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Phylogeny of Chaetanthera (Asteraceae: Mutisieae) Reveals Both Ancient and Recent Origins of the High Elevation Lineages

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Phylogeny of Chaetanthera (Asteraceae: Mutisieae) Reveals Both Ancient and Recent Origins of the High Elevation Lineages Molecular Phylogenetics and Evolution 41 (2006) 594–605 www.elsevier.com/locate/ympev Phylogeny of Chaetanthera (Asteraceae: Mutisieae) reveals both ancient and recent origins of the high elevation lineages Mark A. Hershkovitz a,¤, Mary T.K. Arroyo a,b, Charles Bell c, L. Felipe Hinojosa a,b a Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile b Instituto de Ecología y Biodiversidad (IEB), Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile c School of Computational Science, 150-R Dirac Science Library, Florida State University, Tallahassee, FL 32306-4120, USA Received 1 February 2006; revised 26 April 2006; accepted 2 May 2006 Available online 12 May 2006 Abstract Penalized likelihood analysis of previously published chloroplast DNA (cpDNA) ndhF sequences suggests that the central-southern Andean genus Chaetanthera diverged ca. 16.5 million years (my) ago, well before the uplift of the Andes to their present heights. Penalized likelihood analysis based on new nuclear ribosomal DNA (rDNA) internal transcribed spacer (ITS) sequences indicates that the most relictual lineages occupy high elevation Andean habitats that did not exist until some 10 my later. This result is contrary to the expecta- tion that younger habitats should be occupied by phylogenetically younger lineages. The results are interpreted with respect to the devel- opment of aridity in lowland habitats during the Miocene and Pliocene, which presumably extinguished the lowland relatives of the high elevation taxa or, in eVect, forced them upwards in search of adequate moisture. As the more northerly lineages were being displaced upward, others diversiWed in the mediterranean-type climate area of central Chile, giving rise to additional high elevation taxa again, at an early date, as well as lowland taxa. Some species of Chaetanthera from lowland central Chile appear as the phylogenetically youngest taxa, suggesting secondary adaptation to lowland aridity. At the same time, at least two high elevation species, Chaetanthera peruviana and Chaetanthera perpusilla, appear to have been derived recently from a lower elevation ancestor, while some middle to low elevation taxa seem to have evolved recently out of a high elevation complex. The results suggest that the younger high elevation habitats have served as both “cradle” and “museum” for Chaetanthera lineages. © 2006 Elsevier Inc. All rights reserved. Keywords: Chaetanthera; nrITS; Calibration age; Molecular clock 1. Introduction era of Asteraceae tribe Mutisieae (Bremer, 1994). The high elevation Xora of the western slope of the Andes in Chile The central and southern Andes comprise a continuous alone comprises an estimated 1700 species (Arroyo et al., high mountain range spanning from central Peru and 2004). For the present purposes, high elevation refers to the Bolivia south through Argentina and Chile to Tierra del equivalent of above-treeline or alpine vegetation, a term Fuego. This region harbors a diverse high elevation Xora of that is diYcult to apply in central and northern southern perhaps 3700 species (Arroyo, unpublished data) contain- Andes because of lack of a well-deWned treeline at the driest ing elements that are characteristic of, if not endemic to, latitudes. In the northern part of the central Andes high ele- South America, e.g. Calceolaria (Calceolariaceae; Erhart, vation vegetation occurs between 3000 and 5000 m, 2000), Tropaeolum sect. Chilensia (Tropaeolaceae; Hers- descending to around 1800 and 3000 m heights at mediter- hkovitz et al., 2006), Alstroemeria (Alstroemeriaceae; ranean latitudes in central Chile. Characterization as mid- Muñoz Schick and Moriera Muñoz, 2003), and many gen- elevation refers to plants below treeline or its equivalent along the slopes of the Andes, while lowland refers to * Corresponding author. Fax: +56 2 271 2983. coastal or low valleys below about 300–700 m elevation E-mail address: [email protected] (M.A. Hershkovitz). depending on latitude. 