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Reconstructing the History of Campanulaceae.Pdf Molecular Phylogenetics and Evolution 52 (2009) 575–587 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Reconstructing the history of Campanulaceae with a Bayesian approach to molecular dating and dispersal–vicariance analyses Cristina Roquet a,b,*, Isabel Sanmartín c, Núria Garcia-Jacas a, Llorenç Sáez b, Alfonso Susanna a, Niklas Wikström d, Juan José Aldasoro c a Institut Botànic de Barcelona (CSIC-ICUB), Passeig del Migdia s. n., Parc de Montjuïc, E-08038 Barcelona, Catalonia, Spain b Unitat de Botànica, Facultat de Ciències, Universitat Autònoma de Barcelona, E-08193 Bellaterra, Catalonia, Spain c Real Jardín Botánico de Madrid (CSIC), Plaza de Murillo, 2, E-28014 Madrid, Spain d Evolutionsbiologiskt centrum, University of Uppsala, Norbyvägen 18D, SE-752 36 Uppsala, Sweden article info abstract Article history: We reconstruct here the spatial and temporal evolution of the Campanula alliance in order to better Received 19 June 2008 understand its evolutionary history. To increase phylogenetic resolution among major groups (Wahlen- Revised 6 May 2009 bergieae–Campanuleae), new sequences from the rbcL region were added to the trnL-F dataset obtained Accepted 15 May 2009 in a previous study. These phylogenies were used to infer ancestral areas and divergence times in Cam- Available online 21 May 2009 panula and related genera using a Bayesian approach to molecular dating and dispersal–vicariance anal- yses that takes into account phylogenetic uncertainty. The new phylogenetic analysis confirms Keywords: Platycodoneae as the sister group of Wahlenbergieae–Campanuleae, the two last ones inter-graded into Bayes-DIVA, Molecular dating a well-supported clade. Biogeographic and dating analyses suggest that Western Asia and the Eastern rbcL trnL-F Mediterranean have played a major role as centers of migration and diversification within the Campanula Campanulaceae alliance, probably in relation to the intense orogenic activity that took place in this region during the Late Campanula Neogene, and that could have promoted isolation and allopatric speciation within lineages. Diversifica- tion rates within several Campanula lineages would have increased at the end of the Miocene, coinciding with the Messinian Stage. Strong selective pressures from climate changes and the expansion of moun- tainous regions during this period are suggested to explain the adaptation to drought, cold or disturbed environments observed in many Campanula species. Several independent long-distance dispersal events to North America are inferred within the Rapunculus clade, which seem to be related to high ploidy levels. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction Multidivtime, Thorne and Kishino, 2002; Relaxed Phylogenetics, Drummond et al., 2006). Phylogenetic reconstruction is nowadays an important tool for Similarly, new biogeographical methods that allow incorporat- biologists to understand the processes governing organismal evo- ing the errors usually associated with phylogenetic and ancestral lution. One aspect that has grown in importance is the reconstruc- area reconstruction into the biogeographic inference have been tion of divergence times and past biogeographical ranges. This is developed (e.g., Ree et al., 2005; Moore et al., in press; Ree and reflected in the plethora of new methods developed to infer the Smith, 2008; Sanmartín et al., 2008). Current analytical methods, spatial and temporal evolution of organisms (Sanderson, 2002; including the widely popular dispersal–vicariance analysis method Thorne and Kishino, 2002; Ree et al., 2005; Drummond et al., (DIVA, Ronquist, 1996, 1997), reconstruct biogeographic patterns 2006). Dating methods have evolved from the strict-molecular on a fixed, fully resolved tree, thus ignoring the uncertainty in phy- clock (Zuckerkandl and Paulin, 1965) to more realistic methods logenetic reconstruction (Ronquist, 2004). This requirement can be that use a ‘‘relaxed clock” approach, which models the rate varia- problematic, since phylogenetic hypotheses are usually not fully tion among lineages (e.g., Penalized Likelihood, Sanderson, 2002; resolved (i.e. polytomies) and may contain nodes that are better supported than others. Recently, Nylander et al. (2008) have proposed a new Bayesian * Corresponding author. Address: Institut Botànic de Barcelona (CSIC-ICUB), Passeig del Migdia s. n., Parc de Montjuïc, E-08038 Barcelona, Catalonia, Spain. Fax: approach to dispersal–vicariance analysis (Bayes-DIVA) that aver- +34 932890614. ages DIVA biogeographical reconstructions over a Bayesian sample E-mail addresses: [email protected], [email protected] of trees reflecting the relative confidence (credibility values) on the (C. Roquet), [email protected] (I. Sanmartín), [email protected] different clades in the phylogeny. This method has the advantage (N. Garcia-Jacas), [email protected] (L. Sáez), [email protected] (A. Susanna), that it allows uncertainty in phylogenetic relationships to [email protected] (N. Wikström), [email protected] (J.J. Aldasoro). 