Summit disease, in which infected hosts seek heights (gravitropism), first noted in modern times by nineteenth-century naturalists, has been shown to be induced by disparate pathogens ranging from viruses to fungi. Infection results in dramatic changes in normal activity patterns, and such parasite manipulation of host behaviors suggests a strong selection for convergent outcomes albeit evolved via widely divergent mechanisms. The two best-studied examples involve a subset of viral and fungal pathogens of insects that induce “summiting” in infected hosts. Summiting presumably functions as a means for increasing the dispersal of the pathogen, thus significantly increasing fitness. Here, we review current advances in our understanding of viral- and fungal-induced summit disease and the host behavioral manipulation involved. Viral genes implicated in this process include a host hormone-targeting ecdysteroid UDP-glucosyltransferase (apparently essential for mediating summit disease induced by some viruses but not all) and a protein tyrosine phosphatase, with light dependance implicated. For summit disease-causing fungi, though much remains obscure, targeting of molting, circadian rhythms, sleep, and responses to light patterns appear involved. Targeting of host neuronal pathways by summit-inducing fungi also appears to involve the production of effector molecules and secondary metabolites that affect host muscular, immune, and/or neurological processes. It is hypothesized that host brain structures, particularly Mushroom Bodies (no relation to the fungus itself), important for olfactory association learning and control of locomotor activity, are critical targets for mediating summiting during infection. This phenomenon expands the diversity of microbial pathogen-interactions and host dynamics. Key points: • Summit disease or height seeking (gravitropism) results from viral and fungal pathogens manipulating insect host behaviors presumably to increase pathogen dispersal. • Insect baculoviruses and select fungal pathogens exhibit convergent evolution in host behavioral manipulation but use disparate molecular mechanisms. • Targets for affecting host behavior include manipulation of host hormones, feeding, locomotion, and immune, circadian, and neurological pathways.

Characterization of fungal spider pathogens lags far behind their insect counterparts. In addition, little to nothing is known concerning the ecological reservoir and/or fungal entomopathogen community surrounding infection sites. Five infected spider cadavers were identified in the neo-tropical climate of north-central Florida, USA, from three of which viable cultures were obtained. Multi-locus molecular phylogenetic and morphological characterization identified one isolate as a new Gibellula species, here named, Gibellula floridensis, and the other isolates highly similar to Parengyodontium album. The fungal entomopathogen community surrounding infected spiders was sampled at different habitats/trophic levels, including soil, leaf litter, leaf, and twig, and analyzed using ITS amplicon sequencing. These data revealed broad but differential distribution of insect-pathogenic fungi between habitats and variation between sites, with members of genera belonging to Metarhizium and Metacordyceps from Clavicipitaceae, Purpureocillium and Polycephalomyces from Ophiocordyceps, and Akanthomyces and Simplicillium from Cordycipitaceae predominating. However, no sequences corresponding to Gibellula or Parengyodontium, even at the genera levels, could be detected. Potential explanations for these findings are discussed. These data highlight novel discovery of fungal spider pathogens and open the broader question regarding the environmental distribution and ecological niches of such host-specific pathogens.

Ambrosia beetles have evolved specialized structures termed “mycangia”, which house and transport symbiotic microbes. Microbial partners include at least one obligate mutualistic filamentous fungus used as food for larvae and adults, and potentially secondary filamentous fungi, yeasts, and bacteria. Beetles in the genus Xyleborus possess paired pre-oral mycangial structures located within the head on either side of the mouth parts. Mycangia develop in pupae, with newly emerged adults acquiring partners from the environment. However, information concerning the cellular structure and function of Xyleborus mycangia remains limited. We show that in X. affinis, mycangia are lined with a layer of striated dense material, enclosing layers of insect epithelial cells, with diverse spine-like structures. Larger (5–10 μm) projections were concentrated within and near the entrance of mycangia, with smaller filaments (4–8 μm) within the mycangia itself. Rows of “eyelash” structures lined the inside of mycangia, with fungal cells free-floating or in close association with these projections. Serial sections revealed mandibular articulations, and mandibular, pharyngeal, and labial muscles, along with the mycangial entry/exit channel. Sheets of comb-like spines at the mycangial entrance and opposite the mycangia attached to the roof of the labrum or epipharynx may serve as an interlocking mechanism for opening/closing the mycangia and guiding fungal cells into entry/exit channels. Additionally, mandibular fibra (muscle tissue) potentially enervating and affecting the mechanism of mycangial functioning were noted. These data add crucial mechanistic detail to the model of pre-oral mycangia in Xyleborus beetles, their cellular structures, and how they house and dispense microbial symbionts.

