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Phylogenetic–Phylogenomic Approach for Species Tree Estimation in African Agama Lizards with Applications to Biogeography, Character Evolution, and Diversification

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Phylogenetic–Phylogenomic Approach for Species Tree Estimation in African Agama Lizards with Applications to Biogeography, Character Evolution, and Diversification Molecular Phylogenetics and Evolution 79 (2014) 215–230 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev A hybrid phylogenetic–phylogenomic approach for species tree estimation in African Agama lizards with applications to biogeography, character evolution, and diversification a, b,c a b d Adam D. Leaché ⇑, Philipp Wagner , Charles W. Linkem , Wolfgang Böhme , Theodore J. Papenfuss , Rebecca A. Chong e, Brian R. Lavin f, Aaron M. Bauer c, Stuart V. Nielsen g, Eli Greenbaum h, Mark-Oliver Rödel i, Andreas Schmitz j, Matthew LeBreton k, Ivan Ineich k, Laurent Chirio k, Caleb Ofori-Boateng l, Edem A. Eniang m, Sherif Baha El Din n, Alan R. Lemmon o, Frank T. Burbrink p a Department of Biology & Burke Museum of Natural History and Culture, University of Washington, Seattle, WA 98195-1800, USA b Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D53113 Bonn, Germany c Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, PA 19085, USA d Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720, USA e Department of Biology, Colorado State University, Fort Collins, CO 80523-1878, USA f Department of Biology, Sonoma State University, Rohnert Park, CA 94928, USA g Department of Biology, Box 1848, University of Mississippi, University, MS 38677, USA h Department of Biological Sciences, University of Texas at El Paso, 500 West University Ave., El Paso, TX 79968, USA i Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity, 10115 Berlin, Germany j Department of Herpetology and Ichthyology, Natural History Museum of Geneva, C.P. 6434, CH-1211, Geneva 6, Switzerland k Muséum National d’Histoire Naturelle, Départment Systématique et Evolution (Reptiles), ISYEB (Institut Systématique, Evolution, Biodiversité, UMR 7205 CNRS/EPHE/MNHN), Paris, France l Forestry Research Institute of Ghana, P.O. Box 63, Fumesua, Kumasi, Ghana m Department of Forestry and Wildlife, University of Uyo, Akwa Ibom State, Nigeria n Nature Conservation Sector, Egyptian Environmental Affairs Agency, 3 Abdalla El Katib, Apt. 3, Dokki, Cairo, Egypt o Department of Scientific Computing, Florida State University, Dirac Science Library, Tallahassee, FL 32306-4102, USA p Department of Biology, The College of Staten Island, The City University of New York, Staten Island, NY 10314, USA article info abstract Article history: Africa is renowned for its biodiversity and endemicity, yet little is known about the factors shaping them Received 18 February 2014 across the continent. African Agama lizards (45 species) have a pan-continental distribution, making Revised 24 May 2014 them an ideal model for investigating biogeography. Many species have evolved conspicuous sexually Accepted 14 June 2014 dimorphic traits, including extravagant breeding coloration in adult males, large adult male body sizes, Available online 25 June 2014 and variability in social systems among colorful versus drab species. We present a comprehensive time-calibrated species tree for Agama, and their close relatives, using a hybrid phylogenetic–phyloge- Keywords: nomic approach that combines traditional Sanger sequence data from five loci for 57 species (146 sam- Africa ples) with anchored phylogenomic data from 215 nuclear genes for 23 species. The Sanger data are Agamidae * Anchored phylogenomics analyzed using coalescent-based species tree inference using BEAST, and the resulting posterior distribu- Next-generation sequencing tion of species trees is attenuated using the phylogenomic tree as a backbone constraint. The result is a Sequence capture time-calibrated species tree for Agama that includes 95% of all species, multiple samples for most species, Xenagama strong support for the major clades, and strong support for most of the initial divergence events. Diver- sification within Agama began approximately 23 million years ago (Ma), and separate radiations in South- ern, East, West, and Northern Africa have been diversifying for >10 Myr. A suite of traits (morphological, coloration, and sociality) are tightly correlated and show a strong signal of high morphological disparity within clades, whereby the subsequent evolution of convergent phenotypes has accompanied diversifi- cation into new biogeographic areas. Ó 2014 Elsevier Inc. All rights reserved. Corresponding author. ⇑ E-mail address: [email protected] (A.D. Leaché). http://dx.doi.org/10.1016/j.ympev.2014.06.013 1055-7903/Ó 2014 Elsevier Inc. All rights reserved. 