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The Evolution of Bird Pollination Syndromes in the Macaronesian Lotus (Leguminosae)

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THE EVOLUTION OF BIRD POLLINATION IN MACARONESIAN LOTUS SECTION RHYNCHOLOTUS (LEGUMINOSAE) by Isidro Ojeda Alayón A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in The Faculty of Graduate Studies (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) March, 2011 © Isidro Ojeda Alayón, 2011 ABSTRACT In order to understand the evolutionary transition from bee pollination (melittophily) to bird pollination (ornithophily), I studied a group of Lotus from Macaronesia. First, I provided a combined phylogenetic framework using nuclear and plastid genes, where I showed that the morphological features adapted to opportunistic passerine birds in Tenerife and La Palma are derived and evolved recently within the last 1.2 Ma in four species. I also identified Lotus sessilifolius as the most likely closely related species with melittophily. I showed that L. sessilifolius and the clade where this syndrome evolved had a pre-adaptation to produce a color change to red flowers (and the associated anthocyanidin pigment, cyanidin) as a possible strategy to increase bee foraging efficiency. The transition from yellow to red flowers in this group required only a redirection in the flux of pigment production and a modification in the proportions of flavonols and anthocyanidins, especially within the cyanidin branch. I also found that petal micromorphology is highly modified between the two syndromes. I found that ornithophilous flowers lack the typical papillose conical cells, which are distributed in the exposed sides of the petals in bee-pollinated flowers. This reduction of conical cells is associated with an early down-regulation of a dorsal identity gene in legumes, LjCYC2. Bird-pollinated flowers also have a higher proportion of tabular rugose cells in all three types of petals in comparison with the bee-pollinated species. The increase of this epidermal type is associated with an up-regulation of LjCYC3, a lateral petal identity gene, during early stages of flower development in the dorsal and lateral petals. Lotus sessilifolius also seems to have this early expression in comparison with other bee-pollinated species. All this evidence suggests that the transition from bee to bird pollination in this group required only heterochronic modifications of the genes involved in flower color and petal micromorphology. It seems that ornithophily in Lotus evolved within a group which has at least two pre-adaptations, production of pigments required for red colors and an increase in the amount of tabular rugose cells, which likely facilitated the evolution of phenotypes associated with this pollination syndrome in the Canary Islands. ii TABLE OF CONTENTS Abstract .................................................................................................................................... ii Table of contents ..................................................................................................................... iii List of tables........................................................................................................................... viii List of figures ........................................................................................................................... xi Acknowledgements ............................................................................................................... xvii Dedication ............................................................................................................................ xviii Co-authorship statement ........................................................................................................ xx 1. Introduction .......................................................................................................................... 1 1.1 Bird pollination .................................................................................................................... 1 1.2 Macaronesian Lotus ............................................................................................................. 2 1.3 Molecular phylogenetics and DNA barcoding of Macaronesian Lotus .................................. 3 1.4 Flower colour and petal micromorpholgy modifications during the transition from bee to bird pollination in Macaronesian Lotus ......................................................................................... 4 1.5 Bibliography ......................................................................................................................... 5 2. Bird-pollinated flowers in an evolutionary and molecular context .................................... 9 2.1 Pollination syndromes....................................................................................................... 9 2.2 The syndrome of ornithophily ......................................................................................... 10 2.2.1 The birds...................................................................................................................... 10 2.2.2 Ecology of bird pollination .......................................................................................... 11 2.2.3 Perching vs. hovering................................................................................................... 12 2.2.4 Hermit vs. non-hermit hummingbirds........................................................................... 13 2.2.5 Major groups of angiosperms with bird pollination ...................................................... 14 2.3 The floral phenotype ........................................................................................................... 16 2.3.1 Types of floral adaptation ............................................................................................ 16 2.3.2 Why red? ..................................................................................................................... 17 2.3.3 Flower colour and its perception .................................................................................. 18 2.3.4 Nectar .......................................................................................................................... 20 2.3.5 Corolla morphology in bird-pollinated flowers ............................................................. 22 2.3.6 Other characters associated with bird pollination.......................................................... 23 2.4 The molecular basis for the evolution of ornithophily ......................................................... 26 2.4.1 Some model systems ..................................................................................................... 26 2.6 Bibliography ....................................................................................................................... 32 iii 3. Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity .................................................................................................................. 40 3.1 Introduction ........................................................................................................................ 40 3.1.1 Objectives of the study .................................................................................................. 42 3.2 Materials and methods ........................................................................................................ 43 3.2.1 Taxon sampling ............................................................................................................ 43 3 2.2 Microscopy and cell type classification ......................................................................... 44 3.2.3 Reconstruction of evolutionary changes ........................................................................ 46 3.3 Results ................................................................................................................................ 46 3.3.1 Epidermal types within Leguminosae ............................................................................ 46 3.3.2 Strong micromorphological variation in petals is exclusive to papilionoid legumes ....... 47 3.3.4 Loss of micromorphological variation in Indigofera, Amorpheae and IRLC .................. 48 3.3.5 Zygomorphy in caesalpinioids is not associated with strong micromorphological variation ............................................................................................................................................ 49 3.3.6 The occurrence of papillose cells in the Leguminosae ................................................... 50 3.4 Discussion .......................................................................................................................... 51 3.4.1 Functional significance of papillose cell types............................................................... 51 3.4.2 Lack of micromorphological variation in the Caesalpinioideae ..................................... 51 3.4.3 Mixing of epidermal types in the same petal surface ..................................................... 52 3.4.4 Contrasting loss of micromorphological variation within flowers of the Amorpheae and IRLC ................................................................................................................................... 53 3.4.5 Genetic control of petal micromorphology and petal identity ........................................ 54 3.4.6 Evolution of petal micromorphology ............................................................................
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