Examination of Modern LeadershipModule 1 Leadership History, F.docx

Examination of Modern Leadership
Module 1: Leadership: History, Fundamentals, and the Modern
Context
Module 1 content establishes the context for the entire course
dedicated to the examination of modern and postmodern
leadership. The introduction of critical theory and its use in
ORG561 provides a framework for investigation. The context of
social, economic, political, and technological environments
informs an exploration of modern and postmodern leadership
approaches. Emphasis on leader self-awareness sets the stage
for reflection, introspection, and personal leadership
development.
Learning Outcomes
1. Compare and contrast historical leadership concepts against
modern and postmodern organization needs.
2. Analyze leadership approaches using a critical framework.
3. Construct a personal leadership biography.
For Your Success & Readings
A key to success in ORG561 is to start early, build, reflect,
reinforce, build, reflect, and reinforce.
Begin each week’s study by reading and comprehending
the learning outcomes. Learning outcomes are always revealed
in assignments, discussions, and lectures. Likewise, learning
outcomes are reflected in rubrics, which are used as objective
measures for scoring and grading. Establish the learning
outcomes as your checklist for success.
In Module 1 criticaltheory is introduced through the readings,
lecture, discussion, and Critical Thinking Assignment. The
critical approach provides new frameworks on which to research
leadership. You may not be familiar with critical inquiry, so
seize the opportunity to advance your analytic skills. You are
expected to use one or more critical frames in each module of
this course. Take the time this week to fully understand the
reasoning and context of critical theory.

Studying the history of leadership requires reading publications
from earlier eras. Notice that some of the required and
recommended readings for Module 1 are not current
publications, but these contribute to understanding the earlier
periods of organization and leadership study.
Postmodern leadership literature expounds on the notion
that self-awareness is a critical component required to lead. In
ORG561, the thread of self-examination is woven throughout
the course. You will have opportunities to move beyond
reflection to develop a better understanding of personal
assumptions and biases, skills and competencies, and
professional development plans, all related to leadership.
Embrace the opportunity!
Required
· Introduction and Chapters 1 & 2 in Leadership: A Critical
Text
· Axley, S. R. (1990). The practical qualities of effective
leaders. Industrial Management, 32(5), 29-31.
· Brocato, B., Jelen, J., Schmidt, T., & Gold, S.
(2011). Leadership conceptual ambiguities.Journal of
Leadership Studies, 5(1), 35-50. doi:10.1002/jls.20203
· Gandolfi, F., & Stone, S. (2016). Clarifying leadership: High-
impact leaders in a time of leadership crisis. Revista De
Management Comparat International, 17(3), 212-224.
· Blom, M. (2016). Leadership studies – A Scandinavian
inspired way forward? Scandinavian Journal of Management,
32(2), 106-111. Retrieved from, https://www-sciencedirect-
com.csuglobal.idm.oclc.org/science/article/pii/S0956522116300
215 .
· Kooskora, M., & Piigli, M. (2015). Discussion of the
leadership profile of female top executives. Journal of
Management & Change, 34/35(1/2), 107-122.
· Mumford, E. (1906, September). The origins of
leadership. American Journal of Sociology 12(2) 216-240.
Retrieved from http://www.jstor.org/stable/2762385.
· Parker, M. (1992). Post-modern organizations or postmodern

organization theory? Organization Studies, 13(1), 001-17.
Recommended
· Cheng, B. S., Chou, L. F., Wu, T. Y., Huang, M. P., & Farh, J.
L. (2004). Paternalistic leadership and subordinate responses:
Establishing a leadership model in Chinese organizations. Asian
Journal of Social Psychology, 7(1), 89-117.
· Joplin, J. R., & Daus, C. S. (1997). Challenges of leading a
diverse workforce. Academy of Management Executive, 11(3),
32-47. doi:10.5465/AME.1997.9709231662
· Snaebjornsson, I. M., & Vaiciukynaite, E. (2016). Emotion
contagion in leadership: Followercentric approach.Business and
Economic Horizons, 12(2), 53-62.
· Ulrich, D. (2015). Leadership capital index. [n.p.]: Berrett-
Koehler Publishers.
. A Critical Investigation of Leadership
From early childhood we learn about leaders—and that they are
meant to be followed. Simple active games, such as follow the
leader or movie song lyrics from the likes of Peter
Pan (click here and read the first two stanzas) begin to frame
our references and perceptions about meaning, purpose, and
actions of leaders. Children learn that leaders are to be followed
and extolled for their virtues. Becoming a leader, many of us
might deduce, carries a notion of supremacy, and children move
into adulthood with those early assumptions about leadership.
But after more than a century of scientific research on the topic,
we know that the term leadership has different meanings and
evokes emotional responses based on circumstances, situations,
and personal beliefs. Snaebjornsson and Vaiciukynaite (2016),
for example, pointed out that leadership is studied more than
other management fields. So what happens between the time
that children follow the leader and that time when they grow up
and face the complexity of leadership and the question they
once thought they understood?
Likely, some of the confusion about terminology comes from
language used and concept development during youth. With

