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Insights in the Evolution of Neotropical Bamboos Bol.Soc.Bot.Méx. 88:67-75 (2011) BIOGEOGRAFÍA BIOGEOGRAPHY AND DIVERGENCE TIME ESTIMATES OF WOODY BAMBOOS: INSIGHTS IN THE EVOLUTION OF NEOTROPICAL BAMBOOS EDUARDO RUIZ-SANCHEZ Instituto de Ecología, A. C. Actual adcription: University of California, Berkeley email: [email protected] Abstract: The Neotropical woody bamboos are a monophyletic lineage with three subtribes in the Bambusoideae: Arthrostyli- diinae, Chusqueinae and Guaduainae. The geographical distribution of these subtribes extends from Mexico, Central America, Caribbean Islands, to South America. In order to understand the biogeographical patterns and origin of these bamboos, a phy- logeny of Neotropical woody bamboos was first inferred. Then divergence time estimation of particular nodes using a Bayesian approach and ancestral area reconstruction using S-DIVA were performed. The results suggest a Miocene origin of Neotropical bamboos where the subtribe Chusqueinae was the oldest, followed by the Arthrostylidiinae and the Guaduinae. The ancestral area reconstruction indicated a complex scenario in which the ancestral area for Chusqueinae was Andean South America followed by multiple dispersal events to Atlantic Brazil and Mesoamerica. Overall, the results support the hypothesis of a South American ori- gin of the Neotropical woody bamboos, corroborated by the molecular dating, ancestral area reconstruction and the fossil record. Keywords: Andes, Atlantic forests, Mesoamerica, Neotropical woody bamboos, South America. Resumen: Los bambúes leñosos Neotropicales son un linaje monofilético dentro de Bambusoideae con tres subtribus: Arthro- stylidiinae, Chusqueinae y Guaduinae. La distribución geográfica de éstas va desde México, Centroamérica, Islas del Caribe hasta Sudamérica. Para entender los patrones biogeográficos y el origen de estos bambúes se realizó un análisis filogenético. Posterior- mente las estimaciones de los tiempos de divergencia de nodos particulares bajo una aproximación Bayesiana y la reconstrucción de las áreas ancestrales utilizando S-DIVA fueron realizadas. Los resultados sugieren un origen en el Mioceno para los bambúes Neotropicales, donde la subtribu Chusqueinae fue la más antigua, seguida de Arthrostylidiinae y Guaduinae. La reconstrucción de las áreas ancestrales, indican un escenario complejo donde el área ancestral para Chusqueinae fueron Los Andes, seguido de múltiples eventos de dispersión hacia el bosque Atlántico y Mesoámerica. Los resultados soportan la hipótesis de un origen Sudamericano para los bambúes Neotropicales, corroborado por la datación molecular, la reconstrucción del área ancestral y el registro fósil. Palabras clave: Andes, bambúes leñosos Neotropicales, bosque Atlántico, Mesoámerica, Sudamérica. he bamboo subfamily (Bambusoideae) is one of the thir- Ehrhartoidaeae (rice subfamily) (see also GPWG, 2001). Tteen known subfamilies in Poaceae (GPWG, 2001; Sán- Bouchenak-Khelladi et al. (2008) found that the bamboo chez-Ken et al., 2007; Bouchenak-Khelladi et al., 2008). subfamily is monophyletic but found paraphyly in the Bam- Comprising 80-90 genera and more than 1,500 species buseae (woody bamboos), while the Paleotropical and Neo- distributed world wide except in the Antarctica and Europe tropical woody bamboos are sister to the Olyreae (herba- (McClure, 1966; Soderstrom and Ellis, 1987; Judziewicz et ceous bamboos), and this clade sister to temperate woody al., 1999; Ohrnberger, 1999), bamboos grow from see level bamboos. These results were later confirmed by a multi-gene up to 4,000 m in altitude and are economically important in phylogeny of the Bambusoideae (Sungkaew et al., 2009). Asia and South America (Judziewicz et al., 1999; Bystria- In the paraphyletic woody bamboos with nine recognized kova et al., 2003). subtribes, only three subtribes, (Chusquineae, Guaduinae The latest molecular phylogeny of Poaceae (Bouchenak- and Melocanniinae) have been recovered as monophyletic Khelladi et al., 2008) recovered two main supported clades groups (Kelchner and Clark, 1997; Clark et al., 2007; Ruiz- where the Bambusoideae in the BEP clade is sister to the Sanchez et al., 2008; Fisher et al., 2009; Sungkaew et al., Pooideae (wheat subfamily) and these two are sister to the 2009), and the rest of the subtribes are not monophyletic 67 EDUARDO RUIZ-SANCHEZ groups (Guo et al., 2001, 2002; Guo and Li, 2004; Clark due the Milankovitch cycles caused global changes in the et al., 2007; Yang et al., 2008; Bouchenak-Khelladi et al., distribution of tropical forests during the Cenozoic (Tertia- 2008; Peng et al., 2008; Sungkaew et al., 2009; Triplett and ry-Quaternary) and before (Haffer and Prance, 2001). The Clark, 2010). Andean uplift and the climate change are responsible for The Neotropical