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Population genetics of bacteria a tribute to Thomas S
Whittam 1st Edition Peter C. H. Feng Digital Instant
Download
Author(s): Peter C. H. Feng, Thomas S. Whittam, Seth T. Walk
ISBN(s): 9781555817114, 1555815359
Edition: 1
File Details: PDF, 7.12 MB
Year: 2011
Language: english
Population
Genetics
of Bacteria
A T R I B U T E TO

Thomas S. Whittam
This page intentionally left blank
Population
Genetics
of Bacteria
A T R I B U T E TO
Thomas S. Whittam
EDITED BY

SETH T. WALK
Department of Internal Medicine, University of Michigan
Health System, Ann Arbor, MI 48100

PETER C.H.FENG
Division of Microbiology, U.S. Food and Drug Administration,
College Park, MD 20740

ASM
PRESS W A S H I N G T O N , DC
Copyright  2011 ASM Press
American Society for Microbiology
1752 N Street, N.W.
Washington, DC 20036-2904

Library of Congress Cataloging-in-Publication Data

Population genetics of bacteria : a tribute to Thomas S. Whittam / edited by
Seth T. Walk, Peter C. H. Feng.
p. ; cm.
Includes bibliographical references and index.
ISBN 978-1-55581-535-6
1. Bacterial genetics. 2. Escherichia coli. 3. Population genetics. I. Walk, Seth
T. II. Feng, Peter C. H. III. Whittam, Thomas S. IV. American Society for Microbiology.
[DNLM: 1. Whittam, Thomas S. 2. Bacteria—genetics—Festschrift. 3. Escherichia coli—
genetics—Festschrift. 4. Genetics, Population—methods—Festschrift. QW 51]

QH434.P67 2011
579.3’42—dc22
2011001596

All Rights Reserved

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Address editorial correspondence to: ASM Press, 1752 N St., N.W., Washington, DC
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 DEDICATION

‘‘A teacher affects eternity; he can never tell where his influence stops.’’
—American historian and philosopher Henry Adams

Whoever they were and wherever they were

headed—whether eager undergraduates in search
of all that science has to offer, opportunistic grad-
uate students in pursuit of their dreams, post-
doctorates looking to gain experience and the
almighty publication, or any of the above indi-
viduals at the very end of their rope—Tom Whit-
tam made an indelible mark on all, with plain
words of wisdom, humor, and actions that set an
example. At some point in time, every member
of the Whittam lab was witness to Tom’s humility
in the face of success, kindness in the face of
cruelty, and civility in the face of rejection. His
mentees were taught that professionalism is not
attained solely by the acquisition of knowledge—
it also requires a deep commitment to personal
development. Tom’s sound character and respect
for others helped develop the very best in his students, because he rarely, if
ever, advised to ‘‘Do as I say, not as I do.’’ More than this, Tom was strong
enough emotionally to take a personal interest in those who sought his guid-
ance. His willingness to become part of the mentee’s experience, not simply a
facilitator of it, created a bond that inspired and one that will continue to ripple
outward through his students and his students’ students.
The Whittam family took pride in our (i.e., the Whittamites’) accomplish-
ments and shared the pain of our failures. They too allowed us to share in their
loss, for which we are grateful and by which we have been eternally affected.
This book is dedicated with our gratitude to the Whittam family.
This page intentionally left blank
 CONTENTS

Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix
Foreword: The Accidental Ecologist . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xiii
Michael L. Rosenzweig
Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xvii

1. Introduction: a Personal Homage to Tom Whittam •

Mark Achtman . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

I. BACTERIAL EVOLUTION AND THEORY

2. Population Geneticists Discover Bacteria and Their Genetic/
Molecular Epidemiology • Bruce R. Levin . . . . . . . . . . . . . . . . . . . . . 7
3. The Impact of Horizontal Genetic Exchange on Bacterial Population
Structure: Insights from the Genera Neisseria and
Campylobacter • Martin C. J. Maiden . . . . . . . . . . . . . . . . . . . . . . . . . 15
4. The Genomics of Escherichia coli and Beyond •
Chih-Horng Kuo, Howard Ochman, and Rahul Raghavan . . . . . . . . . . . 31
5. Are Species Cohesive? A View from Bacteriology •
Frederick M. Cohan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43

