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The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study

BACKGROUND AND AIMS: Large clades of angiosperms are often characterized by diverse interactions with pollinators, but how these pollination systems are structured phylogenetically and biogeographically is still uncertain for most families. Apocynaceae is a clade of >5300 species with a worldwide...

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Autores principales: Ollerton, Jeff, Liede-Schumann, Sigrid, Endress, Mary E, Meve, Ulrich, Rech, André Rodrigo, Shuttleworth, Adam, Keller, Héctor A, Fishbein, Mark, Alvarado-Cárdenas, Leonardo O, Amorim, Felipe W, Bernhardt, Peter, Celep, Ferhat, Chirango, Yolanda, Chiriboga-Arroyo, Fidel, Civeyrel, Laure, Cocucci, Andrea, Cranmer, Louise, da Silva-Batista, Inara Carolina, de Jager, Linde, Deprá, Mariana Scaramussa, Domingos-Melo, Arthur, Dvorsky, Courtney, Agostini, Kayna, Freitas, Leandro, Gaglianone, Maria Cristina, Galetto, Leo, Gilbert, Mike, González-Ramírez, Ixchel, Gorostiague, Pablo, Goyder, David, Hachuy-Filho, Leandro, Heiduk, Annemarie, Howard, Aaron, Ionta, Gretchen, Islas-Hernández, Sofia C, Johnson, Steven D, Joubert, Lize, Kaiser-Bunbury, Christopher N, Kephart, Susan, Kidyoo, Aroonrat, Koptur, Suzanne, Koschnitzke, Cristiana, Lamborn, Ellen, Livshultz, Tatyana, Machado, Isabel Cristina, Marino, Salvador, Mema, Lumi, Mochizuki, Ko, Morellato, Leonor Patrícia Cerdeira, Mrisha, Chediel K, Muiruri, Evalyne W, Nakahama, Naoyuki, Nascimento, Viviany Teixeira, Nuttman, Clive, Oliveira, Paulo Eugenio, Peter, Craig I, Punekar, Sachin, Rafferty, Nicole, Rapini, Alessandro, Ren, Zong-Xin, Rodríguez-Flores, Claudia I, Rosero, Liliana, Sakai, Shoko, Sazima, Marlies, Steenhuisen, Sandy-Lynn, Tan, Ching-Wen, Torres, Carolina, Trøjelsgaard, Kristian, Ushimaru, Atushi, Vieira, Milene Faria, Wiemer, Ana Pía, Yamashiro, Tadashi, Nadia, Tarcila, Queiroz, Joel, Quirino, Zelma
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6344220/
https://www.ncbi.nlm.nih.gov/pubmed/30099492
http://dx.doi.org/10.1093/aob/mcy127
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author Ollerton, Jeff
Liede-Schumann, Sigrid
Endress, Mary E
Meve, Ulrich
Rech, André Rodrigo
Shuttleworth, Adam
Keller, Héctor A
Fishbein, Mark
Alvarado-Cárdenas, Leonardo O
Amorim, Felipe W
Bernhardt, Peter
Celep, Ferhat
Chirango, Yolanda
Chiriboga-Arroyo, Fidel
Civeyrel, Laure
Cocucci, Andrea
Cranmer, Louise
da Silva-Batista, Inara Carolina
de Jager, Linde
Deprá, Mariana Scaramussa
Domingos-Melo, Arthur
Dvorsky, Courtney
Agostini, Kayna
Freitas, Leandro
Gaglianone, Maria Cristina
Galetto, Leo
Gilbert, Mike
González-Ramírez, Ixchel
Gorostiague, Pablo
Goyder, David
Hachuy-Filho, Leandro
Heiduk, Annemarie
Howard, Aaron
Ionta, Gretchen
Islas-Hernández, Sofia C
Johnson, Steven D
Joubert, Lize
Kaiser-Bunbury, Christopher N
Kephart, Susan
Kidyoo, Aroonrat
Koptur, Suzanne
Koschnitzke, Cristiana
Lamborn, Ellen
Livshultz, Tatyana
Machado, Isabel Cristina
Marino, Salvador
Mema, Lumi
Mochizuki, Ko
Morellato, Leonor Patrícia Cerdeira
Mrisha, Chediel K
Muiruri, Evalyne W
Nakahama, Naoyuki
Nascimento, Viviany Teixeira
Nuttman, Clive
Oliveira, Paulo Eugenio
Peter, Craig I
Punekar, Sachin
Rafferty, Nicole
Rapini, Alessandro
Ren, Zong-Xin
Rodríguez-Flores, Claudia I
Rosero, Liliana
Sakai, Shoko
Sazima, Marlies
Steenhuisen, Sandy-Lynn
Tan, Ching-Wen
Torres, Carolina
Trøjelsgaard, Kristian
Ushimaru, Atushi
Vieira, Milene Faria
Wiemer, Ana Pía
Yamashiro, Tadashi
Nadia, Tarcila
Queiroz, Joel
Quirino, Zelma
author_facet Ollerton, Jeff
Liede-Schumann, Sigrid
