Species- and Caste-Specific Gut Metabolomes in Fungus-Farming Termites

Fungus-farming termites host gut microbial communities that contribute to the pre-digestion of plant biomass for manuring the fungal mutualist, and potentially to the production of defensive compounds that suppress antagonists. Termite colonies are characterized by complex division of labor and differences in diet between termite size (minor and major) and morphological (worker and soldier) castes, and this extends to the composition of their gut microbial communities. We hypothesized that gut metabolomes should mirror these differences and tested this through untargeted LC-MS/MS analyses of three South African species of fungus-farming termites. We found distinct metabolomes between species and across castes, especially between soldiers and workers. Primary metabolites dominate the metabolomes and the high number of overlapping features with the mutualistic fungus and plant material show distinct impacts of diet and the environment. The identification of a few bioactive compounds of likely microbial origin underlines the potential for compound discovery among the many unannotated features. Our untargeted approach provides a first glimpse into the complex gut metabolomes and our dereplication suggests the presence of bioactive compounds with potential defensive roles to be targeted in future studies.

Endemic Jeffrey Pine Beetle Associates: Beetle/Mite Fungal Dissemination Strategies and Interactions That May Influence Beetle Population Levels

Fungal and mite associates may drive changes in bark beetle populations, and mechanisms constraining beetle irruptions may be hidden in endemic populations. We characterized common fungi of endemic-level Jeffrey pine beetle (JPB) in western USA and analyzed their dissemination by JPB (maxillae and fecal pellet) and fungivorous mites to identify if endogenous regulation drove the population. We hypothesized that: (1) as in near-endemic mountain pine beetle populations, JPB’s mutualistic fungus would either be less abundant in endemic than in non-endemic populations or that another fungus may be more prevalent; (2) JPB primarily transports its mutualistic fungus, while its fungivorous mites primarily transport another fungus, and (3) based on the prevalence of yeasts in bark beetle symbioses, that a mutualistic interaction with blue-stain fungi present in that system may exist. Grosmannia clavigera was the most frequent JPB symbiont; however, the new here reported antagonist, Ophiostoma minus, was second in frequency. As hypothesized, JPB mostly carried its mutualist fungus while another fungus (i.e., antagonistic) was mainly carried by mites, but no fungal transport was obligate. Furthermore, we found a novel mutualistic interaction between the yeast Kuraishia molischiana and G. clavigera which fostered a growth advantage at temperatures associated with beetle colonization.

The Potential Global Distribution of Sirex juvencus (Hymenoptera: Siricidae) under Near Current and Future Climatic Conditions as Predicted by the Maximum Entropy Model

Wood wasp species in the genus Sirex are known pests of forestry. They cause significant economic losses due to their impacts on plant health and wood quality. S. juvencus (Hymenoptera: Siricidae), widely distributed in Asia, Europe, and North America, is known to negatively impact forestry, infesting Picea, Pinus, Larix, Abies, Cupressus, and Pseudotsuga species. This pest destroys plants by depositing eggs, mucus, and its obligate mutualistic fungus, Amylostereum areolatum. Its obligate mutualistic fungus is to provide nutrition for S. juvencus larva. Despite its extensive distribution range, little is known about which environmental variables significantly impact current and future distribution patterns of S. juvencus for pest control and monitoring. Here we used the maximum entropy model in conjunction with occurrence points of S. juvencus and environmental variables to predict the current and future global potential distribution of S. juvencus. We used the jackknife method and Pearson’s correlation analysis to select the environmental variables that influence the geographic distribution of S. juvencus, which resulted in the inclusion of the monthly average maximum temperature in February, the max temperature of warmest month, monthly average minimum temperature in July, monthly total precipitation in June, precipitation of the driest month, monthly total precipitation in September, and the temperature annual range. Temperature and precipitation are mainly likely to drive the distribution enabled by its obligate mutualistic fungus and the potential to co-infect with other Sirex species. The high temperature and low humidity influence S. juvencus eggs and larvae directly and indirectly via fungus-growth, which enables the larvae to survive. Furthermore, S. juvencus may increase its distribution to moderately suitable areas due to competition or dependency on other Sirex species during the infestation. Under the future climatic conditions, the highly suitable area increased by 32.79%, while the moderately suitable area, low suitable area, and unsuitable area increased by 28.14%, 3.30%, and 2.15%. Under climate changes, S. juvencus may spread in previously unsuitable areas rapidly.

Non-Inseminated Queens Have Worker-Like Behaviors in Colonies of Fungus-Growing Ants, Mycetomoellerius turrifex Wheeler (Attini, Hymenoptera)

In eusocial Hymenoptera such as ants, bees, and wasps, the queen numbers are fundamentally important to maintain the social systems. In Texas, USA, a fungus growing ant, Mycetomoellerius turrifex Wheeler (1903) (the genus name was changed from Trachymyrmex to Mycetomoellerius in 2019 (Solomon et al., 2019)) was observed to have several non-inseminated queens that wandered outside the nest long after the mating season. However, the evolutionary and ecological factors causing the occurrence of such non-inseminated queens are still unclear. Thus, I examined the worker-like behaviors of non-inseminated queens of M. turrifex in Texas. Fifteen ant colonies were collected over three years, between 1999 and 2001. The frequencies of non-inseminated queens, workers, and broods, as well as the depths of nest chambers, were observed in each collecting year. In Nov. 1999 and May 2000, multiple nests contained queens that did not mate with males within their nests. These nests had a relatively larger colony size than those collected in Oct. 2001. Conversely, the colonies collected in Oct. 2001 were completely monogynous, i.e., there were no non-inseminated queens in the nests. Behavioral observations of each female revealed that the non-inseminated queensbehaved significantly differently from the workers and the inseminated queens. The behaviors that distinguished different female castes were mutualistic fungus garden care, digging of nest floors, guarding, and resting in the nest. These data suggest that queens failed to mate due to severe environmental fluctuations in southern Texas, but were accepted by the colony as a temporary labor force.

Incidental Fungi in Host Trees Disrupt the Development of Sirex noctilio (Hymenoptera: Siricidae) Symbiotic Fungus and Larvae

The woodwasp, Sirex noctilio Fabricius, is an exotic pest of Pinus L. in the southern hemisphere and North America, and it is an emerging threat in northeastern China. Adult woodwasps have numerous insect competitors for oviposition substrates, and developing larvae must compete for resources with other subcortical invaders. Its mutualistic fungus Amylostereum areolatum (Fr.) Boidon, is less competitive than many other fungal colonists present in pine ecosystems. This study investigated the effects of incidental, host-colonizing fungi on the growth and development of woodwasp larvae and A. areolatum. Fungi were isolated from dead S. noctilio larvae within galleries (primarily Trichoderma Pers, Ophiostoma Sydow, and Sphaeropsis Sacc.), and effects of these fungi on woodwasp brood survival were investigated via inoculations of S. noctilio-infested logs. Larval mortality was significantly increased in sample logs inoculated with Ophiostoma minus (Hedgc.) Sydow Phlebiopsis gigantea (Fr.) Jülich, Trichoderma atroviride Bissett, Trichoderma viride Pers, and Trichoderma harzianum Rifai. Inoculation of logs with O. minus resulted in the highest mortality and greatest reductions in wood moisture content. When grown on artificial media, these fungi grew faster than and inhibited growth of A. areolatum mycelium. We propose that the adverse effects of incidental fungi on the survival of S. noctilio larvae may be caused at least in part by an indirect mechanism involving inhibition of the fungal symbiont. The findings provide potentially valuable information for suppressing S. noctilio populations using microbial control agents.