Termite eusociality and contrasting selective pressure on social and innate immunity

Abstract

The evolution of termite eusociality has been influenced by their nesting and foraging ecology. This includes the evolution of a separate developmental line for specialized workers that forego direct reproduction (true workers), which coincides with the transition from inhabiting a dead-wood nest to foraging for food outside the nest. Foraging for extranidal food requires that termites move through an entomopathogen-rich rhizosphere. This suggests that improved defenses against these pathogens were required for the successful transition to foraging outside the nest. Soil is especially rich in insect pathogens such as Metarhizium, and termites use secreted salivary β-1,3-glucanases for protection from this fungus. These enzymes are likely to be dependent on hygiene behaviors, such as allogrooming of external surfaces after contact with fungal conidial spores or ingestion or burying of infected nestmates prior to sporulation of the cadaver. These social mechanisms of defense could compensate for internal innate mechanisms of defense and even relax selective pressure on these innate mechanisms. Here, we investigated whether the selective pressure was intensified or relaxed on secreted β-1,3-glucanases as well as internal innate immune proteins, especially those putatively involved in antifungal defense. An analysis of the molecular evolution of two termite β-1,3-glucanases (GNBP1,2) indicates that the intensity of selection on them significantly increased with the transition to foraging. The shift to foraging for extranidal food apparently required adaptive modification of secreted GNBPs to help cope with increased exposure to pathogenic conidia in the soil. This included modification of a conserved binding site in GNBP2. In contrast, there was either significant relaxation or no change of selection pressure on Toll and phenoloxidase pathway immune genes with the transition to foraging. Relaxation was also observed with the evolution of drywood termites, but this likely reflects a transition to a microhabitat with fewer pathogens. Selection intensified on a subset of immune genes that regulate intestinal microbes with the more recent radiation of the Termitidae and the diversification of their feeding strategies.

Significance statement

The evolution of termite worker eusociality coincides with a relaxation of selective pressure on innate components of the immune system, especially those involved in antifungal defense. In contrast, the selective pressure intensified on two β-1,3-glucanases that contribute to the elimination of fungal pathogens by social behaviors such as allogrooming, cannibalism, and undertaking. This change in selective pressure appears to reflect an increased reliance on social immunity by dedicated altruistic workers in response to novel or enhanced threat by fungal pathogens. This supports other studies in social insects that indicate that the evolution of social immunity not only compensates for an increased vulnerability to infectious disease associated with living in crowded conditions but relaxes selective pressure on components of the internal innate immune system. Our results also indicate that a shift to microbially depauperate habitats relaxed selective pressure on termite immune defenses whereas a more recent diversification of diet intensified selection on mechanisms for regulating intestinal microbes.