expanding experiences, adult perceptions change and our
childhood beliefs do not match the reality of the way
organizations work and attempt to survive. Click through each
item for examples of how the term leadership might be
considered by different people in varying roles in organizations.
Leadership: Interpretations of Term
· Leadership as group
· Leadership as individual
· Leadership as influence
For leadership scholars, even the reasoning behind the
examination is unsettled. Zehndorfer (2014) offered
explanations for why leadership study is important and
suggested that leadership study reduces organizational risk by
using history to inform decisions and to avoid mistakes. But
Zehndorfer also questioned how leadership success can be
measured.
Northhouse (as cited in Snaebjornsson & Vaiciukynaite, 2016,
p. 54) offered a structure for study by identifying four common
elements found in most leadership studies:
Snaebjornsson and Vaiciukynaite (2016) advised that numerous
definitions and theories present many options for research
approaches—and so many choices, the authors contended,
compound the difficulty of agreeing on common standards,
which makes comparing results and finding commonalities even
tougher.
With no common definition or structure—or even conceptual
agreement on leadership or how leaders lead—scholars and
organizational managers are wise to continue to probe for
answers. To simply accept theories, principles, and concepts
based on the latest leadership studies results in trends, altered
practices, and fads that may or may not be effective. There may
be no guiding star to understanding the definition of leadership,
but there are rational methods to help mitigate the risk to
organizations.

For the purposes of ORG561: Examination of Modern
Leadership, in-depth analysis is the core of discovery.
Using critical theory (CT) to ground the investigation, we
explore leadership taking a critical approach in an attempt to
challenge assumptions about the role of the leader and
leadership’s practical application in the modern organization
(Western, 2013). Content in Table 1 below displays two
common approaches to using critical theory in leadership
research.
Table 1
Two approaches for using critical theory in leadership research
Critical Theoretical Approaches to Study Leadership
1. To examine the less obvious and deeper leadership theories
and practices in the name of attaining organizational goals.
Or
2. To rethink and reinvent leadership through new discoveries
in the attempt to build a better society.
Adapted from Western, 2013
Authors such as Western (2013) and Snaebjornsson and
Vaiciukynaite (2016) posited that scholars and managers must
move beyond their biases to improve organizations. Critiquing
common assumptions and beliefs about leadership is at the heart
of critical theory, as noted above. A relatively small but
growing number of scholars have adopted critical management
studies (CMS) as an approach to study leadership and
management in organizations and work (Western, 2013).
To conduct critical analysis, Western purported that frameworks
may be used to provide a structure for research. As we move
forward in this course to examine leadership, recall that
Western (2013) proposed a four-frame structure for critical
inquiry—see Table 2, below. This framework will be revisited
throughout the course in lectures, discussions, and assignments;
study the contents thoroughly.
Table 2
Summary of critical frameworks

Western, 2013, pp. 22-23
Any of the four frames described in Table 2, above,may be used
to conduct critical investigation. Of special note is that Western
(2013) indicated a preference for the emancipation
analysis frame illustrated in Table 2. Zehndorfer (2014), in the
book Leadership: A critical introduction, uses a combination of
frames such as depth analysis and network analysis to reveal the
importance of key theory deconstruction and personal self-
discovery as means for advancing knowledge. And, by
introducing a new concept, emotion contagion, to study
leadership, Snaebjornsson and Vaiciukynaite (2016) may have
used the frame of looking awry to identify alternatives.
2. Modern Leadership: From the Historical to the Present
Leadership in History
Much has been written about the origin and evolution of
leadership. Documentation in ancient times suggested that our
childhood notions of follow the leader, as described earlier in
this lecture, were supported by such philosophers
as Aristotle and Plato. Observe also that many historical
examples of leadership pertained to war and battles, suggesting
heroism and grandeur.
In ancient times and especially in some cultures, leaders were
expected to motivate and inspire as depicted in the following
quote:
A leader is best when people barely know he exists, when the
work is done, they will say: we did it ourselves.Lao Tzu,
Chinese philosopher
Thoughts about leadership were widely documented in the form
of drama, letters, pictures, and public oratory. From multiple
forms of communication, scholars were able to classify
discourses and authors in time. A brief overview of early,
predominant leadership discourses are presented in Table 3
below.
Table 3
Leadership discourses: A historical perspective

Higgs, 2003, p. 275
In ORG561, modern discourses are studied in depth in later
modules. Here, data displayed in Table 3 established the
progression of leadership thought as influenced by social,
political, and economic conditions.
Historically, the terms leader and leadership are most noticeably
associated with successful outcomes. This hasn’t always been
the case, however. Throughout history, there have been leaders
who were exposed as deceptive, as in the case of the 37th
president of the United States, Richard Nixon. In the United
States, the president is considered the national political leader;
Nixon resigned in the wake of public outcry against illegal and
covert acts associated with political scandal. Other leaders such
as Adolf Hitler managed to lead and inspire even while
conducting mass genocide. The dichotomy between the label or
term of leader and deceptive or destructive practices seems
incongruous to many. The idea that leadership can be associated
with the “dark side” of human behavior has been studied by
researchers such as Kiazad, Restubog, Zagenczyk, Kiewitz, and
Tang (2010).
Leadership History in ORG561
For purposes of ORG561, the historical context of leadership is
limited to the 20th century and the relationship of leadership to
organizations. Articles by Axley (1990); Black (1990);
Mumford (1906); and Hunter and Bedell-Avers; and Mumford
(2007) [required readings] provide a snapshot into traditional
thinking about leadership.
Mumford (1906), for example, explained leadership origins in
the context of sociology. Mumford suggested the research
purpose was not to identify the fundamental principles of
leadership, but rather to provide grounding for further
investigation. Social science focuses on associations among
living organisms, and leadership is explored by searching for
characteristics that are similar or different between one
association and another, according to Mumford. Even at this

