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Dated Historical Biogeography of the Temperate Lohinae (Poaceae, Pooideae) Grasses in the Northern and Southern Hemispheres

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Dated Historical Biogeography of the Temperate Lohinae (Poaceae, Pooideae) Grasses in the Northern and Southern Hemispheres -<'!'%, -^,â Availableonlineatwww.sciencedirect.com --~Î:Ùt>~h\ -'-'^ MOLECULAR s^"!! ••;' ScienceDirect PHJLOGENETICS .. ¿•_-;M^ EVOLUTION ELSEVIER Molecular Phylogenetics and Evolution 46 (2008) 932-957 ^^^^^^^ www.elsevier.com/locate/ympev Dated historical biogeography of the temperate LoHinae (Poaceae, Pooideae) grasses in the northern and southern hemispheres Luis A. Inda^, José Gabriel Segarra-Moragues^, Jochen Müller*^, Paul M. Peterson'^, Pilar Catalán^'* ^ High Polytechnic School of Huesca, University of Zaragoza, Ctra. Cuarte km 1, E-22071 Huesca, Spain Institute of Desertification Research, CSIC, Valencia, Spain '^ Friedrich-Schiller University, Jena, Germany Smithsonian Institution, Washington, DC, USA Received 25 May 2007; revised 4 October 2007; accepted 26 November 2007 Available online 5 December 2007 Abstract Divergence times and biogeographical analyses liave been conducted within the Loliinae, one of the largest subtribes of temperate grasses. New sequence data from representatives of the almost unexplored New World, New Zealand, and Eastern Asian centres were added to those of the panMediterranean region and used to reconstruct the phylogeny of the group and to calculate the times of lineage- splitting using Bayesian approaches. The traditional separation between broad-leaved and fine-leaved Festuca species was still main- tained, though several new broad-leaved lineages fell within the fine-leaved clade or were placed in an unsupported intermediate position. A strong biogeographical signal was detected for several Asian-American, American, Neozeylandic, and Macaronesian clades with dif- ferent aifinities to both the broad and the fine-leaved Festuca. Bayesian estimates of divergence and dispersal-vicariance analyses indicate that the broad-leaved and fine-leaved Loliinae likely originated in the Miocene (13 My) in the panMediterranean-SW Asian region and then expanded towards C and E Asia from where they colonized the New World. Further expansions in America (10-3.8 My) showed a predominant migratory route from North to South (N America <-> the Andes <-> Patagonia). This late Tertiary scenario of successive col- onizations and secondary polyploid radiations in the southern hemisphere from the northern hemisphere was accompanied by occasional transcontinental long-distance dispersal events between South America and New Zealand. Multiple Pliocene dispersal events (3.6- 2.5 My) from the near SW European and NW African continents gave rise to the Macaronesian Loliinae flora, while a more recent Pleis- tocene origin (2-1 My) is hypothesized for the high polyploid lineages that successfully colonized newly deglaciated areas in both hemispheres. © 2007 Elsevier Inc. All rights reserved. Keywords: Biogeography; Divergence times; ITS and /•TF; Loliinae; Northern and southern hemisphere dispersals; Past reticulate history 1. Introduction et al., 2001), in contrast to that of oceanic islands for which long-distance dispersals have been compulsory prior to The theory of evolution for most of the continental bio- local radiations (Wagner and Funk, 1995; Francisco-Orte- tas has been largely based on vicariance and speciation ga et al., 1996). However, recent biogeographical studies caused by geographical or genetic barriers (Raven and have demonstrated that transcontinental dispersals have Axelrod, 1972, 1974; Morrone and Crisci, 1995; Sanmartin been more common than previously thought and that those events have affected a large number of angiosperm lineages (Soreng, 1990; Vargas et al., 1998; Vijverberg et al., 1999; * Corresponding author. Fax: +34 974 239302. Colcman ct al., 2003; Blattner, 2006). These biogeographi- E-mail address: [email protected] (P. Catalán). cal patterns sccm to have Occurred in the northern 1055-7903/$ - see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2007.11.022 L.A. Inda et al. /Molecular Phylogenetics and Evolution 46 (2008) 932-957 933 hemisphere where species relationships are more complex 2. Material and methods and highly reticulate (Wendel et al., 1995; Coleman et al., 2003) as well as in the southern hemisphere where the spe- 2.1. DNA sampling and sequencing cies appear more geographically structured (Baum et al., 1998; Sanmartín and Ronquist, 2004). Compiled data indi- Our sampling scheme was designed to cover those taxo- cate that the overwhelming predominance of long-distance nomic and geographic Loliinae groups that were underrep- dispersals over vicariances detected in austral plants, con- resented in previous analyses, especially from the New trary to those observed in animals, might have been