PHYLOGENETIC SYSTEMATICS AND THE EVOLUTIONARY HISTORY OF SOME INTESTINAL FLATWORM PARASITES (TREMATODA: DIGENEA: PLAGIORCHI01DEA) OF ANURANS by RICHARD TERENCE 0'GRADY B.Sc, University Of British Columbia, 1978 M.Sc, McGill University, 1981 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES Department Of Zoology We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA March 1987 © Richard Terence O'Grady, 1987 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of Zoology The University of British Columbia 2075 Wesbrook Place Vancouver, Canada V6T 1W5 Date: March 24, 1987 i i Abstract Historical structuralism is presented as a research program in evolutionary biology. It uses patterns of common ancestry as initial hypotheses in explaining evolutionary history. Such patterns, represented by phylogenetic trees, or cladograms, are postulates of persistent ancestral traits. These traits are evidence of historical constraints on evolutionary change. Patterns and processes consistent with a cladogram are considered to be consistent with an initial hypothesis of historical constraint. As an application of historical structuralism, a phylogenetic analysis is presented for members of the digenean plagiorchioid genera Glypthelmins Stafford, 1905 and Haplometrana Lucker, 1931. The eight species studied are intestinal parasites of frogs and toads in North, Central, and South America. In a Wagner parsimony analysis of 21 morphological characters with both the PAUP and PHYSYS computer programs, a single phylogenetic tree with a consistency index of 84.8% can be inferred. This suggests strong historical constraint in the evolution of the characters examined. It is postulated that the eight species form a monophyletic group (clade), consisting of two less inclusive clades. Glypthelmins hyloreus and G. pennsylvaniensis comprise one of these clades; G. robustus, G. shastai, H. intestinalis, G. californiensis, G. quieta, and G. facioi comprise the other. G. robustus, found in Bufo marinus in Colombia, is both the southernmost and the most plesiomorphic member of its clade. Glypthelmins californiensis, G. quieta, and G. facioi form a clade, and parasitize frogs in the Rana pipiens complex in Mexico, eastern North America, and Central America, respectively. Glypthelmins shastai and H. intestinalis, the latter of which is the only member of its genus, form a western North American clade, and parasitize Bufo boreas and Rana pretiosa, respectively. The phylogenetic analysis includes a redescription of G. shastai, the synonymy of the genus Haplometrana with Glypthelmins, the redescription of H. intest inali s as G. intestinalis, an emended diagnosis of the genus Glypthelmins, and the first account of the life cycle of G. californiensis. Three aspects of phylogenetic analysis are examined in detail. These are the coding of multistate character trees, the use of parasite data to infer host relationships, and the properties of the Consistency Index and the F-Ratio. It is proposed that the Consistency Index be calculated without non-homoplasious autapomorphic characters. For the present study, this modification gives a value of 76.9%. Using the phylogenetic tree as a general reference system of patterns of common ancestry, it is inferred from developmental studies that (1) there is no conflict between the phylogenetic relationships indicated by only larval or only adult characters, and that (2) the evolution of some of the characters involved certain types of heterochrony. Paedomorphic heterochrony is inferred to have occurred in the evolution of the uterus in G. shastai, H. intestinalis, G. californiensis, G. quieta, and G. facioi. Peramorphic heterochrony is inferred i v to have occurred in the evolution of the penetration glands in G. facioi, and of the hindbody in H. intestinalis. The relatively longer hindbody of H. intestinalis was experimentally induced to show paedomcrphic development by raising specimens of H. intestinalis in Bufo boreas, which is the host of G. shastai, its sister-species. By one year after infection, the relative length of the hindbody is shorter, and is equal to that of the primitive state found in G. shastai. The phylogenetic relationships among the anuran hosts are re-analyzed. There is 80% congruence between them and the postulated phylogenetic tree for their parasites, suggesting strong historical association between the parasite and host groups. This inference of coevolution is further supported by the concordance of