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 Deprá; Arthur 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

doi:10.1093/aob/mcy127

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

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › peer-review

72 Citations (Scopus)

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 language	English
Pages (from-to)	311-325
Number of pages	15
Journal	Annals of Botany
Volume	123
Issue number	2
Early online date	7 Aug 2018
DOIs	https://doi.org/10.1093/aob/mcy127
Publication status	Published - 23 Jan 2019

User-Defined Keywords

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

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10.1093/aob/mcy127

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Ollerton, J., Liede-Schumann, S., Endress, M. E., Meve, U., Rech, A. R., Shuttleworth, A., Keller, H. A., Fishbein, M., Alvarado-Cárdenas, L. O., Amorim, F. W., Bernhardt, P., Celep, F., Chirango, Y., Chiriboga-Arroyo, F., Civeyrel, L., Cocucci, A., Cranmer, L., da Silva-Batista, I. C., de Jager, L., ... Quirino, Z. (2019). The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study. Annals of Botany, 123(2), 311-325. https://doi.org/10.1093/aob/mcy127

@article{23ae608bf25949c2a9c94da8fb7a2f4f,

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

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.",

keywords = "Apocynaceae, Asclepiadaceae, bimodal pollination system, biogeography, fly pollination, generalization, mutualism, phylogeny, plant–pollinator interactions, pollination ecology, specialization, stapeliads",

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 Ren, {Zong Xin} and Rodr{\'i}guez-Flores, {Claudia I} and Liliana Rosero and Shoko Sakai and Marlies Sazima and Steenhuisen, {Sandy Lynn} and Tan, {Ching Wen} 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",

note = "Funding information: We offer grateful thanks to all of the authors of studies that we have included in our database, which reflects a research effort that goes back over 100 years. Funding for fieldwork to JO and his group was obtained from The British Ecological Society, the Percy Sladen Memorial Fund, the Royal Society and the University of Northampton. JO would like to thank the many field assistants and in-country contacts who helped with data collection, species identification, accommodation and field sites in Australia, Gabon, Guyana, Namibia, Tanzania, Peru and South Africa. AAC, APW, LG and CT thank CONICET, FONCyT and SECyT for financial support. LPCM thanks S{\~a}o Paulo Research Foundation – Fapesp (grants #2013/50155-0, #2010/51307-0) and National Council for Scientific and Technological Development – CNPq (PVE 400717/2013-1; PQ 1D Researcher) for funding, and PELD-CRSC-17, Serra do Cip{\'o} National Park, Cedro Company, and Vellozia Reserve for supporting fieldwork. MS thanks Fapesp, Faepex/Unicamp/CAPES and CNPq for financial support. AS, SLS, CIP, SDJ and YC thank the National Research Foundation (NRF) of South Africa for funding; AS, SLS and YC also thank Jeremy Midgley for collaborative support. AR and LF are CNPq Pq-1D researchers. HK wishes to thank the following entomologists for identifying specimens: Alan Martin (Sphingidae), Ezequiel Osvaldo N{\'u}{\~n}ez Bustos (Lepidoptera), Bol{\'i}var R. Garcete-Barrett (Vespidae), Helcio Gil Santana (Hemiptera), Leopoldo {\'A}lvarez and Mariano Lucia (Apidae), Ayr Bello (Coleoptera), Cecilia Waichert (Pompilidae), Carolina Paris (Formicidae) and Woody Fitzgerald (Bibionidae). CK thanks FAPERJ, and ICSB thanks CAPES, for financial support, and both are grateful to the following entomologists who identified insects: Felipe Vivallo (Apidae), Fabio Prezoto (Vespidae), Dalton de Souza Amorim (Diptera), Leandro Silva Barbosa (Diptera), Alexandre Soares (Lepidoptera), Luiz Alves da Costa (Hemiptera) and Paulo Roberto Magno (Coleoptera). SP acknowledges funding support from the Science and Engineering Research Board of India for systematic and ecological studies of Indian Ceropegia. MCG thanks Rio de Janeiro Research Foundation – Faperj (grant E-26111.271-2014) and CNPq (PQ 2 Researcher) and also thanks the following entomologists for identifying specimens: Gabriel A. R. Melo and Brunno B. Rosa (Hymenoptera), Diego R. Dolibaina (Lepidoptera) and Paschoal C. Grossi (Coleoptera). LHF was supported by a Masters scholarship from CAPES. L. Civeyrel was supported by the French Laboratory of Excellence project “TULIP” (ANR-10-LABX-41; ANR-11-IDEX-0002-02). Publisher copyright: {\textcopyright} The Author(s) 2018.",