Endress, Mary E
Meve, Ulrich
Rech, André Rodrigo
Shuttleworth, Adam
Keller, Héctor A
Fishbein, Mark
Alvarado-Cárdenas, Leonardo O
Amorim, Felipe W
Bernhardt, Peter
Celep, Ferhat
Chirango, Yolanda
Chiriboga-Arroyo, Fidel
Civeyrel, Laure
Cocucci, Andrea
Cranmer, Louise
da Silva-Batista, Inara Carolina
de Jager, Linde
Deprá, Mariana Scaramussa
Domingos-Melo, Arthur
Dvorsky, Courtney
Agostini, Kayna
Freitas, Leandro
Gaglianone, Maria Cristina
Galetto, Leo
Gilbert, Mike
González-Ramírez, Ixchel
Gorostiague, Pablo
Goyder, David
Hachuy-Filho, Leandro
Heiduk, Annemarie
Howard, Aaron
Ionta, Gretchen
Islas-Hernández, Sofia C
Johnson, Steven D
Joubert, Lize
Kaiser-Bunbury, Christopher N
Kephart, Susan
Kidyoo, Aroonrat
Koptur, Suzanne
Koschnitzke, Cristiana
Lamborn, Ellen
Livshultz, Tatyana
Machado, Isabel Cristina
Marino, Salvador
Mema, Lumi
Mochizuki, Ko
Morellato, Leonor Patrícia Cerdeira
Mrisha, Chediel K
Muiruri, Evalyne W
Nakahama, Naoyuki
Nascimento, Viviany Teixeira
Nuttman, Clive
Oliveira, Paulo Eugenio
Peter, Craig I
Punekar, Sachin
Rafferty, Nicole
Rapini, Alessandro
Ren, Zong-Xin
Rodríguez-Flores, Claudia I
Rosero, Liliana
Sakai, Shoko
Sazima, Marlies
Steenhuisen, Sandy-Lynn
Tan, Ching-Wen
Torres, Carolina
Trøjelsgaard, Kristian
Ushimaru, Atushi
Vieira, Milene Faria
Wiemer, Ana Pía
Yamashiro, Tadashi
Nadia, Tarcila
Queiroz, Joel
Quirino, Zelma
author_sort Ollerton, Jeff
collection PubMed
description BACKGROUND AND AIMS: Large clades of angiosperms are often characterized by diverse interactions with pollinators, but how these pollination systems are structured phylogenetically and biogeographically is still uncertain for most families. Apocynaceae is a clade of >5300 species with a worldwide distribution. A database representing >10 % of species in the family was used to explore the diversity of pollinators and evolutionary shifts in pollination systems across major clades and regions. METHODS: The database was compiled from published and unpublished reports. Plants were categorized into broad pollination systems and then subdivided to include bimodal systems. These were mapped against the five major divisions of the family, and against the smaller clades. Finally, pollination systems were mapped onto a phylogenetic reconstruction that included those species for which sequence data are available, and transition rates between pollination systems were calculated. KEY RESULTS: Most Apocynaceae are insect pollinated with few records of bird pollination. Almost three-quarters of species are pollinated by a single higher taxon (e.g. flies or moths); 7 % have bimodal pollination systems, whilst the remaining approx. 20 % are insect generalists. The less phenotypically specialized flowers of the Rauvolfioids are pollinated by a more restricted set of pollinators than are more complex flowers within the Apocynoids + Periplocoideae + Secamonoideae + Asclepiadoideae (APSA) clade. Certain combinations of bimodal pollination systems are more common than others. Some pollination systems are missing from particular regions, whilst others are over-represented. CONCLUSIONS: Within Apocynaceae, interactions with pollinators are highly structured both phylogenetically and biogeographically. Variation in transition rates between pollination systems suggest constraints on their evolution, whereas regional differences point to environmental effects such as filtering of certain pollinators from habitats. This is the most extensive analysis of its type so far attempted and gives important insights into the diversity and evolution of pollination systems in large clades.