early stage of leadership research, assumptions were put forth
that served as guideposts for other scholars. Early assumptions
about leadership were described as functions by Mumford. That
is, leadership occurred:
· within every stage of the social process
· within social interests of individuals and groups and the
combinations of both.
Over time, assumptions about leadership changed when more
academic fields became engaged in leadership study.
Disciplines such as behavioral psychology, social psychology,
political science, and, later, neuroscience are examples of
branches of learning that advanced the study of leadership. In
later modules, we’ll take a closer look at research methods
associated with some of these disciplines.
Leadership Approaches
For purposes of ORG561, we will examine leadership from
many different angles, with the major emphasis on leadership in
the context of contemporary organizations loosely defined as
post-World War II. Within that time span, modern and
postmodern organization thought was developing.
In Module 3, leadership theories are discussed against the
backdrop of modern and postmodern organizations. In Module
3, leadership theories are discussed against the backdrop of
modern and postmodern organizations. These variables greatly
influenced the movement of leadership study over time. These
variables greatly influenced the movement of leadership study
over time.
Prior to the turn of the 21st century, leadership was often
explained according to different approaches to
leadership. Approaches are sometimes labeled as styles,
combining traits with approaches. Examining leadership
approaches offers a way to test knowledge and assumptions
against our individual experiences. Following, in Table 4, are
examples of often-cited leadership approaches with which you
may be familiar. Take the time to think about when and where
you might have encountered some of these examples in your

reading and real-world experiences.
Table 4
Modern leadership-approach examples with overviews
Individualist
A common reference to focus on the individual in a leader
capacity.
The basis of leadership-development programs.
Much research on traits and behaviors of the individual.
Contingency
In response to the simplistic view of common leadership
characteristics and traits.
Suggests organizational situations require specific types of
leaders.
Addresses social context.
Paternalistic
In response to leadership approaches from Western scholars.
Adopts cultural norms, e.g., from China and East Asia.
Combines authority with discipline, benevolence, and personal
virtues.
Authoritarian
Emphasis is on command and control. Structure, rules, and
policies are valuable contributors.
Often studied in context of organizational performance: tactical
vs contextual.
Note: Approach examples were randomly selected for
illustration purposes only.
Cheng, Chou, Wu, Huang, & Farh, 2004; Eagly, Johannesen-
Schmidt, & Van Engen, 2003; Kiazad, Restubog, Zagenczyk,
Kiewitz, & Tang, 2010; Mumford, 1906; and Western, 2013).
The approaches described in Table 4, above, may be scrutinized
in relationship to the business environment. For example, the
business environment in the 1950s was one of rapid industrial
growth. Management expectations centered on control and
efficiency. Thus, an authoritarian leadership approach was
common and valued by investors. Look for specific instances of
how contextual variables influenced organizational leadership

approaches to reinforce comprehension. In that context, Table 4
provides examples of modern and postmodern leadership
approaches that are representative of more recent thinking.
Table 5
Postmodern leadership approach examples with overviews
Authentic
In response to corporate scandals. Emphasis on moral character
and self-awareness.
Authenticity of followers included. Transparency of
information. Some distinctions associated with components of
transformational leadership.
Value-based
In response to perceived ethical and moral deficiencies in
leaders. Values at the center of decision making for individual,
organization, community, and greater social good.
Public organizations emphasized but not limited to those. Have
a strong sense of purpose and make values actionable.
Post-heroic
Built around shared and collaborative leadership. In contrast to
earlier “hero” approach, which is construed as masculine. Seen
as aligned with more feminized approach.
More empowering. Relinquishes control.
Egalitarian
In response to shifts from function- to process-driven
organizations. Intended to promote collaboration and decrease
resistance.
Shared decision making. Empowerment.
Hoch, Bommer, Dulebohn, & Wu, 2016; Iqbal, Nadeem &
Zaheer, 2015; Parush & Koivunen, 2014; van Niekerk & Botha,
2017).
Check your understanding of the concepts before moving on to
the next portion of this lecture.
3. The Leader in You
To grasp the significance of you in the study of modern
leadership, recallthe table Overview of Modern and Post-
modern Time-frame and Characteristics. As organizations were

challenged to respond to social, political, economic, and
technological changes leading up to the turn of the 21st century,
transformation required effective leadership to meet new
organizational needs in postmodern times.
As we learned in Module 1, postmodern leadership approaches
have yet to be developed around a single definition or standard.
However, a common element emerges in postmodern leadership
literature: the call for leaders to possess an understanding
of self. Many terms—such as self-assessment, self-reflection,
self-realization, and self-awareness—were used to make the
case that to be effective postmodern leaders, we must embrace a
willingness and ability to reveal ourselves (Gandolfi & Stone,
2016; Higgs, 2003; Rubens, Leah, & Schoenfeld, 2016 ; Shamir
& Eilam, 2005).
Gandolfi and Stone (2016) suggested that emotional
intelligence is associated with understanding personal
behaviors. For purposes of ORG561, we’ll use the term self-
knowledge as an overarching label representing the ideas of
self.
Social psychologists have developed multitudes of tools to
expand self-knowledge. A simple internet keyword search of
“leadership self-assessment” in 2017 produced more than four
million results. And most high schools and colleges administer
self-assessment instruments. The CSU-Global Career
Center provides leadership self-assessment resources.
Tested, alternative techniques to expand leadership self-
knowledge originated from educational research. Five such
techniques are highlighted here and include:
· Personal interpretation of leadership
· Locate yourself
· Life story
· Leadership metaphor
· Leadership biography
Let’s look at each of these in more depth.
· Personal Interpretation of Leadership
· Locate Yourself

