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

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

doi:10.1093/aob/mcy127

Abstract

Background and AimsLarge 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shifts in pollination systems across major clades and regions.MethodsThe database was compiled from published and unpublished reports.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 ResultsMost 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.ConclusionsWithin 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.

Highlights

Interactions between plants and their pollinators are considered to have played a major role in the diversification of some large angiosperm groups (Darwin, 1877; Crepet, 1984; Johnson, 2006; Kay and Sargent, 2009; Vamosi and Vamosi, 2010; van der Niet and Johnson, 2012; van der Niet et al., Ollerton et al — Diversity and evolution of pollination systems in Apocynaceae2014)
Other clades are conservative with respect to the broad range of pollinators that individual species use, e.g. insect generalist Asclepias species in North America
In this study we have shown that Apocynaceae is probably one of the best-studied large families from the perspective of understanding the diversity of pollinators that interact with flowering plants

Summary

Introduction

Interactions between plants and their pollinators are considered to have played a major role in the diversification of some large angiosperm groups (Darwin, 1877; Crepet, 1984; Johnson, 2006; Kay and Sargent, 2009; Vamosi and Vamosi, 2010; van der Niet and Johnson, 2012; van der Niet et al., Ollerton et al — Diversity and evolution of pollination systems in Apocynaceae2014). Smith et al, 2006; Wilson et al, 2006; Whittall and Hodges, 2007; Ogutcen et al, 2017 – but see Armbruster and Muchhala, 2009, for a different perspective) In other cases, such as the family Asteraceae, an evolutionary trend from specialist- to generalist-pollination systems within a clade has been suggested (Torres and Galetto, 2002). Most large flowering plant clades lack extensive data on pollination systems; there is limited understanding of the evolutionary transitions between different types of pollinators and the biogeographical patterns of those interactions with pollinators in large families of flowering plants. Growth forms in Apocynaceae cover almost the whole spectrum of plant types, including vines, scramblers, shrubs, herbs with fibrous and tuberous roots, caudiciforms, epiphytes, large and small stem succulents, leaf succulents, and small and large trees, truly aquatic species are conspicuously absent (Ollerton, 1986; Judd et al, 2002; Fishbein et al, 2018)

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