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

Autores
Gundel, Pedro Emilio; Ueno, Andrea Celeste; Casas, Cecilia; Miller, Tom E. X.; Perez, Luis Ignacio; Cuyeu, 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.
Fil: Gundel, Pedro Emilio. Universidad de Talca; Chile. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Ueno, Andrea Celeste. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Universidad de Talca; Chile
Fil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Recursos Naturales y Ambiente. Cátedra de Edafología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Miller, Tom E. X.. Rice University; Estados Unidos
Fil: Perez, Luis Ignacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Cuyeu, Romina. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación En Ciencias Veterinarias y Agronómicas. Instituto de Agrobiotecnología y Biología Molecular. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Agrobiotecnología y Biología Molecular; Argentina
Fil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Materia
ANNUAL PLANTS
EPICHLOE OCCULTANS
FUNGAL ENDOPHYTES
INCIDENCE OF SYMBIOSYS
LOLIUM MULTIFLORUM
MUTUALISM
PLANT POPULATION AND COMMUNITY DYNAMICS
PLANT-MICROORGANISM INTERACTION
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/265315
Acceder
id CONICETDig_9ee4a17760e8e849aa0d994953f5530b
oai_identifier_str oai:ri.conicet.gov.ar:11336/265315
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Temporal host–symbiont dynamics in community contexts: Impacts of host fitness and vertical transmission efficiency on symbiosis prevalenceGundel, Pedro EmilioUeno, Andrea CelesteCasas, CeciliaMiller, Tom E. X.Perez, Luis IgnacioCuyeu, RominaOmacini, MarinaANNUAL PLANTSEPICHLOE OCCULTANSFUNGAL ENDOPHYTESINCIDENCE OF SYMBIOSYSLOLIUM MULTIFLORUMMUTUALISMPLANT POPULATION AND COMMUNITY DYNAMICSPLANT-MICROORGANISM INTERACTIONhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Symbiotic 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.Fil: Gundel, Pedro Emilio. Universidad de Talca; Chile. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Ueno, Andrea Celeste. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Universidad de Talca; ChileFil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Recursos Naturales y Ambiente. Cátedra de Edafología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Miller, Tom E. X.. Rice University; Estados UnidosFil: Perez, Luis Ignacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Cuyeu, Romina. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación En Ciencias Veterinarias y Agronómicas. Instituto de Agrobiotecnología y Biología Molecular. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Agrobiotecnología y Biología Molecular; ArgentinaFil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaWiley Blackwell Publishing, Inc2024-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/265315Gundel, Pedro Emilio; Ueno, Andrea Celeste; Casas, Cecilia; Miller, Tom E. X.; Perez, Luis Ignacio; et al.; Temporal host–symbiont dynamics in community contexts: Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence; Wiley Blackwell Publishing, Inc; Functional Ecology; 38; 12; 10-2024; 2610-26220269-8463CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2435.14681info:eu-repo/semantics/altIdentifier/doi/10.1111/1365-2435.14681info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:48:57Zoai:ri.conicet.gov.ar:11336/265315instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 09:48:58.023CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
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
ANNUAL PLANTS
EPICHLOE OCCULTANS
FUNGAL ENDOPHYTES
INCIDENCE OF SYMBIOSYS
LOLIUM MULTIFLORUM
MUTUALISM
PLANT POPULATION AND COMMUNITY DYNAMICS
PLANT-MICROORGANISM INTERACTION
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 Celeste
Casas, Cecilia
Miller, Tom E. X.
Perez, Luis Ignacio
Cuyeu, Romina
Omacini, Marina
author Gundel, Pedro Emilio
author_facet Gundel, Pedro Emilio
Ueno, Andrea Celeste
Casas, Cecilia
Miller, Tom E. X.
Perez, Luis Ignacio
Cuyeu, Romina
Omacini, Marina
author_role author
author2 Ueno, Andrea Celeste
Casas, Cecilia
Miller, Tom E. X.
Perez, Luis Ignacio
Cuyeu, Romina
Omacini, Marina
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv ANNUAL PLANTS
EPICHLOE OCCULTANS
FUNGAL ENDOPHYTES
INCIDENCE OF SYMBIOSYS
LOLIUM MULTIFLORUM
MUTUALISM
PLANT POPULATION AND COMMUNITY DYNAMICS
PLANT-MICROORGANISM INTERACTION
topic ANNUAL PLANTS
EPICHLOE OCCULTANS
FUNGAL ENDOPHYTES
INCIDENCE OF SYMBIOSYS
LOLIUM MULTIFLORUM
MUTUALISM
PLANT POPULATION AND COMMUNITY DYNAMICS
PLANT-MICROORGANISM INTERACTION
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
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.
Fil: Gundel, Pedro Emilio. Universidad de Talca; Chile. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Ueno, Andrea Celeste. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Universidad de Talca; Chile
Fil: Casas, Cecilia. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Recursos Naturales y Ambiente. Cátedra de Edafología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Miller, Tom E. X.. Rice University; Estados Unidos
Fil: Perez, Luis Ignacio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina
Fil: Cuyeu, Romina. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación En Ciencias Veterinarias y Agronómicas. Instituto de Agrobiotecnología y Biología Molecular. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Agrobiotecnología y Biología Molecular; Argentina
Fil: Omacini, Marina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; 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 2024-10
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/11336/265315
Gundel, Pedro Emilio; Ueno, Andrea Celeste; Casas, Cecilia; Miller, Tom E. X.; Perez, Luis Ignacio; et al.; Temporal host–symbiont dynamics in community contexts: Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence; Wiley Blackwell Publishing, Inc; Functional Ecology; 38; 12; 10-2024; 2610-2622
0269-8463
CONICET Digital
CONICET
url http://hdl.handle.net/11336/265315
identifier_str_mv Gundel, Pedro Emilio; Ueno, Andrea Celeste; Casas, Cecilia; Miller, Tom E. X.; Perez, Luis Ignacio; et al.; Temporal host–symbiont dynamics in community contexts: Impacts of host fitness and vertical transmission efficiency on symbiosis prevalence; Wiley Blackwell Publishing, Inc; Functional Ecology; 38; 12; 10-2024; 2610-2622
0269-8463
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://besjournals.onlinelibrary.wiley.com/doi/10.1111/1365-2435.14681
info:eu-repo/semantics/altIdentifier/doi/10.1111/1365-2435.14681
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
publisher.none.fl_str_mv Wiley Blackwell Publishing, Inc
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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