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The Evolutionary Ecology of Ultraviolet Floral Pigmentation

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The Evolutionary Ecology of Ultraviolet Floral Pigmentation THE EVOLUTIONARY ECOLOGY OF ULTRAVIOLET FLORAL PIGMENTATION by Matthew H. Koski B.S., University of Michigan, 2009 Submitted to the Graduate Faculty of the Kenneth P. Dietrich School of Arts and Sciences in partial fulfillment of the requirements for the degree of Doctor of Philosophy, Biological Sciences University of Pittsburgh 2015 UNIVERSITY OF PITTSBURGH KENNETH P. DIETRICH SCHOOL OF ARTS AND SCIENCES This dissertation was presented by Matthew H. Koski It was defended on May 4, 2015 and approved by Dr. Susan Kalisz, Professor, Dept. of Biological Sciences, University of Pittsburgh Dr. Nathan Morehouse, Assistant Professor, Dept. of Biological Sciences, University of Pittsburgh Dr. Mark Rebeiz, Assistant Professor, Dept. of Biological Sciences, University of Pittsburgh Dr. Stacey DeWitt Smith, Assistant Professor, Dept. of Ecology and Evolutionary Biology, University of Pittsburgh Dissertation Advisor: Dr. Tia-Lynn Ashman, Professor, Dept. of Biological Sciences, University of Pittsburgh ii Copyright © by Matthew H. Koski 2015 iii THE EVOLUTIONARY ECOLOGY OF ULTRAVIOLET FLORAL PIGMENTATION Matthew H. Koski, PhD University of Pittsburgh, 2015 The color of flowers varies widely in nature, and this variation has served as an important model for understanding evolutionary processes such as genetic drift, natural selection, speciation and macroevolutionary transitions in phenotypic traits. The flowers of many taxa reflect ultraviolet (UV) wavelengths that are visible to most pollinators. Many taxa also display UV reflectance at petal tips and absorbance at petal bases, which manifests as a ‘bullseye’ color patterns to pollinators. Most previous research on UV floral traits has been largely descriptive in that it has identified species with UV pattern and speculated about its function with respect to pollination. This dissertation addresses the ecological and evolutionary relevance of UV floral pattern at micro- and macroevolutionary scales. First I use a widespread plant (Argentina anserina) to describe the degree to which UV floral pattern varies, and determine the genetic contribution to variation. With the same system, I then use experimental manipulation to test whether and how the UV bullseye pattern mediates plant-pollinator interactions in the field. I then evaluate whether spatial variation in biotic (pollinator) and abiotic selective agents contribute to geographic variation in UV floral traits at regional (Colorado Rocky Mountains elevation gradient) and global (four latitudinal gradients) scales. Finally, I create a molecular phylogeny of the species-rich cinquefoil (Potentilla) group to address whether variation in UV pattern among taxa is constrained by evolutionary history, and whether biogeography and bioclimatic factors contribute to interspecific variation. Findings from this dissertation that pollinators contribute to variation in UV pattern, broaden the understanding of the traits that contribute to pollinator-mediated reproductive success of flowering plants. UV irradiance can also impose selection on UV pattern and drive latitudinal trends in floral iv pigmentation, extending an ecological rule formulated for animals—Gloger’s rule—to plants. Finally, I detected low phylogenetic signal for UV pigmentation in Potentilla, but strong biogeographic associations, which together suggest that selection could play a role in shaping UV floral variation among taxa. Overall, this dissertation enhances the understanding of how spatially varying selection regimes contribute to geographic variation and macroevolutionary patterns in a cryptic pigmentation trait in flowers. v TABLE OF CONTENTS TITLE PAGE...................................................................................................................................i ABSTRACT………………………………………………………………………………………iv TABLE OF CONTENTS………………………………………………………………………...vi PREFACE…………………………………………………………………………………….....xix 1.0 INTRODUCTION…………………………………………………………………………….1 2.0 QUANTITATIVE VARIATION, HERITABILITY, AND TRAIT CORRELATIONS FOR ULTRAVIOLET FLORAL TRAITS IN ARGENTINA ANSERINA (ROSACEAE): IMPLICATIONS FOR FLORAL EVOLUTION………………………………………………3 2.1 INTRODUCTION…………………………………………………………………….3 2.2 METHODS…….……………………………………………………………………...7 2.2.1 Study system………………………………………………………………...7 2.2.2 Phenotypic variation in the field…………………………………………...8 2.2.3 UV photography and measurement of UVP………………………………8 2.2.4 Plant material for broad sense heritability and trait correlations.............9 2.2.5 Phenotypic variation in the greenhouse …………………………………10 2.2.6 Statistical analyses…………………………………………………………11 2.3 RESULTS……..