Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence

Autores
Gundel, Pedro Emilio; Ueno, Andrea C.; Casas, Cecilia; Miller, Tom E. X.; Pérez, Luis; Cuyeu, Alba Romina; Omacini, Marina
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Symbiotic associations play a role in plant ecology and evolution, but the outcome of the interaction depends on the life-history traits of the partners and the environmental context. Although symbiosis with vertically transmitted microorganisms should result in mutualism, it is not clear how the transmission process aligns with the outcome of the context-dependent symbiosis. For 3 years, we sampled individuals of an annual plant species that forms symbiosis with a vertically transmitted fungal endophyte, in paired stands of two contrasting vegetation communities (humid mesophytic meadows [HMM]: productive/low stress, and humid prairies [HP]: less productive/high stress). We estimated the prevalence of symbiosis at the population level, and the fitness of the plant, the symbiotic status and vertical transmission efficiency at the individual level. Over 3 years, the prevalence of symbiosis was ≈100% in HMM and ≈75% in HP. Plant fitness was very low and high in years with precipitation below and above the yearly mean, respectively. The higher fitness of endophyte-symbiotic plants was evident in the HMM and high precipitation years. Vertical transmission of endophytes was higher in HMM (≈96%) compared to HP (≈93%) and was not related to plant fitness. Despite transmission inefficiencies in HP, changes in prevalence within the growing season (from seeds to the final plant stand) suggest a fitness advantage for symbiotic plants. Vertical transmission is expected to promote mutualism as it aligns partners' fitness. Although symbiotic plants showed higher fitness and the probability of transmission failures was higher among low-fitness plants, the variation in transmission efficiency between plants and vegetation communities was not related to the fitness of the individual host. Our study provides evidence that context-dependent vertical transmission efficiency and endophyte-mediated fitness advantages interact complexly to determine the prevalence of symbiosis in populations that occur in contrasting vegetation communities.
Instituto de Genética
Fil: Gundel, Pedro E. Universidad de Talca. Instituto de Ciencias Biológicas. Centro de Ecología Integrativa; Chile
Fil: Gundel, Pedro E. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Gundel, Pedro E. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ueno, Andrea C. Universidad de Talca. Instituto de Ciencias Biológicas. Centro de Ecología Integrativa; Chile
Fil: Ueno, Andrea C. Universidad de Talca. Instituto de Investigación Interdisciplinaria; Chile
Fil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Casas, Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Recursos Naturales y Ambiente. Cátedra de Edafología; Argentina
Fil: Miller, Tom E. X. Rice University. Program in Ecology and Evolutionary Biology. Department of BioSciences; Estados Unidos
Fil: Pérez, Luis. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Pérez, Luis. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Cuyeu, Alba Romina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina
Fil: Omacini, Marina. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fuente
Functional Ecology 38 (12) : 2610-2622 (Diciembre 2024)
Materia
Annuals
Epichloe
Endophytes
Lolium multiflorum
Mutualism
Plant Population
Biological Interaction
Symbionts
Symbiosis
Plantas Anuales
Endofitas
Mutualismo
Población Vegetal
Interacción Biológica
Simbiontico
Simbiosis
Epichloë occultans
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
oai:localhost:20.500.12123/21996
Acceder
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oai_identifier_str oai:localhost:20.500.12123/21996
network_acronym_str INTADig
repository_id_str l
network_name_str INTA Digital (INTA)
spelling Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalenceGundel, Pedro EmilioUeno, Andrea C.Casas, CeciliaMiller, Tom E. X.Pérez, LuisCuyeu, Alba RominaOmacini, MarinaAnnualsEpichloeEndophytesLolium multiflorumMutualismPlant PopulationBiological InteractionSymbiontsSymbiosisPlantas AnualesEndofitasMutualismoPoblación VegetalInteracción BiológicaSimbionticoSimbiosisEpichloë occultansSymbiotic associations play a role in plant ecology and evolution, but the outcome of the interaction depends on the life-history traits of the partners and the environmental context. Although symbiosis with vertically transmitted microorganisms should result in mutualism, it is not clear how the transmission process aligns with the outcome of the context-dependent symbiosis. For 3 years, we sampled individuals of an annual plant species that forms symbiosis with a vertically transmitted fungal endophyte, in paired stands of two contrasting vegetation communities (humid mesophytic meadows [HMM]: productive/low stress, and humid prairies [HP]: less productive/high stress). We estimated the prevalence of symbiosis at the population level, and the fitness of the plant, the symbiotic status and vertical transmission efficiency at the individual level. Over 3 years, the prevalence of symbiosis was ≈100% in HMM and ≈75% in HP. Plant fitness was very low and high in years with precipitation below and above the yearly mean, respectively. The higher fitness of endophyte-symbiotic plants was evident in the HMM and high precipitation years. Vertical transmission of endophytes was higher in HMM (≈96%) compared to HP (≈93%) and was not related to plant fitness. Despite transmission inefficiencies in HP, changes in prevalence within the growing season (from seeds to the final plant stand) suggest a fitness advantage for symbiotic plants. Vertical transmission is expected to promote mutualism as it aligns partners' fitness. Although symbiotic plants showed higher fitness and the probability of transmission failures was higher among low-fitness plants, the variation in transmission efficiency between plants and vegetation communities was not related to the fitness of the individual host. Our study provides evidence that context-dependent vertical transmission efficiency and endophyte-mediated fitness advantages interact complexly to determine the prevalence of symbiosis in populations that occur in contrasting vegetation communities.Instituto de GenéticaFil: Gundel, Pedro E. Universidad de Talca. Instituto de Ciencias Biológicas. Centro de Ecología Integrativa; ChileFil: Gundel, Pedro E. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; ArgentinaFil: Gundel, Pedro E. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Ueno, Andrea C. Universidad de Talca. Instituto de Ciencias Biológicas. Centro de Ecología Integrativa; ChileFil: Ueno, Andrea C. Universidad de Talca. Instituto de Investigación Interdisciplinaria; ChileFil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; ArgentinaFil: Casas, Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Recursos Naturales y Ambiente. Cátedra de Edafología; ArgentinaFil: Miller, Tom E. X. Rice University. Program in Ecology and Evolutionary Biology. Department of BioSciences; Estados UnidosFil: Pérez, Luis. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; ArgentinaFil: Pérez, Luis. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Cuyeu, Alba Romina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; ArgentinaFil: Omacini, Marina. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; ArgentinaFil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaWiley2025-04-23T09:49:38Z2025-04-23T09:49:38Z2024-12info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/21996https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2435.146811365-2435https://doi.org/10.1111/1365-2435.14681Functional Ecology 38 (12) : 2610-2622 (Diciembre 2024)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)2025-09-11T10:25:41Zoai:localhost:20.500.12123/21996instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-11 10:25:42.19INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
title Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
spellingShingle Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
Gundel, Pedro Emilio
Annuals
Epichloe
Endophytes
Lolium multiflorum
Mutualism
Plant Population
Biological Interaction
Symbionts
Symbiosis
Plantas Anuales
Endofitas
Mutualismo
Población Vegetal
Interacción Biológica
Simbiontico
Simbiosis
Epichloë occultans
title_short Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
title_full Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
title_fullStr Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
title_full_unstemmed Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
title_sort Temporal host–symbiont dynamics in community contexts : Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence
dc.creator.none.fl_str_mv Gundel, Pedro Emilio
Ueno, Andrea C.
Casas, Cecilia
Miller, Tom E. X.
Pérez, Luis
Cuyeu, Alba Romina
Omacini, Marina
author Gundel, Pedro Emilio
author_facet Gundel, Pedro Emilio
Ueno, Andrea C.
Casas, Cecilia
Miller, Tom E. X.
Pérez, Luis
Cuyeu, Alba Romina
Omacini, Marina
author_role author
author2 Ueno, Andrea C.
Casas, Cecilia
Miller, Tom E. X.
Pérez, Luis
Cuyeu, Alba Romina
Omacini, Marina
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Annuals
Epichloe
Endophytes
Lolium multiflorum
Mutualism
Plant Population
Biological Interaction
Symbionts
Symbiosis
Plantas Anuales
Endofitas
Mutualismo
Población Vegetal
Interacción Biológica
Simbiontico
Simbiosis
Epichloë occultans
topic Annuals
Epichloe
Endophytes
Lolium multiflorum
Mutualism
Plant Population
Biological Interaction
Symbionts
Symbiosis
Plantas Anuales
Endofitas
Mutualismo
Población Vegetal
Interacción Biológica
Simbiontico
Simbiosis
Epichloë occultans
dc.description.none.fl_txt_mv Symbiotic associations play a role in plant ecology and evolution, but the outcome of the interaction depends on the life-history traits of the partners and the environmental context. Although symbiosis with vertically transmitted microorganisms should result in mutualism, it is not clear how the transmission process aligns with the outcome of the context-dependent symbiosis. For 3 years, we sampled individuals of an annual plant species that forms symbiosis with a vertically transmitted fungal endophyte, in paired stands of two contrasting vegetation communities (humid mesophytic meadows [HMM]: productive/low stress, and humid prairies [HP]: less productive/high stress). We estimated the prevalence of symbiosis at the population level, and the fitness of the plant, the symbiotic status and vertical transmission efficiency at the individual level. Over 3 years, the prevalence of symbiosis was ≈100% in HMM and ≈75% in HP. Plant fitness was very low and high in years with precipitation below and above the yearly mean, respectively. The higher fitness of endophyte-symbiotic plants was evident in the HMM and high precipitation years. Vertical transmission of endophytes was higher in HMM (≈96%) compared to HP (≈93%) and was not related to plant fitness. Despite transmission inefficiencies in HP, changes in prevalence within the growing season (from seeds to the final plant stand) suggest a fitness advantage for symbiotic plants. Vertical transmission is expected to promote mutualism as it aligns partners' fitness. Although symbiotic plants showed higher fitness and the probability of transmission failures was higher among low-fitness plants, the variation in transmission efficiency between plants and vegetation communities was not related to the fitness of the individual host. Our study provides evidence that context-dependent vertical transmission efficiency and endophyte-mediated fitness advantages interact complexly to determine the prevalence of symbiosis in populations that occur in contrasting vegetation communities.