caused World and the southern hemisphere, and to build on previ- by the accumulation of those recent events in terminal taxa ous studies (Torrecilla et al., 2004; Catalán et al., 2004). that could have obscured a deeper vicariance signal or just Seventy-eight taxa from North and South America (43), correspond to young-age lineages (Sanmartín and Ron- New Zealand (9), Eastern Asia (4) and the panMediterra- quist, 2004). The biogeography of any angiosperm group nean region (22) were incorporated in the study totaling should therefore be shaped within a timescale frame, allow- 176 taxa in the present data set. Some taxa were repre- ing one to unravel the overlapping histories of those groups sented by more than one sample (totalhng 186 samples). which commonly spanned the Tertiary and the Quaternary Sampling was enlarged with 10 representatives of the clo- ages (Wikström et al., 2001; Bell et al., 2005). sely related subtribes Parapholiinae/Cynosurinae (8) and Subtribe Loliinae, one of the largest groups of temperate Dactylidinae (2), and with 10 representatives of the more grasses, is presently distributed in all continents except Ant- distant subtribes Poinae plus Puccinellinae (2) and tribes arctica (Catalán, 2006). The largest genus of the Loliinae, Aveneae (5), Seslerieae (1), Triticeae (1) and Brachypodieae Festuca, encompasses more than 500 species which are wide- (1) as outgroups. Our selection of Loliinae included 130 spread in the holarctic region but also inhabit cool and tem- Festuca taxa corresponding to the seven major subgenera perate areas in the southern hemisphere. Species of Festuca (out of 11; c. 70% of the total) and 22 sections, 14 Vulpia grow in a large variety of different habitats, from wetlands taxa corresponding to the five sections recognized in this to xeric ecosystems, and are especially well adapted to genus, four taxa of Lolium, and eight taxa of other Loliinae extreme conditions in mountains, and arctic and subantarc- genera (see Supplementary data in Table 1). Both fresh and tic areas. Based on its large taxonomic diversity and wide herbarium materials were collected for this study, and 119 geographical and ecological amplitude, different authors samples analyzed in our previous surveys (Catalán et al., have speculated on the putative ancient origin of Festuca 2004) were incorporated and used in the analysis. System- and postulated an evolutionary trend from more basal atic emendations followed those indicated in Catalán et al. broad-leaved lineages to more advanced fine-leaved lineages (2007), Müller and Catalán (2006) and Catalán (2006) (Hackel, 1882; Holub, 1984; Tzvelev, 1971). However, no though several New World and New Zealand taxa have attempt has been made to estimate the ages of those lineages. not been reahgned. Species of Festuca show an intricate history of past and DNA isolation and sequencing of the nuclear ribo- recent hybridization and polyploidization (Jauhar, 1975; somal ITS region, which included the ITSl spacer, the Catalán, 2006, and references therein), including interge- 5.8S gene, and the ITS2 spacer, and of the plastid ir«TL neric crosses with other Loliinae (Ainscough et al., 1986; and trnLF regions, which included the trnTL spacer and Jauhar, 1993), that might obscure the recovery of diver- the trnL intron, and the trnhF spacer, respectively, fol- gence ages and geographical scenarios. Nonetheless, the lowed the procedures indicated in Catalán et al. (2004). recovered phylogenies have mostly shown a congruent sys- One hundred and sixty three new trnTh, 70 new trnLF tematics-based resolution (Catalán et al., 2004; Catalán, and 60 new ITS sequences have been deposited in Gen- 2006). Our study aims at analyzing the biogeography of Bank. ITS and trnLF sequences of nine and seven taxa, Loliinae, one of the largest and most ecologically and eco- respectively, were retrieved from GenBank and incorpo- nomically important groups of temperate grasses, within a rated into the phylogenetic analysis (Table 1). The final temporal and geological framework. Loliinae have been data matrices consisted of 176 ITS sequences, 178 trnJF traditionally considered to be of very recent, possibly late sequences, and 183 trnLF sequences. A concatenated plas- Miocene origin (Charmet et al., 1997). However, fossil tid data matrix of 188 samples was constructed; 171 sam- studies (Linder, 1987; Jacobs et al., 1999; Prasad et al., ples included both trnTF and trnLF, whereas 17 included 2005) support the past existence of open-habitat Pooi- only one of the two regions. A combined trnTL/lTS data deae-like grasses in the boundaries between the Mesozoic set was created by union of the concatenated plastid and the Cenozoic. Properly dated historical scenarios need trnTL region and the ITS region for 157 samples for to be reconstructed for the Loliinae that are based on more which both sequences were available. Sequences were first
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