1055-7903/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2006.05.003 M.A. Hershkovitz et al. / Molecular Phylogenetics and Evolution 41 (2006) 594–605 595 Various lines of geological evidence indicate that uplift- analysis. Specimens were identiWed according to Cabrera ing of the central and southern Andes to their current ele- (1937) and more recent publications on particular taxa. In vations occurred between the Pliocene and Pleistocene addition, most identiWcations were veriWed by A. Davies (Arroyo et al., 1988; Farías et al., 2005; Gregory-Wodzicki, (Munich, Germany), who is undertaking a revision of the 2000; Giambiagi, 2003; Hartley, 2003; Irigoyen et al., 2000; genus in collaboration with the second author. Hinojosa and Villagrán, 1997; Simpson, 1983). Collectively, In order to estimate the divergence date of Chaetanthera the data indicate that this region achieved far less to no (see below), chloroplast DNA (cpDNA) ndhF sequences more than one half of its current height by the end of the from Asteridae and Asteraceae listed in Kim et al. (2005) Miocene (Giambiagi, 2003; Gregory-Wodzicki, 2000). and partial ndhF sequences (3Ј end, ca. 1000 bp) listed in Assuming a correlation between the age of a habitat and Kim et al. (2002) were obtained from GenBank and aligned the age of its biota, the geological data implicate a corre- manually. In addition, the sequence of Cornus Xorida (Gen- spondingly recent origin of the central and southern high Bank Accession No. AF130220) was obtained. The align- Andean Xora. In terms of phylogenetic trees, the expecta- ment was trimmed to include only the 3Ј end used in the tion is that the stems of high elevation lineages should be Kim et al. (2002) analysis. Cornus was selected as a calibra- relatively shorter than and nested among those of lower ele- tion point based on an approximate fossil dating, as in vation lineages. Indeed, upward migration of lowland ele- Bremer et al. (2004). ments (Arroyo et al., 1983), along with recent long distance Nuclear ribosomal DNA (rDNA) internal transcribed dispersal of high elevation plants established elsewhere (e.g. spacer (ITS) region sequences were obtained from 82 samples Soltis et al., 2001), have been proposed as important of Chaetanthera following the extraction, ampliWcation, and sources of the high Andean Xora. sequencing protocols described in Hershkovitz (2006). Elimi- Among the taxa endemic to southern South America and nating 19 of the taxonomically duplicated samples, the present well represented in both higher and lower elevations is Chae- analysis is based on 63 samples (Table 1). Some samples did tanthera Ruiz & Pav. (Asteraceae: Mutisieae). As currently not amplify following the extraction protocol and were fur- conceived, Chaetanthera comprises 44 species in seven sub- ther puriWed using Chelex 100 resin (BioRad). 10l of geno- genera (Cabrera, 1937). Subgenus Egania (perennial herbs) is mic DNA is added to 250 l of 5% aqueous Chelex, mixed, restricted to high elevation habitats ranging from central heated at 100°C for 15min, and the supernatant containing Chile and Argentina to Peru and Bolivia. Subgenus Oria- puriWed DNA removed to a new tube. This procedure strum (annuals to short-lived perennials) comprises high and removes heavy metal cations that apparently inhibited the high to mid-elevation species of central Chile and adjacent PCR. Other puriWcation methods (PEG precipitation and/or Argentina. Subgenus Carmelita (perennial herbs) comprise silica-NaI) were tried, but they did not alleviate this inhibition. mostly high elevation species of central Chile and Argentina The resulting ITS sequences were aligned manually. The with occasional populations of some species occurring at sequences included 56 apparently polymorphic sites, usu- mid-elevations. Subgenus Glandulosa (one subshrub) occurs ally C/T, among the total 43,533 aligned sites. These sites in central Chile at mid-elevation to treeline. Subgenera Tyl- were scored as ambiguities (“N”) in the phylogenetic analy- loma (mostly annual) and Euchaetanthera (all annuals) may sis. The polymorphisms are mainly restricted to taxonomi- be found from sea level to high elevations in central Chile, in cally diYcult species. Cloning of polymorphic samples is the Andes in adjacent Argentina, and less frequently in underway and the taxonomic and evolutionary implica- northern Chile, Peru, Bolivia, and southern Argentina. Sub- tions will be considered in a future publication. genus Proselia (perennials) is mostly concentrated in low to Maximum parsimony (MP) and maximum likelihood mid-elevation habitats, including in Araucaria forest clear- (ML) analysis of the ndhF and ITS sequences were under- ings in south-central Chile, just getting into Argentina. Here, taken using PAUP 4.0 (SwoVord, 2002) version b10. The as part of a more comprehensive study into the evolution of MP analysis of the ITS sequences included alignable gaps Chaetanthera, we undertake phylogenetic reconstruction and scored as separate characters. The MP analysis and boot- estimation of divergence dates in order to provide insights strap (500 replicates) were performed using the default heu- into the evolution of the autochthonous central-southern ristic search procedure. For the bootstrap analysis, Andean Xora in relation to the Andean uplift. We Wrst cali- maxtrees was set at 100. For the ML analysis, Modeltest brate the age of Chaetanthera by comparison to other Asteri- (Posada and Crandall,
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