A THESIS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Systematic review of subfamily Phylinae (Hemiptera: Miridae) in Korean Peninsula with molecular phylogeny of Miridae By Ram Keshari Duwal Program in Entomology Department of Agricultural Biotechnology Seoul National University February, 2013 Systematic review of subfamily Phylinae (Hemiptera: Miridae) in Korean Peninsula with molecular phylogeny of Miridae UNDER THE DIRECTION OF ADVISER SEUNGHWAN LEE SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL OF SEOUL NATIONAL UNIVERSIITY By Ram Keshari Duwal Program in Entomology Department of Agricultural Biotechnology Seoul National University February, 2013 APRROVED AS A QUALIFIED DISSERTATION OF RAM KESHARI DUWAL FOR THE DEGREE OF DOCTOR OF PHILOSOPHY BY THE COMMITTEE MEMBERS CHAIRMAN Si Hyeock Lee VICE CHAIRMAN Seunghwan Lee MEMBER Young-Joon Ahn MEMBER Yang-Seop Bae MEMBER Ki-Jeong Hong ABSTRACT Systematic review of subfamily Phylinae (Hemiptera: Miridae) in Korean Peninsula with molecular phylogeny of Miridae Ram Keshari Duwal Program of Entomology, Department of Agriculture Biotechnology The Graduate School Seoul National University The study conducted two themes: (1) The systematic review of subfamily Phylinae (Heteroptera: Miridae) in Korean Peninsula, with brief zoogeographic discussion in East Asia, and (2) Molecular phylogeny of Miridae: (i) Higher group relationships within family Miridae, and (ii) Phylogeny of subfamily Phylinae. In systematic review a total of eighty four species in twenty eight genera of Phylines are recognized from the Korean Peninsula. During this study, twenty new reports including six new species were investigated; and purposed a synonym and revised recombination. Keys to genera and species, diagnosis, descriptions including male and female genitalia, illustrations and short biological notes are provided for each of the species. Molecular based higher group relationships, and detail phylogenetic relationships of subfamily Phylinae were conducted. The higher group relationships were analyzed using 159 taxa, including seven subfamilies and six outgroups. The results of analysis indicated that subfamilies Cylapinae, Deraeocorinae, Isometopinae, Mirinae and Phylinae are monophyly, whereas Bryocorinae and Orthotylinae are paraphyletic. Dicyphini (of Bryocorinae) occurs as i a sister group to all remaining mirid taxa. Further, the phylogenetic analyses of subfamily Phylinae based on 68 taxa including 57 ingroup and 11 outgroup taxa (which include taxa of other subfamilies in Miridae except Psallopinae) were conducted. The results of analyses assure that, tribes Auricillocorini and Hallodapini are monophyletic, tribe Phylini is non-monophyletic but its member do not fall into other tribes, Teleorhinus (of Pronotocrepini) lies within Phylini, and Lasiolabops is separated from Phylini. Similary, present analyses argue with the monophyly of Leucophoropterini and Pilophorini. Key words: Miridae, Molecular Phylogeny, Phylinae, Taxonomy, The Korean Peninsula Student number: 2007-31066 ii TABLE OF CONTENTS Abstract……………………………………………………………………………………….i Table of Contents……………………………………………………………………………..iii List of Tables…………………………………………………………………...………...…..vii List of Figures…………………………………………………………………….………....viii PART I. Taxonomic review of the sub-family Phylinae (Heterptera: Miridae) in the Korean Peninsula. Abstract…………………………………………………………………………………1 Historical Review……………………………………………………………………….2 Introduction……………………………………………………………………………..4 Material and Methods…………………………………………………………………...6 Results………………………………………………………………..…………………8 Subfamily Phylinae Douglas and Scott, 1865…………………………….…………….8 Keys to tribes of subfamily Phylinae …………………………………………………..9 Tribe Hallodapini Van Duzee, 1916……………………………….……………..……10 Key to Korean genera of tribe Hallodapini ………......…….…………...…………….10 Genus Acrorrhinium Noualhier, 1895…………………………………………..11 Genus Hallodapus Fieber, 1858………………………………………………...13 Genus Systellonotus Fieber, 1858……………………………………………….19 Tribe Leucophoropterini Schuh, 1974…………………………………………………21 Genus Sejanus Distant, 1910……………………………………………………22 Tribe Phylini Douglas and Scott, 1865………………………………………………...24 Key to Korean genera of tribe Phylini………………..………………………………..25 Genus Atomoscelis Reuter, 1875………………………………………………..28 iii Genus Atractotomus Fieber, 1858………………………………………………30 Genus Atractotomoidea Yasunaga, 1999………………………………………..32 Genus Campylomma Reuter, 1878……………………………………………...34 Genus Chlamydatus Curtis, 1833……………………………………………….41 Genus Compsidolon Reuter, 1899………………………………………………44 Genus Euplagiognathus Duwal n. gen. ………………………………...