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

Jeff Ollerton, Sigrid Liede-Schumann, Mary E Endress, Ulrich Meve, André Rodrigo Rech, Adam Shuttleworth, Héctor A Keller, Mark Fishbein, Leonardo O Alvarado-Cárdenas, Felipe W Amorim, Peter Bernhardt, Ferhat Celep, Yolanda Chirango, Fidel Chiriboga-Arroyo, Laure Civeyrel, Andrea Cocucci, Louise Cranmer, Inara Carolina da Silva-Batista, Linde de Jager, Mariana Scaramussa DepráArthur Domingos-Melo, Courtney Dvorsky, Kayna Agostini, Leandro Freitas, Maria Cristina Gaglianone, Leo Galetto, Mike Gilbert, Ixchel González-Ramírez, Pablo Gorostiague, David Goyder, Leandro Hachuy-Filho, Annemarie Heiduk, Aaron Howard, Gretchen Ionta, Sofia C Islas-Hernández, Steven D Johnson, Lize Joubert, Christopher N Kaiser-Bunbury, Susan Kephart, Aroonrat Kidyoo, Suzanne Koptur, Cristiana Koschnitzke, Ellen Lamborn, Tatyana Livshultz, Isabel Cristina Machado, Salvador Marino, Lumi Mema, Ko Mochizuki, Leonor Patrícia Cerdeira Morellato, Chediel K Mrisha, Evalyne W Muiruri, Naoyuki Nakahama, Viviany Teixeira Nascimento, Clive Nuttman, Paulo Eugenio Oliveira, Craig I Peter, Sachin Punekar, Nicole Rafferty, Alessandro Rapini, Zong-Xin Ren, Claudia I Rodríguez-Flores, Liliana Rosero, Shoko Sakai, Marlies Sazima, Sandy-Lynn Steenhuisen, Ching-Wen Tan, Carolina Torres, Kristian Trøjelsgaard, Atushi Ushimaru, Milene Faria Vieira, Ana Pía Wiemer, Tadashi Yamashiro, Tarcila Nadia, Joel Queiroz, Zelma Quirino

Research output: Contribution to journalArticle

Abstract

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 Methods The database was compiled from published and unpublished reports.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.
Original languageEnglish
JournalAnnals of Botany
Volumemcy127
DOIs
Publication statusPublished - 7 Aug 2018

Fingerprint

Apocynaceae
pollination
case studies
pollinating insects
flowers
insects
moths
Angiospermae

Keywords

  • Apocynaceae
  • Asclepiadaceae
  • bimodal pollination system
  • biogeography
  • fly pollination
  • generalization
  • mutualism
  • phylogeny
  • plant–pollinator interactions
  • pollination ecology
  • specialization
  • stapeliads

Cite this

Ollerton, J., Liede-Schumann, S., Endress, M. E., Meve, U., Rech, A. R., Shuttleworth, A., ... Quirino, Z. (2018). The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study. Annals of Botany, mcy127. https://doi.org/10.1093/aob/mcy127
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. In: Annals of Botany. 2018 ; Vol. mcy127.
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abstract = "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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author = "Jeff Ollerton and Sigrid Liede-Schumann and Endress, {Mary E} and Ulrich Meve and Rech, {Andr{\'e} Rodrigo} and Adam Shuttleworth and Keller, {H{\'e}ctor A} and Mark Fishbein and Alvarado-C{\'a}rdenas, {Leonardo O} and Amorim, {Felipe W} and Peter Bernhardt and Ferhat Celep and Yolanda Chirango and Fidel Chiriboga-Arroyo and Laure Civeyrel and Andrea Cocucci and Louise Cranmer and {da Silva-Batista}, {Inara Carolina} and {de Jager}, Linde and Depr{\'a}, {Mariana Scaramussa} and Arthur Domingos-Melo and Courtney Dvorsky and Kayna Agostini and Leandro Freitas and Gaglianone, {Maria Cristina} and Leo Galetto and Mike Gilbert and Ixchel Gonz{\'a}lez-Ram{\'i}rez and Pablo Gorostiague and David Goyder and Leandro Hachuy-Filho and Annemarie Heiduk and Aaron Howard and Gretchen Ionta and Islas-Hern{\'a}ndez, {Sofia C} and Johnson, {Steven D} and Lize Joubert and Kaiser-Bunbury, {Christopher N} and Susan Kephart and Aroonrat Kidyoo and Suzanne Koptur and Cristiana Koschnitzke and Ellen Lamborn and Tatyana Livshultz and Machado, {Isabel Cristina} and Salvador Marino and Lumi Mema and Ko Mochizuki and Morellato, {Leonor Patr{\'i}cia Cerdeira} and Mrisha, {Chediel K} and Muiruri, {Evalyne W} and Naoyuki Nakahama and Nascimento, {Viviany Teixeira} and Clive Nuttman and Oliveira, {Paulo Eugenio} and Peter, {Craig I} and Sachin Punekar and Nicole Rafferty and Alessandro Rapini and Zong-Xin Ren and Rodr{\'i}guez-Flores, {Claudia I} and Liliana Rosero and Shoko Sakai and Marlies Sazima and Sandy-Lynn Steenhuisen and Ching-Wen Tan and Carolina Torres and Kristian Tr{\o}jelsgaard and Atushi Ushimaru and Vieira, {Milene Faria} and Wiemer, {Ana P{\'i}a} and Tadashi Yamashiro and Tarcila Nadia and Joel Queiroz and Zelma Quirino",
year = "2018",
month = "8",
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doi = "10.1093/aob/mcy127",
language = "English",
volume = "mcy127",
journal = "Annals of Botany",
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Ollerton, J, Liede-Schumann, S, Endress, ME, Meve, U, Rech, AR, Shuttleworth, A, Keller, HA, Fishbein, M, Alvarado-Cárdenas, LO, Amorim, FW, Bernhardt, P, Celep, F, Chirango, Y, Chiriboga-Arroyo, F, Civeyrel, L, Cocucci, A, Cranmer, L, da Silva-Batista, IC, de Jager, L, Deprá, MS, Domingos-Melo, A, Dvorsky, C, Agostini, K, Freitas, L, Gaglianone, MC, Galetto, L, Gilbert, M, González-Ramírez, I, Gorostiague, P, Goyder, D, Hachuy-Filho, L, Heiduk, A, Howard, A, Ionta, G, Islas-Hernández, SC, Johnson, SD, Joubert, L, Kaiser-Bunbury, CN, Kephart, S, Kidyoo, A, Koptur, S, Koschnitzke, C, Lamborn, E, Livshultz, T, Machado, IC, Marino, S, Mema, L, Mochizuki, K, Morellato, LPC, Mrisha, CK, Muiruri, EW, Nakahama, N, Nascimento, VT, Nuttman, C, Oliveira, PE, Peter, CI, Punekar, S, Rafferty, N, Rapini, A, Ren, Z-X, Rodríguez-Flores, CI, Rosero, L, Sakai, S, Sazima, M, Steenhuisen, S-L, Tan, C-W, Torres, C, Trøjelsgaard, K, Ushimaru, A, Vieira, MF, Wiemer, AP, Yamashiro, T, Nadia, T, Queiroz, J & Quirino, Z 2018, 'The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study', Annals of Botany, vol. mcy127. https://doi.org/10.1093/aob/mcy127

