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Evolution of Oil-Producing Trichomes in Sisyrinchium (Iridaceae): Insights from the first Comprehensive Phylogenetic Analysis of the Genus

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Evolution of Oil-Producing Trichomes in Sisyrinchium (Iridaceae): Insights from the first Comprehensive Phylogenetic Analysis of the Genus Annals of Botany 107: 1287–1312, 2011 doi:10.1093/aob/mcr080, available online at www.aob.oxfordjournals.org Evolution of oil-producing trichomes in Sisyrinchium (Iridaceae): insights from the first comprehensive phylogenetic analysis of the genus Olivier Chauveau1,*, Lilian Eggers2, Christian Raquin3, Adriano Silve´rio1,2, Spencer Brown4, Arnaud Couloux5, Corine Cruaud5, Eliane Kaltchuk-Santos6, Roxana Yockteng7, Tatiana T. Souza-Chies2 and Sophie Nadot1 1Universite´ Paris-Sud, Laboratoire Ecologie Syste´matique et Evolution, UMR 8079, Orsay, F-91405, France, 2Instituto de Biocieˆncias, Departamento de Botaˆnica, Universidade Federal do Rio Grande do Sul, Porto Alegre, Av. Bento Gonc¸alves, Downloaded from 9500 – Pre´dio 43433, Brazil, 3CNRS, Laboratoire Ecologie Syste´matique et Evolution, UMR 8079, Orsay, F-91405, France, 4CNRS, Dynamique de la compartimentation cellulaire, Institut des Sciences du ve´ge´tal, UPR 2355, Gif-sur-Yvette, F-91198, France, 5GENOSCOPE, Centre National de Se´quenc¸age. 2, rue Gaston Cre´mieux, CP5706, F-91057 Evry Cedex, France, 6Instituto de Biocieˆncias, Departamento de Gene´tica, Universidade Federal do Rio Grande do Sul, Av. Bento Gonc¸alves, 7 9500 – Pre´dio 43323 M, CEP 91501–970, Porto Alegre, Brazil and MNHN, UMR 7205 Origine, Structure et Evolution de la http://aob.oxfordjournals.org/ Biodiversite´, Paris, F-75005, France * For correspondence. E-mail [email protected] Received: 5 November 2010 Returned for revision: 10 December 2010 Accepted: 22 February 2011 Published electronically: 27 April 2011 † Background and Aims Sisyrinchium (Iridaceae: Iridoideae: Sisyrinchieae) is one of the largest, most widespread and most taxonomically complex genera in Iridaceae, with all species except one native to the American conti- nent. Phylogenetic relationships within the genus were investigated and the evolution of oil-producing structures related to specialized oil-bee pollination examined. at UNIVERSITY OF CALIFORNIA, Berkeley on February 23, 2012 † Methods Phylogenetic analyses based on eight molecular markers obtained from 101 Sisyrinchium accessions representing 85 species were conducted in the first extensive phylogenetic analysis of the genus. Total evidence analyses confirmed the monophyly of the genus and retrieved nine major clades weakly connected to the subdivi- sions previously recognized. The resulting phylogenetic hypothesis was used to reconstruct biogeographical pat- terns, and to trace the evolutionary origin of glandular trichomes present in the flowers of several species. † Key Results and Conclusions Glandular trichomes evolved three times independently in the genus. In two cases, these glandular trichomes are oil-secreting, suggesting that the corresponding flowers might be pollinated by oil- bees. Biogeographical patterns indicate expansions from Central America and the northern Andes to the suban- dean ranges between Chile and Argentina and to the extended area of the Parana´ river basin. The distribution of oil-flower species across the phylogenetic trees suggests that oil-producing trichomes may have played a key role in the diversification of the genus, a hypothesis that requires future testing. Key words: Oil-bee pollination, glandular trichomes, elaiophores, lipids, phylogeography, Sisyrinchieae, Olsynium, Solenomelus. INTRODUCTION Relationships between oil-secreting flowers and oil-collecting bees constitute an example of a functional specialization and During their evolution, flowering plants have developed a wide uncommon interaction between plants and pollinators variety of strategies to attract and reward pollinators. Plant– (Minckley and Roulston, 2006). Flowers offering an oil pollinator interactions are key components of the dynamics resource are found in 11 families according to the APG of most terrestrial ecosystems and, in a world where biodiver- system (APG III, 2009), distributed across the angiosperms sity is jeopardized by anthropogenic changes, analysing the among unrelated orders (Buchmann, 1987; Rasmussen and evolutionary history of species and understanding the mechan- Olesen, 2000; Steiner and Whitehead, 2002; Neff and isms involved in their evolution, such as plant–pollinator Simpson, 2005; Renner and Schaefer, 2010). The latest com- interactions, is crucial (Steffan Dewenter et al., 2006; Waser, prehensive study found that oil-bee pollination has evolved 2006). Furthermore, since species interactions are considered at least 28 times independently, and 1500–1800 species to play a central role in many speciation events, studying the have