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      Beyond buzz‐pollination – departures from an adaptive plateau lead to new pollination syndromes

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          Summary

          • Pollination syndromes describe recurring adaptation to selection imposed by distinct pollinators. We tested for pollination syndromes in Merianieae (Melastomataceae), which contain bee‐ (buzz‐), hummingbird‐, flowerpiercer‐, passerine‐, bat‐ and rodent‐pollinated species. Further, we explored trait changes correlated with the repeated shifts away from buzz‐pollination, which represents an ‘adaptive plateau’ in Melastomataceae.

          • We used random forest analyses to identify key traits associated with the different pollinators of 19 Merianieae species and estimated the pollination syndromes of 42 more species. We employed morphospace analyses to compare the morphological diversity (disparity) among syndromes.

          • We identified three pollination syndromes (‘buzz‐bee’, ‘mixed‐vertebrate’ and ‘passerine’), characterized by different pollen expulsion mechanisms and reward types, but not by traditional syndrome characters. Further, we found that ‘efficiency’ rather than ‘attraction’ traits were important for syndrome circumscription. Contrary to syndrome theory, our study supports the pooling of different pollinators (hummingbirds, bats, rodents and flowerpiercers) into the ‘mixed‐vertebrate’ syndrome, and we found that disparity was highest in the ‘buzz‐bee’ syndrome.

          • We conclude that the highly adaptive buzz‐pollination system may have prevented shifts towards classical pollination syndromes, but provided the starting point for the evolution of a novel set of distinct syndromes, all having retained multifunctional stamens that provide pollen expulsion, reward and attraction.

          Abstract

          See also the Commentary on this article by Vallejo‐Marín, 221: 618–620 .

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          Most cited references62

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          Generalization in Pollination Systems, and Why it Matters

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            Adaptive Radiation of Reproductive Characteristics in Angiosperms, I: Pollination Mechanisms

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              Random forests for classification in ecology.

              Classification procedures are some of the most widely used statistical methods in ecology. Random forests (RF) is a new and powerful statistical classifier that is well established in other disciplines but is relatively unknown in ecology. Advantages of RF compared to other statistical classifiers include (1) very high classification accuracy; (2) a novel method of determining variable importance; (3) ability to model complex interactions among predictor variables; (4) flexibility to perform several types of statistical data analysis, including regression, classification, survival analysis, and unsupervised learning; and (5) an algorithm for imputing missing values. We compared the accuracies of RF and four other commonly used statistical classifiers using data on invasive plant species presence in Lava Beds National Monument, California, USA, rare lichen species presence in the Pacific Northwest, USA, and nest sites for cavity nesting birds in the Uinta Mountains, Utah, USA. We observed high classification accuracy in all applications as measured by cross-validation and, in the case of the lichen data, by independent test data, when comparing RF to other common classification methods. We also observed that the variables that RF identified as most important for classifying invasive plant species coincided with expectations based on the literature.
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                Author and article information

                Contributors
                agnes.dellinger@univie.ac.at
                juerg.schoenenberger@univie.ac.at
                Journal
                New Phytol
                New Phytol
                10.1111/(ISSN)1469-8137
                NPH
                The New Phytologist
                John Wiley and Sons Inc. (Hoboken )
                0028-646X
                1469-8137
                12 October 2018
                January 2019
                : 221
                : 2 ( doiID: 10.1111/nph.2019.221.issue-2 )
                : 1136-1149
                Affiliations
                [ 1 ] Department of Botany and Biodiversity Research University of Vienna Rennweg 14 1030 Vienna Austria
                [ 2 ] Herbario Nacional del Ecuador (QCNE) Instituto Nacional de Biodiversidad Río Coca E06‐115 e Isla Fernandina Quito Ecuador
                [ 3 ] Department of Biology and Marine Biology University of North Carolina Wilmington 601 S. College Road Wilmington NC 28403 USA
                [ 4 ] Institute of Biodiversity Science and Sustainability California Academy of Sciences 55 Music Concourse Drive San Francisco CA 94118‐4503 USA
                [ 5 ] Institute of Systematic Botany The New York Botanical Garden 2900 Southern Blvd Bronx NY 10458‐5126 USA
                [ 6 ] School of Biological Science University of Portsmouth King Henry 1 Street Portsmouth P01 2DY UK
                [ 7 ] Institute of Arctic Biology University of Alaska Fairbanks Fairbanks AK 99775 USA
                Author notes
                [*] [* ] Authors for correspondence:

                Agnes S. Dellinger

                Tel: +43 660 3572098

                Email: agnes.dellinger@ 123456univie.ac.at

                Jürg Schönenberger

                Tel: +43 1 4277 54080

                Email: juerg.schoenenberger@ 123456univie.ac.at

                Author information
                http://orcid.org/0000-0003-1394-3414
                http://orcid.org/0000-0001-6757-4760
                http://orcid.org/0000-0003-0727-2829
                http://orcid.org/0000-0001-7348-143X
                http://orcid.org/0000-0002-0688-6995
                http://orcid.org/0000-0001-8057-4116
                http://orcid.org/0000-0001-6791-2731
                Article
                NPH15468 2018-27344
                10.1111/nph.15468
                6492237
                30368819
                fb421b41-394c-440a-ac60-7637f544d884
                © 2018 The Authors. New Phytologist © 2018 New Phytologist Trust

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 20 June 2018
                : 01 August 2018
                Page count
                Figures: 3, Tables: 3, Pages: 14, Words: 11544
                Funding
                Funded by: Austrian Science Fund
                Award ID: P30669‐B29
                Funded by: Division of Environmental Biology
                Award ID: 1146409
                Funded by: NSF
                Categories
                Full Paper
                Research
                Full Papers
                Custom metadata
                2.0
                nph15468
                January 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.6.2.1 mode:remove_FC converted:01.05.2019

                Plant science & Botany
                buzz‐pollination,floral evolution,morphospace,pollinator shifts,vertebrate pollination

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