· Life Story
· Leadership Metaphor
· Leadership Biography
Leadership Approach and Assumption
Biographical Explanation
Feminized leadership approach
Characterized by feminine rather than masculine ways of
leading. Relies on experiences of equal treatment and self-
confidence
I grew up in Iowa, which at the time was one of only three
states in the nation offering interscholastic sports for girls.
Playing high school sports provided rich opportunities to
experience teamwork and the power of competition. In my small
rural town, people of the community valued both girls’ and
boys‘ sports’ teams equally.
As a summary of this lecture, review the following video.
Consider how leadership approaches, critical thinking, and self-
knowledge might be characterized in the leadership lessons
here.
Video: How to Start a Movement
DOI: 10.1126/science.1251688
, 1280 (2014);344 Science
et al.Andrés Moreno-Estrada
and affects biomedical traits
The genetics of Mexico recapitulates Native American
substructure
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HUMAN GENETICS
The genetics of Mexico recapitulates
Native American substructure and
affects biomedical traits
Andrés Moreno-Estrada,
1
*† Christopher R. Gignoux,
2
†‡ Juan Carlos Fernández-López,
3
†
Fouad Zakharia,
1
Martin Sikora,
1

Alejandra V. Contreras,
3
Victor Acuña-Alonzo,
4,5
Karla Sandoval,
1
Celeste Eng,
6
Sandra Romero-Hidalgo,
3
Patricia Ortiz-Tello,
1
Victoria Robles,
1
Eimear E. Kenny,
1
§ Ismael Nuño-Arana,
7
Rodrigo Barquera-Lozano,
4
Gastón Macín-Pérez,
4
Julio Granados-Arriola,
8

Scott Huntsman,
6
Joshua M. Galanter,
6,9
Marc Via,
6
|| Jean G. Ford,
10
Rocío Chapela,
11
William Rodriguez-Cintron,
12
Jose R. Rodríguez-Santana,
1,3
Isabelle Romieu,
14
Juan José Sienra-Monge,
15
Blanca del Rio Navarro,
15
Stephanie J. London,
16
Andrés Ruiz-Linares,
5

Rodrigo Garcia-Herrera,
3
Karol Estrada,
3
¶ Alfredo Hidalgo-Miranda,
3
Gerardo Jimenez-Sanchez,
3
# Alessandra Carnevale,
3
Xavier Soberón,
3
Samuel Canizales-Quinteros,
3,17
Héctor Rangel-Villalobos,
7
Irma Silva-Zolezzi,
3
**
Esteban Gonzalez Burchard,
6,9
* Carlos D. Bustamante
1
*

Mexico harbors great cultural and ethnic diversity, yet fine-
scale patterns of human
genome-wide variation from this region remain largely
uncharacterized. We studied
genomic variation within Mexico from over 1000 individuals
representing 20 indigenous
and 11 mestizo populations. We found striking genetic
stratification among indigenous
populations within Mexico at varying degrees of geographic
isolation. Some groups were as
differentiated as Europeans are from East Asians. Pre-
Columbian genetic substructure is
recapitulated in the indigenous ancestry of admixed mestizo
individuals across the
country. Furthermore, two independently phenotyped cohorts of
Mexicans and Mexican
Americans showed a significant association between
subcontinental ancestry and lung
function. Thus, accounting for fine-scale ancestry patterns is
critical for medical and
population genetic studies within Mexico, in Mexican-descent
populations, and likely in
many other populations worldwide.
U

nderstanding patterns of human popula-
tion structure, where regional surveys are
key for delineating geographically restricted
variation, is important for the design and
interpretation of medical genetic studies.
In particular, we expect rare genetic variants,
including functionally relevant sites, to exhibit
little sharing among diverged populations (1).
Native Americans display the lowest genetic
diversity of any continental group, but there is
high divergence among subpopulations (2). As
a result, present-day American indigenous pop-
ulations (and individuals with indigenous an-
cestry) may harbor local private alleles rare or
absent elsewhere, including functional and med-
ically relevant variants (3, 4). Mexico serves as
an important focal point for such analyses, be-
cause it harbors one of the largest sources of

pre-Columbian diversity and has a long history
of complex civilizations with varying contribu-
tions to the present-day population.
Previous estimates of Native Mexican genetic
diversity examined single loci or were limited to
a reduced number of populations or small sam-
ple sizes (5–8). We examined local patterns of
variation from nearly 1 million genome-wide
autosomal single-nucleotode polymorphisms
(SNPs) for 511 Native Mexican individuals from
20 indigenous groups, covering most geographic
regions across Mexico (table S1). Standard prin-
cipal components analysis (PCA) summarizes
the major axes of genetic variation in the data
set [see (9)]. Whereas PC1 and PC2 separate
Africans and Europeans from Native Mexicans,
PC3 differentiates indigenous populations with-
in Mexico, following a clear northwest-southeast

