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Phylogenetic Relationships of Orb-Weaving Spiders from Species to Superfamily

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Phylogenetic Relationships of Orb-Weaving Spiders from Species to Superfamily Phylogenetic Relationships of Orb-weaving Spiders from Species to Superfamily by Robert James Kallal B.A. in Political Science, May 2009, Frostburg State University M.S. in Biology, May 2011, Towson University 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 August 31, 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 Robert James Kallal has passed the Final Examination for the degree of Doctor of Philosophy as of June 5, 2017. This is the final and approved form of the dissertation. Phylogenetic Relationships of Orb-weaving Spiders from Species to Superfamily Robert James Kallal Dissertation Research Committee: Gustavo Hormiga, Ruth Weintraub Professor of Biology, Dissertation Director Guillermo Ortí, Louis Weintraub Professor of Biology, Committee Member Robert Alexander Pyron, Robert F. Griggs Assistant Professor of Biology, Committee Member ii © Copyright 2017 by Robert James Kallal. All rights reserved iii Disclaimer New taxon names and nomenclatural changes referred to this dissertation are disclaimed and unavailable for nomenclatural purposes (ICZN Art. 8.3). iv Acknowledgments The author wishes to acknowledge the Department of Biological Sciences, and specifically the Weintraub and Harlan families, for their support throughout the completion of this dissertation via fellowships and teaching assistantships. Additional support was provided by the United States National Science Foundation grants DEB 1144492, 114417, 1457300, and 1457539 to Gustavo Hormiga and Gonzalo Giribet (Harvard University). I would like to thank Gustavo Hormiga for all he has done for me, including guidance, spider expertise, field excursions, conference travel, and pop culture recommendations. One of the only things that did not improve in my time in his lab was my Spanish. I must also acknowledge the other members of the lab, both long term and short, over the course my time here: Jesus Ballesteros, Thiago da Silva Moreira, Ligia Benavides, Siddharth Kulkarni, Daniela Andriamalala, Jimmy Cabra, and Lidianne Salvatierra. I am especially indebted to Chuy after our southeastern USA collecting excursion in 2014 and his guidance in the computational aspects of my dissertation. I would also like to acknowledge my dissertation committee, including Guillermo Ortí, Alex Pyron, Diana Lipscomb, and Hannah Wood, whose comments, critiques, and suggestions undoubtedly improved this work. Also at GWU, I would like to acknowledge Adam Wong and the high performance cluster Colonial One resource, without which much of this work would still be processing. Gonzalo Giribet and his lab warrant special acknowledgment. The resources of Gonzalo and Harvard University made the transcriptome chapter possible. I am indebted v to him and the expertise of his lab, namely Rosa Fernández, Caitlin Baker, Julia Cosgrove, and Vanessa Knutson, for their assistance, patience, and expertise. I would also like to thank Charles Griswold and Lauren Esposito for hosting me at the California Academy of Sciences. The field trip to New Zealand and Australia in early 2016 was the experience of a life time, including Gustavo Hormiga, Gonzalo Giribet, Rosa Fernández, Fernando Álvarez-Padilla, Caitlin Baker, and Miquel Arnedo, as well as Cor Vink, Robert Raven, Barbara Baehr, and Michael Rix. As Gustavo is fond of saying, good on you, mates! Additionally, we acknowledge the following individuals for their contributions from collecting in Taiwan: Prof. Man-Miao Yang (NCHU Insect Collection, Department of Entomology, National Chung Hsing University, Taichung) and her students and staff (Yi- Shuo Liang, Bao-Cheng Lai, Yi-Chuan Li, Chang-Ti Tang, Wesley M. Hunting, Fu-Shen Huang), Dimitar Dimitrov, Charles Griswold, Facundo Labarque, and Daniele Polotow. I would like to acknowledge the following people and institutions for loans for this work: Gonzalo Giribet and Laura Leibensperger (Museum of Comparative Zoology, USA),Charles Griswold, Lauren Esposito, Anthea Carmichael, and Darrel Ubick (California Academy of Sciences, USA), Matjaž Kuntner (Slovenian Academy of Arts and Sciences, Slovenia), Robert Raven and Owen Seeman (Queensland Museum, Australia), Mark Harvey and Julianne Waldock (Western Australia Museum, Australia), Graham Milledge (Australian Museum, Australia), Jon Coddington, Hannah Wood, and Dana de Roche (National Museum of Natural History, USA), Catherine Byrne (Tasmania Museum and Art Gallery, Australia), Peter Lilywhite (Museum Victoria, Australia), Volker Framenau (Phoenix Environmental Sciences), and Jeremy Miller (Naturalis, vi