……………………………………………………………………...14 2.3.1 Phenotypic variation in the field………………………………………….14 2.3.2 Phenotypic variation in the greenhouse………………………………….15 2.3.3 Broad-sense heritability …………………………………………………..15 2.3.4 Broad-sense genetic correlation…………………………………………..16 2.4 DISCUSSION ……………………………………………………………………….16 2.4.1 Variation in UV pattern…………………………………………………..17 vi 2.4.2 Broad-sense heritability of UV pattern and spectral properties………..18 2.4.3 Trait correlations within flowers, and between flowers and leaves…….19 2.4.4 Conclusions ……..…………………………………………………………21 3.0 DISSECTING POLLINATOR RESPONSES TO A UBIQUITOUS ULTRAVIOLET FLORAL PATTERN IN THE WILD………………………………………………………….29 3.1 INTRODUCION………………………………………………..……………………29 3.2 METHODS………………………………………………..…………………………33 3.2.1 Study system……………………………………………………………….33 3.2.2 Study area and plant material………………………………….…………33 3.2.3 Floral manipulation…………………………………………………….….34 3.2.4 Array set up and pollinator observations………………………………..35 3.2.5 Statistical analyses…………………………………………………………38 3.3 RESULTS………………………………………………..…………………………...39 3.3.1 Absorbing arrays…………………………………………………………..39 3.3.2 Reflecting arrays…………………………………………………………..40 3.3.3 Inverse arrays……………………………………………………………...41 3.4 DISCUSSION………………………………………………..………………………41 3.4.1 Is the UV bullseye a nectar guide? ………………………………………42 3.4.2 UV reflectance or pattern: which mediates visitation?............................44 3.4.3 Pervasiveness of the UV bullseye flower pattern………………………..45 3.4.4 Implications for naturally-occurring variation in UV pattern…………46 4.0 AN ALTITUDINAL CLINE IN UV FLORAL PATTERN CORRESPONDS WITH A BEHAVIORAL CHANGE OF A GENERALIST POLLINATOR ASSEMBLAGE……….51 4.1 INTRODUCTION………………………………..………………………………….51 vii 4.2 METHODS………………………………..…………………………………………53 4.2.1 Study system………………………………..……………………………...53 4.2.2 Floral traits and altitude………………………………..…………………54 4.2.3 Pollinator assemblage and altitude………………………………..……...55 4.2.4 Pollinator response to floral bullseye size………………………………..56 4.2.5 Relationship between visit number and pollen receipt and export…….58 4.2.6 Relationship between natural variation in floral traits and pollen receipt……..………………………………..……………………………….……59 4.3 RESULTS………………………………..…………………………………………...60 4.3.1 Floral traits, pollinator assemblage, and altitude………………………..61 4.3.2 Pollinator response to floral bullsye size…………………………………61 4.3.3 Relationship between visit number and pollen receipt and export…….62 4.3.4 Relationship between natural variation in floral traits and pollen receipt……..………………………………..………………………………….…63 4.4 DISCUSSION………………………………………………………………………..63 5.0 FLORAL PIGMENTATION PATTERNS PROVIDE AN EXAMPLE OF GLOGER’S RULE IN PLANTS..………………………………..……………..…………………….……….74 5.1 INTRODUCTION..………………………………..………………………………...74 5.2 METHODS AND RESULTS..………………………………..……………………..75 5.3 DISCUSSION..………………………………..……………………………………..78 6.0 MACROEVOLUTIONARY PATTERNS OF FLOWER COLOR TRAITS AN ASSOCIATIONS WITH BIOGEOGRAPHY IN THE SPECIOSE CINQUEFOIL……….86 6.1 INTRODUCTION..………………………………..………………….……………..86 6.2 METHODS..………………………………..………………………………………..88 viii 6.2.1 System ……………………………..……………………………………….88 6.2.2 Phylogeny……………………………..……………………………………89 6.2.3 Phenotypic and bioclimatic data……………………………..…………...91 6.2.4 Phylogenetic signal……………………………..………………………….93 6.2.5 Correlated trait evolution……………………………..…………………..94 6.2.6 Abiotic and biogeographic associations with floral phenotype…………95 6.3 RESULTS……………………………..………………….…………………………..96 6.3.1 Phylogeny……………………………..……………………………………96 6.3.2 Floral phenotypes……………………………..…………………………...97 6.3.3 Biogeographic parameters ……………………………..…………………98 6.3.4 Phylogenetic signal……………………………..……………………….....98 6.3.5 Phylogenetic trait correlations……………………………..……………..99 6.3.6 Phylogenetically controlled geographic and abiotic associations………99 6.4 DISCUSSION……………………………..………………………………………..100 7.0 APPENDICES……………………………..………………….……………………………108 APPENDIX A……………………………..……………………………………………108 APPENDIX B……………………………..…………………………………………….111 APPENDIX C……………………………..……………………………………………112 APPENDIX D……………………………..……………………………………………115 APPENDIX E……………………………..……………………………………………127 BIBLIOGRPAHY……………………………..………………….……………………………138 ix LIST OF TABLES Table 2-1: Variation for components of UV pattern (UV-absorbing area, petal area, UV proportion) measured from field-collected plants of Argentina pacifica, A. anserina, and both taxa combined (Argentina aggregate)………………………………………………………………………………22 Table 2-2: Mean (± SD) and coefficient of variation for concentration of foliar UV-absorbing compounds, components of UV pattern (UV-absorbing area, petal area, UV proportion) and spectral traits (brightness, UV reflectance, UV chroma and green chroma ) measured at the petal apex and base measured on greenhouse-grown plants of Argentina pacifica and A. anserina. …………………………………………………………………………………………………...…23 Table 2-3: Broad-sense heritability (diagonal) and trait correlations
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