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      Characterizing Floral Symmetry in the Core Goodeniaceae with Geometric Morphometrics

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          Abstract

          Core Goodeniaceae is a clade of ~330 species primarily distributed in Australia. Considerable variation in flower morphology exists within this group and we aim to use geometric morphometrics to characterize this variation across the two major subclades: Scaevola sensu lato (s.l.) and Goodenia s.l., the latter of which was hypothesized to exhibit greater variability in floral symmetry form. We test the hypothesis that floral morphological variation can be adequately characterized by our morphometric approach, and that discrete groups of floral symmetry morphologies exist, which broadly correlate with subjectively determined groups. From 335 images of 44 species in the Core Goodeniaceae, two principal components were computed that describe >98% of variation in all datasets. Increasing values of PC1 ventralize the dorsal petals (increasing the angle between them), whereas increasing values of PC2 primarily ventralize the lateral petals (decreasing the angle between them). Manipulation of these two morphological “axes” alone was sufficient to recreate any of the general floral symmetry patterns in the Core Goodeniaceae. Goodenia s.l. exhibits greater variance than Scaevola s.l. in PC1 and PC2, and has a significantly lower mean value for PC1. Clustering clearly separates fan-flowers (with dorsal petals at least 120° separated) from the others, whereas the distinction between pseudo-radial and bilabiate clusters is less clear and may form a continuum rather than two distinct groups. Transitioning from the average fan-flower to the average non-fan-flower is described almost exclusively by PC1, whereas PC2 partially describes the transition between bilabiate and pseudo-radial morphologies. Our geometric morphometric method accurately models Core Goodeniaceae floral symmetry diversity.

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          Most cited references22

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          Bmp4 and morphological variation of beaks in Darwin's finches.

          Darwin's finches are a classic example of species diversification by natural selection. Their impressive variation in beak morphology is associated with the exploitation of a variety of ecological niches, but its developmental basis is unknown. We performed a comparative analysis of expression patterns of various growth factors in species comprising the genus Geospiza. We found that expression of Bmp4 in the mesenchyme of the upper beaks strongly correlated with deep and broad beak morphology. When misexpressed in chicken embryos, Bmp4 caused morphological transformations paralleling the beak morphology of the large ground finch G. magnirostris.
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            Pollinator shifts drive increasingly long nectar spurs in columbine flowers.

            Directional evolutionary trends have long garnered interest because they suggest that evolution can be predictable. However, the identification of the trends themselves and the underlying processes that may produce them have often been controversial. In 1862, in explaining the exceptionally long nectar spur of Angraecum sesquipedale, Darwin proposed that a coevolutionary 'race' had driven the directional increase in length of a plant's spur and its pollinator's tongue. Thus he predicted the existence of an exceptionally long-tongued moth. Though the discovery of Xanthopan morgani ssp. praedicta in 1903 with a tongue length of 22 cm validated Darwin's prediction, his 'race' model for the evolution of long-spurred flowers remains contentious. Spurs may also evolve to exceptional lengths by way of pollinator shifts as plants adapt to a series of unrelated pollinators, each with a greater tongue length. Here, using a species-level phylogeny of the columbine genus, Aquilegia, we show a significant evolutionary trend for increasing spur length during directional shifts to pollinators with longer tongues. In addition, we find evidence for 'punctuated' change in spur length during speciation events, suggesting that Aquilegia nectar spurs rapidly evolve to fit adaptive peaks predefined by pollinator morphology. These findings show that evolution may proceed in predictable pathways without reversals and that change may be concentrated during speciation.
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              The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches.

              A classic textbook example of adaptive radiation under natural selection is the evolution of 14 closely related species of Darwin's finches (Fringillidae, Passeriformes), whose primary diversity lies in the size and shape of their beaks. Thus, ground finches have deep and wide beaks, cactus finches have long and pointed beaks (low depth and narrower width), and warbler finches have slender and pointed beaks, reflecting differences in their respective diets. Previous work has shown that even small differences in any of the three major dimensions (depth, width and length) of the beak have major consequences for the overall fitness of the birds. Recently we used a candidate gene approach to explain one pathway involved in Darwin's finch beak morphogenesis. However, this type of analysis is limited to molecules with a known association with craniofacial and/or skeletogenic development. Here we use a less constrained, complementary DNA microarray analysis of the transcripts expressed in the beak primordia to find previously unknown genes and pathways whose expression correlates with specific beak morphologies. We show that calmodulin (CaM), a molecule involved in mediating Ca2+ signalling, is expressed at higher levels in the long and pointed beaks of cactus finches than in more robust beak types of other species. We validated this observation with in situ hybridizations. When this upregulation of the CaM-dependent pathway is artificially replicated in the chick frontonasal prominence, it causes an elongation of the upper beak, recapitulating the beak morphology of the cactus finches. Our results indicate that local upregulation of the CaM-dependent pathway is likely to have been a component of the evolution of Darwin's finch species with elongated beak morphology and provide a mechanistic explanation for the independence of beak evolution along different axes. More generally, our results implicate the CaM-dependent pathway in the developmental regulation of craniofacial skeletal structures.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                5 May 2016
                2016
                : 11
                : 5
                : e0154736
                Affiliations
                [1 ]Department of Biology, Rhodes College, 2000 N. Parkway, Memphis, Tennessee, United States of America
                [2 ]Science and Conservation Division, Department of Parks and Wildlife, Kensington, Western Australia, Australia
                [3 ]Department of Biological Sciences, St. John’s University, Queens, New York, United States of America
                Università di Pisa, ITALY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AG JF JM KS RJ. Performed the experiments: AG JF KS. Analyzed the data: AG JF. Wrote the paper: AG JF JM KS DH RJ.

                [¤]

                Current address: Department of Biological Sciences, California State University, Stanislaus, Turlock, California, United States of America

                Article
                PONE-D-15-36396
                10.1371/journal.pone.0154736
                4858217
                27148960
                9cd10d0f-13b6-43e9-a715-d7acf684cbdc
                © 2016 Gardner et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 18 August 2015
                : 18 April 2016
                Page count
                Figures: 5, Tables: 1, Pages: 22
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB 1256946
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB 1256946
                Award Recipient :
                This work was supported by the National Science Foundation of the U.S.A. [NSF DEB 1256946 to R.S.J., D.G.H.]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flower Anatomy
                Petals
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flowers
                Research and Analysis Methods
                Imaging Techniques
                Morphometry
                Physical Sciences
                Mathematics
                Geometry
                Symmetry
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flower Anatomy
                Corolla
                Biology and Life Sciences
                Developmental Biology
                Evolutionary Developmental Biology
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Developmental Biology
                People and Places
                Geographical Locations
                Oceania
                Australia
                Biology and Life Sciences
                Developmental Biology
                Evolutionary Developmental Biology
                Functional Morphology
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Developmental Biology
                Functional Morphology
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Physiology
                Functional Morphology
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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