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Ecological Specialization in Predatory Lasiopogon Robber Flies and Its Role in Facilitating Diversification and Species Coexistence By

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Ecological Specialization in Predatory Lasiopogon Robber Flies and Its Role in Facilitating Diversification and Species Coexistence By Ecological Specialization in Predatory Lasiopogon Robber Flies and its Role in Facilitating Diversification and Species Coexistence by Tristan Alexander McKnight A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in The University of Michigan 2017 Doctoral Committee: Professor L. Lacey Knowles, Chair Associate Professor Johannes Foufopoulos Associate Professor Timothy Y. James Assistant Professor Stephen A. Smith Tristan A. McKnight [email protected] ORCID iD: 0000-0001-9400-3445 © Tristan A. McKnight 2017 ACKNOWLEDGMENTS Authorship for chapters II and III is shared with Dr. Robert A. Cannings (Royal BC Museum, Victoria, BC, Canada), who generously shared specimen records, personal experience, taxonomic insights, and encouragement to assist this work. However, the taxonomic decisions, specimen review, molecular work, and vast majority of the writing in these chapters are my own responsibility. Funding for collecting trips and molecular lab work was provided by the National Science Foundation (DEB•1601389), the Society for the Study of Evolution Rosemary Grant Award, the Smithsonian Williston Dipterology Fund, the University of Michigan Rackham Graduate School, Department of Ecology and Evolutionary Biology, and Museum of Zoology, and the Royal BC Museum Research Associate program. Labmates at the University of Michigan provided technical and theoretical assistance at various stages of this project: Dr. L. Lacey Knowles, Dr. Raquel Marchan, Dr. Jen-Pan Huang, Andrea Thomaz, Carlos Muñoz, Dr. Rob Massatti, Dr. Diego Alvarado Serrano, Pascal Title. Other associates at the University of Michigan were instrumental in shaping this work: Dr. Barry O’Connor, Dr. Jo Kurdziel, Dr. Pavel Klimov, Dr. Ted Cohn, Dr. Dan Rabosky and the EEB administrative staff (Robbin Murrell, Cynthia Carl, Jane Sullivan, Carol Solomon, Amber Stadler). Sean Ooi assisted with transcribing specimen labels and measurements, Dr. Andre Bochkov (ZIN) photographed type specimens of Stackelberginia in St. Petersburg, Dr. H. Don Cameron helped us coin new species etymologies from a sound classical foundation, Kirsten Ruth McKnight Ward prepared figures for the tabular key, Heather Myler helped edit the manuscript, and my mother Joan Boyce McKnight transcribed thousands of specimen labels and helped add new identification labels. Many friends, colleagues, and extended family members opened their homes and assisted me on collecting trips: Bill and Cheryl Boyce, Dr. Eric Fisher, Dr. Martin Hauser, Dan Swanson, Mark and Suzy McKnight, Dana, Susan, and Edward Fleming, Charlotte Herbert, Shelle Hyde, Bruce Conn, Brent and Kris Gardner, Tom and Karen Tingey, Garth Tingey, Stephen and ii Shauna Allen, Sherry Ward, Alma Boyce, Larry and Kathy McKnight. Friends from the online entomology community contributed specimens and ecological data: Alice Abela, Giff Beaton, Paul Bedell. Many curators and collection managers went out of their way to personally assist us during visits: we note the RBCM staff, Dr. Doug Yanega (UCRC), Larry Stevens (MNAZ), Dr. Scott Shaw (ESUW), Gary Shugart and Peter Wimberger (University of Puget Sound), Dr. Rod Crawford (UWBM). Finally, my father, Dr. Karl B McKnight, provided immeasurable logistical and moral support as a camping, driving, and collecting assistant, analytical partner, and mentor. iii TABLE OF CONTENTS ACKNOWLEDGMENTS………………………………………………………………………...ii LIST OF TABLES……………………………………………………………………………….vii LIST OF FIGURES……………………………………………………………………………..viii ABSTRACT…………………………………………………………………………………….....x CHAPTER I. Introduction………………………………………………………………………...1 Background ……………………………………………………………………………….1 Chapter summaries ………………………………………………………………………..2 Terminology of asilid morphology ……………………………………………………….3 CHAPTER II. Stackelberginia cerberus sp. n. (Diptera: Asilidae): morphological description, phylogenetic placement and first Nearctic records of the genus………………………………….7 Abstract……………………………………………………………………………………7 Introduction………………………………………………………………………………..7 Materials and Methods…………………………………………………………………….8 Taxonomy………………………………………………………………………………..11 Phylogeny………………………………………………………………………………..16 Discussion………………………………………………………………………………..17 CHAPTER III. Molecular phylogeny of the genus Lasiopogon (Diptera: Asilidae) and a taxonomic revision of the bivittatus group………………………………………………………24 Abstract…………………………………………………………………………………..24 Introduction………………………………………………………………………………25 Materials and Methods…………………………………………………………………...26 Sources of Material………………………………………………………………26 Species Concept………………………………………………………………….28 Presentation of