Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite.

Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites host complex gut bacterial communities with evolutionary histories indicative of mixed-mode transmission. Here, we document that vertical transmission of gut bacterial strains is congruent across parent to offspring colonies in four pedigrees of the fungus-farming termite Macrotermes natalensis. We show that 44% of the offspring colony microbiome, including more than 80 bacterial genera and pedigree-specific strains, are consistently inherited. We go on to demonstrate that this is achieved because colony-founding reproductives are selectively enriched with a set of non-random, environmentally sensitive and termite-specific gut microbes from their colonies of origin. These symbionts transfer to offspring colony workers with high fidelity, after which priority effects appear to influence the composition of the establishing microbiome. Termite reproductives thus secure transmission of complex communities of specific, co-evolved microbes that are critical to their offspring colonies. Extensive yet imperfect inheritance implies that the maturing colony benefits from acquiring environmental microbes to complement combinations of termite, fungus and vertically transmitted microbes; a mode of transmission that is emerging as a prevailing strategy for hosts to assemble complex adaptive microbiomes.

Resistance and Vulnerability of Honeybee (Apis mellifera) Gut Bacteria to Commonly Used Pesticides.

Agricultural and apicultural practices expose honeybees to a range of pesticides that have the potential to negatively affect their physiology, neurobiology, and behavior. Accumulating evidence suggests that these effects extend to the honeybee gut microbiome, which serves important functions for honeybee health. Here we test the potential effects of the pesticides thiacloprid, acetamiprid, and oxalic acid on the gut microbiota of honeybees, first in direct in vitro inhibition assays and secondly in an in vivo caged bee experiment to test if exposure leads to gut microbiota community changes. We found that thiacloprid did not inhibit the honeybee core gut bacteria in vitro, nor did it affect overall community composition or richness in vivo. Acetamiprid did also not inhibit bacterial growth in vitro, but it did affect community structure within bees. The eight bacterial genera tested showed variable levels of susceptibility to oxalic acid in vitro. In vivo, treatment with this pesticide reduced amplicon sequence variant (ASV) richness and affected gut microbiome composition, with most marked impact on the common crop bacteria Lactobacillus kunkeei and the genus Bombella. We conducted network analyses which captured known associations between bacterial members and illustrated the sensitivity of the microbiome to environmental stressors. Our findings point to risks of honeybee exposure to oxalic acid, which has been deemed safe for use in treatment against Varroa mites in honeybee colonies, and we advocate for more extensive assessment of the long-term effects that it may have on honeybee health.

Female-biased sex allocation and lack of inbreeding avoidance in Cubitermes termites.

Sexually reproducing organisms face a strong selective pressure to find a mate and ensure reproduction. An important criterion during mate-selection is to avoid closely related individuals and subsequent potential fitness costs of resulting inbred offspring. Inbreeding avoidance can be active through kin recognition during mate choice, or passive through differential male and female-biased sex ratios, which effectively prevents sib-mating. In addition, sex allocation, or the resources allotted to male and female offspring, can impact mating and reproductive success. Here, we investigate mate choice, sex ratios, and sex allocation in dispersing reproductives (alates) from colonies of the termite Cubitermes tenuiceps. Termites have a short time to select a mate for life, which should intensify any fitness consequences of inbreeding. However, alates did not actively avoid inbreeding through mate choice via kin recognition based on genetic or environmental cues. Furthermore, the majority of colonies exhibited a female-biased sex ratio, and none exhibited a male-bias, indicating that differential bias does not reduce inbreeding. Sex allocation was generally female-biased, as females also were heavier, but the potential fitness effect of this costly strategy remains unclear. The bacterium Wolbachia, known in other insects to parasitically distort sex allocation toward females, was present within all alates. While Wolbachia is commonly associated with termites, parasitism has yet to be demonstrated, warranting further study of the nature of the symbiosis. Both the apparent lack of inbreeding avoidance and potential maladaptive sex allocation implies possible negative effects on mating and fitness.

Camponotusfloridanus Ants Incur a Trade-Off between Phenotypic Development and Pathogen Susceptibility from Their Mutualistic Endosymbiont Blochmannia.

Various insects engage in microbial mutualisms in which the reciprocal benefits exceed the costs. Ants of the genus Camponotus benefit from nutrient supplementation by their mutualistic endosymbiotic bacteria, Blochmannia, but suffer a cost in tolerating and regulating the symbiont. This cost suggests that the ants face secondary consequences such as susceptibility to pathogenic infection and transmission. In order to elucidate the symbiont's effects on development and disease defence, Blochmannia floridanus was reduced in colonies of Camponotus floridanus using antibiotics. Colonies with reduced symbiont levels exhibited workers of smaller body size, smaller colony size, and a lower major-to-minor worker caste ratio, indicating the symbiont's crucial role in development. Moreover, these ants had decreased cuticular melanisation, yet higher resistance to the entomopathogen Metarhizium brunneum, suggesting that the symbiont reduces the ants' ability to fight infection, despite the availability of melanin to aid in mounting an immune response. While the benefits of improved growth and development likely drive the mutualism, the symbiont imposes a critical trade-off. The ants' increased susceptibility to infection exacerbates the danger of pathogen transmission, a significant risk given ants' social lifestyle. Thus, the results warrant research into potential adaptations of the ants and pathogens that remedy and exploit the described disease vulnerability.