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The Role of Pollinators in the Evolution of Corolla Shape Variation, Disparity and Integration in a Highly Diversified Plant Family with a Conserved Floral Bauplan

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The Role of Pollinators in the Evolution of Corolla Shape Variation, Disparity and Integration in a Highly Diversified Plant Family with a Conserved Floral Bauplan Annals of Botany 117: 889–904, 2016 doi:10.1093/aob/mcv194, available online at www.aob.oxfordjournals.org PART OF A SPECIAL ISSUE ON DEVELOPMENTAL ROBUSTNESS AND SPECIES DIVERSITY The role of pollinators in the evolution of corolla shape variation, disparity and integration in a highly diversified plant family with a conserved floral bauplan Jose´M.Gomez 1,2*, Ruben Torices1,3, Juan Lorite4, Christian Peter Klingenberg5 and Francisco Perfectti6 1Department of Functional and Evolutionary Ecology, Estacion Experimental de Zonas A´ridas (EEZA-CSIC), Almerı´a, Spain, 2Department of Ecology, 4Department of Botany, 6Department of Genetics, University of Granada, Granada, Spain, 3Centre for Functional Ecology, Department of Life Science, University of Coimbra, Coimbra, Portugal and 5Faculty of Life Sciences, University of Manchester, Manchester, UK * For correspondence. E-mail [email protected] Received: 29 March 2015 Returned for revision: 17 September 2015 Accepted: 14 October 2015 Published electronically: 15 February 2016 Downloaded from Background and Aims Brassicaceae is one of the most diversified families in the angiosperms. However, most species from this family exhibit a very similar floral bauplan. In this study, we explore the Brassicaceae floral mor- phospace, examining how corolla shape variation (an estimation of developmental robustness), integration and dis- parity vary among phylogenetically related species. Our aim is to check whether these floral attributes have evolved http://aob.oxfordjournals.org/ in this family despite its apparent morphological conservation, and to test the role of pollinators in driving this evolution. Methods Using geometric morphometric tools, we calculated the phenotypic variation, disparity and integration of the corolla shape of 111 Brassicaceae taxa. We subsequently inferred the phylogenetic relationships of these taxa and explored the evolutionary lability of corolla shape. Finally, we sampled the pollinator assemblages of every taxon included in this study, and determined their pollination niches using a modularity algorithm. We explore the relationship between pollination niche and the attributes of corolla shape. Key Results Phylogenetic signal was weak for all corolla shape attributes. All taxa had generalized pollination systems. Nevertheless, they belong to different pollination niches. There were significant differences in corolla shape among pollination niches even after controlling for the phylogenetic relationship of the plant taxa. Corolla at University of Manchester on April 29, 2016 shape variation and disparity was significantly higher in those taxa visited mostly by nocturnal moths, indicating that this pollination niche is associated with a lack of developmental robustness. Corolla integration was higher in those taxa visited mostly by hovering long-tongued flies and long-tongued large bees. Conclusions Corolla variation, integration and disparity were evolutionarily labile and evolved very recently in the evolutionary history of the Brassicaceae. These floral attributes were strongly related to the pollination niche. Even in a plant clade having a very generalized pollination system and exhibiting a conserved floral bauplan, polli- nators can drive the evolution of important developmental attributes of corolla shape. Key words: corolla shape, phenotypic integration, canalization, robustness, plant–pollinator interactions, Brassicaceae, floral morphospace, geometric morphometrics, phenotypic disparity. INTRODUCTION enhancing plant reproduction depends on the coordinated func- tioning of their elements (Cordoba and Cocucci, 2011). Due to Phenotypic integration is the coordinated variation of morpho- its direct association with plant fitness, it is widely assumed logical traits within functional modules (Olson and Miller, that floral integration has been optimized by selection (Berg, 1958; Pigliucci and Preston, 2004). Trait covariation and phe- 1960; Armbruster et al., 2004; Ordano et al., 2008). Berg notypic integration may be the consequences of natural selec- (1960), in her seminal study, showed that plant species with tion acting to improve the functioning of those modules, a specialized pollination systems exhibit ‘correlation pleiades’ or phenomenon called functional integration (Pigliucci, 2003; modules of integrated traits. Following these ideas, subsequent Armbruster et al., 2014; Klingenberg, 2014). Phenotypic inte- studies have reported that self-compatible plants display weaker gration may also be the