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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Molecular Phylogenetics and Evolution 62 (2012) 263–274 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny, diversification rates and species boundaries of Mesoamerican firs (Abies, Pinaceae) in a genus-wide context Érika Aguirre-Planter a,1, Juan P. Jaramillo-Correa a,b,1, Sandra Gómez-Acevedo a, Damase P. Khasa b, ⇑ Jean Bousquet b, Luis E. Eguiarte a, a Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, Apartado Postal 70-275, México, D.F., Mexico b Canada Research Chair in Forest and Enrionmental Genomics, Centre for Forest Research and Institute for Systems and Integrative Biology, Université Laval, Québec, Canada G1V 0A6 article info abstract Article history: The genus Abies is distributed discontinuously in the temperate and subtropical montane forests of the Received 18 May 2011 northern hemisphere. In Mesoamerica (Mexico and northern Central America), modern firs originated Revised 26 September 2011 from the divergence of isolated mountain populations of migrating North American taxa. However, the Accepted 28 September 2011 number of ancestral species, migratory waves and diversification speed of these taxa is unknown. Here, Available online 10 October 2011 variation in repetitive (Pt30204, Pt63718, and Pt71936) and non-repetitive (rbcL, rps18-rpl20 and trnL- trnF) regions of the chloroplast genome was used to reconstruct the phylogenetic relationships of the Keywords: Mesoamerican Abies in a genus-wide context. These phylogenies and two fossil-calibrated scenarios were Biogeography further employed to estimate divergence dates and diversification rates within the genus, and to test the Chloroplast DNA Conifer hypothesis that, as in many angiosperms, conifers may exhibit accelerated speciation rates in the sub- Mexico tropics. All phylogenies showed five main clusters that mostly agreed with the currently recognized sec- Transverse Volcanic Belt tions of Abies and with the geographic distribution of species. The Mesoamerican taxa formed a single Molecular phylogeny group with species from southwestern North America of sections Oiamel and Grandis. However, popula- Diversification rates tions of the same species were not monophyletic within this group. Divergence of this whole group dated back to the late Paleocene and the early Miocene depending on the calibration used, which translated in very low diversification rates (r0.0 = 0.026–0.054, r0.9 = 0.009–0.019 sp/Ma). Such low rates were a con- stant along the entire genus, including both the subtropical and temperate taxa. An extended phylogeo- graphic analysis on the Mesoamerican clade indicated that Abies flinckii and A. concolor were the most divergent taxa, while the remaining species (A. durangensis, A. guatemalensis, A. hickelii, A. religiosa and A. vejari) formed a single group. Altogether, these results show that divergence of Mesoamerican firs coin- cides with a model of environmental stasis and decreased extinction rate, being probably prompted by a series of range expansions and isolation-by-distance. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction the fastest speciation rates are usually attained in taxa with high background substitution rates and that have recently expanded Diversification and speciation rates seem to be higher in taxa into new habitats, while the lowest are most often observed in spe- from tropical or subtropical ecosystems than from temperate or cies with both low substitution and extinction rates, and which in- boreal zones (e.g. Wright et al., 2006; Gillman et al., 2010). Such habit stable environments (Lancaster, 2010). Conifers are slowly differences can be prompted by contrasting patterns of population evolving taxa that should conform to this last low speciation mod- isolation, adaptation speed, extinction rates and/or stochastic el. However, based on morphology, conifer taxa appear to be more events that cause reproductive isolation (e.g. Wright et al., 2006; diversified in the subtropical than in the temperate environments Glor, 2010). For instance, in angiosperms, it has been shown that (Farjon, 1990), which might suggest some kind of divergence accel- eration towards the equator. In subtropical conifers, speciation re- lated to geographical isolation is expected to be a predominant ⇑ Corresponding author. Fax: +52 55 5616 1976. driver for diversification, while slow reproductive isolation should E-mail addresses: [email protected] (É. Aguirre-Planter), jaramillo@ be a delaying factor (e.g. Bouille´ et al., 2011). Thus, it could be ecologia.unam.mx (J.P. Jaramillo-Correa), [email protected] (S. Gómez-Acevedo), hypothesized that the higher number of conifer species observed [email protected] (D.P. Khasa), [email protected] (J. in the subtropics is either the result of accelerated speciation due Bousquet), [email protected] (L.E. Eguiarte). 