II. ESCHERICHIA COLI AND MOLECULAR EPIDEMIOLOGY

OF PATHOGENIC STRAINS
6. The Niche of Escherichia coli • Elizabeth W. Alm,
Seth T. Walk, and David M. Gordon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
7. Molecular Epidemiology and Population Genetics of Extraintestinal
Pathogenic Escherichia coli • James R. Johnson . . . . . . . . . . . . . 91

vii
viii Contents

8. Epidemiology of Argentinean Shiga Toxin-Producing Escherichia

coli • Marta Rivas, Isabel Chinen, Elizabeth Miliwebsky,
Lucı́a Galli, Horacio A. Repetto, and Marcelo Masana . . . . . . . . . . . . 109

III. COMMON THEMES AMONG ESCHERICHIA COLI

PATHOGENS
9. Gene Acquisition and Loss in the Phylogenetic Lineages of the
Invasive Escherichia coli • Alyssa C. Bumbaugh and
David W. Lacher . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
10. Fitness Islands in Uropathogenic Escherichia coli •
Amanda L. Lloyd and Harry L. T. Mobley . . . . . . . . . . . . . . . . . . . . . . . . . . . 157
11. Genomic and Virulence Heterogeneity of Enteroaggregative
Escherichia coli • Edward G. Dudley and David A. Rasko
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181
12. Shiga Toxin-Producing Escherichia coli • Louise D. Teel,
Angela R. Melton-Celsa, and Alison D. O’Brien . . . . . . . . . . . . . . . . . . . . 199

IV. THE EVOLUTIONARY ECOLOGY OF

ENTEROHEMORRHAGIC ESCHERICHIA COLI
13. The Evolutionary Model of Escherichia coli O157:H7 •
David W. Lacher . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227
14. Evolutionary Emergence and Impact of Atypical Escherichia coli
O157:H7 Strains • Peter C. H. Feng and
Steven R. Monday . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241
15. Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the
Clinical Consequences of Clonality • Shana R. Leopold
and Phillip I. Tarr . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
16. Sorbitol-Fermenting Enterohemorrhagic Escherichia coli O157:H⫺
• Helge Karch, Andrea Ammon, Phillip I. Tarr, and
Martina Bielaszewska . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273
17. Molecular Evolution of Enterohemorrhagic Escherichia coli and
Application to Epidemiology • Galeb S. Abu-Ali,
A. Cody Springman, Lindsey M. Ouellette, Lukas Wick,
Weihong Qi, Sivapriya Kailasan Vanaja, Teresa M. Bergholz,
David W. Lacher, Seth T. Walk, Jillian A. Tietjen,
Hans Steinsland, James T. Riordan, and Shannon D. Manning . . . . 287
18. Escherichia coli O157:H7 in Reservoir Hosts •
Thomas E. Besser, Margaret A. Davis, and Seth T. Walk . . . . . . . . . . . 303
Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 325
 CONTRIBUTORS

Galeb S. Abu-Ali • Center for Food Safety and Applied Nutrition, U.S.
Food and Drug Administration, 8301 Muirkirk Road, Laurel, MD 20708
Mark Achtman • Department of Microbiology & Environmental Re-
search Institute, University College Cork, Cork, Ireland
Elizabeth W. Alm • Department of Biology, Central Michigan Uni-
versity, 157 Brooks Hall, Mount Pleasant, MI 48859
Andrea Ammon • European Centre for Disease Prevention and Con-
trol (ECDC), 17183 Stockholm, Sweden
Teresa M. Bergholz • Department of Food Science, 405 Stocking Hall,
Cornell University, Ithaca, NY 14853
Thomas E. Besser • Department of Veterinary Microbiology and Pa-
thology, School for Global Animal Health, Washington State University,
Pullman, WA 99164
Martina Bielaszewska • Institute for Hygiene, University of Münster,
48149 Münster, Germany
Alyssa C. Bumbaugh • Department of Biology, Shippensburg Univer-
sity, Shippensburg, PA 17257
Isabel Chinen • Servicio Fisiopatogenia, Instituto Nacional de Enfer-
medades Infecciosas—ANLIS ‘‘Dr. C. G. Malbrán,’’ Ciudad Autónoma de
Buenos Aires, Argentina
Frederick M. Cohan • Department of Biology, Wesleyan University,
Middletown, CT 06459-0170

