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Biology and Evolution of the Mexican Cavefish This page intentionally left blank Biology and Evolution of the Mexican Cavefish Alex C. Keene Department of Biology, Florida Atlantic University, Jupiter, FL, USA Masato Yoshizawa Department of Biology, University of Hawai’i at Manoa, Honolulu, HI, USA Suzanne E. McGaugh Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN, USA AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 225 Wyman Street, Waltham, MA 02451, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 125 London Wall, London, EC2Y 5AS, UK The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK © 2016 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library ISBN: 978-0-12-802148-4 For information on all Academic Press publications visit our website at http://store.elsevier.com/ Typeset by SPi Global, India www.SPi-global.com Printed in USA Contents Preface xiii Introduction: The Emergence of the Mexican Cavefish as an Important Model System for Understanding Phenotypic Evolution 1 Clifford J. Tabin Part I Ecology and Evolution 1. Cave Exploration and Mapping in the Sierra de El Abra Region 9 William R. Elliott Introduction 9 Physiography and Hydrogeology 11 History of Exploration and Mapping 17 Mapping and Cartography Methods 22 Geographic Information Systems 25 Cave Descriptions 26 Gómez Farías Area (Sierra de Guatemala) 26 Glossary of Mexican, Geographic, and Geologic Terms 37 Acknowledgments 39 References 39 2. Hydrogeology of Caves in the Sierra de El Abra Region 41 Luis Espinasa and Monika Espinasa Preface 41 Current Surface Streams and Springs 41 Current Underground Drainages 45 Geology 46 Age of the Caves 47 Evolution of the Hydrogeology at the El Abra Region 49 Discussion 55 Conclusions 56 References 57 v vi Contents 3. Cave Biodiversity and Ecology of the Sierra de El Abra Region 59 William R. Elliott Introduction 59 Biodiversity 59 General Cave Ecology 61 Hazards to Cave Visitors 61 Temperatures 62 Cavefish Food 62 Bats 63 Crustaceans 63 Ecology of Four Caves 65 Sótano de Yerbaniz 65 La Cueva Chica 66 Cueva de Los Sabinos 70 Sótano de Soyate 72 Conclusions 74 Acknowledgments 75 References 75 4. Phylogeny and Evolutionary History of Astyanax mexicanus 77 C.P. Ornelas-García and C. Pedraza-Lara The Astyanax Genus 77 Taxonomy of Troglobite Astyanax from the Huasteca Region 78 Cave Invasion by Astyanax Lineages 85 References 87 Part II Genetic Diversity and Quantitative Genetics 5. Regressive Evolution: Testing Hypotheses of Selection and Drift 93 Richard Borowsky Introduction 93 Eyes and Pigmentation, Hypotheses and Their Tests 94 Testing the First Prediction 95 Testing the Second Prediction 95 Testing the Third Prediction 100 Melanin Traits 102 Contents vii Albinism 102 Brown Phenotype 104 oca2 and mc1r Interact Epistatically 104 Conclusion 105 Materials and Methods 106 Tinaja/Surface Cross 106 Mapping and QTL Analysis 106 Assessment of Pigmentation 106 References 107 6. Mapping the Genetic Basis of Troglomorphy in Astyanax: How Far We Have Come and Where Do We Go from Here? 111 Kelly O’Quin and Suzanne E. McGaugh Introduction 111 Part I: Quantitative Genetics and QTL Mapping in Astyanax 112 Mendelian vs. Quantitative Traits 112 Quantitative Trait Locus Mapping: Complex Traits and QTL Clusters 115 Quantitative Trait Nucleotide (QTN) Fine-Mapping: Success for Mendelian Traits 121 Part II: Looking Forward: Remaining Questions and New Approaches 124 The Future of QTL Mapping in Astyanax 124 Increasing the Accuracy and Precision of QTL Mapping 124 Additional Methods: Population Scans, Genome Sequencing, and Sampling 126 The Final Step: Genotype-to-Phenotype-to-Fitness 129 References 129 7. Selection Through Standing Genetic Variation 137 Nicolas Rohner De novo Versus Standing