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Phylogeography of Darlingtonea Kentuckensis and Molecular Systematics of Kentucky Cave Trechines

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Phylogeography of Darlingtonea Kentuckensis and Molecular Systematics of Kentucky Cave Trechines Western Kentucky University TopSCHOLAR® Masters Theses & Specialist Projects Graduate School 5-2015 Phylogeography of Darlingtonea Kentuckensis and Molecular Systematics of Kentucky Cave Trechines Olivia Frances Boyd Western Kentucky University, [email protected] Follow this and additional works at: http://digitalcommons.wku.edu/theses Part of the Biology Commons, and the Other Ecology and Evolutionary Biology Commons Recommended Citation Boyd, Olivia Frances, "Phylogeography of Darlingtonea Kentuckensis and Molecular Systematics of Kentucky Cave Trechines" (2015). Masters Theses & Specialist Projects. Paper 1477. http://digitalcommons.wku.edu/theses/1477 This Thesis is brought to you for free and open access by TopSCHOLAR®. It has been accepted for inclusion in Masters Theses & Specialist Projects by an authorized administrator of TopSCHOLAR®. For more information, please contact [email protected]. PHYLOGEOGRAPHY OF DARLINGTONEA KENTUCKENSIS ​ AND MOLECULAR SYSTEMATICS OF KENTUCKY CAVE TRECHINES A Thesis Presented to The Faculty of the Department of Biology Western Kentucky University Bowling Green, Kentucky In Partial Fulfillment Of the Requirements for the Degree Master of Science By Olivia Frances Boyd May 2015 ACKNOWLEDGMENTS This research was made possible by funding from Dr. Keith Philips, Dr. Jarrett Johnson, and internal funding from Western Kentucky University including a Graduate Student Research Grant and a Research and Creative Activities Program (RCAP) grant. Naomi Rowland (WKU Biotechnology Center) provided valuable advice and assistance with molecular work. We thank Dr. Matthew Niemiller (Illinois Natural History Survey) and Dr. Karen Ober (College of the Holy Cross) for their guidance and specimen contributions and Elise Valkanas (University of Maryland) for her work on Neaphaenops ​ which inspired and contributed to this project. We also thank the many landowners who gave permission for us to sample caves on private property, the National Park Service for permits to collect at several locations within Mammoth Cave National Park, Jim Currens (Kentucky Geological Survey), Julian Lewis (Cave, Karst & Groundwater Biological Consulting), Ben Miller and Jason Polk (Department of Geology and Geography), Lee Florea (Ball State University), Kurt Helf (Cumberland Piedmont Network, National Park Service), The Rockcastle Karst Conservancy, the Green River Grotto at WKU, John Andersland (Department of Biology), Rob Neidlinger, and the Kentucky Speleological Society. iii CONTENTS INTRODUCTION.......................................................................................................... 1 MATERIALS AND METHODS.................................................................................... 15 RESULTS....................................................................................................................... 23 DISCUSSION................................................................................................................. 27 LITERATURE CITED................................................................................................... 60 iv LIST OF FIGURES Figure 1. Map showing the major geologic features.................................................. 41 Figure 2. Estimated distribution of Pseudanophthalmus. ......................................... 41 ​ ​ Figure 3. Dorsal habitus photomicrographs of Pseudanophthalmus......................... 42 ​ ​ Figure 4. Known distributions of Neaphaenops and Darlingtonea........................... 42 ​ ​ ​ ​ Figure 5. Dorsal habitus photomicrograph of Darlingtonea kentuckensis................. 43 ​ ​ Figure 6. Agarose gel of PCR products from an annealing temperature gradient..... 43 Figure 7. Distribution map of individual collecting localities................................... 44 Figure 8. Maps showing frequencies and diversity of COI haplotypes..................... 45-46 Figure 9. Split network of 81 COI sequences............................................................ 47 Figure 10. Minimum spanning network of 28 COI haplotypes................................. 48-49 Figure 11. Strict consensus of 10,000 trees from parsimony (COI)........................... 50 Figure 12. Strict consensus of 306 trees from parsimony (wingless)........................ 51 Figure 13. Strict consensus of 352 trees from parsimony (combined)....................... 52 Figure 14. Majority-rule consensus of trees sampled in Bayesian (COI).................. 53 Figure 15. Majority-rule consensus of trees sampled in Bayesian (wingless)........... 54 Figure 16. Majority-rule consensus of trees sampled in Bayesian (combined)......... 