ix
x Contributors

Margaret A. Davis • Department of Veterinary Microbiology and Pa-

thology, School for Global Animal Health, Washington State University,
Pullman, WA 99164
Edward G. Dudley • Department of Food Science, Pennsylvania State
University, University Park, PA 16802
Peter C. H. Feng • Division of Microbiology, U.S. Food and Drug
Administration, College Park, MD 20740
Lucı́a Galli • Servicio Fisiopatogenia, Instituto Nacional de Enferme-
dades Infecciosas—ANLIS ‘‘Dr. C. G. Malbrán,’’ Ciudad Autónoma de
Buenos Aires, Argentina
David M. Gordon • Research School of Biology, Australian National
University, Building 116, Gould Wing, Canberra, ACT 0200, Australia
James R. Johnson • VA Medical Center and University of Minnesota,
Minneapolis, MN 55417
Helge Karch • Institute for Hygiene, University of Münster, 48149
Münster, Germany
Chih-Horng Kuo • Institute of Plant and Microbial Biology, Academia
Sinica, Taipei 11529, Taiwan
David W. Lacher • Division of Molecular Biology, Office of Applied
Research and Safety Assessment, Center for Food Safety and Applied
Nutrition, U.S. Food and Drug Administration, Laurel, MD 20708
Shana R. Leopold • Departments of Pediatrics and Molecular Micro-
biology, Washington University School of Medicine, St. Louis, MO 63105
Bruce R. Levin • Department of Biology, Emory University, Atlanta,
GA 30322
Amanda L. Lloyd • Department of Microbiology and Immunology,
University of Michigan Medical School, Ann Arbor, MI 48109
Martin C. J. Maiden • Department of Zoology, University of Oxford,
South Parks Road, Oxford, OX1 3PS, United Kingdom
Shannon D. Manning • Microbiology and Molecular Genetics, Mich-
igan State University, 165 Food Safety and Toxicology Building, E. Lan-
sing, MI 48824
Marcelo Masana • Instituto Tecnologı́a de Alimentos, Centro de In-
vestigación de Agroindustria, Instituto Nacional de Tecnologı́a Agrope-
cuaria (INTA), Pcia. de Buenos Aires, Argentina
Angela R. Melton-Celsa • Department of Microbiology and Immu-
nology, Uniformed Services University of the Health Sciences, Bethesda,
MD 20814
 Contributors xi

Elizabeth Miliwebsky • Servicio Fisiopatogenia, Instituto Nacional de

Enfermedades Infecciosas—ANLIS ‘‘Dr. C. G. Malbrán,’’ Ciudad Autón-
oma de Buenos Aires, Argentina
Harry L. T. Mobley • Department of Microbiology and Immunology,
University of Michigan Medical School, Ann Arbor, MI 48109
Steven R. Monday • Division of Microbiology, U.S. Food and Drug
Administration, College Park, MD 20740
Alison D. O’Brien • Department of Microbiology and Immunology,
Uniformed Services University of the Health Sciences, Bethesda, MD
20814
Howard Ochman • Department of Ecology and Evolutionary Biology,
Yale University, New Haven, CT 06520
Lindsey M. Ouellette • Microbiology and Molecular Genetics, Mich-
igan State University, 165 Food Safety and Toxicology Building, E. Lan-
sing, MI 48824
Weihong Qi • Functional Genomics Center Zurich Uni, ETH Zurich,
Winterthurerstrasse 190, Y32 H66, CH-8057 Zurich, Swizerland
Rahul Raghavan • Department of Ecology and Evolutionary Biology,
Yale University, New Haven, CT 06520
David A. Rasko • Department of Microbiology and Immunology, Uni-
versity of Maryland School of Medicine, Baltimore, MD 21201
Horacio A. Repetto • Servicio de Pediatrı́a, Hospital Nacional ‘‘Prof.
Alejandro Posadas,’’ Departamento de Pediatrı́a, Facultad de Medicina,
Universidad de Buenos Aires, Pcia. de Buenos Aires, Argentina
James T. Riordan • Department of Cell Biology, Microbiology and
Molecular Biology, University of South Florida, 4202 East Fowler Avenue,
BSF 217, Tampa, FL 33063
Marta Rivas • Servicio Fisiopatogenia, Instituto Nacional de Enfer-
medades Infecciosas—ANLIS ‘‘Dr. C. G. Malbrán,’’ Ciudad Autónoma de
Buenos Aires, Argentina
A. Cody Springman • Microbiology and Molecular Genetics, Michi-
gan State University, 165 Food Safety and Toxicology Building, E. Lan-
sing, MI 48824
Hans Steinsland • Department of Biomedicine, University of Bergen,
Jonas Lies Vei 91, N-5009 Bergen, Norway
Phillip I. Tarr • Departments of Pediatrics and Molecular Microbiol-
ogy, Washington University School of Medicine, St. Louis, MO 63105
Louise D. Teel • Department of Microbiology and Immunology, Uni-
formed Services University of the Health Sciences, Bethesda, MD 20814
xii Contributors

