, and distributions of species are seldom summarized. Significant diversity of hosts, poor molecular data availability, and poor resolution of the phylogenetic relationships within this fungal order suggest that the diversity of these fungi is not sufficiently described. The subfamily Erynioideae includes 111 arthropod pathogens, divided among six genera, with the genus Pandora being one of the most diverse genera. Sequences of 18S, 28S, and ITS for two species are used to place these Pandora species in a phylogenic tree of the subfamily; this tree also supports our synonymy of the genus Furia with Pandora. Among the two species specifically covered in this paper, Pandora gloeospora was observed during epizootics occurring in mushroom flies (Diptera: Sciaridae) on Agaricus bisporus cultures in Pennsylvania, Delaware, and Maryland (US) mushroom farms and also in Florida on Pleurotus sp. Outside the US, P. gloeospora was found infecting several Nematocera (Diptera) in Europe (France) and Asia (China). Pandora sylvestris n. sp. was collected during epizootics occurring in larvae of hickory tussock moths, Lophocampa caryae (Lepidoptera: Erebidae), in hardwood forests in Michigan and Vermont. [ABSTRACT FROM AUTHOR]

Biological control is often a key component of management strategies for invasive species. Yet, the effectiveness of biological control can be limited by a poor understanding of natural enemy ecology. To overcome this, habitat suitability models can predict distributions of invasive species and identify areas of potential overlap between invaders and natural enemies to guide biological control. Here we used data from a coordinated national monitoring network and a novel modeling method that incorporates physiology into correlative niche models to predict potential distributions of the brown marmorated stink bug, Halyomorpha halys, and two natural enemies (a parasitoid, Trissolcus japonicus, and a microsporidian, Nosema maddoxi) in current and future climates (2070s). We show all three species have broad similarity in habitat suitability, with especially high overlap in the mid-Atlantic and southeastern US where H. halys populations were first established. Each species will likely expand their range across the northern US in the future, but the overlap between species may decrease. In much of the central and southeastern US, H. halys may decrease its range over time, although natural enemies may be less impacted, and overlap between species may increase. Our study shows that biological control provided by T. japonicus and N. maddoxi could be key for managing H. halys given their overlapping niches, and our models can aid in delineating areas where biocontrol may be most effective. Our method of linking field data with correlative niche models can also be used for other insects. [ABSTRACT FROM AUTHOR]

Insect pest species are generally expected to become more destructive with climate change because of factors such as weakened host tree defences during droughts and increased voltinism under rising temperatures; however, responses will vary by species due to a variety of factors, including altered interactions with their natural enemies. Entomopathogens are a substantial source of mortality in insects, but the likelihood of epizootics can depend strongly on climatic conditions. Previous research indicates that rates of infection of the spongy moth (Lymantria dispar) by its host-specific fungal pathogen, Entomophaga maimaiga, increase with environmental moisture and decrease as temperatures rise. High temperatures may have direct and indirect (due to the associated drying) effects on the fungus, but the interactive effects between temperature and moisture level on larval infection are unclear. Here, we test the hypothesis that warmer, drier conditions will decrease rates of infection of spongy moth larvae by E. maimaiga. We evaluated the effects of precipitation and temperature on larval mortality caused by E. maimaiga with a manipulative field experiment, conducted in one of the northernmost and coldest parts of the spongy moth's non-native range in North America. We caged laboratory-reared spongy moth larvae in experimentally warmed open-air forest plots, exposing the larvae to soil inoculated with E. maimaiga resting spores during two consecutive trials. Caged larvae were exposed to three temperature treatments — ambient, 1.7 °C above ambient and 3.4 °C above ambient — and either supplemental precipitation (+173 mm per trial) or ambient precipitation. Opposite to our hypothesis, there was no significant effect of supplemental precipitation, nor an interaction between precipitation and temperature. There was, however, a significant positive effect of increasing temperature on the number of larvae infected. On average, in each respective trial, larval infection increased by 44% and 50% under the elevated temperature treatments compared to ambient temperature. Experimental warming may have increased infections because ambient temperatures at the field site were suboptimal for fungal germination. The results from this experiment suggest that, in colder portions of the spongy moth's invasive range, increasing temperatures due to climate change may enhance the ability of E. maimaiga to help control populations of the spongy moth. [ABSTRACT FROM AUTHOR]