Cargando…

Convergent evolution of a labile nutritional symbiosis in ants

Ants are among the most successful organisms on Earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have evolved symbioses repeate...

Descripción completa

Detalles Bibliográficos
Autores principales: Jackson, Raphaella, Monnin, David, Patapiou, Patapios A., Golding, Gemma, Helanterä, Heikki, Oettler, Jan, Heinze, Jürgen, Wurm, Yannick, Economou, Chloe K., Chapuisat, Michel, Henry, Lee M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9381600/
https://www.ncbi.nlm.nih.gov/pubmed/35701539
http://dx.doi.org/10.1038/s41396-022-01256-1
_version_ 1784769114311491584
author Jackson, Raphaella
Monnin, David
Patapiou, Patapios A.
Golding, Gemma
Helanterä, Heikki
Oettler, Jan
Heinze, Jürgen
Wurm, Yannick
Economou, Chloe K.
Chapuisat, Michel
Henry, Lee M.
author_facet Jackson, Raphaella
Monnin, David
Patapiou, Patapios A.
Golding, Gemma
Helanterä, Heikki
Oettler, Jan
Heinze, Jürgen
Wurm, Yannick
Economou, Chloe K.
Chapuisat, Michel
Henry, Lee M.
author_sort Jackson, Raphaella
collection PubMed
description Ants are among the most successful organisms on Earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have evolved symbioses repeatedly to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Plagiolepis, Formica and Cardiocondyla ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine. We also show that in certain multi-queen lineages that have co-diversified with their symbiont for millions of years, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived resources. Our results imply that symbioses can arise to solve common problems, but hosts may differ in their dependence on symbionts, highlighting the evolutionary forces influencing the persistence of long-term endosymbiotic mutualisms.
format Online
Article
Text
id pubmed-9381600
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-93816002022-08-18 Convergent evolution of a labile nutritional symbiosis in ants Jackson, Raphaella Monnin, David Patapiou, Patapios A. Golding, Gemma Helanterä, Heikki Oettler, Jan Heinze, Jürgen Wurm, Yannick Economou, Chloe K. Chapuisat, Michel Henry, Lee M. ISME J Article Ants are among the most successful organisms on Earth. It has been suggested that forming symbioses with nutrient-supplementing microbes may have contributed to their success, by allowing ants to invade otherwise inaccessible niches. However, it is unclear whether ants have evolved symbioses repeatedly to overcome the same nutrient limitations. Here, we address this question by comparing the independently evolved symbioses in Camponotus, Plagiolepis, Formica and Cardiocondyla ants. Our analysis reveals the only metabolic function consistently retained in all of the symbiont genomes is the capacity to synthesise tyrosine. We also show that in certain multi-queen lineages that have co-diversified with their symbiont for millions of years, only a fraction of queens carry the symbiont, suggesting ants differ in their colony-level reliance on symbiont-derived resources. Our results imply that symbioses can arise to solve common problems, but hosts may differ in their dependence on symbionts, highlighting the evolutionary forces influencing the persistence of long-term endosymbiotic mutualisms. Nature Publishing Group UK 2022-06-14 2022-09 /pmc/articles/PMC9381600/ /pubmed/35701539 http://dx.doi.org/10.1038/s41396-022-01256-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Jackson, Raphaella
Monnin, David
Patapiou, Patapios A.
Golding, Gemma
Helanterä, Heikki
Oettler, Jan
Heinze, Jürgen
Wurm, Yannick
Economou, Chloe K.
Chapuisat, Michel
Henry, Lee M.
Convergent evolution of a labile nutritional symbiosis in ants
title Convergent evolution of a labile nutritional symbiosis in ants
title_full Convergent evolution of a labile nutritional symbiosis in ants
title_fullStr Convergent evolution of a labile nutritional symbiosis in ants
title_full_unstemmed Convergent evolution of a labile nutritional symbiosis in ants
title_short Convergent evolution of a labile nutritional symbiosis in ants
title_sort convergent evolution of a labile nutritional symbiosis in ants
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9381600/
https://www.ncbi.nlm.nih.gov/pubmed/35701539
http://dx.doi.org/10.1038/s41396-022-01256-1
work_keys_str_mv AT jacksonraphaella convergentevolutionofalabilenutritionalsymbiosisinants
AT monnindavid convergentevolutionofalabilenutritionalsymbiosisinants
AT patapioupatapiosa convergentevolutionofalabilenutritionalsymbiosisinants
AT goldinggemma convergentevolutionofalabilenutritionalsymbiosisinants
AT helanteraheikki convergentevolutionofalabilenutritionalsymbiosisinants
AT oettlerjan convergentevolutionofalabilenutritionalsymbiosisinants
AT heinzejurgen convergentevolutionofalabilenutritionalsymbiosisinants
AT wurmyannick convergentevolutionofalabilenutritionalsymbiosisinants
AT economouchloek convergentevolutionofalabilenutritionalsymbiosisinants
AT chapuisatmichel convergentevolutionofalabilenutritionalsymbiosisinants
AT henryleem convergentevolutionofalabilenutritionalsymbiosisinants