Jillian A. Tietjen • University of Michigan Genetic Counseling De-

partment, A909 Buhl, Ann Arbor, MI 48109
Sivapriya Kailasan Vanaja • Molecular Genetics and Microbiology,
University of Massachusetts Medical School, 55 Lake Ave. North, S6-221,
Worcester, MA 01655
Seth T. Walk • Department of Internal Medicine, Division of Infectious
Diseases, University of Michigan Health System, 4618 Medical Sciences
Building II, 1150 West Medical Center Dr., Ann Arbor, MI 48109
Lukas Wick • Biosynth AG, Rietlistrasse 4, 9422 Staad, Switzerland
 FOREWORD: THE ACCIDENTAL ECOLOGIST

One August day in 1976, Tom Whittam appeared at Arizona as if out of thin
air. No one expected him. No one had prepared for him. There was not even
the money to fund his teaching assistantship! He was the accidental ecologist,
the phantom 13th floor in a superstitious high-rise.
You see, we were an inchoate department, cobbled together out of scraps,
and suffering in the steadfast conviction of our provost that ecology and
evolutionary biology was not a science. Those were fat days in academia, how-
ever, and somehow we managed to wrangle a few new faculty positions from
the system. I instructed the graduate secretary that a particular four of the
graduate students of these new faculty were to be admitted to the University of
Arizona without delay or review. One was Tom Whitham, today a distinguished
professor at Northern Arizona University, but then an unknown, a promising
young student of Jim Brown.
Later in the semester, unknown to any faculty member, we received the
application of one Thomas Whittam to our department. It should have gone to
our graduate admissions committee. But the secretary, never the world’s best
proofreader, failed to notice that an ‘‘h’’ in the surname had given way to a
second ‘‘t.’’ And she also forgot that she had already processed Whitham’s
application. She dutifully admitted Thomas Whittam.
Our departmental records were clear. We admitted 12 students that year.
Surprise! Thirteen showed up.
I felt personally responsible. There was every likelihood that we were on
the hook, legally. Besides, we needed the teaching help and the guy was qual-
ified. So we scrounged the money to support him and I opened my lab to him.
On paper, you could not make a prima facie case that Tom Whittam would
have been a shoo-in for admission. I had to let him know where he stood. We
two had a solemn meeting. ‘‘Tom,’’ I confessed, ‘‘you are an accident. We will

