Macroevolution of the plant–hummingbird pollination system

Author:

Barreto Elisa1ORCID,Boehm Mannfred M. A.2ORCID,Ogutcen Ezgi3ORCID,Abrahamczyk Stefan45ORCID,Kessler Michael6ORCID,Bascompte Jordi7ORCID,Dellinger Agnes S.8ORCID,Bello Carolina9ORCID,Dehling D. Matthias110ORCID,Duchenne François1ORCID,Kaehler Miriam11ORCID,Lagomarsino Laura P.12ORCID,Lohmann Lúcia G.1314ORCID,Maglianesi María A.15ORCID,Morlon Hélène16ORCID,Muchhala Nathan17ORCID,Ornelas Juan Francisco18ORCID,Perret Mathieu19ORCID,Salinas Nelson R.20ORCID,Smith Stacey D.21ORCID,Vamosi Jana C.22ORCID,Varassin Isabela G.111ORCID,Graham Catherine H.1ORCID

Affiliation:

1. Swiss Federal Institute for Forest Snow and Landscape Research WSL Zürcherstrasse 111 Birmensdorf 8903 Switzerland

2. Biodiversity Research Centre University of British Columbia 2212 Main Mall Vancouver BC Canada

3. Department of Environment and Biodiversity Paris Lodron University of Salzburg Hellbrunner Straße 34 Salzburg 5020 Austria

4. Nees Institute for Biodiversity of Plant University of Bonn Meckenheimer Allee 170 Bonn 53115 Germany

5. State Museum of Natural History Stuttgart Botany Department Rosenstein 1 Stuttgart 70191 Germany

6. Systematic and Evolutionary Botany University of Zurich Zollikerstrasse 107 Zurich 8008 Switzerland

7. Department of Evolutionary Biology and Environmental Studies University of Zurich Winterthurestrasse 190 Zurich 8057 Switzerland

8. Department of Botany and Biodiversity Research University of Vienna Rennweg 14 Vienna 1030 Austria

9. Department of Environmental Systems Science Institute of Integrative Biology, ETH Zurich Universitätstrasse 16 Zurich 8092 Switzerland

10. Securing Antarctica's Environmental Future, School of Biological Sciences Monash University 25 Rainforest Walk Clayton 3800 Victoria Australia

11. Departamento de Botânica Universidade Federal do Paraná Avenida Coronel Francisco H. dos Santos 100 Curitiba 81531‐980 Brazil

12. Department of Biological Sciences, Shirley C. Tucker Herbarium Louisiana State University Life Science Annex Building A257 Baton Rouge 70803 LA USA

13. Departamento de Botânica, Instituto de Biociências Universidade de São Paulo Rua do Matão 277, Butantã São Paulo 05508‐090 Brazil

14. Department of Integrative Biology, University and Jepson Herbaria University of California, Berkeley 1001 Valley Life Sciences Building Berkeley 94720‐2465 CA USA

15. Escuela de Ciencias Exactas y Naturales Universidad Estatal a Distancia San José 474‐2050 Costa Rica

16. Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure CNRS, INSERM, Université PSL UMR 8197, 46 rue d'Ulm Paris 75005 France

17. Department of Biology University of Missouri – St. Louis St. Louis 63121 MO USA

18. Departamento de Biología Evolutiva Instituto de Ecología, A.C. (INECOL) Xalapa Veracruz 91073 Mexico

19. Department of Plant Sciences, Conservatoire et Jardin Botaniques de Genève University of Geneva Chem. de l'Impératrice 1, 1292 Pregny‐Chambésy Geneva Switzerland

20. Pfizer Plant Research Laboratory New York Botanical Garden 2900 Southern Blvd., Bronx New York City 10458 NY USA

21. Department of Ecology and Evolutionary Biology University of Colorado‐Boulder 1900 Pleasant St Boulder 80302 CO USA

22. Department of Biological Sciences University of Calgary 2500 University Drive NW Calgary T2N1N4 AB Canada

Abstract

ABSTRACTPlant–hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant–hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre‐dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build‐up of both diversities coinciding temporally, and hence suggesting co‐diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species‐level interaction data in macroevolutionary studies.

Funder

H2020 European Research Council

Australian Research Council

Consejo Nacional de Ciencia y Tecnología

Conselho Nacional de Desenvolvimento Científico e Tecnológico

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Publisher

Wiley

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