1 These authors contributed equally to this work. to increased historical isolation, or simply an artifact produced 1055-7903/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2011.09.021 Author's personal copy 264 É. Aguirre-Planter et al. / Molecular Phylogenetics and Evolution 62 (2012) 263–274 by an elevated phenotypic plasticity that has misled experts when 2. Materials and methods describing species based solely on morphological variation (e.g. De Kroon et al., 2005; Prada et al., 2008). 2.1. Sampling and Mesoamerican species The knowledge of diversification rates and speciation pro- cesses are of particular importance in megadiverse countries like Between one and five individuals were collected for 31 Abies Mexico, where the lack of such information collides with the species in natural populations, botanical gardens and arboretums large conservation needs (Callmander et al., 2005). Mexico has (see Table A1). These taxa are naturally distributed in North Amer- approximately 30,000 plant taxa (Rzedowski, 1993), from which ica, Europe and Asia, and represent most of the sections described about 10% are of conservation concern (SEMARNAT, 2010). This by Liu (1971), and Farjon and Rushforth (1989) (Table 1). Sampled species richness has been explained by the habitat variation pro- outgroups included Keteleeria davidiana (Bertrand) Beissner (the duced by a complex geological history (Espinosa-Organista et al., sister genus of Abies) and Larix kaempferi (Lambert) Carrière. 2008; Jaramillo-Correa et al., 2009), which provides ideal condi- For the Mesoamerican firs, sampling was far more extensive in tions for the diversification of the many taxa that expanded from an effort to disentangle their evolutionary and phylogeographic both North and South America during the last 30 million years relationships. Needles were collected from between 10 and 30 (Rzedowski, 1978; Graham, 1999). Conifers were among the first adult cone-bearer trees in 36 populations in both Mexico and Gua- of such temperate elements that arrived into Mexico (i.e. some temala, which covered as much as possible the ranges of the eight 23 Ma; Graham, 1999), and since then, they have become one taxa currently described for this region (Fig. 1, Table A1). These the most diverse and important components of the montane for- taxa include: ests of this country. However, in spite of this, the taxonomic sta- tus of many Mexican conifers remains dubious and has been 1. Abies guatemalensis Rehder. It is the most southerly dis- questioned in different occasions (e.g. Farjon and Rushforth, tributed species of the genus. It forms small-scattered 1989; Farjon, 1990; Strandby et al., 2009). mountain populations between central Mexico and Hon- Firs (Abies Miller; a predominantly temperate northern genus) duras and El Salvador, at altitudes between 2000 and are among the most abundant and less studied taxa of the mon- 4000 m above the sea level (a.s.l.) (Martínez, 1948; Dona- tane forests of Mesoamerica (i.e. Mexico and northern Central hue et al., 1985; Andersen et al., 2006). America). They are represented by eight threatened species, six 2. Abies religiosa (Humboldt, Bonpland et Kunth) Schlechten- of which are endemic to Mexico (Liu, 1971; Farjon and Rush- dal et Chamisso. This taxon is relatively common along the forth, 1989; SEMARNAT, 2010). Their first appearance in the Transverse Volcanic Belt (TVB) in central Mexico, and is Mesoamerican fossil record points to a late arrival in the Plio- distributed in mostly continuous stands between 2000 cene (i.e. about 5 Ma; Graham, 1976, 1999), which implies a and 3500 m.a.s.l. (Martínez, 1948). Populations of this spe- rather rapid diversification after their establishment. However, cies are the preferred overwintering habitat of the mon- it is unclear whether this date correctly
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