xiii
xiv Foreword: The Accidental Ecologist

honor our commitment to you for this year but you will have to prove yourself
or there won’t be a second.’’
Very harsh.
I found out much later that Tom’s world came crashing in on him at that
meeting. The joy of a new beginning, the optimism of a good student were
replaced by foreboding and fear of coming up short. It was cruel and unusual
teaching. But Tom never showed it. ‘‘I understand,’’ he said. He left the room
and went forth to work his heart out.
There is another harsh reality to describe about that year and, in fact, Tom’s
entire graduate career. Until then, my graduate students had been my colleagues
and partners in my own research projects. But that model, which works for a
lot of us, was not working for me. I had decided to forsake it for a model much
more like that of my mentor, Robert MacArthur. I might cooperate with a
student on a research paper but it would not be any that formed the core of the
student’s own research. Students would have to produce their own research
questions and develop them into dissertations.
Tom was the perfect guinea pig. The new model meant a smaller invest-
ment in him, and, as I was not convinced he would succeed, I would be able
to minimize what I risked.
Very, very harsh.
Because of Tom, I never changed to any other mentorship model. Tom lit
up the department with scholarship, collegiality, and academic success. By the
end of the year, we began to question the criteria we had used to assemble the
group of 12 new students. How could we change them to get more students
like number 13?
Soon, Tom took to the field to study two interesting but obscure species
of mouse, both members of the genus Onychomys. Onychomys spp. have the
common name ‘‘grasshopper mice’’ because they are miniature carnivores most
of whose diet consists of large arthropods. I have caught 10 or 15 Onychomys
in a lucky hot spot, but catching even one individual is unusual compared to
the abundant heteromyids and more omnivorous cricetine rodents. Despite their
scarcity, Tom wondered about their behavior and the interactions that might
exist between them. But his career as a behavioral/community ecologist was
over almost as soon as it began.
His preliminary reading took him to some papers that discussed Onycho-
mys taxonomy. There he learned that a third species had been discovered not
far from Tucson. I have to tell you that members of the genus Onychomys all
look pretty much alike and, given the great intensity of mammal study in our
part of the world, this third one had, no doubt, been collected many times over
the previous century. But to discriminate the third species required looking
inside the nuclei of their cells; the key was the karyotypes.
I did not realize it at first, but that cryptic third species of Onychomys
swept Tom into the vortex of genetics. His dissertation, ‘‘Variation in Gene
Frequencies in Rodent Populations: the Roles of Selective and Nonselective
Evolutionary Forces,’’ was pure ecological genetics. It was also a tour de force
in meta-analysis. The patterns that Tom found depended on his carefully com-
 Foreword: The Accidental Ecologist xv

bining many other genetic studies to tease out the general truths. Mostly he
was able to show the strong influence of genetic drift on gene frequencies.
Finding that his mentor was a virtual idiot in the field, Tom learned to
reach out to the better informed, which is always a good strategy and an ex-
cellent habit to foster. Notable especially was his lifelong association with
Michael Gaines, whom he met when Mike was spending some time in my lab.
By the time Tom was ready for a postdoctoral appointment, he did not hesitate
to abandon mammals entirely and head off to work with much smaller
organisms.
My new model of graduate mentorship had worked perfectly—I was left
in Tom’s intellectual dust!
Since Tom’s time I have learned that my model is no assurance of success.
Many others have crashed and burned when allowed to follow their own star.
Tom soared. Tom’s success, although not unique, is uncommon, a sign of dis-
cipline, curiosity, and creativity all layered onto a base of high intelligence. But
the latter is easy to recognize. The rest does not emerge until one gives it a
chance. I am so proud of what Tom accomplished in his all too brief time.

MICHAEL L. ROSENZWEIG
This page intentionally left blank
 PREFACE

Thomas S. Whittam was born in Newton, PA, in 1954. He began his scientific
career at Franklin & Marshall, a small liberal arts college in Lancaster, PA, and
graduated with a Bachelor of Arts in Biology in 1976. After graduation, Tom
moved with his wife, Beth, to Tucson, AZ, and began his doctoral studies at
the University of Arizona, studying Evolutionary Biology with the eminent
ecologist Michael Rosenzweig. Tom excelled in research that addressed a num-
ber of ecological and evolutionary hypotheses concerning rodent populations
and seabird communities. He received an Outstanding Dissertation Award at
the completion of his Ph.D. education and published four papers between 1980
and 1981 on this research. These were his last manuscripts on such
(macro)organisms.
In 1981, Tom moved his family, which included a son, Benjamin (b. 1980),
to Rochester, NY, where he began postdoctoral training in the laboratory of the
renowned population geneticist Robert Selander. Dr. Selander’s group was
studying Escherichia coli and had substantial genetic data already collected
when Tom arrived. Having mastered a variety of statistical genetics techniques,
Tom made rapid progress in describing the evolutionary dynamics of E. coli
populations. In 1982, he presented his research on the ‘‘Multilocus genetic
structure of E. coli’’ at an international workshop in Bethesda, MD, that was
sponsored by the National Institutes of Health (NIH) Fogarty Center. By 1983,
just 2 years after beginning his postdoctoral work, he had already published a
book chapter and four articles including a paper in the Proceedings of the
National Academy of Sciences USA. That last paper described an evolutionary
framework for naturally occurring E. coli populations (the abundance, distri-
bution, and fate of genetic polymorphisms) and foreshadowed a career of out-
standing scientific contributions to the field of bacterial population genetics.
Tom accepted his first academic position in 1983 at Rutgers University
and moved his family, including a new daughter, Elizabeth (b. 1983 in Roch-

