It has long been recognized that an important factor in human evolution is the struggle against infectious disease, and more recently, it has been revealed that complex genetic polymorphisms are the direct result of that struggle. As molecular biological techniques become more sophisticated, a number of breakthroughs in the area of host–pathogen evolution have led to an increased interest in this field.
From the historical beginnings of J. B. S. Haldane’s original hypothesis to current research, this book strives to evaluate infectious diseases from an evolutionary perspective. It provides a survey of the latest information regarding host–pathogen evolution related to major infectious diseases and parasitic infections, including malaria, influenza, and leishmaniasis.
Written by leading authorities in the field, and edited by a former pupil of Haldane, Infectious Disease and Host–Pathogen Evolution will be a valuable reference for those working in related areas of microbiology, parasitology, immunology, and infectious disease medicine, as well as genetics, evolutionary biology, and epidemiology.
Krishna R. Dronamraju is currently the President of the Foundation for Genetic Research in Houston, Texas. He has authored or edited 13 books and has authored over 200 research papers in the field of genetics. A former student of J. B. S. Haldane, whose pioneering work in epidemiologic research he cites as the basis for this book, Dronamraju holds several distinguished honorary positions in both the United States and Europe.

Krishna R. Dronamraju at the U.K. Genome Center (courtesy of Michele Wambaugh).
OTHER BOOKS BY KRISHNA R. DRONAMRAJU
Biological Wealth and Other Essays (World Scientific, 2002)
Biological and Social Issues in Biotechnology Sharing (Ashgate Publishing, 1998)
Science and Society (University Press of America, 1998)
Haldane’s Daedalus Revisited (Oxford University Press, 1995)
If I Am Remembered: The Life and Work of Julian Huxley (World Scientific, 1993)
The History and Development of Human Genetics: Progress in Different Countries (World Scientific, 1992)
Selected Genetic Papers of JBS Haldane (Garland Publishing Company, 1990)
The Foundations of Human Genetics (C. C. Thomas, 1989)
Cleft Lip and Palate: Aspects of Reproductive Biology (C. C. Thomas, 1986)
Haldane: The Life and Work of JBS Haldane with Special Reference to India
(Aberdeen University Press, 1985)
Haldane and Modern Biology (The Johns Hopkins University Press, 1968)
Edited by
Krishna R. Dronamraju
Foundation for Genetic Research, Houston, TX
PUBLISHED BY THE PRESS SYNDICATE OF THE UNIVERSITY OF CAMBRIDGE
The Pitt Building, Trumpington Street, Cambridge, United Kingdom
CAMBRIDGE UNIVERSITY PRESS
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http://www.cambridge.org
© Cambridge University Press 2004
Chapter 8 is a work of the United States Government and is not protected
by Copyright in the United States
Quote from Before Eden used with kind permission of Arthur C. Clarke
This book is in copyright. Subject to statutory exception
and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without
the written permission of Cambridge University Press.
First published 2004
Printed in the United States of America
Typefaces ITC Stone Serif 9/12.5 pt. and ITC Symbol System LATEX 2e [TB]
A catalog record for this book is available from the British Library.
Library of Congress Cataloging in Publication Data
Infectious diseases and host–pathogen evolution / edited by Krishna R. Dronamraju.
p. cm.
Includes bibliographical references and index.
ISBN 0-521-82066-9
1. Microorganisms – Evolution. 2. Host–parasite relationship. 3. Evolutionary genetics.
4. Human evolution. I. Dronamraju, Krishna R.
QR13.I546 2004
616.9′041 – dc21 2003055194
ISBN 0 521 82066 9 hardback
To my friend Sir Arthur C. Clarke
“Likewise it absorbed a whole microcosmos of living creatures – the bacteria and viruses which, upon an older planet, had evolved into a thousand deadly strains.
“Even as the Morning Star set course for her distant home, Venus was dying. The films and photographs and specimens that Hutchins was carrying in triumph were more precious even than he knew. They were the only record that would ever exist of life's third attempt to gain a foothold in the solar system. Beneath the clouds of Venus, the story of Creation was ended.”