Instituto de Genética
Fil: Gundel, Pedro E. Universidad de Talca. Instituto de Ciencias Biológicas. Centro de Ecología Integrativa; Chile
Fil: Gundel, Pedro E. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Gundel, Pedro E. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ueno, Andrea C. Universidad de Talca. Instituto de Ciencias Biológicas. Centro de Ecología Integrativa; Chile
Fil: Ueno, Andrea C. Universidad de Talca. Instituto de Investigación Interdisciplinaria; Chile
Fil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Casas, Cecilia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Recursos Naturales y Ambiente. Cátedra de Edafología; Argentina
Fil: Miller, Tom E. X. Rice University. Program in Ecology and Evolutionary Biology. Department of BioSciences; Estados Unidos
Fil: Pérez, Luis. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Pérez, Luis. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Cuyeu, Alba Romina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Genética; Argentina
Fil: Omacini, Marina. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Departamento de Recursos Naturales y Ambiente. Cátedra de Ecología; Argentina
Fil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Symbiotic associations play a role in plant ecology and evolution, but the outcome of the interaction depends on the life-history traits of the partners and the environmental context. Although symbiosis with vertically transmitted microorganisms should result in mutualism, it is not clear how the transmission process aligns with the outcome of the context-dependent symbiosis. For 3 years, we sampled individuals of an annual plant species that forms symbiosis with a vertically transmitted fungal endophyte, in paired stands of two contrasting vegetation communities (humid mesophytic meadows [HMM]: productive/low stress, and humid prairies [HP]: less productive/high stress). We estimated the prevalence of symbiosis at the population level, and the fitness of the plant, the symbiotic status and vertical transmission efficiency at the individual level. Over 3 years, the prevalence of symbiosis was ≈100% in HMM and ≈75% in HP. Plant fitness was very low and high in years with precipitation below and above the yearly mean, respectively. The higher fitness of endophyte-symbiotic plants was evident in the HMM and high precipitation years. Vertical transmission of endophytes was higher in HMM (≈96%) compared to HP (≈93%) and was not related to plant fitness. Despite transmission inefficiencies in HP, changes in prevalence within the growing season (from seeds to the final plant stand) suggest a fitness advantage for symbiotic plants. Vertical transmission is expected to promote mutualism as it aligns partners' fitness. Although symbiotic plants showed higher fitness and the probability of transmission failures was higher among low-fitness plants, the variation in transmission efficiency between plants and vegetation communities was not related to the fitness of the individual host. Our study provides evidence that context-dependent vertical transmission efficiency and endophyte-mediated fitness advantages interact complexly to determine the prevalence of symbiosis in populations that occur in contrasting vegetation communities.
publishDate 2024
dc.date.none.fl_str_mv 2024-12
2025-04-23T09:49:38Z
2025-04-23T09:49:38Z
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/21996
https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2435.14681
1365-2435
https://doi.org/10.1111/1365-2435.14681
url http://hdl.handle.net/20.500.12123/21996
https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2435.14681
https://doi.org/10.1111/1365-2435.14681
identifier_str_mv 1365-2435
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Wiley
publisher.none.fl_str_mv Wiley
dc.source.none.fl_str_mv Functional Ecology 38 (12) : 2610-2622 (Diciembre 2024)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
collection INTA Digital (INTA)
instname_str Instituto Nacional de Tecnología Agropecuaria
repository.name.fl_str_mv INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria
repository.mail.fl_str_mv tripaldi.nicolas@inta.gob.ar
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