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Species Delimitation of the Orchard-Spider

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Species Delimitation of the Orchard-Spider Species Delimitation of the Orchard-spider Leucauge venusta (Araneae, Tetragnathidae), the Phylogeny of Leucauge and the Identification of Orthologous Genes from Transcriptomes by Jes´us Alfonso Ballesteros Ch´avez B.S. in Biological Sciences, December 2006, Instituto Polit´ecnico Nacional M.S. in Biological Sciences, February 2010, Universidad Nacional Aut´onoma de M´exico A Dissertation submitted to The Faculty of The Columbian College of Arts and Sciences of The George Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy May 21, 2017 Dissertation directed by Gustavo Hormiga Ruth Weintraub Professor of Biology The Columbian College of Arts and Sciences of The George Washington University certifies that Jes´us Alfonso Ballesteros Ch´avez has passed the Final Examination for the degree of Doctor of Philosophy as of March 20, 2017 . This is the final and ap- proved form of the dissertation. Species Delimitation of the Orchard-spider Leucauge venusta (Araneae, Tetragnathidae), the Phylogeny of Leucauge and the Identification of Orthologous Genes from Transcriptomes Jes´us Alfonso Ballesteros Ch´avez Dissertation Research Committee: Gustavo Hormiga, Ruth Weintraub Professor of Biology, Dissertation Director Guillermo Ort´ı, Louis Weintraub Professor of Biology, Committee Member Robert Alexander Pyron, Robert F. Griggs Assistant Professor of Biology, Committee Member ii c Copyright 2017 by Jes´us A. Ballesteros Ch´avez All rights reserved iii Dedication In memory of Prof. Alfonso Ch´avez Aguilar. iv Acknowledgments I am extremely grateful to The Department of Biological Sciences for supporting and funding my research and studies through a graduate teaching assistantship and Weintraub and Harlan fellowships. Additional support was provided by the National Science Foundation through the following grants: DEB1144492, DEB114417, DEB1457300, and DEB1457539 to Gustavo Hormiga and Gonzalo Giribet (Harvard University). I am obliged to my research adviser, Dr. Gustavo Hormiga, for sharing his lab, resources, expertise in spider systematics and his very peculiar sense of humor. He was very supportive during my whole doctorate and allowed me to follow my own, and at times unconventional, research interests (up to the point of accepting LATEXdrafts for revision). I am very grateful to current and past members of the Hormiga lab: Thiago da Silva Moreira, Robert (Bob) Kallal, Maya Wolf, Siddarth Kulkarni, Ligia Benavides and Daniela Andriamalala. Thanks for the all the help in the field, discussions, proofreading, troubleshooting, listening PCR frustrations and their friendship. In particular, I am very grateful to Bob for all the help, driving, camping, collecting, navigating during our Leucauge expedition in USA-2014. Thiago has always been a true friend and my partner in crimes (in and out of the lab) during all these years: muito obrigado Thiaginho. I wish to thank all the members of my graduate (g) and dissertation (d) commit- tee: Diana Lipscompgd, James Clarkg, R. Alexander Pyron gd and Hannah Woodd. Their guidance, comments, and suggestions improved the quality of my research and manuscripts. I would like to specially thank Guillermo Ort´ıgd for encouraging my early interest in bioinformatics, inviting me to collaborate in some of his research projects and giving me access to his research computer and lab space. I am indebted to the following colleagues and their institutions for facilitating v specimens through loans and donations: Jeremy Miller (Naturalis, Biodiversity Cen- ter, Netherlands); Alexandre Bonaldo and Regiane Saturnino (Museu Paraense Emilio Goeldi, Brazil); Ricardo Pinto da Rocha and Jimmy Cabra (Universidad de S˜ao Paulo, Brazil); Oscar Francke and Griselda Montiel Parra (Instituto de Biolog´ıa-UNAM, Mexico); Gonzalo Giribet and Laura Leibensperger (Museum of Comparative Zool- ogy, Harvard University); Charles Griswold (California Academy of Sciences); Carlos Viquez (INBIO, Costa Rica), Abel Perez Gonzalez (Museo Argentino de Ciencias Naturales) and Michael Draney (University of Wisconsin). I was privileged to participate in several collecting trips during my doctorate. With my fellow Hormiga-lab members I traveled across the USA with Bob, and to Costa Rica with Thiago and the invaluable assistance of Carlos Viquez. The expedition to the Amazon rainforest (2012) stands out as a unique experience. I want to express my gratitude to Ana Tourinho, Gonzalo Giribet, Cristina Rheims, Lidiane Salvatierra, Williams Porto and Rafael Prezzi Indicatti and Pio Colmenares and Sidclay Dias, Ligia, Gustavo and Thiago for sharing the journey on board of the Uap´e-a¸cu and the city of Manaus. I am also grateful of the computing time in the high