Abstract
The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.
Highlights
Immunity is closely tied with evolutionary transitions, such as the evolution of multicellular organisms from single-celled ancestors and the evolution of eusocial animals from solitary ancestors
We find evidence of thioredoxin peroxidases undergoing a contraction in the Termitidae crown group, while defensins underwent an expansion in the same group
We found evidence of GNBP undergoing an expansion in the common ancestor of subsocial cockroaches and contractions of CLIP in the most recent common ancestor (MRCA) of Rhinotermitidae and Termitidae and autophagy-related genes in the MRCA of Termitidae
Summary
Immunity is closely tied with evolutionary transitions, such as the evolution of multicellular organisms from single-celled ancestors and the evolution of eusocial animals from solitary ancestors. As with the evolution of the metazoan immune system, which is thought to have emerged via the co-option of preexisting molecular modules and functions into novel defensive pathways, it has been hypothesized that social immune systems originated via similar processes [10], with a potentially crucial role for behavioural [11] as well as immune gene adaptations [12,13]. In line with this view, many genes, including immune-related genes, have been shown to display castespecific expression patterns [14,15,16,17,18]. Following an investigation into immune gene evolution across a termite phylogeny, we carried out comparative gene expression analyses on representative species bordering the social transition in order to gain deeper insight into the structure of termite immunity
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