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Sub-Paratethyan Origin and Middle to Late Miocene Principal

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TAXON 66 (3) • June 2017: 675–703 Kilian & al. • Diversification of the Lactucinae (Compositae) Sub-Paratethyan origin and Middle to Late Miocene principal diversification of the Lactucinae (Compositae: Cichorieae) inferred from molecular phylogenetics, divergence-dating and biogeographic analysis Norbert Kilian,1* Alexander Sennikov,2 Ze-Huan Wang,3 Birgit Gemeinholzer4 & Jian-Wen Zhang3 1 Botanic Garden and Botanical Museum Berlin, Freie Universität Berlin, Königin-Luise-Str. 6–8, 14195 Berlin, Germany 2 Botanical Museum, Finnish Museum of Natural History, P.O. Box 7, 00014 University of Helsinki, Finland; and Herbarium, Komarov Botanical Institute of Russian Academy of Sciences, Prof. Popov str. 2, 197376 St. Petersburg, Russia 3 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, People’s Republic of China 4 AG Spezielle Botanik, Justus-Liebig-Universität Giessen, Heinrich-Buff-Ring 38, 35392 Giessen, Germany * Sequence of authors determines credit Author for correspondence: Norbert Kilian, [email protected] ORCID AS, http://orcid.org/0000-0001-6664-7657 DOI https://doi.org/10.12705/663.9 Abstract The Lactucinae or Lactuca alliance include approximately 200 species distributed across the Northern Hemisphere and Africa. They were not recognised as a separate lineage until the late 20th century and their circumscription is still not fully settled. The generic classification of no other group of the Cichorieae has faced as many controversies as the Lactuca alliance and competing taxonomies coexist. This paper provides the first molecular phylogeny of the subtribe on a global scale as a major step towards its revised systematics. The sampling includes almost 60% of the species-level diversity and spans all species groups. Two datasets were created, one including the nrDNA ITS region, the other five concatenated non-coding plastid DNA loci. Maximum parsimony, maximum likelihood and Bayesian inference were used to produce a robust phylogenetic backbone. The diversification and expansion of the Lactucinae in a geohistorical context was reconstructed by estimating the age of their lineages using relaxed molecular clock dating and by inferring the ancestral areas using Bayesian binary analysis. The redelimited monophyletic Lactucinae are composed of seven lineages that also include Prenanthes, which is confirmed to have a single species, P. purpurea. The positions of two further lineages shift between Lactucinae and Crepidinae in the nuclear and plastid DNA phylogenies. Incongruence between the phylogenies suggests events of ancient reticulation or incomplete lineage sorting in the formation of these latter two lineages and in two of the seven other Lactucinae lineages. The phyloge- netic results show a dilemma for Lactucinae systematics: most generic concepts proposed to date are highly artificial but the resolved phylogenetic lineages do not constitute practicable taxonomic entities with our current knowledge. Diversification of the subtribe is inferred to have taken place since the Middle Miocene. Biogeographic analysis proposes that the clade originated in the mountains of the landmass mediating between the European and Asian continents and delimited in the south by the Tethys Sea and in the north by the Paratethys Sea. Several independent migrations have occurred into various parts of Asia, Europe, tropical Africa and North America. Keywords Asteraceae; biogeography; Lactuca alliance; Miocene; phylogenetics; uncorrelated relaxed molecular clock Supplementary Material DNA sequence alignment files are available in the Supplementary Data section of the online version of this article at http://ingentaconnect.com/content/iapt/tax INTRODUCTION Cichorium L. represent distantly related lineages, which are classified as subtribes Lactucinae and Cichoriinae, respectively, The Asteraceae as the largest family of flowering plants in the recent taxonomy of the tribe by Kilian & al. (2009a), who provide only a handful of important food crops (Dempewolf recognised 11 subtribes. The Lactucinae include approximately & al., 2008). Among them, the Cichorieae are the tribe with 200 species (Kilian & al., 2009b–), form the fourth-largest the strongest representation, contributing lettuce (Lactuca subtribe and are distributed across the Northern Hemisphere sativa L.), endive (Cichorium endivia L.) and chicory (Cichorium and Africa. With respect to systematics, the Lactucinae are one intybus L.). In this tribe, the two genera Lactuca L. and of the least known subtribes of Cichorieae. Received: 27 Jun 2016 | returned for (first) revision: 5 Oct 2016 | (last) revision received: 6 Feb 2017 | accepted: 7 Feb 2017 || publication