performance computer clus- ter of GWU (Colonial one) that made possible many of the analyses I performed during my doctoral research. In particular, Adam Wong was instrumental in making available libraries and programs required during my research. I was very fortunate to share this journey with many colleagues and friends with whom I shared thoughts, rants, laughs and drinks: Andrew and Jackie Thomp- son, Tara Scully, Mariana Abarca, Pablo Frank, Sanghamitra Singh, Cristina Rade, Joseph Stiegler, Lily Hughes, Jo˜ao Tonini and Larissa Rozindo, Laura Skipper, An- drew Moore, Cat Hendry, Bonnie Lu, Dahiana Arcila, Ricardo Betancur, Daniela Campanella, Dominic White, and Jimmy Munoz. And my extended family in the US: Nawa, Rob, Yos, Cindy, Ella, Aki, Koji, Masano, Eric, Beth (plus new baby), vi Volkan, Preethi, Jason, Chandini and Mrinali. I am (and so is Bel) thankful to Sandra Lara and Thiago for opening the doors of their house, and welcome us as family, during the last stretch of this journey in the DC area. Thanks for the meals together, beers, rants, dances, walks, hot sauces, patience and overall awkwardness. And at last, I wish to thank my parents (Daniel and Patricia), my siblings (Monica and Daniel) and above everyone Bel´en. vii Abstract of Dissertation Species Delimitation of the Orchard-spider Leucauge venusta (Araneae, Tetragnathidae), the Phylogeny of Leucauge and the Identification of Orthologous Genes from Transcriptomes The genus Leucauge (Tetragnathidae, Leucauginae) includes 174 described species from the tropical and subtropical regions of all continents with the exception of Europe and Antarctica. In this dissertation, evolutionary questions at different hierarchical levels are explored using the spider genus Leucauge as case study. At the microevo- lutionary scale, we test the species boundaries of the North American orchard spider Leucauge venusta using two genetic markers. The analyses clearly separate USA pop- ulations in two deeply divergent and geographically structured groups (North-South) We restrict the name L. venusta to the Northern clade and remove L. argyrobapta from its synonymy for the southern clade. We present the first attempt to unravel the phylogenetic relationships within this genus and their placement within Leucauginae based on traditional PCR targeted sequences from five loci commonly used in spider systematics plus Histone H4, used for the first time in spider phylogenetics. We in- clude an assessment of the informativeness of the standard markers and test for base composition biases in the dataset. The results suggest Leucauge is not monophyletic as it includes species currently placed in the genera Opas, Opadometa, Mecynometa and Alcimosphenus. Evolutionary studies in spiders have been limited to comparisons of a relatively small number of genetic markers. At the same time, high throughput sequencing technologies are making available large amount of data which can poten- tially be used in the search of orthologous loci of utility in spider phylogenetics. We present a bioinformatic pipeline, including a new phylogenetic orthology criterion, to find orthologous gene groups from a collection of anonymous genomic sequences. The pipeline is demonstrated on a trivial gene family tree using vertebrate hemoglobins, a small dataset from insect genomes and collection of 27 spider transcriptomes includ- viii ing Leucauge venusta. Using this new method, we were able to identify thousands of orthologous loci potentially useful for spider phylogenetics. ix PhylogeographyandIBD. 19 EcologicalNicheModeling . 20 Results...................................... 21 SpeciesdelimitationAnalyses . 21 Phylogeography andisolationbydistance . 24 Phylogenetic structure and dated phylogeny . 28 Ecologicalnichemodels. 30 Nicheequivalencecomparisons. 33 Taxonomicchanges............................... 33 Taxonomy.................................... 36 Discusion .................................... 39 Speciesdelimitation............................ 39 IBD .................................... 40 Phylogeneticstructure . 42 Ecologicalmodelsandnicheequivalence . 43 Conclusion.................................... 44 Chapter 3: Molecular phylogeny of the orb-weaving spider genus Leucauge and the intergeneric relationships of Leu- cauginae (Araneae, Tetragnathidae) 45 Abstract..................................... 45 Introduction................................... 45 The taxonomic history and current status of the genus Leucauge . 46 Previousphylogeneticwork . 48 MaterialandMethods ............................. 50 Taxonsamplingandspecimenacquisition. 50 DNAamplificationandsequencing . 55 Model selection and base composition homogeneity test . 56 xi Phylogeneticinformativeness. 57 Phylogenetic analyses and dated phylogeny . 57 Timecalibration ............................
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