Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)

Autores
Deanna, Rocío; Larter, Maximilien; Barboza, Gloria Estela; Smith, Stacey Dewitt
Año de publicación
2019
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The evolution of novel fruit morphologies has been integral to the success of angiosperms. The inflated fruiting calyx, in which the balloon-like calyx swells to completely surround the fruit, has evolved repeatedly across angiosperms and is postulated to aid in protection and dispersal. We investigated the evolution of this trait in the tomatillos and their allies (Physalideae, Solanaceae). METHODS: The Physalideae phylogeny was estimated using four regions (ITS, LEAFY, trnL-F, waxy) with maximum likelihood (ML) and Bayesian inference. Under the best-fitting ML model of trait evolution, we estimated ancestral states along with the numbers of gains and losses of fruiting calyx accrescence and inflation with Bayesian stochastic mapping. Also, phylogenetic signal in calyx morphology was examined with two metrics (parsimony score and Fritz and Purvis?s D).KEY RESULTS: Based on our well-resolved and densely sampled phylogeny, we infer that calyx evolution has proceeded in a stepwise and directional fashion, from non-accrescent to accrescent to inflated. In total, we inferred 24 gains of accrescence, 24 subsequent transitions to a fully inflated calyx, and only two reversals. Despite this lability, fruiting calyx accrescence and inflation showed strong phylogenetic signal. Our phylogeny greatly improves the resolution of Physalideae and highlights the need for taxonomic work. The comparative analyses reveal that the inflated fruiting calyx has evolved many times and that the trajectory toward this phenotype is generally stepwise and irreversible. These results provide a strong foundation for studying the genetic and developmental mechanisms responsible for the repeated origins of this charismatic fruit trait.
Fil: Deanna, Rocío. University of Colorado; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Farmacia; Argentina
Fil: Larter, Maximilien. University of Colorado; Estados Unidos
Fil: Barboza, Gloria Estela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Farmacia; Argentina
Fil: Smith, Stacey Dewitt. University of Colorado; Estados Unidos
Materia
CONVERGENCE
IRREVERSIBILITY
PHYSALOIDS
STOCHASTIC MAPPING
TRAIT EVOLUTION
TRANSITION RATES
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/109233

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network_name_str CONICET Digital (CONICET)
spelling Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)Deanna, RocíoLarter, MaximilienBarboza, Gloria EstelaSmith, Stacey DewittCONVERGENCEIRREVERSIBILITYPHYSALOIDSSTOCHASTIC MAPPINGTRAIT EVOLUTIONTRANSITION RATEShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The evolution of novel fruit morphologies has been integral to the success of angiosperms. The inflated fruiting calyx, in which the balloon-like calyx swells to completely surround the fruit, has evolved repeatedly across angiosperms and is postulated to aid in protection and dispersal. We investigated the evolution of this trait in the tomatillos and their allies (Physalideae, Solanaceae). METHODS: The Physalideae phylogeny was estimated using four regions (ITS, LEAFY, trnL-F, waxy) with maximum likelihood (ML) and Bayesian inference. Under the best-fitting ML model of trait evolution, we estimated ancestral states along with the numbers of gains and losses of fruiting calyx accrescence and inflation with Bayesian stochastic mapping. Also, phylogenetic signal in calyx morphology was examined with two metrics (parsimony score and Fritz and Purvis?s D).KEY RESULTS: Based on our well-resolved and densely sampled phylogeny, we infer that calyx evolution has proceeded in a stepwise and directional fashion, from non-accrescent to accrescent to inflated. In total, we inferred 24 gains of accrescence, 24 subsequent transitions to a fully inflated calyx, and only two reversals. Despite this lability, fruiting calyx accrescence and inflation showed strong phylogenetic signal. Our phylogeny greatly improves the resolution of Physalideae and highlights the need for taxonomic work. The comparative analyses reveal that the inflated fruiting calyx has evolved many times and that the trajectory toward this phenotype is generally stepwise and irreversible. These results provide a strong foundation for studying the genetic and developmental mechanisms responsible for the repeated origins of this charismatic fruit trait.Fil: Deanna, Rocío. University of Colorado; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Farmacia; ArgentinaFil: Larter, Maximilien. University of Colorado; Estados UnidosFil: Barboza, Gloria Estela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Farmacia; ArgentinaFil: Smith, Stacey Dewitt. University of Colorado; Estados UnidosBotanical Society of America2019-02info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/109233Deanna, Rocío; Larter, Maximilien; Barboza, Gloria Estela; Smith, Stacey Dewitt; Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae); Botanical Society of America; American Journal of Botany; 106; 2; 2-2019; 270-2790002-91221537-2197CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://bsapubs.onlinelibrary.wiley.com/doi/10.1002/ajb2.1242info:eu-repo/semantics/altIdentifier/doi/10.1002/ajb2.1242info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:21:09Zoai:ri.conicet.gov.ar:11336/109233instacron: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 10:21:09.308CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
title Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
spellingShingle Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
Deanna, Rocío
CONVERGENCE
IRREVERSIBILITY
PHYSALOIDS
STOCHASTIC MAPPING
TRAIT EVOLUTION
TRANSITION RATES
title_short Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
title_full Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
title_fullStr Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
title_full_unstemmed Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