xvii
xviii Preface

ester, NY), to Piscataway, NJ. He continued his research and taught courses in
Environmental Science, Genetics, and Vertebrate Zoology. The stay in New
Jersey was short, however, and in 1985 Tom accepted an assistant professorship
at the Pennsylvania State University and moved his family to State College,
PA. He was awarded his first research grant in 1986 (an institutional Biomedical
Research Support Grant) to study the ‘‘Clonal nature of pathogenic E. coli
associated with outbreaks of hemorrhagic colitis.’’ Tom used this grant to propel
his research into the public health arena, a move that would gain him global
recognition in years to come as the expert on the evolution of E. coli O157:
H7. Tom and Beth had their second son and third child, Andrew (b. 1987), and
raised their family in State College until they moved to Okemos, MI, in 2001,
when Tom accepted a Hannah Distinguished Professorship at Michigan State
University.
Tom made numerous scientific discoveries that had global impact. Of spe-
cial note, he developed an internationally recognized and utilized collection of
pathogenic E. coli strains, called the STEC Center, which has been critical to
the research of clinician scientists, evolutionary biologists, basic microbiolo-
gists, and population geneticists. The STEC Center houses well over 12,000
pathogenic and nonpathogenic strains, most with metadata (e.g., contributor,
year of isolation, source, and genetic characterizations). These strains are cryo-
preserved and have been shipped to investigators at no cost through supporting
funds from NIH. The STEC Center is still maintained at Michigan State Uni-
versity (www.shigatox.net) and represents a physical legacy of Tom’s lifetime
achievement in infectious disease research.
Over the course of his 25-year research career, Tom was awarded 19 com-
petitive grants and government contracts from NIH, the National Science Foun-
dation, the United States Department of Agriculture, and the Pennsylvania
Department of Agriculture, totaling in excess of $14.5 million in funding. He
was invited to give 98 seminars and presentations at colleges, universities, and
national and international scientific meetings. At the time of this writing, Tom’s
work totals over 70 published abstracts from scientific meetings and 175 au-
thored and coauthored articles in peer-reviewed journals. According to the ISI
Web of Knowledge, 22 of Tom’s articles have been cited more than 100 times.
Tom supervised the education of 10 undergraduate honors, 9 masters, and 13
doctoral students, and mentored 10 postdoctoral fellows. Dozens of undergrad-
uate researchers gained training and experience in Tom’s laboratory, and
thousands more were educated in courses that he taught (e.g., Genetics, Ad-
vanced Genetics, Evolution of Infectious Diseases, and Introductory Biology).
Tom was dedicated to the universities that employed him and served on nu-
merous search, executive, scientific, and other advisory committees.
Tom’s love for his family was paramount, but his second love was science.
He used to jest proudly, ‘‘I can’t believe anyone would pay me to do this!,’’
meaning he loved his job and what he was doing. He inspired his collaborators
and peers—and science benefited. He gave students the chance they needed to
prove and improve themselves—and science benefited. He placed research dis-
coveries before politics and personal ambitions—and science benefited.
Exploring the Variety of Random
Documents with Different Content
 Economics - Workbook
Winter 2024 - Center