Biodiversity Center, Netherlands). I would also like to acknowledge the following individuals for graciously allowing me to reproduce their photographs: Robert Whyte, Laurence Sanders, and Iain Macaulay. I also would like to acknowledge the following individuals for their support, friendship, comments, and more throughout the last five years: Andrew Moore, Lily C. Hughes, Dominic and Ethel White, Andrew and Jacqueline Thompson, Catriona Hendry, Belen Chavez, Sandra Lara, João Tonini and Larissa Rozindo, Josef Stiegler, Dimitar Dimitrov, Sarah Crews, Dahiana Arcila, Hartmut Doebel, Tara Scully, Rob Donaldson, John LaPolla, Lauren Spearman, and Martin, Jessie, and John Wiener Stolark. Last but not least I must thank my family (Robin and Donald Micheletti; Mark, Mandy, and Jennifer Kallal), and in particular my wife, Laura Kallal, who all now know more about spiders than they ever wanted or thought possible. vii Abstract of Dissertation Phylogenetic Relationships of Orb-weaving Spiders from Species to Superfamily Spiders are a speciose group of arachnids that are a dominant predator of terrestrial arthropods. Among these, perhaps the most iconic are the orb-weavers, which spin webs from silk produced in abdominal glands. Despite steps forward in spider phylogenetics, there are still many undescribed species and a number of difficult problems in understanding their phylogeny that must be remedied before one can understand evolution of morphology and behavior that define these fascinating creatures. In this work, I focus on two families of orb-weavers: Tetragnathidae and Araneidae. First, I discuss the tetragnathid subfamily Metainae, which has not been previously revised, has low support in previous works, and questionable inclusion of certain genera. My target gene analyses on an increased taxon sampling of metaines found good support for the subfamily for the first time, and suggest inclusion of a new genus, Zhinu, from Taiwan. After synonymy of Prolochus and Menosira, I determined there are four genera in Metainae: Zhinu, Meta, Metellina, and Dolichognatha. I also describe a new species of Orsinome with exaggerated genitalic morphology. Second, I revise the Australasian leaf- curling araneid genera Phonognatha and Deliochus using molecular and morphological characters. I place these genera in the wider context of Araneidae, which lacks a family- level treatment. Based on resulting phylogenies, I found evidence for a third genus, Artifex, and monophyly of Araneidae following recent taxonomy changes. Furthermore, this phylogeny allowed me to explore two comparative questions relating to these genera: evolution of leaf retreats in orb-webs and biogeography. I found evolution and subsequent loss of an integrated leaf retreat in these genera, and colonization of New viii Caledonia consistent with geology of the island. Finally, I used next next-generation transcriptome-based techniques to explore the phylogeny of Araneidae, which has been limited by the resolution power of current markers and morphology. Using a diverse sampling of 19 araneids, I examined the effects of orthology assessment methods and gene occupancy/missing data on the resulting topologies. The results showed broad congruence across most analytical treatments regardless of orthology method, occupancy, or tree inference method, with more genes (and more missing data) to be the best predictor of high node supports. I also found little overlap between transcripts used by orthology programs, suggesting good signal in the data. ix Table of Contents Acknowledgments ......................................................................................................... v Abstract of Dissertation ..............................................................................................vi ii List of Figures ............................................................................................................... xi List of Tables .............................................................................................................. xiv Chapter 1: Introduction ................................................................................................. 1 Chapter 2: An expanded molecular phylogeny of metaine spiders (Araneae, Tetragnathidae) with description of new taxa from Taiwan and the Philippines ......... 6 Chapter 3: Systematics and phylogeny of the Australasian orb-weaver genera Phonognatha Simon 1894, Deliochus Simon 1894, and Artifex new genus (Araneae, Araneidae), with comments on biogeography and retreat evolution ......... 49 Chapter 4: Phylogenetic relationships within the orb-weaving spider family Araneidae, and the effects of orthology assessment and gene occupancy on phylogenomic analyses
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