year = "2019",

month = jan,

day = "23",

doi = "10.1093/aob/mcy127",

language = "English",

volume = "123",

pages = "311--325",

journal = "Annals of Botany",

issn = "0305-7364",

publisher = "Oxford University Press",

number = "2",

}

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, ZX, Rodríguez-Flores, CI, Rosero, L, Sakai, S, Sazima, M, Steenhuisen, SL, Tan, CW, Torres, C, Trøjelsgaard, K, Ushimaru, A, Vieira, MF, Wiemer, AP, Yamashiro, T, Nadia, T, Queiroz, J & Quirino, Z 2019, 'The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study', Annals of Botany, vol. 123, no. 2, pp. 311-325. https://doi.org/10.1093/aob/mcy127

TY - JOUR

T1 - The diversity and evolution of pollination systems in large plant clades

T2 - 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

N1 - Funding information: We offer grateful thanks to all of the authors of studies that we have included in our database, which reflects a research effort that goes back over 100 years. Funding for fieldwork to JO and his group was obtained from The British Ecological Society, the Percy Sladen Memorial Fund, the Royal Society and the University of Northampton. JO would like to thank the many field assistants and in-country contacts who helped with data collection, species identification, accommodation and field sites in Australia, Gabon, Guyana, Namibia, Tanzania, Peru and South Africa. AAC, APW, LG and CT thank CONICET, FONCyT and SECyT for financial support. LPCM thanks São Paulo Research Foundation – Fapesp (grants #2013/50155-0, #2010/51307-0) and National Council for Scientific and Technological Development – CNPq (PVE 400717/2013-1; PQ 1D Researcher) for funding, and PELD-CRSC-17, Serra do Cipó National Park, Cedro Company, and Vellozia Reserve for supporting fieldwork. MS thanks Fapesp, Faepex/Unicamp/CAPES and CNPq for financial support. AS, SLS, CIP, SDJ and YC thank the National Research Foundation (NRF) of South Africa for funding; AS, SLS and YC also thank Jeremy Midgley for collaborative support. AR and LF are CNPq Pq-1D researchers. HK wishes to thank the following entomologists for identifying specimens: Alan Martin (Sphingidae), Ezequiel Osvaldo Núñez Bustos (Lepidoptera), Bolívar R. Garcete-Barrett (Vespidae), Helcio Gil Santana (Hemiptera), Leopoldo Álvarez and Mariano Lucia (Apidae), Ayr Bello (Coleoptera), Cecilia Waichert (Pompilidae), Carolina Paris (Formicidae) and Woody Fitzgerald (Bibionidae). CK thanks FAPERJ, and ICSB thanks CAPES, for financial support, and both are grateful to the following entomologists who identified insects: Felipe Vivallo (Apidae), Fabio Prezoto (Vespidae), Dalton de Souza Amorim (Diptera), Leandro Silva Barbosa (Diptera), Alexandre Soares (Lepidoptera), Luiz Alves da Costa (Hemiptera) and Paulo Roberto Magno (Coleoptera). SP acknowledges funding support from the Science and Engineering Research Board of India for systematic and ecological studies of Indian Ceropegia. MCG thanks Rio de Janeiro Research Foundation – Faperj (grant E-26111.271-2014) and CNPq (PQ 2 Researcher) and also thanks the following entomologists for identifying specimens: Gabriel A. R. Melo and Brunno B. Rosa (Hymenoptera), Diego R. Dolibaina (Lepidoptera) and Paschoal C. Grossi (Coleoptera). LHF was supported by a Masters scholarship from CAPES. L. Civeyrel was supported by the French Laboratory of Excellence project “TULIP” (ANR-10-LABX-41; ANR-11-IDEX-0002-02). Publisher copyright: © The Author(s) 2018.

PY - 2019/1/23

Y1 - 2019/1/23

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

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U2 - 10.1093/aob/mcy127

DO - 10.1093/aob/mcy127

M3 - Journal article

SN - 0305-7364

VL - 123

SP - 311

EP - 325

JO - Annals of Botany

JF - Annals of Botany

IS - 2

ER -

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

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