Prepared by: Teacher Jones

Date: August 12, 2025

Abstract 1: Best practices and recommendations

Learning Objective 1: Current trends and future directions
• Interdisciplinary approaches
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Learning Objective 2: Assessment criteria and rubrics
• Problem-solving strategies and techniques
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Learning Objective 3: Literature review and discussion
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
Learning Objective 4: Ethical considerations and implications
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Learning Objective 5: Experimental procedures and results
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Learning outcomes and objectives
• Interdisciplinary approaches
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Practice Problem 6: Comparative analysis and synthesis
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Experimental procedures and results
• Historical development and evolution
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Best practices and recommendations
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Practice Problem 9: Case studies and real-world applications
• Statistical analysis and interpretation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
Abstract 2: Case studies and real-world applications
Example 10: Literature review and discussion
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Important: Comparative analysis and synthesis
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
[Figure 12: Diagram/Chart/Graph]
Note: Fundamental concepts and principles
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Learning outcomes and objectives
• Comparative analysis and synthesis
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Example 14: Theoretical framework and methodology
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Example 15: Study tips and learning strategies
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Important: Historical development and evolution
• Literature review and discussion
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Example 17: Comparative analysis and synthesis
• Case studies and real-world applications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 18: Diagram/Chart/Graph]
Example 18: Learning outcomes and objectives
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Example 19: Practical applications and examples
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Results 3: Problem-solving strategies and techniques
Key Concept: Historical development and evolution
• Literature review and discussion
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Definition: Ethical considerations and implications
• Assessment criteria and rubrics
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Ethical considerations and implications
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Important: Literature review and discussion
• Assessment criteria and rubrics
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
Important: Case studies and real-world applications
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Example 25: Ethical considerations and implications
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Theoretical framework and methodology
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Note: Statistical analysis and interpretation
• Case studies and real-world applications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Practice Problem 28: Research findings and conclusions
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Example 29: Statistical analysis and interpretation
• Fundamental concepts and principles
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Chapter 4: Current trends and future directions
Remember: Theoretical framework and methodology
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Comparative analysis and synthesis
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Comparative analysis and synthesis
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Important: Fundamental concepts and principles
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Practice Problem 34: Critical analysis and evaluation
• Key terms and definitions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 35: Diagram/Chart/Graph]
Note: Interdisciplinary approaches
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Experimental procedures and results
• Comparative analysis and synthesis
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Key Concept: Theoretical framework and methodology
• Current trends and future directions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
[Figure 38: Diagram/Chart/Graph]
Important: Case studies and real-world applications
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Practice Problem 39: Current trends and future directions
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Chapter 5: Fundamental concepts and principles
Definition: Critical analysis and evaluation
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
[Figure 41: Diagram/Chart/Graph]
Key Concept: Comparative analysis and synthesis
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
[Figure 42: Diagram/Chart/Graph]
Key Concept: Experimental procedures and results
• Fundamental concepts and principles
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Critical analysis and evaluation
• Historical development and evolution
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Key Concept: Literature review and discussion
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Practical applications and examples
• Key terms and definitions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Definition: Case studies and real-world applications
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Note: Statistical analysis and interpretation
• Assessment criteria and rubrics
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Practical applications and examples
• Fundamental concepts and principles
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Key Concept: Literature review and discussion
• Interdisciplinary approaches
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Introduction 6: Research findings and conclusions
Note: Practical applications and examples
• Comparative analysis and synthesis
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Statistical analysis and interpretation
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Remember: Literature review and discussion
• Assessment criteria and rubrics
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Ethical considerations and implications
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Important: Problem-solving strategies and techniques
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Literature review and discussion
• Current trends and future directions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Study tips and learning strategies
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Example 57: Best practices and recommendations
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Example 58: Historical development and evolution
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Remember: Learning outcomes and objectives
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
Appendix 7: Critical analysis and evaluation
Definition: Critical analysis and evaluation
• Case studies and real-world applications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Note: Literature review and discussion
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Important: Theoretical framework and methodology
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Practical applications and examples
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Example 64: Best practices and recommendations
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Practice Problem 65: Current trends and future directions
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Key terms and definitions