Genetic Variation 137 Cryptic Genetic Variation and Canalization 140 HSP90 as a Capacitor of Evolution 141 HSP90 in Cavefish Evolution 142 Is Eye Loss in Cavefish an Adaptive Trait 145 Detecting Standing Genetic Variation 146 Examples from Astyanax Mexicanus 147 Gene Flow 148 Open Questions 149 References 149 viii Contents Part III Morphology and Development 8. Pigment Regression and Albinism in Astyanax Cavefish 155 William R. Jeffery, Li Ma, Amy Parkhurst and Helena Bilandžija Introduction 155 Astyanax Pigmentation and Depigmentation 156 Control of Melanogenesis 160 Developmental Basis of Cavefish Depigmentation 162 Genetic Basis of Cavefish Depigmentation 164 The Brown Gene Encodes mc1r 166 The Albinism Gene Encodes oca2 167 Evolution of Cavefish Depigmentation 168 Conclusions and Future Prospects 170 References 171 9. Molecular Mechanisms of Eye Degeneration in Cavefish 175 Yoshiyuki Yamamoto Adult Cavefish Eye 175 Eye Development 176 Eye Degeneration 178 Mechanisms of PCD in the Cavefish Lens 181 Evolutionary Forces Why Cavefish Fish Have Lost Their Eye 183 The Trend of Eye Degeneration 183 Eye Degeneration in Other Cavefish Species 183 Evolutionary Mechanisms: Neutral Mutation with Genetic Drift 185 Evolutionary Mechanisms: Trade-off Hypothesis 186 Evolutionary Mechanisms: Energy Conservation Hypothesis 187 Why "Build and Destroy"? 188 References 189 10. The Evolution of the Cavefish Craniofacial Complex 193 Joshua B. Gross and Amanda K. Powers Discovery, Characterization, and the Historical Relevance of Craniofacial Evolution in Cavefish 193 Craniofacial Changes Across Independently Derived Cave Populations 196 The Nature of Morphological Changes to the Craniofacial Complex in Cave-Dwelling Populations 198 Contents ix Mechanisms of Craniofacial Evolution in Cave-Dwelling Populations 199 Coordinated Changes Between the Craniofacial Complex and Other Cave-Associated Traits 201 Genetic Analyses of Craniofacial Evolution 202 Conclusions 204 Acknowledgments 205 References 205 11. Evolution and Development of the Cavefish Oral Jaws: Adaptations for Feeding 209 A.D.S. Atukorala and Tamara A. Franz-Odendaal Introduction 209 Adult Dentition and Jaw bones 210 Development of the Jaws Supporting the Dentition 212 Development of the Dentitions 213 Development of Tastebuds on the Oral Jaws 215 Relationship Between the Constructive Traits of Teeth and Tastebud Expansion and Eye Loss 217 Gene Networks Underlying These Traits 217 Tooth-Tastebud Linkages 219 Teeth-Eye Linkages 219 Modularity and Adaptive Evolution 220 Conclusion 221 Acknowledgments 222 References 222 12. Neural Development and Evolution in Astyanax mexicanus: Comparing Cavefish and Surface Fish Brains 227 Sylvie Rétaux, Alexandre Alié, Maryline Blin, Lucie Devos, Yannick Elipot and Hélène Hinaux Introduction 227 Adult Brain Anatomy and Brain Networks 229 A Special Case: Development and Degeneration of the Cavefish Visual System 231 Early Embryonic Development: The Origin of Cavefish Differences? 233 Larval Brain Development: Establishing Subtle Differences 235 Sensory Systems 236 Chemosensory System 237 Lateral Line 238 Cavefish Brain Neurochemistry 239 Conclusions and Perspectives 240 Acknowledgments 241 References 241 x Contents Part IV Behavior 13. The Evolution of Sensory Adaptation in Astyanax mexicanus 247 M. Yoshizawa Introduction 247 Enhanced Sensory Systems 248 The Mechanosensory Lateral Line System and Associated Vibration Attraction Behavior 248 Chemical Sensory System 257 Regressed Sensory Systems 258 Visual System: Binocular Eyes 258 Sensory Systems that Potentially Contribute to Cave Adaptation 259 Inner Ear Sensory System: Sound Localization 259 Other Unsolved Sensory Systems: Tactile Sensing and the Pineal Light-Sensing Organs 260 Concluding Remarks 261 References 263 14. Feeding Behavior,