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spelling pubmed-63442202019-01-29 The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study Ollerton, Jeff Liede-Schumann, Sigrid Endress, Mary E Meve, Ulrich Rech, André Rodrigo Shuttleworth, Adam Keller, Héctor A Fishbein, Mark Alvarado-Cárdenas, Leonardo O Amorim, Felipe W Bernhardt, Peter Celep, Ferhat Chirango, Yolanda Chiriboga-Arroyo, Fidel Civeyrel, Laure Cocucci, Andrea Cranmer, Louise da Silva-Batista, Inara Carolina de Jager, Linde Deprá, Mariana Scaramussa Domingos-Melo, Arthur Dvorsky, Courtney Agostini, Kayna Freitas, Leandro Gaglianone, Maria Cristina Galetto, Leo Gilbert, Mike González-Ramírez, Ixchel Gorostiague, Pablo Goyder, David Hachuy-Filho, Leandro Heiduk, Annemarie Howard, Aaron Ionta, Gretchen Islas-Hernández, Sofia C Johnson, Steven D Joubert, Lize Kaiser-Bunbury, Christopher N Kephart, Susan Kidyoo, Aroonrat Koptur, Suzanne Koschnitzke, Cristiana Lamborn, Ellen Livshultz, Tatyana Machado, Isabel Cristina Marino, Salvador Mema, Lumi Mochizuki, Ko Morellato, Leonor Patrícia Cerdeira Mrisha, Chediel K Muiruri, Evalyne W Nakahama, Naoyuki Nascimento, Viviany Teixeira Nuttman, Clive Oliveira, Paulo Eugenio Peter, Craig I Punekar, Sachin Rafferty, Nicole Rapini, Alessandro Ren, Zong-Xin Rodríguez-Flores, Claudia I Rosero, Liliana Sakai, Shoko Sazima, Marlies Steenhuisen, Sandy-Lynn Tan, Ching-Wen Torres, Carolina Trøjelsgaard, Kristian Ushimaru, Atushi Vieira, Milene Faria Wiemer, Ana Pía Yamashiro, Tadashi Nadia, Tarcila Queiroz, Joel Quirino, Zelma Ann Bot Original Articles BACKGROUND AND AIMS: Large clades of angiosperms are often characterized by diverse interactions with pollinators, but how these pollination systems are structured phylogenetically and biogeographically is still uncertain for most families. Apocynaceae is a clade of >5300 species with a worldwide distribution. A database representing >10 % of species in the family was used to explore the diversity of pollinators and evolutionary shifts in pollination systems across major clades and regions. METHODS: The database was compiled from published and unpublished reports. Plants were categorized into broad pollination systems and then subdivided to include bimodal systems. These were mapped against the five major divisions of the family, and against the smaller clades. Finally, pollination systems were mapped onto a phylogenetic reconstruction that included those species for which sequence data are available, and transition rates between pollination systems were calculated. KEY RESULTS: Most Apocynaceae are insect pollinated with few records of bird pollination. Almost three-quarters of species are pollinated by a single higher taxon (e.g. flies or moths); 7 % have bimodal pollination systems, whilst the remaining approx. 20 % are insect generalists. The less phenotypically specialized flowers of the Rauvolfioids are pollinated by a more restricted set of pollinators than are more complex flowers within the Apocynoids + Periplocoideae + Secamonoideae + Asclepiadoideae (APSA) clade. Certain combinations of bimodal pollination systems are more common than others. Some pollination systems are missing from particular regions, whilst others are over-represented. CONCLUSIONS: Within Apocynaceae, interactions with pollinators are highly structured both phylogenetically and biogeographically. Variation in transition rates between pollination systems suggest constraints on their evolution, whereas regional differences point to environmental effects such as filtering of certain pollinators from habitats. This is the most extensive analysis of its type so far attempted and gives important insights into the diversity and evolution of pollination systems in large clades. Oxford University Press 2019-01 2018-08-07 /pmc/articles/PMC6344220/ /pubmed/30099492 http://dx.doi.org/10.1093/aob/mcy127 Text en © The Author(s) 2018. Published by Oxford University Press on behalf of the Annals of Botany Company. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Ollerton, Jeff
Liede-Schumann, Sigrid
Endress, Mary E
Meve, Ulrich
Rech, André Rodrigo
Shuttleworth, Adam
Keller, Héctor A
Fishbein, Mark
Alvarado-Cárdenas, Leonardo O
Amorim, Felipe W
Bernhardt, Peter
Celep, Ferhat
Chirango, Yolanda
Chiriboga-Arroyo, Fidel
Civeyrel, Laure
Cocucci, Andrea
Cranmer, Louise
da Silva-Batista, Inara Carolina
de Jager, Linde
Deprá, Mariana Scaramussa
Domingos-Melo, Arthur
Dvorsky, Courtney
Agostini, Kayna
Freitas, Leandro