cline (Fig. 1A). A total of 0.89% of the variation
is explained by PC3, nearly three times as much
as the variation accounted for by the north-south
axis of differentiation within Europe [0.30%, in
(10)]. The northernmost (Seri) and southern-
most (Lacandon) populations define the extremes
of the distribution, with very clear clustering
of individuals by population, indicating high
levels of divergence among groups (fig. S1).
Seri and Lacandon show the highest level of
population differentiation as measured with
Wright’s fixation index FST (0.136, Fig. 1B and
table S4), higher than the FST between Euro-
peans and Chinese populations in HapMap3
(0.11) (11). Other populations within Mexico
also show extreme FST values; for example, the
Huichol and Tojolabal have a pairwise FST of
0.068, similar to that observed between the

Gujarati Indians and the Chinese in HapMap3
(0.076).
The high degree of differentiation between
populations measured by FST argues that these
populations have experienced high degrees of
isolation. Indeed, when autozygosity is inferred
using runs of homozygosity (ROH), all popula-
tions on average have long homozygous tracts,
with the Huichol, Lacandon, and Seri all having
on average over 10% of the genome in ROH [figs.
S2 and S3 (9)]. These populations are relatively
small, increasing the effects of genetic drift and
driving some of the high FST values. In contrast,
the Mayan and Nahuan populations have much
smaller proportions of the genome in ROH, con-
sistent with ROH levels found in Near Eastern
populations in HGDP (12). These populations
are the descendants of large Mesoamerican ci-

vilizations, and concordant with large historical
populations, have relatively low proportions of
ROH. The high degree of variance in ROH among
populations is an additional indicator of popu-
lation substructure and suggests a large variance
in historical population sizes. Comparing the ob-
served ROH patterns to those derived from coa-
lescent simulations, we find that Native American
groups within Mexico are characterized by small
effective population sizes under a model with a
strong bottleneck, in agreement with otherstudies
of Native American populations (13). The degree
of population size recovery to the current day is
consistent with the degree of isolation of the ex-
tant populations, ranging from 1196 chromosomes
[95% confidence interval (CI) 317 to 1548] for the
Seri in the Sonora desert, to 3669 (95% CI 2588 to
5522) for the Mayans from Quintana Roo (figs. S4

to S6; (9)).
1
Department of Genetics, Stanford University School of
Medicine, Stanford, CA, USA.
2
Department of Bioengineering
and Therapeutic Sciences, University of California, San
Francisco, CA, USA.
3
Instituto Nacional de Medicina
Genómica (INMEGEN), Mexico City, Mexico.
4
Escuela
Nacional de Antropología e Historia (ENAH), Mexico City,
Mexico.
5
Department of Genetics, Evolution and
Environment, University College London, London, UK.
6
Department of Medicine, University of California, San
Francisco, CA, USA.
7
Instituto de Investigación en Genética
Molecular, Universidad de Guadalajara, Ocotlán, Mexico.
8
Instituto Nacional de Ciencias Médicas y Nutrición Salvador

Zubirán, Mexico City, Mexico.
9
Department of Bioengineering
and Therapeutic Sciences, University of California, San
Francisco, CA, USA.
10
The Brooklyn Hospital Center,
Brooklyn, NY, USA.
11
Instituto Nacional de Enfermedades
Respiratorias (INER), Mexico City, Mexico.
12
Veterans
Caribbean Health Care System, San Juan, Puerto Rico.
13
Centro de Neumología Pediatrica, San Juan, Puerto Rico.
14
International Agency for Research on Cancer, Lyon, France.
15
Hospital Infantil de México Federico Gomez, Mexico City,
Mexico.
16
National Institute of Environmental Health
Sciences, National Institutes of Health, Department of Health
and Human Services, Research Triangle Park, NC, USA.
17

Facultad de Química, Universidad Nacional Autónoma de
México, Mexico City, Mexico.
*Corresponding author. E-mail: [email protected]
(C.D.B.); [email protected] (A.M.-E.); [email protected]
ucsf.edu (E.G.B.) †These authors contributed equally to this
work. ‡Present address: Department of Genetics, Stanford
University
School of Medicine, Stanford, CA, USA. (C.R.G.) §Present
address:
Center for Statistical Genetics, Mount Sinai School of
Medicine, New
York, USA. (E.E.K.) ||Present address: Department of
Psychiatry and
Clinical Psychobiology - IR3C, Universitat de Barcelona, Spain.
(M.V.).
¶Present address: Analytic and Translational Genetics Unit,
Massachusetts General Hospital, Boston, USA. (K.E.) #Present
address: Harvard School of Public Health and Global Biotech
Consulting Group. (G.J.-S.) **Present address: Nutrition and
Health Department Nestec Ltd, Nestle Research Center,
Lausanne,
Switzerland. (I.S.-Z.)
1280 13 JUNE 2014 • VOL 344 ISSUE 6189 sciencemag.org