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.05.014 576 C. Roquet et al. / Molecular Phylogenetics and Evolution 52 (2009) 575–587 influence ancestral area reconstructions, sometimes helping to re- natural. These studies show that the tribe Platycodoneae (includ- duce biogeographic uncertainty by favoring some areas (with high- ing all the genera with colpate or colporate pollen) is the sister er marginal probability) over others (Nylander et al., 2008). This is group of the tribes Wahlenbergieae and Campanuleae, which con- the first time that this approach is applied to a group of plants. stitute together a well-supported clade (Cosner et al., 2004). Recent The Campanulaceae sensu stricto comprise about 600–950 spe- works about the phylogenetic relationships of the genus Campanu- cies and 35–55 genera, and their allied families are the Lobeliaceae, la and allied genera (Eddie et al., 2003; Cosner et al., 2004; Roquet Cyphiaceae, Cyphocarpaceae, Nemacladaceae, Pentaphragmata- et al., 2008) have shown that the tribe Campanuleae sensu Yeo ceae, and Sphenocleaceae (Cosner et al., 2004). All these families (1993) should include also Edraianthus DC., which was originally are grouped as Campanulaceae sensu lato by some authors. The placed in Wahlenbergieae (Schönland, 1889) because of its irregu- Campanulaceae s. str. have a nearly cosmopolitan distribution lar fruit dehiscence. Following these studies, here we consider that (Fig. 1). Campanula L. is the largest genus of the family, with c. Platycodoneae includes the genera with sepals alternating with 350–500 species inhabiting a wide range of habitats in the North- carpels and colpate or colporate pollen, while Wahlenbergieae ern Hemisphere (Fedorov, 1957). It is mainly distributed in Eurasia, and Campanuleae show opposite sepals and porate pollen (Dunbar, and poorly represented in North America and Africa. A large con- 1975; Thulin, 1975; Yeo, 1993; Cosner et al., 2004). centration of Campanula species is found in the Eastern Mediterra- According to previous studies (Eddie et al., 2003; Shulkina et al., nean region and the Caucasus (Fig. 1). 2003; Cosner et al., 2004; Roquet et al., 2008; Stefanovic et al., Taxonomic treatments within Campanulaceae differ depending 2008), Campanula is paraphyletic in its current generic circum- on the author (see Cosner et al., 2004 for a review). Schönland scription, with many satellite genera nested within it. Campanula (1889) defined three subtribes based on ovarian characters. Kov- appears divided into two main clades: a large core of Campanula anda (1978) followed this classification. Later, Yeo (1993) up- species that includes related genera (Adenophora Fisch., Asyneuma graded these to tribal rank: Campanuleae, Wahlenbergieae and Griseb. and Schenk, Azorina Feer, Campanulastrum Small, Diosphae- Platycodoneae. The tribe Campanuleae differs from tribes Wahlen- ra Feer, Edraianthus, Githopsis Nutt., Hanabusaya Nakai, Heteroc- bergieae and Platycodoneae in that the ovary is inferior and the odon Nutt., Legousia Durand, Michauxia L’Hér., Petromarula Vent. capsule dehisces at the sides (indehiscent in few cases), while in ex R. Hedw., Physoplexis Schur, Phyteuma L., Trachelium L. and Tri- Wahlenbergieae the capsule dehisces at the top. In Platycodoneae odanis Raf.), plus a clade constituted by Musschia Dumort. and the carpels alternate with the sepals (Yeo, 1993). Following this two Campanula species (Eddie et al., 2003; Roquet et al., 2008). classification, Platycodoneae is monotypic, including only Platyc- Characters related to flower morphology have proven to be of little odon. However, Thulin (1975) suggested that all taxa with colpo- usefulness in the natural delimitation of the group, as they are rate or colpate grains related to Campanula should be included probably under strong selective pressures from pollinators (Roquet also in Platycodoneae: (Campanumoea Blume, Canarina L., Codonop- et al., 2008). Fruit dehiscence has also been used as a diagnostic sis Wall., Cyananthus Wall. ex Benth., Leptocodon Lem. and Platyc- character by some authors, but Kolakovsky (1986) and Stefanovic odon A. DC.). Recent phylogenetic analyses based on ITS-DNA et al. (2008) have shown that this character is homoplasic. sequence data (Eddie et al., 2003) and cpDNA gene order (Cosner There has been considerable debate regarding the
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