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.

In: Annals of Botany, Vol. mcy127, 07.08.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study

AU - Ollerton, Jeff

AU - Liede-Schumann, Sigrid

AU - Endress, Mary E

AU - Meve, Ulrich

AU - Rech, André Rodrigo

AU - Shuttleworth, Adam

AU - Keller, Héctor A

AU - Fishbein, Mark

AU - Alvarado-Cárdenas, Leonardo O

AU - Amorim, Felipe W

AU - Bernhardt, Peter

AU - Celep, Ferhat

AU - Chirango, Yolanda

AU - Chiriboga-Arroyo, Fidel

AU - Civeyrel, Laure

AU - Cocucci, Andrea

AU - Cranmer, Louise

AU - da Silva-Batista, Inara Carolina

AU - de Jager, Linde

AU - Deprá, Mariana Scaramussa

AU - Domingos-Melo, Arthur

AU - Dvorsky, Courtney

AU - Agostini, Kayna

AU - Freitas, Leandro

AU - Gaglianone, Maria Cristina

AU - Galetto, Leo

AU - Gilbert, Mike

AU - González-Ramírez, Ixchel

AU - Gorostiague, Pablo

AU - Goyder, David

AU - Hachuy-Filho, Leandro

AU - Heiduk, Annemarie

AU - Howard, Aaron

AU - Ionta, Gretchen

AU - Islas-Hernández, Sofia C

AU - Johnson, Steven D

AU - Joubert, Lize

AU - Kaiser-Bunbury, Christopher N

AU - Kephart, Susan

AU - Kidyoo, Aroonrat

AU - Koptur, Suzanne

AU - Koschnitzke, Cristiana

AU - Lamborn, Ellen

AU - Livshultz, Tatyana

AU - Machado, Isabel Cristina

AU - Marino, Salvador

AU - Mema, Lumi

AU - Mochizuki, Ko

AU - Morellato, Leonor Patrícia Cerdeira

AU - Mrisha, Chediel K

AU - Muiruri, Evalyne W

AU - Nakahama, Naoyuki

AU - Nascimento, Viviany Teixeira

AU - Nuttman, Clive

AU - Oliveira, Paulo Eugenio

AU - Peter, Craig I

AU - Punekar, Sachin

AU - Rafferty, Nicole

AU - Rapini, Alessandro

AU - Ren, Zong-Xin

AU - Rodríguez-Flores, Claudia I

AU - Rosero, Liliana

AU - Sakai, Shoko

AU - Sazima, Marlies

AU - Steenhuisen, Sandy-Lynn

AU - Tan, Ching-Wen

AU - Torres, Carolina

AU - Trøjelsgaard, Kristian

AU - Ushimaru, Atushi

AU - Vieira, Milene Faria

AU - Wiemer, Ana Pía

AU - Yamashiro, Tadashi

AU - Nadia, Tarcila

AU - Queiroz, Joel

AU - Quirino, Zelma

PY - 2018/8/7

Y1 - 2018/8/7

N2 - 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.

AB - 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.

KW - Apocynaceae

KW - Asclepiadaceae

KW - bimodal pollination system

KW - biogeography

KW - fly pollination

KW - generalization

KW - mutualism

KW - phylogeny

KW - plant–pollinator interactions

KW - pollination ecology

KW - specialization

KW - stapeliads

UR - https://academic.oup.com/aob/advance-article/doi/10.1093/aob/mcy127/5067583

UR - http://www.mendeley.com/research/diversity-evolution-pollination-systems-large-plant-clades-apocynaceae-case-study

U2 - 10.1093/aob/mcy127

DO - 10.1093/aob/mcy127

M3 - Article

VL - mcy127

JO - Annals of Botany

JF - Annals of Botany

SN - 0305-7364

ER -