Gaglianone, Maria Cristina
Galetto, Leo
Gilbert, Mike
González-Ramírez, Ixchel
Gorostiague, Pablo
Goyder, David
Hachuy-Filho, Leandro
Heiduk, Annemarie
Howard, Aaron
Ionta, Gretchen
Islas-Hernández, Sofia C
Johnson, Steven D
Joubert, Lize
Kaiser-Bunbury, Christopher N
Kephart, Susan
Kidyoo, Aroonrat
Koptur, Suzanne
Koschnitzke, Cristiana
Lamborn, Ellen
Livshultz, Tatyana
Machado, Isabel Cristina
Marino, Salvador
Mema, Lumi
Mochizuki, Ko
Morellato, Leonor Patrícia Cerdeira
Mrisha, Chediel K
Muiruri, Evalyne W
Nakahama, Naoyuki
Nascimento, Viviany Teixeira
Nuttman, Clive
Oliveira, Paulo Eugenio
Peter, Craig I
Punekar, Sachin
Rafferty, Nicole
Rapini, Alessandro
Ren, Zong-Xin
Rodríguez-Flores, Claudia I
Rosero, Liliana
Sakai, Shoko
Sazima, Marlies
Steenhuisen, Sandy-Lynn
Tan, Ching-Wen
Torres, Carolina
Trøjelsgaard, Kristian
Ushimaru, Atushi
Vieira, Milene Faria
Wiemer, Ana Pía
Yamashiro, Tadashi
Nadia, Tarcila
Queiroz, Joel
Quirino, Zelma
The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study
title The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study
title_full The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study
title_fullStr The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study
title_full_unstemmed The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study
title_short The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study
title_sort diversity and evolution of pollination systems in large plant clades: apocynaceae as a case study
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6344220/
https://www.ncbi.nlm.nih.gov/pubmed/30099492
http://dx.doi.org/10.1093/aob/mcy127
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AT kaiserbunburychristophern diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT kephartsusan diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT kidyooaroonrat diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT koptursuzanne diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT koschnitzkecristiana diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT lambornellen diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT livshultztatyana diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT machadoisabelcristina diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT marinosalvador diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT memalumi diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT mochizukiko diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT morellatoleonorpatriciacerdeira diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT mrishachedielk diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT muirurievalynew diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT nakahamanaoyuki diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT nascimentovivianyteixeira diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT nuttmanclive diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT oliveirapauloeugenio diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT petercraigi diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT punekarsachin diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT raffertynicole diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT rapinialessandro diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT renzongxin diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT rodriguezfloresclaudiai diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT roseroliliana diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT sakaishoko diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT sazimamarlies diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT steenhuisensandylynn diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT tanchingwen diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT torrescarolina diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT trøjelsgaardkristian diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT ushimaruatushi diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT vieiramilenefaria diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT wiemeranapia diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT yamashirotadashi diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT nadiatarcila diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT queirozjoel diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy
AT quirinozelma diversityandevolutionofpollinationsystemsinlargeplantcladesapocynaceaeasacasestudy