Cargando…

Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence

BACKGROUND: Nectar gain and loss are important flower transitions observed in angiosperms, and are particularly common in orchids. To understand such transitions, the availability of detailed anatomical data and species-level phylogenies are crucial. We investigated the evolution of food deception i...

Descripción completa

Detalles Bibliográficos
Autores principales: Cardoso-Gustavson, Poliana, Saka, Mariana Naomi, Pessoa, Edlley Max, Palma-Silva, Clarisse, Pinheiro, Fabio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6122447/
https://www.ncbi.nlm.nih.gov/pubmed/30180799
http://dx.doi.org/10.1186/s12870-018-1398-y
_version_ 1783352658149507072
author Cardoso-Gustavson, Poliana
Saka, Mariana Naomi
Pessoa, Edlley Max
Palma-Silva, Clarisse
Pinheiro, Fabio
author_facet Cardoso-Gustavson, Poliana
Saka, Mariana Naomi
Pessoa, Edlley Max
Palma-Silva, Clarisse
Pinheiro, Fabio
author_sort Cardoso-Gustavson, Poliana
collection PubMed
description BACKGROUND: Nectar gain and loss are important flower transitions observed in angiosperms, and are particularly common in orchids. To understand such transitions, the availability of detailed anatomical data and species-level phylogenies are crucial. We investigated the evolution of food deception in Epidendrum, one of the largest orchid genera, using genus phylogeny to map transitions between nectar gain and loss among different clades. Associations between anatomical and histochemical changes and nectar gain and loss were examined using fresh material available from 27 species. The evolution of nectar presence/absence in Epidendrum species was investigated in a phylogenetic framework of 47 species, using one nuclear and five plastid DNA regions available from GenBank and sequenced in this study. RESULTS: The presence or absence of nectar was strongly associated with changes in the inner epidermal tissues of nectaries. Nectar-secreting species have unornamented epidermal tissue, in contrast to the unicellular trichomes found on the epidermis of food deceptive species. Bayesian tests confirmed that transitions occurred preferentially from nectar presence to nectar absence across the Epidendrum phylogeny. In addition, independent nectar loss events were found across the phylogeny, suggesting a lack of constraint for these transitions. CONCLUSIONS: Ornamented nectaries may play an important role in the deceptive pollination strategy by secreting volatile organic compounds and providing tactile stimuli to pollinators. The recurrent and apparently irreversible pattern of nectar loss in Epidendrum suggests that food deception may constitute an alternative evolutionarily stable strategy, as observed in other orchid groups. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1398-y) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6122447
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-61224472018-09-05 Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence Cardoso-Gustavson, Poliana Saka, Mariana Naomi Pessoa, Edlley Max Palma-Silva, Clarisse Pinheiro, Fabio BMC Plant Biol Research Article BACKGROUND: Nectar gain and loss are important flower transitions observed in angiosperms, and are particularly common in orchids. To understand such transitions, the availability of detailed anatomical data and species-level phylogenies are crucial. We investigated the evolution of food deception in Epidendrum, one of the largest orchid genera, using genus phylogeny to map transitions between nectar gain and loss among different clades. Associations between anatomical and histochemical changes and nectar gain and loss were examined using fresh material available from 27 species. The evolution of nectar presence/absence in Epidendrum species was investigated in a phylogenetic framework of 47 species, using one nuclear and five plastid DNA regions available from GenBank and sequenced in this study. RESULTS: The presence or absence of nectar was strongly associated with changes in the inner epidermal tissues of nectaries. Nectar-secreting species have unornamented epidermal tissue, in contrast to the unicellular trichomes found on the epidermis of food deceptive species. Bayesian tests confirmed that transitions occurred preferentially from nectar presence to nectar absence across the Epidendrum phylogeny. In addition, independent nectar loss events were found across the phylogeny, suggesting a lack of constraint for these transitions. CONCLUSIONS: Ornamented nectaries may play an important role in the deceptive pollination strategy by secreting volatile organic compounds and providing tactile stimuli to pollinators. The recurrent and apparently irreversible pattern of nectar loss in Epidendrum suggests that food deception may constitute an alternative evolutionarily stable strategy, as observed in other orchid groups. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1398-y) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-04 /pmc/articles/PMC6122447/ /pubmed/30180799 http://dx.doi.org/10.1186/s12870-018-1398-y Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Cardoso-Gustavson, Poliana
Saka, Mariana Naomi
Pessoa, Edlley Max
Palma-Silva, Clarisse
Pinheiro, Fabio
Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence
title Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence
title_full Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence
title_fullStr Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence
title_full_unstemmed Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence
title_short Unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in Epidendrum (Orchidaceae): insights from anatomical and molecular evidence
title_sort unidirectional transitions in nectar gain and loss suggest food deception is a stable evolutionary strategy in epidendrum (orchidaceae): insights from anatomical and molecular evidence
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6122447/
https://www.ncbi.nlm.nih.gov/pubmed/30180799
http://dx.doi.org/10.1186/s12870-018-1398-y
work_keys_str_mv AT cardosogustavsonpoliana unidirectionaltransitionsinnectargainandlosssuggestfooddeceptionisastableevolutionarystrategyinepidendrumorchidaceaeinsightsfromanatomicalandmolecularevidence
AT sakamariananaomi unidirectionaltransitionsinnectargainandlosssuggestfooddeceptionisastableevolutionarystrategyinepidendrumorchidaceaeinsightsfromanatomicalandmolecularevidence
AT pessoaedlleymax unidirectionaltransitionsinnectargainandlosssuggestfooddeceptionisastableevolutionarystrategyinepidendrumorchidaceaeinsightsfromanatomicalandmolecularevidence
AT palmasilvaclarisse unidirectionaltransitionsinnectargainandlosssuggestfooddeceptionisastableevolutionarystrategyinepidendrumorchidaceaeinsightsfromanatomicalandmolecularevidence
AT pinheirofabio unidirectionaltransitionsinnectargainandlosssuggestfooddeceptionisastableevolutionarystrategyinepidendrumorchidaceaeinsightsfromanatomicalandmolecularevidence