From Before Eden, by Arthur C. Clarke (1961)
| List of Contributors | page xi |
| Introduction Krishna R. Dronamraju |
1 |
| PART ONE. J. B. S. HALDANE | |
| 1 Haldane's Ideas in Biology with Special Reference to Disease and Evolution James F. Crow |
11 |
| 2 J. B. S. Haldane and the Malaria Hypothesis D. J. Weatherall |
18 |
| PART TWO. MALARIAL PARASITES | |
| 3 Evolutionary Genetics of Plasmodium falciparum, the Agent of Malignant Malaria Stephen M. Rich and Francisco J. Ayala |
39 |
| 4 Evolutionary Biology of Malarial Parasites Ananias A. Escalante and Altaf A. Lal |
75 |
| 5 G6PD Deficiency and Malarial Resistance in Humans: Insights from Evolutionary Genetic Analyses Sarah A. Tishkoff and Brian C. Verrelli |
113 |
| 6 The Enigma of Plasmodium vivax Malaria and Erythrocyte Duffy Negativity Peter A. Zimmerman |
141 |
| PART THREE. OTHER PARASITES | |
| 7 Influenza Evolution Robin M. Bush and Nancy J. Cox |
175 |
| 8 Free-Living to Freewheeling: The Evolution of Vibrio cholerae from Innocence to Infamy Rita R. Colwell, Shah M. Faruque, and G. Balakrish Nair |
198 |
| 9 Evolutionary Dynamics of Daphnia and Their Microparasites Tom Little and Dieter Ebert |
222 |
| 10 Human Susceptibility to Visceral Leishmaniasis (Leishmania donovani) and to Schistosomiasis (Schistosoma mansoni) Is Controlled by Major Genetic Loci A. Dessein, B. Bucheton, L. Argiro, N. M. A. Elwali, V. Rodrigues, C. Chevillard, S. Marquet, H. Dessein, S. H. El-Safi, and L. Abel |
241 |
| PART FOUR. GENETIC AND EVOLUTIONARY CONSIDERATIONS | |
| 11 The Evolution of Pathogen Virulence in Response to Animal and Public Health Interventions Andrew F. Read, Sylvain Gandon, Sean Nee, and Margaret J. Mackinnon |
265 |
| 12 Infection and the Diversity of Regulatory DNA | 293 |
| Lindsay G. Cowell, N. Avrion Mitchison, and Brigitte Muller | |
| 13 Genetic Epidemiology of Infectious Diseases: The First Half-Century Newton E. Morton |
307 |
| 14 The Impact of Human Genetic Diversity on the Transmission and Severity of Infectious Diseases Michel Tibayrenc |
315 |
| 15 Evolution and the Etiology of Diabetes Mellitus Kyle D. Cochran and Gregory M. Cochran |
