Superorganism Immunity: A Major Transition in Immune System Evolution

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...

Full description

Bibliographic Details
Main Authors: Christopher D. Pull, Dino P. McMahon
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fevo.2020.00186/full
_version_ 1818457480359837696
author Christopher D. Pull
Dino P. McMahon
Dino P. McMahon
author_facet Christopher D. Pull
Dino P. McMahon
Dino P. McMahon
author_sort Christopher D. Pull
collection DOAJ
description 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 maximize the fitness of advanced social insect colonies, fulfilling the same function as the immune system of Metazoa.
first_indexed 2024-12-14T22:43:14Z
format Article
id doaj.art-bac2a51f7e884917b37b333224a5ebec
institution Directory Open Access Journal
issn 2296-701X
language English
last_indexed 2024-12-14T22:43:14Z
publishDate 2020-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Ecology and Evolution
spelling doaj.art-bac2a51f7e884917b37b333224a5ebec2022-12-21T22:44:55ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2020-06-01810.3389/fevo.2020.00186525331Superorganism Immunity: A Major Transition in Immune System EvolutionChristopher D. Pull0Dino P. McMahon1Dino P. McMahon2Department of Biological Sciences, School of Life Sciences and the Environment, Royal Holloway University of London, Egham, United KingdomInstitut für Biologie, Freie Universität Berlin, Berlin, GermanyDepartment for Materials and the Environment, BAM Federal Institute for Materials Research and Testing, Berlin, GermanySocial 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 maximize the fitness of advanced social insect colonies, fulfilling the same function as the immune system of Metazoa.https://www.frontiersin.org/article/10.3389/fevo.2020.00186/fullsuperorganismdiseasesocial evolutionmajor evolutionary transitionsocial immunity
spellingShingle Christopher D. Pull
Dino P. McMahon
Dino P. McMahon
Superorganism Immunity: A Major Transition in Immune System Evolution
Frontiers in Ecology and Evolution
superorganism
disease
social evolution
major evolutionary transition
social immunity
title Superorganism Immunity: A Major Transition in Immune System Evolution
title_full Superorganism Immunity: A Major Transition in Immune System Evolution
title_fullStr Superorganism Immunity: A Major Transition in Immune System Evolution
title_full_unstemmed Superorganism Immunity: A Major Transition in Immune System Evolution
title_short Superorganism Immunity: A Major Transition in Immune System Evolution
title_sort superorganism immunity a major transition in immune system evolution
topic superorganism
disease
social evolution
major evolutionary transition
social immunity
url https://www.frontiersin.org/article/10.3389/fevo.2020.00186/full
work_keys_str_mv AT christopherdpull superorganismimmunityamajortransitioninimmunesystemevolution
AT dinopmcmahon superorganismimmunityamajortransitioninimmunesystemevolution
AT dinopmcmahon superorganismimmunityamajortransitioninimmunesystemevolution