title_sort Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae)
dc.creator.none.fl_str_mv Deanna, Rocío
Larter, Maximilien
Barboza, Gloria Estela
Smith, Stacey Dewitt
author Deanna, Rocío
author_facet Deanna, Rocío
Larter, Maximilien
Barboza, Gloria Estela
Smith, Stacey Dewitt
author_role author
author2 Larter, Maximilien
Barboza, Gloria Estela
Smith, Stacey Dewitt
author2_role author
author
author
dc.subject.none.fl_str_mv CONVERGENCE
IRREVERSIBILITY
PHYSALOIDS
STOCHASTIC MAPPING
TRAIT EVOLUTION
TRANSITION RATES
topic CONVERGENCE
IRREVERSIBILITY
PHYSALOIDS
STOCHASTIC MAPPING
TRAIT EVOLUTION
TRANSITION RATES
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The evolution of novel fruit morphologies has been integral to the success of angiosperms. The inflated fruiting calyx, in which the balloon-like calyx swells to completely surround the fruit, has evolved repeatedly across angiosperms and is postulated to aid in protection and dispersal. We investigated the evolution of this trait in the tomatillos and their allies (Physalideae, Solanaceae). METHODS: The Physalideae phylogeny was estimated using four regions (ITS, LEAFY, trnL-F, waxy) with maximum likelihood (ML) and Bayesian inference. Under the best-fitting ML model of trait evolution, we estimated ancestral states along with the numbers of gains and losses of fruiting calyx accrescence and inflation with Bayesian stochastic mapping. Also, phylogenetic signal in calyx morphology was examined with two metrics (parsimony score and Fritz and Purvis?s D).KEY RESULTS: Based on our well-resolved and densely sampled phylogeny, we infer that calyx evolution has proceeded in a stepwise and directional fashion, from non-accrescent to accrescent to inflated. In total, we inferred 24 gains of accrescence, 24 subsequent transitions to a fully inflated calyx, and only two reversals. Despite this lability, fruiting calyx accrescence and inflation showed strong phylogenetic signal. Our phylogeny greatly improves the resolution of Physalideae and highlights the need for taxonomic work. The comparative analyses reveal that the inflated fruiting calyx has evolved many times and that the trajectory toward this phenotype is generally stepwise and irreversible. These results provide a strong foundation for studying the genetic and developmental mechanisms responsible for the repeated origins of this charismatic fruit trait.
Fil: Deanna, Rocío. University of Colorado; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Farmacia; Argentina
Fil: Larter, Maximilien. University of Colorado; Estados Unidos
Fil: Barboza, Gloria Estela. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Córdoba. Instituto Multidisciplinario de Biología Vegetal. Universidad Nacional de Córdoba. Facultad de Ciencias Exactas Físicas y Naturales. Instituto Multidisciplinario de Biología Vegetal; Argentina. Universidad Nacional de Córdoba. Facultad de Ciencias Químicas. Departamento de Farmacia; Argentina
Fil: Smith, Stacey Dewitt. University of Colorado; Estados Unidos
description The evolution of novel fruit morphologies has been integral to the success of angiosperms. The inflated fruiting calyx, in which the balloon-like calyx swells to completely surround the fruit, has evolved repeatedly across angiosperms and is postulated to aid in protection and dispersal. We investigated the evolution of this trait in the tomatillos and their allies (Physalideae, Solanaceae). METHODS: The Physalideae phylogeny was estimated using four regions (ITS, LEAFY, trnL-F, waxy) with maximum likelihood (ML) and Bayesian inference. Under the best-fitting ML model of trait evolution, we estimated ancestral states along with the numbers of gains and losses of fruiting calyx accrescence and inflation with Bayesian stochastic mapping. Also, phylogenetic signal in calyx morphology was examined with two metrics (parsimony score and Fritz and Purvis?s D).KEY RESULTS: Based on our well-resolved and densely sampled phylogeny, we infer that calyx evolution has proceeded in a stepwise and directional fashion, from non-accrescent to accrescent to inflated. In total, we inferred 24 gains of accrescence, 24 subsequent transitions to a fully inflated calyx, and only two reversals. Despite this lability, fruiting calyx accrescence and inflation showed strong phylogenetic signal. Our phylogeny greatly improves the resolution of Physalideae and highlights the need for taxonomic work. The comparative analyses reveal that the inflated fruiting calyx has evolved many times and that the trajectory toward this phenotype is generally stepwise and irreversible. These results provide a strong foundation for studying the genetic and developmental mechanisms responsible for the repeated origins of this charismatic fruit trait.
publishDate 2019
dc.date.none.fl_str_mv 2019-02
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/11336/109233
Deanna, Rocío; Larter, Maximilien; Barboza, Gloria Estela; Smith, Stacey Dewitt; Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae); Botanical Society of America; American Journal of Botany; 106; 2; 2-2019; 270-279
0002-9122
1537-2197
CONICET Digital
CONICET
url http://hdl.handle.net/11336/109233
identifier_str_mv Deanna, Rocío; Larter, Maximilien; Barboza, Gloria Estela; Smith, Stacey Dewitt; Repeated evolution of a morphological novelty: A phylogenetic analysis of the inflated fruiting calyx in the Physalideae tribe (Solanaceae); Botanical Society of America; American Journal of Botany; 106; 2; 2-2019; 270-279
0002-9122
1537-2197
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://bsapubs.onlinelibrary.wiley.com/doi/10.1002/ajb2.1242
info:eu-repo/semantics/altIdentifier/doi/10.1002/ajb2.1242
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Botanical Society of America
publisher.none.fl_str_mv Botanical Society of America
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instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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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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