developed oil-producing organs called elaiophores evolutionary history of traits closely linked to uncommon (Renner and Schaefer, 2010). These structures, located on interactions could contribute to improve our knowledge of various floral parts, constitute local glandular fields within the mechanisms involved (Rieseberg and Willis, 2007). the flower and can be anatomically separated into two cat- Insects represent the largest group of animals visiting egories (Vogel, 1969, 1974, 2009). Epithelial elaiophores flowers to collect resources. Most visit flowers to collect consist of glandular epithelial or epidermal cells and their oil pollen and nectar, but some insects seek other resources. secretions are stored below a protective cuticle, forming # The Author 2011. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: [email protected] 1288 Chauveau et al. — Evolution of oil-producing trichomes in Sisyrinchium small blisters, whereas trichomatic elaiophores consist of hun- evolved from elaiophores (Cocucci and Vogel, 2001). Other dreds to thousands of oil-producing glandular trichomes species have pollen flowers, devoid of trichomes either on (Buchmann, 1987; Silvera, 2002; Machado, 2004). The latter the filamental column or on the adaxial side of tepals. produce oil continuously and secretion is often unprotected, Members of this third category are widely distributed through- but oil can in some cases be accumulated in a subcuticular out the range of the genus. space at the tip of the trichome (Vogel, 1974; Buchmann, The goal of this study was to elucidate the phylogenetic 1987; Cocucci and Vogel, 2001). Epithelial and trichomatic relationships among Sisyrinchium species and genera of elaiophores produce non-volatile oils gathered by the females Sisyrinchieae (Fig. 1), using a total evidence approach, and of specialized oil-collecting bees belonging to two families to test the monophyly of the subgeneric divisions as defined of Hymenoptera, Mellitidae and Apidae (Michener, 2007), in the existing classifications. The resulting historical frame- which have developed morphological adaptations on their work was used to analyse geographical patterns, optimize the legs or abdomen to harvest and store lipids (Schlindwein, evolutionary history of elaiophores and make hypotheses Downloaded from 1998; Cocucci et al., 2000; Vogel, 2009). Documented uses about potential shifts in the pollination system. of floral lipids by oil-collecting bees show that females mix oils with pollen and use this mixture to feed their larvae (Vogel, 1974; Simpson and Neff, 1981). In some species, it MATERIALS AND METHODS has been observed that females also cover the brood cell Taxonomic sampling http://aob.oxfordjournals.org/ walls of their nest with a complex set of different substances that contains floral lipids (Buchmann, 1987; Cane et al., Taxa sampled, voucher information and GenBank accession 1983; Alves-dos-Santos et al., 2002). numbers are listed in Appendix 1. A total of 101 Sisyrinchium (Iridaceae: Iridoideae: Sisyrinchieae) is a large Sisyrinchium accessions from South and North America, repre- and complex genus with a distribution spanning the American senting 85 species covering the different subgeneric arrange- continents from subarctic areas to Tierra del Fuego. Many ments proposed in the literature, were sampled. With the taxonomic studies have already been conducted, mainly exception of S. jamesonii, it was not possible to obtain plant based on morphological traits (Klatt, 1861; Baker, 1878; material from section Segetia (Ravenna, 2003b), which includes approximately four Andean species from Argentina, Bentham and Hooker, 1883; Rudall et al., 1986; Goldblatt at UNIVERSITY OF CALIFORNIA, Berkeley on February 23, 2012 et al., 1990; Ravenna, 2000, 2002, 2003b), but the systematics Bolivia, Peru, Ecuador and Venezuela. Outgroups were of the genus remain poorly resolved. The number of recog- selected from the genera Olsynium (five species), nized species varies from approx. 80 (Goldblatt et al., 1989) Orthrosanthus (one species) and Solenomelus (two species), to approx. 200 (Rudall et al., 1986) and the subgeneric div- which are closely related to Sisyrinchium within isions are not well defined and are, as such, unsatisfactory Sisyrinchieae (Goldblatt et al., 2008). Plant material was (Goldblatt et al., 1990; Cocucci and Vogel, 2001; Ravenna, mostly sampled from the wild or from cultivated specimens 2003b). Moreover, Central and South American representa- obtained from seeds collected in the wild and held in botanical tives of the genus remain largely unknown: 24 % of the 206 gardens or national collections. A special effort was put into taxa accepted by the World Checklist of Iridaceae were sampling of S. micranthum, a species that exhibits a high described from these areas during the past 10 years (Barker, level of morphological plasticity and is closely
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