Species Descriptions…………………………………………….29 Molecular Processing…………………………………………………………….30 iv Species Accounts………………………………………………………………………...32 L. actius Melander……………………………………………………………….32 L. albidus Cole and Wilcox……………………………………………………...37 L. anaphlecter McKnight sp. nov………………………………………………..41 L. apoecus McKnight sp. nov …………………………………………………...45 L. arenicola (Osten Sacken)……………………………………………………..48 L. asilomar McKnight sp. nov …………………………………………………..53 L. bitumineus McKnight sp. nov ………………………………………………..57 L. bivittatus Loew………………………………………………………………..61 L. californicus Cole and Wilcox…………………………………………………67 L. canningsi McKnight sp. nov ……………………………………………........71 L. condylophorus McKnight sp. nov …………………………………………....76 L. dimicki Cole and Wilcox……………………………………………………...79 L. drabicolum Cole………………………………………………………………83 L. esau McKnight sp. nov ………………………………………………………88 L. gabrieli Cole and Wilcox……………………………………………………...92 L. karli McKnight sp. nov ………………………………………………………97 L. littoris Cole…………………………………………………………………..100 L. martinensis Cole and Wilcox………………………………………………...104 L. nelsoni McKnight sp. nov …………………………………………………..108 L. odontotus McKnight sp. nov ……………………………………………......113 L. puyallupi Cole and Wilcox stat. nov…………………………………...........118 L. ripicola Cole and Wilcox…………………………………………………….123 L. sierra McKnight sp. nov…………………………………………………….128 L. tumulicola McKnight sp. nov………………………………………………..133 L. wilcoxi McKnight sp. nov…………………………………………………...137 L. willametti Cole and Wilcox………………………………………………….142 L. zonatus Cole and Wilcox…………………………………………………….146 Phylogeny………………………………………………………………………………154 Identification Keys……………………………………………………………………...157 v CHAPTER IV. Ecological specialization in predatory Lasiopogon robber flies (Diptera: Asilidae) and its role in facilitating diversification and species coexistence…………………...209 Introduction……………………………………………………………………………..209 Materials and Methods………………………………………………………………….211 Results ………………………………………………………………………………….214 Discussion ……………………………………………………………………………...216 CHAPTER V. Conclusions and Future Directions……………………………………………..222 BIBLIOGRAPHY………………………………………………………………………………226 vi LIST OF TABLES II.1 Primers used for genetic sequencing……………………………………………………..10 II.2 Taxonomy, collection data, genetic sampling, and voucher location for specimens used in the Stichopogoninae species tree………………………………………………………...21 III.1 Taxonomy, collection data, genetic sampling, and voucher location for specimens used in the Lasiopogon species tree…………………………………………………………….187 IV.1 Spearman’s r correlations between phylogenetic distance and niche component disparity, or the degree of geographic sympatry and niche component disparity, for sympatric and allopatric species pairs of Lasiopogon clade A and clade B. ** = p < 0.05, * = p < 0.1 ….……………………………………………………………………………………….216 IV.2 Summary of ecological traits for Lasiopogon species included in analysis (N is number of independent localities): perch, habitat (d= dune, r= river, m= mountain), mystax color, phenology window (5-95% confidence interval of ordinal dates), species distribution area, annual temperature mean and standard deviation, annual precipitation mean and standard deviation, climate variability (temp variance * ppt variance), species diversification rate (estimated from tip of phylogeny) ………………………………...219 vii LIST OF FIGURES I.1 Morphological terminology for asilids discussed in this dissertation, as illustrated with a female Lasiopogon asilomar sp. nov. ……………………………………………………4 II.1 Stackelberginia cerberus sp.n. female habitus and head detail………………………….11 II.2 Stackelberginia cerberus sp.n. genitalia detail: A) epandrium, dorsal; B) epandrium lateral; C) gonostylus, apical; D) subepandrial sclerite, ventral; E) hypandrium complex + gonosylus, ventral; F) hypandrium complex + gonosylus, lateral; G) female ovipositor, lateral; H) phallus, lateral. Scale bars are 0.2 mm……………………………………….14 II.3 Habitat of Stackelberginia cerberus sp.n. in Nevada (see paratype list for more precise locality data): A) Clark Co.: Wheeler wash; B) Nye Co.: Rock Valley wash. Specimens were caught on small stones and sand along the washes………………………………...16 II.4 Species tree for representatives of Stackelberginia, Lasiopogon, Stichopogon, Townsendia, and Asilidae and Mydidae outgroups, estimated via Bayesian inference in STARBEAST2 from one mitochondrial locus (COI) and three nuclear protein coding loci (wingless, PEPCK, AATS). Branch labels show support for nodes when posterior probability <1 ……………………………………………………………………………17 II.5 Holotypes of Stackelberginia tsharykulievi Lehr (A, B, E) and S. gracilis Lehr (C, D, F); lateral, dorsal and head detail…………………………………………………………….18 II.6 Coxal peg types in Stichopogoninae: A) blunt, robust (Stackelberginia cerberus sp.n.); B) sharp, short (Lasiopogon canus Cole and Wilcox); C) no peg (Lasiopogon schizopygus Cannings). Scale bar is 0.2 mm…………………………………………….20
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