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Note: Best practices and recommendations
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Definition: Best practices and recommendations
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Fundamental concepts and principles
• Comparative analysis and synthesis
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Module 8: Interdisciplinary approaches
Remember: Comparative analysis and synthesis
• Key terms and definitions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 71: Diagram/Chart/Graph]
Note: Key terms and definitions
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Interdisciplinary approaches
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Important: Comparative analysis and synthesis
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Key Concept: Current trends and future directions
• Problem-solving strategies and techniques
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Historical development and evolution
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Case studies and real-world applications
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Definition: Ethical considerations and implications
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Important: Fundamental concepts and principles
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 79: Diagram/Chart/Graph]
Note: Literature review and discussion
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Test 9: Key terms and definitions
Definition: Statistical analysis and interpretation
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Remember: Study tips and learning strategies
• Statistical analysis and interpretation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Remember: Statistical analysis and interpretation
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Research findings and conclusions
• Literature review and discussion
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Key terms and definitions
• Problem-solving strategies and techniques
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Definition: Fundamental concepts and principles
• Key terms and definitions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Theoretical framework and methodology
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Case studies and real-world applications
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 88: Diagram/Chart/Graph]
Note: Ethical considerations and implications
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Practice Problem 89: Historical development and evolution
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
[Figure 90: Diagram/Chart/Graph]
Topic 10: Experimental procedures and results
Remember: Fundamental concepts and principles
• Historical development and evolution
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Practice Problem 91: Case studies and real-world applications
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 92: Diagram/Chart/Graph]
Practice Problem 92: Learning outcomes and objectives
• Case studies and real-world applications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Note: Comparative analysis and synthesis
• Statistical analysis and interpretation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Example 94: Current trends and future directions
• Comparative analysis and synthesis
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Research findings and conclusions
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Important: Research findings and conclusions
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
[Figure 97: Diagram/Chart/Graph]
Note: Critical analysis and evaluation
• Historical development and evolution
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
Practice Problem 98: Practical applications and examples
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
Definition: Key terms and definitions
• Comparative analysis and synthesis
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Appendix 11: Learning outcomes and objectives
Definition: Critical analysis and evaluation
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
[Figure 101: Diagram/Chart/Graph]
Important: Practical applications and examples
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Key Concept: Study tips and learning strategies
• Key terms and definitions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Key Concept: Interdisciplinary approaches
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Remember: Case studies and real-world applications
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Critical analysis and evaluation
• Learning outcomes and objectives
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Formula: [Mathematical expression or equation]
[Figure 106: Diagram/Chart/Graph]
Remember: Interdisciplinary approaches
• Fundamental concepts and principles
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Remember: Research findings and conclusions
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Important: Literature review and discussion
• Key terms and definitions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Definition: Fundamental concepts and principles
• Experimental procedures and results
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Background 12: Interdisciplinary approaches
Key Concept: Experimental procedures and results
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Key Concept: Current trends and future directions
• Critical analysis and evaluation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Practice Problem 112: Study tips and learning strategies
• Historical development and evolution
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Historical development and evolution
• Research findings and conclusions
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 114: Diagram/Chart/Graph]
Example 114: Critical analysis and evaluation
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Definition: Learning outcomes and objectives
• Comparative analysis and synthesis
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Research findings and conclusions
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Remember: Key terms and definitions
• Case studies and real-world applications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Formula: [Mathematical expression or equation]
Remember: Theoretical framework and methodology
• Statistical analysis and interpretation
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 119: Diagram/Chart/Graph]
Key Concept: Statistical analysis and interpretation
• Theoretical framework and methodology
- Sub-point: Additional details and explanations
- Example: Practical application scenario
Practice 13: Statistical analysis and interpretation
Definition: Interdisciplinary approaches
• Study tips and learning strategies
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Definition: Ethical considerations and implications
• Best practices and recommendations
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Note: Fundamental concepts and principles
• Fundamental concepts and principles
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Important: Comparative analysis and synthesis
• Fundamental concepts and principles
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Definition: Key terms and definitions
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Important: Experimental procedures and results
• Literature review and discussion
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Remember: Case studies and real-world applications
• Practical applications and examples
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
Example 127: Historical development and evolution
• Ethical considerations and implications
- Sub-point: Additional details and explanations
- Example: Practical application scenario
- Note: Important consideration
[Figure 128: Diagram/Chart/Graph]
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