A High Soldier Proportion Encouraged the Greater Antifungal Immunity in a Subterranean Termite

Abstract

Termites possess a mighty social immune system, serving as one of the key obstacles to controlling them biologically. However, the dynamic mechanism coordinating the social immunologic defense and caste distribution of the termites remains elusive. This study used the Coptotermes formosanus Shiraki and an entomopathogenic fungus as a host–pathogen system and experimentally manipulated a series of groups with different caste compositions of workers and soldiers. Then, the impact of demography on the behavior and innate immunity of termites was explored by analyzing the fungus susceptibility of the respective caste, efficiencies, and caste preferences of sanitary care, as well as the expression of the immune genes and phenoloxidase activity. Overall, to ensure the general health and survival of a group, the infected workers were found to sacrifice their survivorship for maintaining the soldier proportion of the group. If soldier proportion was limited within a threshold, both the survivorship of the workers and soldiers were not significantly affected by the infection. Correspondingly, the infected group with a higher proportion of soldiers stimulated the higher efficiency of a non-caste-biased sanitary care of the workers to the nestmate workers and soldiers. Moreover, the innate immunities of the infected workers were found to be more intensely upregulated in the group with higher soldier proportions. This suggested that the adjustable non-caste-biased sanitary care and innate immunity of the workers would contribute to the flexibility of the worker–soldier caste ratio in C. formosanus. This study, therefore, enhanced our understanding of the functional adaptation mechanism between pathogen-driven social immunity and the demography of the termites.

Involvement of a catalase gene in lignin catalysis and immune defense against pathogenic fungus in Coptotermes formosanus: a potential new target for termite control

“…The tem, lys, and tsf of termites are significantly upregulated by the immune induction of pathogenic fungi and play an important role in the innate immune response of termites. 23,24,28 Therefore, Cfcat RNAi weakened the systemic immune level of C. formosanus in the non-infectious state and had an intense inhibitory effect on the systemic immune response of infected termites from multiple perspectives (expression of antimicrobial peptides and antibacterial factors and PO cascade reactions). During the melanization cascade, multiple immune cells produce large amounts of ROS in the hemocolumn.…”

“…Twenty-four prehomogenized workers per treatment were inoculated with the conidium by submerging them into the conidial suspension of M. anisopliae separately within a microcentrifuge tube, with gentle swirling for 5 s and then drying on filter paper. 10,28 The non-infected treatments were established using sterile 0.1% TW 80 following a similar procedure. Each termite was reared separately in a 24-well culture plate in the same conditions described in the previous paragraph.…”

“…The control group was used as a calibrator to calculate relative expression levels. The relative expression levels for the specific genes, relative to the reference gene GADPH, 28,40 were calculated using the 2 −ΔΔCT method. 41 Three biological replicates were used for each group.…”

“…Studies on the innate immunity of termites have mostly focused on systemic/humoral immunity. The roles of antimicrobial factors such as termicin (TEM), spinigerin, lysozymes (LYS), and transferrin (TSF) in immune defense had been characterized 23–28 . Termite melanin acts through a phenol oxidase cascade reaction to counter pathogenic infection 29–31 .…”

Caste composition contributes to improve the social immunity in a nasute termite species exposed to entomopathogenic fungus

“…The mixed caste group showed a lower prevalence of M. anisopliae in dead termites compared to the single caste group; indicating that soldiers together with workers maximise the resistance to pathogens in groups of N. corniger . Zeng et al (2022) report that workers of Coptotermes formosanus (Isoptera: Rhinotermitidae) implemented sanitary care, with no caste priority, to the infected soldiers or their infected nestmate workers. Furthermore, workers sacrificed their survivorship to maintain the soldier proportion of the group.…”