the present geographical distributions of the parasites and their hosts with the historical geology of the areas in which they occur. This implies an historical association between the areas and the organisms. V Table of Contents Abstract ii List of Tables viii List of Figures ix Acknowledgements xiii Chapter I INTRODUCTION 1 Chapter II HISTORICAL STRUCTURALISM AS A RESEARCH PROGRAM IN EVOLUTIONARY BIOLOGY 7 BIOLOGICAL SYSTEMS 8 END-ATTAINING ACTIVITY 10 HISTORICAL AND NONHISTORICAL APPROACHES IN BIOLOGY .17 NATURAL SELECTION 21 ADAPTATION 25 A SINGLE EXPLANATORY FRAMEWORK 28 1. INTRASPECIFIC INVESTIGATIONS 30 2. PHYLOGENETIC INVESTIGATIONS 31 3. LIFE HISTORY INVESTIGATIONS 33 4. COMMUNITY STRUCTURE INVESTIGATIONS 36 "WHY" QUESTIONS 37 SUMMARY 38 CONCLUSIONS 41 Chapter III PHYLOGENETIC ANALYSIS OF HAPLOMETRANA LUCKER, 1931 AND SPECIES OF GLYPTHELMINS STAFFORD, 1905 (DIGENEA: PLAGIORCHI01DEA) IN NORTH, CENTRAL, AND SOUTH AMERICA 42 INTRODUCTION 42 TAXA STUDIED 4 5 MATERIALS AND METHODS 47 SPECIMENS EXAMINED 47 1. MUSEUM SPECIMENS 47 2. FIELD COLLECTIONS 52 3. EXAMINATION OF SPECIMENS 53 THE INFERENCE OF PHYLOGENETIC RELATIONSHIPS 54 1 . HOMOLOGY 54 2. OUTGROUPS 57 3. MULTISTATE CHARACTERS 59 4. COMPUTER-ASSISTED PARSIMONY ANALYSIS 60 CHARACTER ANALYSIS 63 1. CHARACTERS EXCLUDED FROM ANALYSIS 84 RESULTS AND DISCUSSION 87 PHYLOGENETIC ANALYSIS 87 TAXONOMIC CONSIDERATIONS 91 Chapter IV USING THE PHYLOGENETIC TREE TO STUDY EVOLUTIONARY EVENTS .94 PHYLOGENETIC CONCORDANCE OF LARVAL AND ADULT CHARACTERS 95 INTRODUCTION 95 LIFE HISTORY DATA 100 1. PREVIOUS STUDIES , 101 2. NEW DATA 103 .ANALYSIS OF LARVAL CHARACTERS 107 ANALYSIS OF LIFE CYCLE EVOLUTION 108 HETEROCHRONIC DEVELOPMENT 109 INTRODUCTION 109 ANALYSIS 114 ALLOMETRY AS HETEROCHRONY 118 EXPERIMENTALLY-PRODUCED HETEROCHRONY IN HAPLOMETRANA INTESTINALIS 121 INTRODUCTION 121 ANALYSIS 121 DISCUSSION 124 COEVOLUTION AND BIOGEOGRAPHY OF PARASITES AND HOSTS ..126 INTRODUCTION 126 HOST AND DISTRIBUTION DATA 128 1 . PREVIOUS STUDIES , 128 2. NEW DATA 134 3. DISCUSSION 140 COEVOLUTION ANALYSIS 142 1. FAMILY LEVEL 1 42 2. SPECIES LEVEL 144 BIOGEOGRAPHIC ANALYSIS 152 SUMMARY 156 LITERATURE CITED 275 APPENDIX A - COMPUTER ANALYSES WITH PAUP AND PHYSYS 292 APPENDIX B - HOST AND DISTRIBUTION DATA FOR GLYPTHELMINS QUIETA 303 APPENDIX C - COLLECTION SITES OF ANURANS 306 APPENDIX D - REDESCRIPTION OF GLYPTHELMINS SHASTAI, SYNONYMIZATION OF HAPLOMETRANA WITH GLYPTHELMINS, AND REDESCRIPTION OF G. INTESTINALIS N. COMB 307 APPENDIX E - THE LIFE CYCLE OF GLYPTHELMINS CALIFORNIENSIS 313 vii APPENDIX F - CODING MULTISTATE CHARACTERS 318 APPENDIX G - SOME PROPERTIES OF THE CONSISTENCY INDEX AND THE F-RATIO 327 viii List of Tables I. SPECIES STUDIED ....46 II. CHARACTERS ANALYZED 85 III. CHARACTERS RENUMBERED FROM UNORDERED ANALYSIS 90 ix List of Figures 1. End-Attaining Activity in Biological Systems .159 2. Ultimate and Proximate Causality 159 3. Types of Evolutionary Explanations 161 4. Historical Structuralism in Phylogenetic Systematics 161 5. Using a Cladogram to Study the Evolution of Life History Traits 163 6. The Application of Historical Structuralism to the Study of Community Structure 165 7. Postulated Relationships among Glypthelmins, from Brooks (1977) 167 8. Collection Sites of Anurans in British Columbia 169 9. Collections Sites of Anurans in California 171 10. Tegumental Projections 173 11. Penetration Glands in Adult Glypthelmins facioi 173 12. Medial Glands in Haplometrana intestinalis 175 13. Pharyngeal Glands in Glypthelmins quieta 175 14. Schematic Representation of the Distribution of the Vitellaria in Glypthelmins and Haplometrana 177 15. Distribution of Vitellaria in Glypthelmins quieta and G. facioi 179 16. Distribution of Vitellaria in Glypthelmins californiensis 181 17. Distribution of Vitellaria in Glypthelmins shastai and Haplometrana intestinalis 181 18. Vitelline Ducts in Haplometrana intestinalis and Glypthelmins californiensis 183 19. Shape of the Excretory Vesicle 185 20. Postulated Phylogenetic Relationships among Glypthelmins and Haplometrana 187 X 21. Multistate Character Trees: One 189 22. Multistate Character Trees: Two 191 23. Disruptive Grouping Criteria in Systematics 193 24. Congruence and Consistency in Tree Topologies 195 25. Generalized Life Cycle of a Digenean Flatworm 197 26. Phylogenetic Analysis of Larval Characters of Species of Glypthelmins and Haplometrana 199 27. Phylogenetic Analysis of Life Cycle Evolution in Species of Glypthelmins and Haplometrana