55 Figure 17. Majority-rule consensus of trees from maximum likelihood (COI)......... 56 Figure 18. Majority-rule consensus of trees from maximum likelihood (wingless).. 57 Figure 19. Majority-rule consensus of trees from maximum likelihood (combined) 58 v LIST OF TABLES Table 1. List of Darlingtonea populations................................................................. 37 ​ ​ Table 2. General information about the molecular markers used in this study.......... 38 Table 3. AMOVA results for structure I (4 faunal regions)....................................... 38 Table 4. AMOVA results for structure I (10 watersheds).......................................... 38 Table 5. AMOVA results for structure III (5 genetic clusters).................................. 39 Table 6. Results of Mantel tests................................................................................. 39 Table 7. Summary of support values from each analysis........................................... 40 vi LIST OF APPENDICES Appendix 1. Command blocks: TNT, MrBayes 59 vii PHYLOGEOGRAPHY OF DARLINGTONEA KENTUCKENSIS ​ AND MOLECULAR SYSTEMATICS OF KENTUCKY CAVE TRECHINES Olivia F. Boyd May 2015 64 Pages Directed by: T. Keith Philips, Jarrett Johnson, and Ajay Srivastava Department of Biology Western Kentucky University The monotypic cave carabid genus Darlingtonea is widely distributed along the ​ ​ eastern band of the Mississippian/Pennyroyal plateau in Kentucky and northern Tennessee. DNA sequence data from the mitochondrial gene cytochrome oxidase subunit I (COI) was collected from one to four individuals from 27 populations, and patterns of phylogeography and population structure were inferred from COI haplotypes. A hierarchical analysis of molecular variance found low nucleotide diversity within populations and statistically significant variation among geographically-defined groups tested based on two a priori hypotheses of structure. Population structure among five ​ ​ distinct genetic clusters identifies approximate locations of barriers to gene flow among closely grouped caves in the upper Rockcastle River drainage. Partial sequences of one mitochondrial (COI) and one nuclear (wingless) gene were gathered from 60 to 106 terminal taxa, including representatives of all five genera of cave trechines from Kentucky and Tennessee. Alignments were analyzed using maximum parsimony, Bayesian, and maximum likelihood methods of phylogenetic inference. Comparison of analyses demonstrates conflicting tree topologies among individual markers and different reconstruction methods. Despite a lack of consensus regarding genus-level relationships, most analyses supported each genus as natural (monophyletic) with the exception of Pseudanophthalmus. ​ ​ vii INTRODUCTION The limestone karst regions of the Eastern United States support a remarkable diversity of cave-specialized ground beetles belonging to the tribe Trechini (Carabidae: Trechinae). Cave trechines are true troglobites (obligate and permanent cave dwellers), with adaptations for cave life that define their niche as primary predators of invertebrates in cool, humid subterranean habitats; they lack eyes and wings, possess lengthened appendages and specialized sensory setae, and are depigmented and undersclerotized in comparison with their epigean (surface-dwelling) relatives, including montane members of the genus Trechus. In terms of species diversity, trechine carabids are the dominant terrestrial troglobites in the unglaciated karst regions of eastern North America and the temperate western Palearctic. The southern Appalachian region of North America has served as a hotspot for the rapid, climate-associated diversification of several groups of carabid beetles. The extensive karst regions of the Appalachian Valley (AV) and Interior Low Plateaus (especially the Mississippian Plateau (MP) which covers much of Kentucky and Tennessee) set the stage for an explosive radiation of ground beetles belonging to the tribe Trechini. Adaptive shifts to obligate cave life and accompanying troglomorphy appear to have occurred repeatedly in this group; extant cave trechines probably represent relict lineages descended from soil-dwelling ancestors, most of which became extinct in North America following the Pleistocene (Barr 1969, 1971, 1985b). The European fauna includes a number of examples of morphologically ‘intermediate’ trechines occupying deep soil and interstices in addition to a comparable diversity of obligate cave species; 1 why such intermediate forms did not persist in North America is not entirely clear, but could have been due to a relative scarcity of suitable habitat in sufficiently high-altitude refugia (Barr 1969). Regarding the origin and diversity of cave trechines, most authors have favored some variation of a “Pleistocene-effect” model (Holsinger 1988), summarized as follows: As climate cycles associated
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