date(s): online fast track, n/a; in print and online issues, 23 Jun 2017 || © International Association for Plant Taxonomy (IAPT) 2017 Version of Record 675 Kilian & al. • Diversification of the Lactucinae (Compositae) TAXON 66 (3) • June 2017: 675–703 Recognition of Lactuca and its allies as a lineage of their (e.g., Cicerbita Wallr. in the sense of Wallroth, 1822). The other own is a rather recent achievement, gained by Bremer (1994) is diagnosed by a very limited set of one or a few characters through morphological phylogenetics. Throughout the 19th and (e.g., Cicerbita in the sense of Beauverd, 1910). In this way 20th centuries, the genera of the Lactuca alliance were seen and along with the progressive inventorying of the subtribe’s as parts of a large subtribe Crepidinae, alternatively named species diversity in its wide distribution area, the number of de- as Lactucinae, or of a corresponding entity (Candolle, 1838; scribed (heterotypic) genera rose from 4 in 1800, to 11 in 1900 Hoffmann, 1890–94; Stebbins, 1953; Jeffrey, 1966). Within up to 18 in 2015 (Kilian & al., 2009b–). During this time, com- this subtribe, especially Lactuca in the tradition of Bentham peting classifications have coexisted. Consequently, current (1873) and Hoffmann (1890–94) embraced an extraordinarily taxonomic treatments, exclusively available in the frame of, or wide range of taxa, spanning members of several of the modern preparatory for, Floras, usually greatly vary in the number and subtribes. Bremer (1994) inferred this large subtribe to be poly- concepts of the genera recognised. Taxonomic syntheses on a phyletic, with the three alliances of Lactuca, Sonchus L. and global scale, even for single genera, are lacking altogether and Hieracium L. not being closely related to Crepis L. and its rendered almost impossible as long as the generic delimitation allies. Consequently, he reclassified all of them as separate is entirely unsettled. subtribes. His morphology-based results were confirmed by A first molecular phylogenetic analysis spanning the a phylogenetic analysis using chloroplast DNA restriction site Lactucinae but focussed on its Sino-Himalayan centre of di- variation (Whitton & al., 1995) and subsequently by analy- versity (Wang & al., 2013) has preceded this paper. Based on ses based on the nuclear ribosomal DNA internal transcribed both nuclear and plastid DNA datasets, Wang & al. (2013) pro- spacer (nrITS) region (Kilian & al., 2009a; Tremetsberger & vided evidence that the monophyletic core of the subtribe is al., 2012; Fernández-Mazuecos & al., 2016). The last analyses composed of six lineages with strong statistical support, which revealed that over 80% of the tribe’s species diversity is found they recognised at generic rank: one then unnamed, the others in two of the five main clades of the Cichorieae. The larger of being Cicerbita, Lactuca, Melanoseris Less., Notoseris C.Shih the two, home of two-thirds of the species diversity, includes, and Paraprenanthes C.Shih. Two early diverging lineages were besides the Lactucinae, the Crepidinae (s.str.), Chondrillinae, incongruent between nuclear and plastid data: Prenanthes pur- Hyoseridinae and Hypochaeridinae, and is addressed in the purea L. and Faberia, which is of hybrid origin. They were following as the “C2H2L clade”. only resolved within Lactucinae in the plastid DNA tree or the While delimitation of the Lactucinae from the other sub- nrITS tree, respectively. tribes of the C2H2L clade is rather straightforward, disentan- The case of the isolated Prenanthes purpurea, which is gling Lactucinae and Crepidinae morphologically has proven sister to the core Lactucinae in the plastid DNA phylogeny more difficult. Accordingly, the classification of the Lactucinae (Wang & al., 2013), appears puzzling. While this sister rela- provided by Bremer (1994) and largely maintained by Lack tionship is as expected, its clustering with representatives of (2006) has since received emendations chiefly concerning the Hypochaeridinae in the nrITS phylogenies (Kilian & al., the prenanthoid (Kilian & Gemeinholzer, 2007; Kilian & al., 2009a; Wang & al., 2013; Fernández-Mazuecos & al., 2016) 2009a) and habitually convergent alpine taxa (Kilian & al., strongly contradicts the morphological and cytological data 2009a; Zhang & al., 2011a, b). The scarcity of non-homoplastic (Wang & al., 2013). It arouses suspicion that the latter results morphological synapomorphies for the lineages classified as may be an artefact, perhaps being caused by long-branch attrac- subtribes (Bremer, 1994) is assumed to have a cause in the tion (Bergsten, 2015) due to a sketchy sampling of taxa of the sudden and rapid diversification of the two largest main clades early- diverging lineages of the C2H2L clade in general, in of
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