216 A.D. Leaché et al. / Molecular Phylogenetics and Evolution 79 (2014) 215–230 1. Introduction 2. Materials and methods African Agama lizards are among the most diverse and wide- 2.1. Sanger data spread terrestrial squamates in Africa, making them an ideal group for investigating biogeography and conducting comparative eco- 2.1.1. Molecular methods logical and evolutionary studies (Leaché et al., 2009; Geniez Our taxonomic sampling within Agama includes 95% of the et al., 2011; Gonçalves et al., 2012; Mediannikov et al., 2012). Some described valid taxa (43 of 45 taxa, including described species Agama exhibit extreme sexual dimorphism, and extravagant adult and subspecies) and multiple samples for most species (116 spec- male breeding coloration is among the most conspicuous traits in imens total; average = 2.7 samples/species). Outgroups include six the genus (Wagner et al., 2011). Species with brilliantly colored genera belonging to the African/West Asian Agamidae clade males are also usually larger in size compared to females, but adult (Acanthocercus, Laudakia [recently recognized as Stellagama], male body sizes in Agama can vary widely in maximum snout–vent Phrynocephalus, Pseudotrapelus, Trapelus, and Xenagama), and length (SVL) from small A. gracilimembris (47 mm) in West Africa Calotes versicolor from the South Asian sister clade (Macey et al., and the Sahel to large A. caudospinosa (133 mm) in East Africa. 2000, 2006) is used to root phylogenetic trees when necessary. A Social systems are also variable within Agama, with some species total of 146 specimens representing 57 species are included in forming colonies composed of a single male with many females, the phylogenetic analyses (Table 1). whereas males of some species are solitary. This suite of traits is We collected traditional multilocus data using Sanger sequenc- assumed to be the result of sexual selection, and in this study we ing to obtain nearly complete taxonomic coverage with multiple quantify the correlations among these characters, and investigate samples within species. The Sanger data includes five loci: mito- the evolution of these traits in relation to phylogeny, biogeography chondrial DNA (mtDNA) and four single copy protein coding and diversification. nuclear genes. The mtDNA data (1207 aligned base pairs) includes Comparative genomics data are becoming increasingly easy to fragments of the 16S rRNA gene (16S), the ND4 protein-coding obtain for molecular phylogenetic studies of non-model organisms gene (ND4), and the adjacent histidine, serine, and leucine tRNA (reviewed by Lemmon and Lemmon, 2013; McCormack et al., genes (tRNAs). The nuclear genes (2793 aligned base pairs) include 2013). Sequence capture approaches (also referred to as hybrid neurotrophin-3 (NT3), oocyte maturation factor Mos (CMOS), pinin enrichment) are emerging as a popular option for obtaining phy- gene (PNN), and RNA fingerprint protein 35 (R35). Molecular lab logenomic data, because they can provide data capable of resolving protocols for Sanger sequencing follow Leaché et al. (2009), and difficult phylogenetic problems at deep (Crawford et al., 2012) and primer sequences are provided in Table 2. shallow levels (Smith et al., 2014). Sequence capture methods use short probes (60–120 base pairs) to hybridize to specific genomic 2.1.2. Alignment and partitioning regions that are then isolated and sequenced using next-genera- Multiple sequence alignments were estimated for the indel-rich tion sequencing (Gnirke et al., 2009). Competing techniques for 16S and tRNAs using SATé v2.0.3 (Liu et al., 2011). SATé uses max- sequence capture exploit different aspects of the genome for probe imum likelihood (ML) to estimate phylogenetic trees and multiple hybridization, including ultraconserved elements (Faircloth et al., sequence alignments simultaneously using a divide-and-conquer 2012), conserved regions (Lemmon et al., 2012), or protein-coding realignment technique, which can boost alignment accuracy sub- genes (Li et al., 2013). Regardless of which genomic regions are stantially (Liu et al., 2009). Initial alignments were generated using exploited for hybridization, the approach offers genome-wide sam- ClustalW v2.0.12 (Thompson et al., 1994), and subsequent align- pling of large numbers of loci. ment refinement steps in SATé used MUSCLE v3.8 (Edgar, 2004a, A current challenge in molecular phylogenetics is the integra- 2004b) in conjunction with ML trees estimated with RAxML tion of phylogenomic data with traditional multilocus data (‘‘San- v7.2.6 (Stamatakis, 2006) under the GTRGAMMA model. SATé ger’’ data). The dimensions of the data matrices are typically was run for 12 h with default parameter values. transposed in terms of numbers of samples and numbers of loci, The molecular genetic data were partitioned into 17 distinct with the phylogenomic data containing hundreds of loci for rela- data blocks including 15 blocks for the 1st, 2nd, and 3rd codon tively few samples, whereas Sanger
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