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RESEARCH | REPORTS
Isolation also correlates with the degree of
relatedness within and between ethnic groups, ul-
timately shaping the pattern of genetic relation-
ships among populations. We built a relatedness
graph (Fig. 1C) of individuals sharing >13 cM of
the genome identically by descent (IBD) (cor-
responding to third/fourth cousins or closer
relatives). Almost all the connections are within-
versus among-population, consistent with the
populations being discrete rather than exhib-
iting large-scale gene flow [figs. S7 and S8 (9)].
As seen with the ROH calculations, the Mayan
and Nahuan groups have fewer internal connec-
tions. The few between-population connections
appear in populations close to each coastline,

such as the connections between the Campeche
Mayans and populations to the west along the
Gulf of Mexico.
The long-tract ROH and IBD analyses are es-
pecially relevant to the recent history of isolation
of Native American populations. We ran TreeMix
(14) to generate a probabilistic model of diver-
gence and migration among the Native Amer-
ican populations (Fig. 1D). The inferred tree with
no migration paths recapitulates the north/south
and east/west gradients of differentiation from
the PCA and IBD analyses, with populations
with high ROH values also exhibiting longer
tip branches. The primary branches divide pop-
ulations by geography. All northern populations
(dark blue) branch from the same initial split
at the root. We also find two additional major
clades: a grouping of populations from the south-

ern states of Guerrero and Oaxaca (green labels)
and a “Mayan clade” composed of Mayan-speaking
populations from Chiapas and the Yucatan pe-
ninsula in the southeast (orange labels). Intro-
ducing migratory edges to the model connects
the Maya in Yucatan to a branch leading to the
Totonac, whose ancestors occupied the large pre-
Columbian city of El Tajin in Veracruz (15). This
result points to an Atlantic coastal corridor of
gene flow between the Yucatan peninsula and
central/northern Mexico (fig. S9), consistent with
our IBD analysis. Indeed, the only Mayan lan-
guage outside the Mayan territory is spoken by
the Huastec, nearby in northern Veracruz, sup-
porting a shared history (16).
These signals remain today as a legacy of the
pre-Columbian diversity of Mexican populations.
Over the past 500 years, population dynamics

have changed drastically. Today, the majority of
Mexicans are admixed and can trace their an-
cestry back not only to indigenous groups but
also to Europe and Africa. To investigate patterns
of admixture, we combined data from continental
source populations (including the 20 native
Mexican groups, 16 European populations, and
50 West African Yorubas) with 500 admixed
mestizo individuals from 10 Mexican states
recruited by the National Institute of Genomic
Medicine (INMEGEN) for this study, Mexicans
from Guadalajara in the POPRES collection (17),
and individuals of Mexican descent from Los
Angeles in the HapMap Phase 3 project (table
S1). We ran the unsupervised mixture model al-
gorithm ADMIXTURE (18) to estimate ancestry
proportions for individuals in our combined data
set (Fig. 2, fig. S10, and table S5). Allowing for

three ancestral clusters (K = 3), we find that most
individuals have a large amount of Native and
European ancestry, with a small (typically <5%)
amount of African ancestry. At the best-fit mod-
el for K = 9, the Native American cluster breaks
down into six separate components (Fig. 2B).
Three of these are mostly restricted to isolated
populations (Seri, navy blue; Lacandon, yellow;
and Tojolabal, brown). The other three show a
wider but geographically well-defined distribu-
tion: A northern component (light blue) repre-
sented by Tarahumara, Tepehuano, and Huichol,
gradually decreases southward. Corresponding-
ly, a southern component (blue), which includes
Triqui, Zapotec, and Mazatec, gradually decreases
northward. In the Yucatan peninsula and the
neighboring state of Chiapas, we found what we
termed the “Mayan component” (orange in Fig.

2B, bottom panel), found primarily in Mayan-
speaking groups. This Mayan component is also
Fig. 1. Genetic differentiation of Native Mexican populations.
(A) PCA of Native Mexicans with
HapMap YRI and CEU samples. Population labels as in table
S1. (B) Pairwise FST values among Native
Mexican populations ordered geographically (see also table S4).
(C) Relatedness graph of individuals
sharing more than 13 cM of the genome as measured by the total
of segments IBD. Each node
represents a haploid genome, and edges within clusters attract
nodes proportionally to shared IBD.
The spread of each cluster is thus indicative of the level of
relatedness in each population, as deter-
mined by a force-directed algorithm. Only the layout of nodes
within each cluster is the result of the
algorithm, as populations are localized to their approximate
sampling locations to ease interpreta-
tion. Parentheses indicate the number of individuals represented
out of the total sample size (2N).
The full range of IBD thresholds are shown in fig. S8. (D)
TreeMix graph representing population
splitting patterns of the 20 Native Mexican groups studied. The
length of the branch is proportional

to the drift of each population. African, European, and Asian
samples were used as outgroups to root
the tree (fig. S9).
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6189 1281
RESEARCH | REPORTS
Fig. 2. Mexican population structure. (A) Map of sampled pop-
ulations (detailed in table S1) and admixture average
proportions
(table S5). Dots correspond to Native Mexican populations
color-
coded according to K = 9 clusters identified in (B) (bottom),
and
shaded areas denote states in which cosmopolitan populations
were sampled. Pie charts summarize per-state average propor-
tions of cosmopolitan samples at K = 3 (European in red, West
African in green, and Native American in gray). Bars show the
total Native American ancestry decomposed into average
propor-
tions of the native subcomponents identified at K = 9. (B)