woody bamboos form a monophyletic Amazonian forest refugia, where many extant plant and ani- lineage represented by three subtribes: Arthrostylidiinae, mal species probably originated (Haffer and Prance, 2001). Chusqueinae, and Guaduinae (Clark et al., 1995; Judzie- Almost at the same time during the late Miocene in Cen- wicz et al., 1999; Zhang and Clark, 2000; Bouchenak- tral America the migration of the magmatic front from the Khelladi et al., 2008). The subtribe Arthrostylidiinae has 12 Cordillera del Aguacate to the Cordillera Central resulted in genera and more than 157 species and is distributed in South relocation of the Pacific-Caribbean drainage divide, forma- America, Mesoamerica and the Caribbean Islands, from sea tion of the Valle Central basin, and reorganization of fluvial level up to 3,700 m. The Chusqueinae has only one genus, networks (Marshall et al., 2003), making a complex topo- Chusquea, with more than 155 species distributed from graphic scenario for plant divergence. South America was Mexico to Brazil. Chusquea species grow from sea level the primary center of origin for the New World woody bam- up to 4,000 m in altitude and is one of the most speciose boos, and dispersal to Mesoamerica (Central America to genera in the Poaceae. The Guaduinae has five genera and Mexico) occurred after the Panamanian land bridge formed more than 40 species, is distributed from Mexico to Brazil, about 2.8-2.9 Ma (Judziewicz et al., 1999; Bartoli et al., but never grows above 2,500 m in altitude. In some parts of 2005). Mesoamerica (Mexico and Costa Rica) and South America Due to the limited sample of neotropical woody bam- (Brazil and Colombia) species of the three subtribes are boos (three and four respectively) in previous phylogenet- sympatric (Judziewicz et al., 1999). The three Neotropical ic and biogeographic studies (i.e. Sungkaew et al., 2009; subtribes have distributions in three main areas of highest Bouchenak-Khelladi et al., 2010), we used the molecular bamboo diversity and endemism; Brazil, the Northern and data from Kelchner and Clark (1997) and Ruiz-Sanchez Central Andes, and Mexico. Brazil (including the Amazon et al. (2008) to reconstruct a dated phylogenetic tree of basin and the Atlantic forests) has the greatest diversity of the Neotropical woody bamboos. This paper aims to study genera and species, followed by the Andes (Venezuela to the temporal patterns of Neotropical woody bamboos bio- Bolivia), and Mexico and Central America (Soderstrom et geography and temporal evolution: (1) producing a dated al., 1988; Clark, 1990; Judziewicz et al., 1999). phylogenetic tree of the subfamily Bambusoideae and the The Poaceae originated in the late Cretaceous (c. 96 Ma) Neotropical woody lineage, (2) inferring the evolution of and the center origin was either African or South Ameri- geographical range and reconstructing ancestral areas, and can regions of Gondwana, based on three plastid markers (3) inferring biogeographical patterns of dispersal-vicariance and four fossil calibration points (Bouchenak-Khelladi et from South America to Mesoamerica based on fossil and al., 2010). The BEP clade has been inferred to have origi- Yule based divergence estimation and ancestral area recon- nated in the early Eocene in closed habitats in Africa, ac- struction. cording with the results of the ancestral area reconstructions of Bouchenak-Khelladi et al. (2010). The diversification Material and methods of bamboos occurred during the Miocene (23.7 to 5.3) as documented by macrofossils or pollen fossil records (Ber- Phylogeny of the Neotropical woody bamboos. In order to ry, 1929; Thomasson, 1987; Crepet and Feldman, 1991; infer the most complete Neotropical woody bamboo species Worobiec and Worobiec, 2005; Brea and Zucol, 2007; phylogeny, 46 taxa were used. The plastid rpl16 intron was Worobiec et al., 2009). However, the crown node of the used to infer the phylogeny, the sequences were Genbank Bambusoideae originated 30 Ma in the middle Oligocene downloaded <http://www.ncbi.nlm.nih.gov/genbank/> (Bouchenak-Khelladi et al., 2010). Clark (1997) proposed (consulted August 25 2010) following the previous phyloge- that the woody bamboos, arose in the Southern Hemisphere netic analyses of Kelchner and Clark (1997) and Ruiz-San- in lowland, tropical areas and then radiated into tropical chez et al. (2008). Bayesian analyses were conducted using montane habitats. MrBayes 3.2.1 (Huelsenbeck and Ronquist, 2001; Ron- The uplift of the Andean in the Miocene had a profound quist and Huelsenbeck, 2003). First, jMODELTEST.0.1.1 impact on the history of South America; it changed the (Posada, 2008) was run to identify the model of evolution course of the Amazon river system from northwestwards using the AIC values. The best model for the rpl16 intron
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