Superorganism Immunity: A Major Transition in Immune System Evolution

Christopher D Pull,Dino P Mcmahon

doi:10.3389/fevo.2020.00186

Abstract

Social insect colonies can express adaptive, organism-like design. In some cases, colonies so resemble a unique, cohesive and integrated “individual” that they are termed superorganisms. The major evolutionary transitions framework explains, via inclusive fitness theory, how new levels of biological individuality, including genes into genomes within cells, cells into multicellular organisms and organisms into superorganisms can emerge. Importantly, it highlights how at each major transition similar challenges arose and why seemingly convergent solutions evolved. One challenge faced at each transition is exploitation, caused internally by social cheaters, and externally by parasites and pathogens. To overcome the problem of exploitation transitions in biological individuality required novel immune systems to maintain the integrity of newly emerged individuals. Multicellular organisms evolved an immune system while social insect colonies evolved a social immune system. In this review, we take a major transitions perspective of immunity to highlight the interdependency between the evolution of immune systems and the emergence of biological individuality. We build on the notion that superorganisms have evolved an immune system to promote the fitness of the colony. We draw parallels between the evolution of the metazoan immune system and the social immune system, and their expression as cognitive networks. Moreover, we discuss how research on other group-living species, such as family-based cooperative breeders, can inform our understanding of how social immune systems evolve. We conclude that “superorganism immunity” is an adaptive suite of organismal traits that evolves to maximise the fitness of advanced social insect colonies, fulfilling the same function as the immune system of Metazoa.

Highlights

“Fixing attention on the honeybee. . .nothing like the immune system for detecting and combatting microbial enemies is known to exist.”
The underlying process governing each of these transitions is social evolution (Bourke, 2011; West et al, 2015) and examples include: genes into genomes within cells giving rise to single-celled life; cells into organisms resulting in the complex multicellular plants and animals; and organisms into superorganisms, the evolution of social insect colonies with obligate reproductive and worker roles
In the years since Hamilton’s original work identifying disease as a major constraint on the evolution of insect sociality (Hamilton, 1987), our view of how social insects overcome the problem of disease has shifted dramatically, from a focus on genetic resistance to a well-developed, comprehensive understanding of the role of disease defense in social insect evolution

Summary

Introduction

“Fixing attention on the honeybee. . .nothing like the immune system for detecting and combatting microbial enemies is known to exist.”. Due to low levels of genetic diversity within these groups, disease should be a major constraint on the evolution of multicellularity and insect sociality (Hamilton, 1987). Hamilton instead proposed outbreeding to increase genetic diversity as the main mechanism that prevents pathogens driving social insects to extinction (Hamilton, 1987). Clearly not evolved as a universal mechanism to reduce disease susceptibility in insect colonies. Our aim is to build on the original hypothesis asserted by Cremer et al

Objectives

Findings

Conclusion