Global
ancestry proportions at K = 3 (top) and K = 9 (bottom)
estimated
with ADMIXTURE, including African, European, Native
Mexican, and
cosmopolitan Mexican samples (tables S1 and S2). From left to
right,
Mexican populations are displayed north-to-south. (C)
Interpola-
tion maps showing the spatial distribution of the six native com-
ponents identified at K = 9. Contour intensities are proportional
to
ADMIXTURE values observed in Native Mexican samples, with
crosses indi-
cating sampling locations. Scatter plots with linear fits show
ADMIXTURE
values observed in cosmopolitan samples versus a distance
metric summariz-
ing latitude and longitude (long axis) for the sampled states.
From left to right:
Yucatan, Campeche, Oaxaca, Veracruz, Guerrero, Tamaulipas,
Guanajuato,
Zacatecas, Jalisco, Durango, and Sonora. Values are adjusted
relative to

the total Native American ancestry of each individual (9).
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RESEARCH | REPORTS
present at ~10 to 20% in central Mexican na-
tives, consistent with the IBD and migration edges
connecting the regions. This relationship between
the Yucatan peninsula and central Mexico, seen
in both recent shared IBD and genetic drift–
based models of allele frequencies (TreeMix and
ADMIXTURE), suggests that gene flow between
the two regions has been ongoing for a long
time. In contrast, Mayan admixture is not found
at appreciable levels in highlanders of the south-
ern state of Oaxaca (Triqui and Zapotec), where
mountain ranges may have acted as geographic
barriers to gene flow.

Patterns of Native American population sub-
structure are recapitulated in the genomes of
Mexican mestizos from cosmopolitan popula-
tions throughout Mexico. Sonora and neighbor-
ing northern states show the highest average
proportions of the northern native component
(15%, light blue in Fig. 2B, bottom), whereas
only traces are detected in Oaxaca and the
Yucatan peninsula. Conversely, the southern
native component is the most prevalent across
states, reaching maximum values in Oaxaca
and decreasing northward. Cosmopolitan sam-
ples from the Yucatan peninsula have Native
American fractions of the genome dominated
by the Mayan component, which diminishes in
northward populations. Likewise, Mayan-related
local components, Tojolabal and Lacandon, are
detected above 1% exclusively among individ-

uals from the states neighboring the Yucatan
peninsula. In contrast, Mexican-Americans sam-
pled in Los Angeles (MXL) do not show a homog-
eneous pattern, consistent with their diverse
origins within Mexico. Overall, the continuous
geographic distribution of each Native American
component across Mexico (fig. S12) demonstrates
a high correlation of individual admixture pro-
portions with geography, even in individuals of
mixed ancestry (Fig. 2C, NW-SE axis F-test for
all native clusters, P <10
−16
).
To further test whether ancestral popula-
tion structure is recapitulated in the genomes
of mestizos, we used an ancestry-specific PCA
(ASPCA) approach [fig. S13 (9, 19)]. We estimated
local ancestry using PCAdmix (20) to identify
segments of the genome belonging to Native

American, European, or African ancestries. We
focused on the European and Native American
components of ancestry, given the low propor-
tions of African ancestry overall. We would expect
the history of Spanish occupation and coloniza-
tion in Mexico to be reflected in the European
segments of Mexican mestizos, as has been seen
previously (21). ASPCA of the European haplo-
types in present-day Mexicans confirms this,
as individuals cluster tightly with present-day
Iberians even with a dense set of European pop-
ulations (17, 22) (fig. S14).
In contrast, given the complex demographic
history of Native Americans, high isolation, and
limited characterization of regional ancestry
patterns (23, 24), it remains unknown whether
the correlation between genes and geography ob-
served in Europe (10) can be similarly recapitu-

lated within Mexico. We used ASPCA to uncover
hidden population structure within Native Am-
erican ancestry beyond that found solely in ex-
tant indigenous groups (Fig. 3A). Consistent
with the previous PCA analyses, we observed the
most diverged indigenous populations defining
the extremes of the top PCs due to high levels of
genetic drift and isolation. However, including
all the indigenous groups in the plot masks the
signal contained in the indigenous segments
of the Mexican mestizos. When plotting the
ASPCA values for the admixed individuals only,
we discovered a strong correlation between Na-
tive American ancestry and geography within
Mexico (Fig. 3B), with ASPC1 representing a west-
to-east dimension and ASPC2 one from north
to south. Both of these correlations are highly
significant and linearly predictive of geographic

location (Pearson’s r
2
of 72% and 38% for ASPC1
and 2, respectively, both P values < 10
−5
). The cor-
relation is strong enough that the overall distri-
bution of mestizo-derived indigenous haplotypes
in ASPCA space resembles a geographic map of
Mexico (Fig. 3B and fig. S15). This finding sug-
gests that the genetic composition of present-day
Mexicans recapitulates ancient Native American
substructure, despite the potential homogeniz-
ing effect of postcolonial admixture. Fine-scale
population structure going back centuries is not
merely a property of isolated or rural indigenous
communities. Cosmopolitan populations still re-
flect the underlying genetic ancestry of local na-
tive populations, arguing for a strong relationship
between the indigenous and the Mexican mes-

