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      Quantifying floral shape variation in 3D using microcomputed tomography: a case study of a hybrid line between actinomorphic and zygomorphic flowers

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          Abstract

          The quantification of floral shape variations is difficult because flower structures are both diverse and complex. Traditionally, floral shape variations are quantified using the qualitative and linear measurements of two-dimensional (2D) images. The 2D images cannot adequately describe flower structures, and thus lead to unsatisfactory discrimination of the flower shape. This study aimed to acquire three-dimensional (3D) images by using microcomputed tomography (μCT) and to examine the floral shape variations by using geometric morphometrics (GM). To demonstrate the advantages of the 3D-μCT-GM approach, we applied the approach to a second-generation population of florist's gloxinia ( Sinningia speciosa) crossed from parents of zygomorphic and actinomorphic flowers. The flowers in the population considerably vary in size and shape, thereby served as good materials to test the applicability of the proposed phenotyping approach. Procedures were developed to acquire 3D volumetric flower images using a μCT scanner, to segment the flower regions from the background, and to select homologous characteristic points (i.e., landmarks) from the flower images for the subsequent GM analysis. The procedures identified 95 landmarks for each flower and thus improved the capability of describing and illustrating the flower shapes, compared with typically lower number of landmarks in 2D analyses. The GM analysis demonstrated that flower opening and dorsoventral symmetry were the principal shape variations of the flowers. The degrees of flower opening and corolla asymmetry were then subsequently quantified directly from the 3D flower images. The 3D-μCT-GM approach revealed shape variations that could not be identified using typical 2D approaches and accurately quantified the flower traits that presented a challenge in 2D images. The approach opens new avenues to investigate floral shape variations.

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          Geometric morphometrics: recent applications to the study of evolution and development

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            Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators.

            An adaptive role of corolla shape has been often asserted without an empirical demonstration of how natural selection acts on this trait. In generalist plants, in which flowers are visited by diverse pollinator fauna that commonly vary spatially, detecting pollinator-mediated selection on corolla shape is even more difficult. In this study, we explore the mechanisms promoting selection on corolla shape in the generalist crucifer Erysimum mediohispanicum Polatschek (Brassicaceae). We found that the main pollinators of E. mediohispanicum (large bees, small bees and bee flies) discriminate between different corolla shapes when offered artificial flowers without reward. Importantly, different pollinators prefer different shapes: bees prefer flowers with narrow petals, whereas bee flies prefer flowers with rounded overlapping petals. We also found that flowers with narrow petals (those preferred by bees) produce both more pollen and nectar than those with rounded petals. Finally, different plant populations were visited by different faunas. As a result, we found spatial variation in the selection acting on corolla shape. Selection favoured flowers with narrow petals in the populations where large or small bees are the most abundant pollinator groups. Our study suggests that pollinators, by preferring flowers with high reward, exert strong selection on the E. mediohispanicum corolla shape. The geographical variation in the pollinator-mediated selection on E. mediohispanicum corolla shape suggests that phenotypic evolution and diversification can occur in this complex floral trait even without specialization.
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              Natural selection on Erysimum mediohispanicum flower shape: insights into the evolution of zygomorphy.

              Paleontological and phylogenetic studies have shown that floral zygomorphy (bilateral symmetry) has evolved independently in several plant groups from actinomorphic (radially symmetric) ancestors as a consequence of strong selection exerted by specialized pollinators. Most studies focused on unraveling the developmental genetics of flower symmetry, but little is known about the adaptive significance of intraspecific flower shape variation under natural conditions. We provide the first evidence for natural selection favoring zygomorphy in a wild population of Erysimum mediohispanicum (Brassicaceae), a plant showing extensive continuous variation in flower shape, ranging from actinomorphic to zygomorphic flowers. By using geometric morphometric tools to describe flower shape, we demonstrate that plants bearing zygomorphic flowers received more pollinator visits and had the highest fitness, measured not only by the number of seeds produced per plant but also by the number of seeds surviving to the juvenile stage. This study provides strong evidence for the existence of significant fitness differences associated with floral shape variation in E. mediohispanicum, thus illuminating a pathway for the evolution of zygomorphy in natural populations.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                10 September 2015
                2015
                : 6
                : 724
                Affiliations
                [1] 1Institute of Ecology and Evolutionary Biology, National Taiwan University Taipei, Taiwan
                [2] 2Department of Life Science, National Taiwan University Taipei, Taiwan
                [3] 3Department of Bio-Industrial Mechatronics Engineering, National Taiwan University Taipei, Taiwan
                Author notes

                Edited by: Christophe Godin, INRIA, France

                Reviewed by: Sarah Robinson, University of Bern, Switzerland; Jasmine Burguet, Institut National de la Recherche Agronomique, France

                *Correspondence: Yan-Fu Kuo, Department of Bio-Industrial Mechatronics Engineering, National Taiwan University, No. 1, Sec. 4, Roosevelt Rd., Taipei 106, Taiwan ykuo@ 123456ntu.edu.tw

                This article was submitted to Technical Advances in Plant Science, a section of the journal Frontiers in Plant Science

                †These authors have contributed equally to this study.

                Article
                10.3389/fpls.2015.00724
                4564768
                26442038
                ee25e18e-de97-4687-81b8-e8c11c67cb71
                Copyright © 2015 Wang, Hsu, Wang, Lee and Kuo.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 14 May 2015
                : 28 August 2015
                Page count
                Figures: 13, Tables: 0, Equations: 0, References: 42, Pages: 11, Words: 6727
                Funding
                Funded by: National Science Council Taiwan 10.13039/501100001868
                Award ID: NSC-101-2313-B-002-050-MY3
                Award ID: NSC-95-2311-B-002-014-MY3
                Categories
                Plant Science
                Methods

                Plant science & Botany
                three-dimensional image analysis,geometric morphometrics,petal shape,dorsoventral asymmetry,flower opening,floral morphology,sinningia speciosa

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