Ambrosia beetles bore into trees, excavating galleries where they farm fungi as their sole source of nutrition. These mutualistic fungi typically do not cause significant damage to host trees; however, since their invasion into the U.S., the beetle Xyleborus glabratus has vectored its fungal partner, Harringtonia lauricola, which has acted as a devastating plant pathogen resulting in the deaths of over 500 million trees. Here, we show differences in the mycangial colonization of the indigenous X. affinis ambrosia beetle by H. lauricola, and the native fungal species, H. aguacate and Raffaelea arxii. While X. affinis was a good host for H. lauricola, the related ambrosia beetle, X. ferrugineus, was only marginally colonized by H. lauricola. X. affinis beetles neither fed on, nor were colonized by, the distantly related fungus, Magnaporthe oryzae. Mycangial colonization was affected by the nutritional state of the fungus. A novel method for direct quantification of mycangial contents based on image cell cytometry was developed and validated. The method was used to confirm mycangial colonization and demonstrate alternating fungal partner switching, which showed significant variation and dynamic turnover. X. affinis pre-oral mycangial pouches were visualized using fluorescent and light microscopy, revealing that newly emerged pupae displayed uncolonized mycangia prior to feeding, whereas beetles fed H. lauricola contained single-celled fungi within 6 h post-feeding. Mixed populations of fungal cells were seen in the mycangia of beetles following alternating colonization. Nuclear counter-staining revealed insect cells surrounding the mycangia. These data highlight variation and specificity in ambrosia beetle–fungal pairings and provide a facile method for direct quantification of mycangial contents.

Ambrosia beetles bore into trees, excavating galleries where they farm fungi as their sole source of nutrition. These mutualistic fungi typically do not cause significant damage to host trees; however, since their invasion into the U.S., the beetle Xyleborus glabratus has vectored its fungal partner, Harringtonia lauricola, which has acted as a devastating plant pathogen resulting in the deaths of over 500 million trees. Here, we show differences in mycangial colonization of the indigenous X. affinis ambrosia beetle by H. lauricola, and the native fungal species, H. aguacate and Raffaelea arxii. While X. affinis was a good host for H. lauricola, the related ambrosia beetle, X. ferrugineus, was only marginally colonized by H. lauricola. X. affinis beetles neither fed on, nor were colonized by, the distantly related fungus, Magnaporthe oryzae. Mycangial colonization was affected by the nutritional state of the fungus. A novel method for direct quantification of mycangial contents based on cell cytometry was developed and validated. The method was used to confirm mycangial colonization and to demonstrate alternating fungal partner switching, which showed significant variation and dynamic turnover. X. affinis pre-oral mycangial pouches were visualized using fluorescent and light microscopy, revealing that newly emerged pupae displayed uncolonized mycangia prior to feeding, whereas beetles fed H. lauricola contained single-celled fungi within 6 h post-feeding. Mixed populations of fungal cells were seen in the mycangia of beetles following alternating colonization. Nuclear counter-staining revealed insect cells surrounding the mycangia. These data highlight variation and specificity in ambrosia beetle-fungal pairings and provide a facile method for direct quantification of mycangial contents.