325 |
| 16 The Future of Human Evolution Luca Cavalli-Sforza |
343 |
| Index | 353 |
L. Abel
Laboratory of Human Genetics of Infectious Diseases
INSERM, U. 550
Paris
France
L. Argiro
Immunology and Genetics of Parasitic Diseases
INSERM, U. 399
Marseille
France
Francisco J. Ayala
University of California, Irvine
Department of Ecology and Evolutionary Biology
321 Steinhaus Hall
Irvine, CA 92697-2525
B. Bucheton
Immunology and Genetics of Parasitic Diseases
INSERM, U. 399
Marseille
France
Robin M. Bush
Department of Ecology and Evolutionary Biology
University of California, Irvine
Irvine, CA 92697
Luca Cavalli-Sforza
Genetics Department, M346
Stanford University Medical School
Stanford, CA 94305-5120
C. Chevillard
Immunology and Genetics of Parasitic Diseases
INSERM, U. 399
Marseille
France
Kyle D. Cochran
57 Robbs Hill Road
Lunenberg, MA 01462
Gregory M. Cochran
6708 Loftus Street, N.E.
Albuquerque, NM 87109
Rita R. Colwell
Center of Marine Biotechnology
University of Maryland Biotechnology Institute
701 East Pratt Street
Baltimore, MD 21202
Lindsay G. Cowell
Department of Immunology
Campus Box 3010
Duke University Medical Center
Durham, NC 27701
Nancy J. Cox
Influenza Branch
Centers for Disease Control & Prevention
Atlanta, GA 30333
James F. Crow
Genetics Department
University of Wisconsin
Madison, WI 53706
A. Dessein
Immunology and Genetics of Parasitic Diseases
INSERM, U. 399
Marseille
France
Helia Dessein
Immunology and Genetics of Parasitic Diseases
INSERM, U. 399
Marseille
France
Krishna R. Dronamraju
Foundation for Genetic Research
PO Box 27701-0
Houston, TX 77227
Dieter Ebert
Université de Fribourg
Departement de Biologie
Ecologie et Evolution, Chemin du Musée 10
1700 Fribourg
Switzerland
S.H. El-Safi
Institute for Tropical Medicine
PO Box 1304
Khartoum
Sudan
N.M.A. Elwali
Institute of Nuclear Medicine and Molecular Biology
University of Gezira
Wad Medani
Sudan
Ananias A. Escalante
Division of Parasitic Diseases
National Center for Infectious Diseases
Centers for Disease Control and Prevention
Public Health Service
US Department of Health and Human Services
Atlanta, Georgia 30333
Shah M. Faruque
International Centre for Diarrhoeal Disease, Bangladesh
Dhaka
Bangladesh
Sylvain Gandon
School of Biological Sciences
University of Edinburgh
Edinburgh EH9 3JT
UK
Altaf A. Lal
U.S. Embassy
New Delhi, 110021
India
Tom Little
Institute for Cell, Animal and Population Biology
University of Edinburgh, Kings Buildings
West Mains Road
Edinburgh EH9 3JT
UK
Margaret J. Mackinnon
School of Biological Sciences
University of Edinburgh
Edinburgh EH9 3JT
UK
S. Marquet
Immunology and Genetics of Parasitic Diseases
INSERM, U. 399
Marseille
France
N. Avrion Mitchison
Department of Immunology
Windeyer Institute of Medical Science
46 Cleveland Street
London W1T 4JF
UK
Newton E. Morton
Human Genetics Division
University of Southampton
Duthie Building (MP 808)
Southampton General Hospital
Tremona Road
Southampton SO16 6YD
UK
Brigitte Muller
Deutsches Rheuma Zentrum Berlin
Shumannstrasse 21/22
10117 Berlin-Mitte
Germany
G. Balakrish Nair
International Centre for Diarrhoeal Disease, Bangladesh
Dhaka
Bangladesh
Sean Nee
School of Biological Sciences
University of Edinburgh
Edinburgh EH9 3JT
UK
Andrew F. Read
School of Biological Sciences
University of Edinburgh
Edinburgh EH9 3JT
UK
Stephen M. Rich
Division of Infectious Disease
Tufts University School of Veterinary Medicine
200 Westboro Road
North Grafton, MA 01536
V. Rodrigues
Laboratory of Immunology
University of Medicine
Triangulo Miniero
Uberaba
Brazil
Michel Tibayrenc
Unité de Recherche “génétique des maladies infectieuses”
Unité Mixte de Recherche no. 9926 Centre National de la Recherche Scientifique/ Institut de Recherche pour le Développement
911 avenue Agropolis, BP 64501
34394 Montpellier Cedex 5
France
Sarah A. Tishkoff
Department of Biology
Biology/Psychology Building
University of Maryland
College Park, MD 20742
Brian C. Verrelli
Department of Biology
Biology/Psychology Building
University of Maryland
College Park, MD 20742
D.J. Weatherall
Weatherall Institute of Molecular Medicine
University of Oxford, UK
Peter A. Zimmerman
The Center for Global Health and Diseases
Case Western Reserve University
School of Medicine, W147D
2109 Adelbert Road
Cleveland, OH