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Wide-ranging consequences of priority effects governed by an overarching factor

Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority ef...

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Autores principales: Chappell, Callie R, Dhami, Manpreet K, Bitter, Mark C, Czech, Lucas, Herrera Paredes, Sur, Barrie, Fatoumata Binta, Calderón, Yadira, Eritano, Katherine, Golden, Lexi-Ann, Hekmat-Scafe, Daria, Hsu, Veronica, Kieschnick, Clara, Malladi, Shyamala, Rush, Nicole, Fukami, Tadashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9671501/
https://www.ncbi.nlm.nih.gov/pubmed/36300797
http://dx.doi.org/10.7554/eLife.79647
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author Chappell, Callie R
Dhami, Manpreet K
Bitter, Mark C
Czech, Lucas
Herrera Paredes, Sur
Barrie, Fatoumata Binta
Calderón, Yadira
Eritano, Katherine
Golden, Lexi-Ann
Hekmat-Scafe, Daria
Hsu, Veronica
Kieschnick, Clara
Malladi, Shyamala
Rush, Nicole
Fukami, Tadashi
author_facet Chappell, Callie R
Dhami, Manpreet K
Bitter, Mark C
Czech, Lucas
Herrera Paredes, Sur
Barrie, Fatoumata Binta
Calderón, Yadira
Eritano, Katherine
Golden, Lexi-Ann
Hekmat-Scafe, Daria
Hsu, Veronica
Kieschnick, Clara
Malladi, Shyamala
Rush, Nicole
Fukami, Tadashi
author_sort Chappell, Callie R
collection PubMed
description Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub, Diplacus (formerly Mimulus) aurantiacus, exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among D. aurantiacus flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments, Acinetobacter nectaris, the bacterium most commonly found in D. aurantiacus nectar, exerted a strongly negative priority effect against Metschnikowia reukaufii, the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that M. reukaufii could evolve rapidly to improve resistance against the priority effect if constantly exposed to A. nectaris-induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization.
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spelling pubmed-96715012022-11-18 Wide-ranging consequences of priority effects governed by an overarching factor Chappell, Callie R Dhami, Manpreet K Bitter, Mark C Czech, Lucas Herrera Paredes, Sur Barrie, Fatoumata Binta Calderón, Yadira Eritano, Katherine Golden, Lexi-Ann Hekmat-Scafe, Daria Hsu, Veronica Kieschnick, Clara Malladi, Shyamala Rush, Nicole Fukami, Tadashi eLife Ecology Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub, Diplacus (formerly Mimulus) aurantiacus, exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among D. aurantiacus flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments, Acinetobacter nectaris, the bacterium most commonly found in D. aurantiacus nectar, exerted a strongly negative priority effect against Metschnikowia reukaufii, the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that M. reukaufii could evolve rapidly to improve resistance against the priority effect if constantly exposed to A. nectaris-induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization. eLife Sciences Publications, Ltd 2022-10-27 /pmc/articles/PMC9671501/ /pubmed/36300797 http://dx.doi.org/10.7554/eLife.79647 Text en © 2022, Chappell et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Ecology
Chappell, Callie R
Dhami, Manpreet K
Bitter, Mark C
Czech, Lucas
Herrera Paredes, Sur
Barrie, Fatoumata Binta
Calderón, Yadira
Eritano, Katherine
Golden, Lexi-Ann
Hekmat-Scafe, Daria
Hsu, Veronica
Kieschnick, Clara
Malladi, Shyamala
Rush, Nicole
Fukami, Tadashi
Wide-ranging consequences of priority effects governed by an overarching factor
title Wide-ranging consequences of priority effects governed by an overarching factor
title_full Wide-ranging consequences of priority effects governed by an overarching factor
title_fullStr Wide-ranging consequences of priority effects governed by an overarching factor
title_full_unstemmed Wide-ranging consequences of priority effects governed by an overarching factor
title_short Wide-ranging consequences of priority effects governed by an overarching factor
title_sort wide-ranging consequences of priority effects governed by an overarching factor
topic Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9671501/
https://www.ncbi.nlm.nih.gov/pubmed/36300797
http://dx.doi.org/10.7554/eLife.79647
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