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Primordial Enemies: Fungal Pathogens in Thrips Societies

Microbial pathogens are ancient selective agents that have driven many aspects of multicellular evolution, including genetic, behavioural, chemical and immune defence systems. It appears that fungi specialised to attack insects were already present in the environments in which social insects first e...

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Autores principales: Turnbull, Christine, Wilson, Peter D., Hoggard, Stephen, Gillings, Michael, Palmer, Chris, Smith, Shannon, Beattie, Doug, Hussey, Sam, Stow, Adam, Beattie, Andrew
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3504084/
https://www.ncbi.nlm.nih.gov/pubmed/23185420
http://dx.doi.org/10.1371/journal.pone.0049737
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author Turnbull, Christine
Wilson, Peter D.
Hoggard, Stephen
Gillings, Michael
Palmer, Chris
Smith, Shannon
Beattie, Doug
Hussey, Sam
Stow, Adam
Beattie, Andrew
author_facet Turnbull, Christine
Wilson, Peter D.
Hoggard, Stephen
Gillings, Michael
Palmer, Chris
Smith, Shannon
Beattie, Doug
Hussey, Sam
Stow, Adam
Beattie, Andrew
author_sort Turnbull, Christine
collection PubMed
description Microbial pathogens are ancient selective agents that have driven many aspects of multicellular evolution, including genetic, behavioural, chemical and immune defence systems. It appears that fungi specialised to attack insects were already present in the environments in which social insects first evolved and we hypothesise that if the early stages of social evolution required antifungal defences, then covariance between levels of sociality and antifungal defences might be evident in extant lineages, the defences becoming stronger with group size and increasing social organisation. Thus, we compared the activity of cuticular antifungal compounds in thrips species (Insecta: Thysanoptera) representing a gradient of increasing group size and sociality: solitary, communal, social and eusocial, against the entomopathogen Cordyceps bassiana. Solitary and communal species showed little or no activity. In contrast, the social and eusocial species killed this fungus, suggesting that the evolution of sociality has been accompanied by sharp increases in the effectiveness of antifungal compounds. The antiquity of fungal entomopathogens, demonstrated by fossil finds, coupled with the unequivocal response of thrips colonies to them shown here, suggests two new insights into the evolution of thrips sociality: First, traits that enabled nascent colonies to defend themselves against microbial pathogens should be added to those considered essential for social evolution. Second, limits to the strength of antimicrobials, through resource constraints or self-antibiosis, may have been overcome by increase in the numbers of individuals secreting them, thus driving increases in colony size. If this is the case for social thrips, then we may ask: did antimicrobial traits and microbes such as fungal entomopathogens play an integral part in the evolution of insect sociality in general?
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spelling pubmed-35040842012-11-26 Primordial Enemies: Fungal Pathogens in Thrips Societies Turnbull, Christine Wilson, Peter D. Hoggard, Stephen Gillings, Michael Palmer, Chris Smith, Shannon Beattie, Doug Hussey, Sam Stow, Adam Beattie, Andrew PLoS One Research Article Microbial pathogens are ancient selective agents that have driven many aspects of multicellular evolution, including genetic, behavioural, chemical and immune defence systems. It appears that fungi specialised to attack insects were already present in the environments in which social insects first evolved and we hypothesise that if the early stages of social evolution required antifungal defences, then covariance between levels of sociality and antifungal defences might be evident in extant lineages, the defences becoming stronger with group size and increasing social organisation. Thus, we compared the activity of cuticular antifungal compounds in thrips species (Insecta: Thysanoptera) representing a gradient of increasing group size and sociality: solitary, communal, social and eusocial, against the entomopathogen Cordyceps bassiana. Solitary and communal species showed little or no activity. In contrast, the social and eusocial species killed this fungus, suggesting that the evolution of sociality has been accompanied by sharp increases in the effectiveness of antifungal compounds. The antiquity of fungal entomopathogens, demonstrated by fossil finds, coupled with the unequivocal response of thrips colonies to them shown here, suggests two new insights into the evolution of thrips sociality: First, traits that enabled nascent colonies to defend themselves against microbial pathogens should be added to those considered essential for social evolution. Second, limits to the strength of antimicrobials, through resource constraints or self-antibiosis, may have been overcome by increase in the numbers of individuals secreting them, thus driving increases in colony size. If this is the case for social thrips, then we may ask: did antimicrobial traits and microbes such as fungal entomopathogens play an integral part in the evolution of insect sociality in general? Public Library of Science 2012-11-21 /pmc/articles/PMC3504084/ /pubmed/23185420 http://dx.doi.org/10.1371/journal.pone.0049737 Text en © 2012 Turnbull et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Turnbull, Christine
Wilson, Peter D.
Hoggard, Stephen
Gillings, Michael
Palmer, Chris
Smith, Shannon
Beattie, Doug
Hussey, Sam
Stow, Adam
Beattie, Andrew
Primordial Enemies: Fungal Pathogens in Thrips Societies
title Primordial Enemies: Fungal Pathogens in Thrips Societies
title_full Primordial Enemies: Fungal Pathogens in Thrips Societies
title_fullStr Primordial Enemies: Fungal Pathogens in Thrips Societies
title_full_unstemmed Primordial Enemies: Fungal Pathogens in Thrips Societies
title_short Primordial Enemies: Fungal Pathogens in Thrips Societies
title_sort primordial enemies: fungal pathogens in thrips societies
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3504084/
https://www.ncbi.nlm.nih.gov/pubmed/23185420
http://dx.doi.org/10.1371/journal.pone.0049737
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