………48 Genus Europiella Reuter, 1909………………………………………………....51 Genus Harpocera Curtis, 1838………………………………............................61 Genus Kasumiphylus Schwartz and Stonedahl, 2004…………………………..65 Genus Macrotylus Fieber, 1858…………………………………………………67 Genus Moissonia Reuter, 1894………………………………………………….71 Genus Monosynamma Scott, 1864……………………………………………...77 Genus Orthonotus Stephens, 1829……………………………………………...79 Genus Orthophylus Duwal and Lee, 2011……………………………………...82 Genus Parapsallus Wagner, 1952………………………………………………84 Genus Phylus Hahn, 1831………………………………………………………87 Genus Pseudophylus Yasunaga, 1999…………………………………………..90 Genus Plagiognathus Fieber, 1858……………………………………………..92 Genus Psallus Fieber, 1858……………………………………………………102 Genus Rubrocuneocoris Schuh, 1984…………………………………………156 Genus Tytthus Fieber, 1864……………………………………………………158 Tribe Pilophorini Douglas and Scott, 1876…………………………………………..160 Key to Korean genera of tribe Pilophorini……………………….…………………..161 Genus Pherolepis Kulik, 1968 ………………………………………………..161 iv Genus Pilophorus Hahn, 1826………………………………………………...166 Zoogeographic discussion in Eastern Asia…………………………………………….……186 PART II. Molecular phylogeny of Miridae (Hemiptera: Heteroptera) (i). Higher group relationships within family Miridae (Heteroptera: Cimicomorpha) Abstract……………………………………………………………………………………..189 Introduction…………………………………………………………………...…………….189 Material and Methods……………………………………………………………………….191 Results………………………………………………………………………………………195 Discussion…………………………………………………………………………………..197 Conclusion ………………………………………………………………………………….200 PART II (ii). Phylogeny of subfamily Phylinae Abstract……………………………………………………………………………………..201 Introduction…………………………………………………………………………………201 Material and Methods……………………………………………………………………….204 Results………………………………………………………………………………………207 Discussion………………………………………………………………………………..…208 Conclusion ………………………………………………………………………………….218 Literature Cited……………………………………………………………………………..220 Checklist of subfamily Phylinae in Korea …………………………………………………239 v Appendix Figure plates ………………………………………………………………………………..245 Table 1………………………………………………………………………………………294 Table 2………………………………………………………………………………………315 Table 3………………………………………………………………………………………322 Table 4………………………………………………………………………………………324 Table 6………………………………………………………………………………………329 vi List of Tables Table 1. Measurements of Phylinae from the Korean Peninsula ..…………………………294 Table 2. Distribution of subfamily Phylinae in Eastasia……………………………………315 Table 3. Collection information for the species [sequenced during this study]…………….322 Table 4. The list species and sequences with Gene bank accession numbers (Downloaded from NCBI)………...…………………………………………………………….....324 Table 5. Primers used for Miridae analyses………………………………………………...193 Table 6. Taxon sampling and Gene bank accession numbers for NCBI data………………329 Table 7. Primers used for Phylinae analyses………………………………………………..205 Table 8. Clades recovered in three analyses, Bayesian estimation (BI), maximum likelihood (ML) and parsimony……..…………………….…………………………210 vii List of Figures Fig. 1. Taxonomic position of the subfamily Phylinae (Douglas and Scott, 1865)…………245 Fig. 2. General morphology of Phylinae. A-C. Hallodapus albofasciatus. D. Atractotomus morio. E. Brachyarthrum limitatum. F. Psallus pullus. G. Moissonia punctata. A. Lateral view. B. Dorsal view. C. Leg. D-G. Parameres (Figs of parameres:Yasunaga, 2001a)………………………………………………………………………………...246 Fig. 3. Dorsal habitus of tribe Hallodapini. A. Acrorrhinium inexpectatum. B. Systellonotus malaise. C. Hallodapus centrimaculatus. D. H. linnavuori. E. H. pumillus. Scale bars: 0.5mm ……...………………………………….……………………………………..247 Fig. 4. Male genitalia of tribe Hallodapini: A-D. Acrorrhinium inexpectatum. E-H. Hallodapus centrimaculatus. A, H. Endosoma. B, E. Left paramere. C, F. Right paramere. D, G.Phallotheca. Scale bar: 0.1mm………………………………………248 Fig. 5. Genital structures of tribe Hallodapini. A-D. Hallodapus linnavuori. E-F. H. pumillus. G-K. Systellonotus malaise. A-D, G-K. Male genitalia. E-F. Female genitalia. A, I-J. Endosoma. B, H. Left paramere. C, K. Right paramere. D, G. Phallotheca. E. Posteriora wall. F. Bursa copulatrix (Dorsal labiate plate). Scale bar: 0.1mm…………………..249 Fig. 6. Dorsal habitus and genital structures of Sejanus potanini. A-C. Male genitalia. D-E. Female genitalia. A. Endosoma. B. Right paramere. C. Left paramere. D. Bursa copulatrix. E. Posterior wall. Scale bar: dorsal: 0.5, genital structure: 0.1…………..250 Fig. 7. Dorsal habitus of tribe Phylini. Scale bar: A. Atomoscelis asiatica. B-C. Atractotomoidea castanea. D-E. Campylomma annulicorne. F. C. lividicorne. G. C. miyamotoi. H-I. C. chinense. 0.5mm………………………..……….……………….251 Fig. 8. Genital structures of Phylini. A-E. Atomoscelis asiatica. F-J. Atractotomoidea castanea. A, F. Endosoma. B, H. Left paramere. C, I. Phallotheca. D, G. Right viii paramere. E, J. Bursa copulatrix. Scale Bar: 0.1mm………………………………...252 Fig. 9. Genital structures of Phylini. A-E. Campylomma annulicorne. F-J.