mere consequence of architectural and floral integration than self-incompatible species (Anderson and developmental processes prompting covariation among traits Busch, 2006), that species with specialized pollination exhibit (Herrera et al., 2002; Armbruster et al., 2014; Klingenberg, greater floral integration than those with generalized pollination 2014). (Pe´rez et al., 2007; Rosas-Guerrero et al., 2011; Ellis et al., Angiosperm flowers are complex structures that perform an 2014; Gomez et al., 2014), and that the type of pollinators may essential function in plants, namely reproduction (Thomson, determine the magnitude of phenotypic integration of the flow- 1983; Harder and Barrett, 2006; Willmer, 2011). In animal- ers (Pe´rez-Barrales et al., 2007, 2014; Gonzalez et al., 2015). pollinated plants, flowers are functional modules composed of This plethora of studies indicates that pollinators may select not integrated units that work together to attract pollinators and only for floral traits but also for floral integration (Nattero boost their pollination effectiveness. Their efficacy in et al., 2011). VC The Author 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 890 Gomez et al. — Corolla shape evolution in Brassicaceae The functioning of integrated complex traits may be hindered of Brassicaceae is its generalized pollination system. Most cru- by the occurrence of phenotypic variation and trait imprecision cifers are pollinated by a high diversity of pollinators belonging (Hansen et al., 2006; Young, 2006; Pe´labon et al., 2012). to many disparate functional groups. Despite this generalized Natural selection, being an optimizing mechanism, tends to in- pollination system, both diversity and type of pollinators varies crease the accuracy of complex traits by, among other sources, among species even within the same genus (Gomez et al., decreasing their variation and increasing their precision (Bell, 2015). The specific goals of the current study are: (1) to quan- 1997; Hansen et al., 2006). Although empirical evidence re- tify the morphological disparity, variation and integration of the mains scarce, it seems that the magnitude of phenotypic varia- corolla shape in Brassicaceae; (2) to examine how corolla shape tion in floral traits, a manifestation of the lack of developmental variation, disparity and integration has evolved along the phy- robustness, is in several plant species a consequence of their logeny of this family; and (3) to determine the role of pollina- interaction with pollinators (Williams & Conner, 2001; tors in the evolution of these corolla shape attributes. Armbruster et al., 2009a, b; Rosas-Guerrero et al., 2011; Pe´labon et al., 2012). A relaxation of the selection imposed by pollinators can cause an increase in the magnitude of floral var- MATERIAL AND METHODS iation (Galen, 1996; Williams and Conner, 2001). Downloaded from An essential but still unsolved key question is how pheno- Study species typic variation and integration is expressed at a macroevolu- We have studied 111 Brassicaceae species and subspecies be- tionary scale (Geber, 2013; Goswami et al., 2014). In longing to 30 genera and 16 tribes (Supplementary Data, Table particular, it is still unknown whether these attributes affect the S1). We have included species belonging to all main phyloge- morphological disparity of the members of a given clade netic lineages identified by Couvreur et al.(2010), in order to (Geber, 2013; Goswami et al., 2014). Morphological disparity, cover as much as possible the Brassicaceae evolutionary diver- http://aob.oxfordjournals.org/ estimated as the phenotypic distinctness of a form in a given sity. Their flowers were polysymmetric, disymmetric or mono- morphospace (Eble, 2004), is an estimate of the magnitude of symetric, as well as tetradynamous, with four inner and long the phenotypic divergences of taxa (Erwin, 2007). In fact, mor- stamens and two outer and short stamens located between the phological disparity has been recently used to estimate floral adaxial and abaxial petals. From each species, we have tried to morphological divergence (Chartier et al., 2014). study at least two populations located in different areas of their Unfortunately, empirical information on the magnitude of vari- distribution range to avoid any local effect on our results, ation of morphological disparity across plant taxa and how this although this was not possible in all cases (Table S1). variation is related to pollination remains scarce, although it would help to reveal how pollinators mediate the divergence in at University of Manchester on April 29, 2016 floral shapes. Phylogenetic relationships among studied Brassicaceae The main goal of this study is to investigate the role of polli- nators in the evolution of phenotypic integration, disparity and We inferred a phylogenetic hypothesis for the species in- variation of the Brassicaceae
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