tizo population, albeit without the extreme drift
exhibited in some current indigenous groups.
Having found these hidden patterns of ances-
try in the native component of Mexican mestizos,
we investigated whether this structure could
have potential biomedical applications. Over
the past decade, genetic ancestry has been as-
sociated with numerous clinical endpoints and
disease risks in admixed populations, including
neutrophil counts (25), creatinine levels (26), and
breast cancer susceptibility (27). Similarly, an-
cestral background is especially important in
pulmonary medicine, where different reference
equations are used for different ethnicities, de-
fining normative predicted volumes and identify-
ing thresholds for disease diagnosis in standard
clinical practice (28). That is, depending on one’s
ethnic background, the same value of forced ex-

piratory volume in 1 s (FEV1, a standard measure
of lung function) could be either within the nor-
mal range or indicative of pulmonary disease.
Previous work has shown that the proportion of
African and European ancestry was associated
with FEV1 in African Americans (29) and Mexicans
(30), respectively, establishing the importance
of genomic ancestry in lung function prediction
equations.
To investigate possible associations between
ancestral structure in Mexicans and FEV1, we
applied our ASPCA approach to two studies mea-
suring lung function in Mexican or Mexican-
American children: the Mexico City Childhood
Asthma Study (MCCAS) (31) and the Genetics of
Asthma in Latino Americans (GALA I) Study
(32). Due to differences in protocols and geno-
typing platforms, we calculated ASPCA values

for the two studies independently (fig. S17) using
the same reference populations described above,
then used fixed-effects meta-analysis to combine
the results (9).
First, in GALA I we looked for significant
ancestry-specific differences between Mexico City
and the San Francisco Bay Area, the two recruit-
ment sites. ASPCA values were associated with
recruitment location, with the receiver-operator
characteristic curve from the Native American
ancestry dimensions resulting in an area under
the curve (AUC) of 80% (fig. S17). After we ad-
justed for overall ancestry proportions (here both
African and Native American), both ASPCs were
significant in a logistic regression: ASPC1 OR per
SD: 0.44 (95% CI 0.22 to 0.68), P = 3.8 × 10
−4
,
ASPC2 OR per SD: 1.68 (95% CI 1.03 to 2.76), P =

0.039. The ASPCs defined similar east-west and
north-south axes as in the previous analysis (fig.
S17) and show that Mexican-Americans in the San
Francisco Bay Area tend to have increased Na-
tive American ancestry from northwest Mexico
as compared to individuals from Mexico City
(joint logistic regression likelihood ratio test
P = 6.4 × 10
−5
).
We then used the ASPCA values for both
studies to test for an association with FEV1 as
transformed to percentile of predicted “normal”
function via the standard set of reference equa-
tions (28) for individuals of Mexican descent.
These equations use population-specific demo-
graphic characteristics to account for age, sex,
and height in estimates of lung function. Ad-
justing for overall ancestry proportions in linear

regressions, we observed a significant associa-
tion between FEV1 and the east-west component
(ASPC1) in both studies, with a meta-analysis
P value of 0.0045 (2.2% decrease in FEV1 per
1 SD, 95% CI 0.69 to 3.74). The effect sizes
were homogeneous (Fig. 3C and table S6) de-
spite differences in recruitment strategy, geog-
raphy, and genotyping platform (9). In contrast,
ASPC2 showed no association with FEV1. Where-
as FEV1 has previously been associated with over-
all ancestry in several populations, the effect seen
here is not correlated with overall admixture
proportions, because we adjusted for those in the
regression model. The combined results here in-
dicate that subcontinental ancestry as measured
by ASPCA is important for characterizing clinical
measurements.
To estimate how variation in genetic ancestry

within Mexico may affect FEV1, we used the re-
sults from GALA I and MCCAS to predict trait
values by state (Fig. 3D) for the INMEGEN
mestizo samples. We found that difference in
subcontinental Native American ancestry as
measured by ASPC1 results in an expected
7.3% change in FEV1, moving from the state of
Sonora in the west to the state of Yucatan in
the east. These results suggest that fine-scale
patterns of native ancestry alone could have
significant impacts on clinical measurements
of lung function in admixed individuals with-
in Mexico.
6189 1283
RESEARCH | REPORTS
These changes due to ancestry are compar-

able to other factors affecting lung function. Com-
paring the expected effect of ancestry across
Mexico with the known effects of age in the
standard Mexican-American reference equa-
tions (28), the inferred 7.3% change in FEV1
associated with subcontinental ancestry is sim-
ilar to the decline in FEV1 that a 30-year-old
Mexican-American individual of average height
would experience by aging 10.3 years if male
and 11.8 years if female. Similarly, comparing
our results from the Mexican data with the
model incorporating ancestry in African Amer-
icans, a difference of 7.3% in FEV1 would corre-
spond to a 33% difference in African ancestry
(29). The association between FEV1 and ASPC1
is not an indicator of impaired lung function
on its own–rather, it contributes to the distribu-
tion of FEV1 values and would modify clinical
thresholds. This finding indicates that diagnoses

of diseases such as asthma and chronic obstruc-
tive pulmonary disease (COPD) relying on spe-
cific lung function thresholds may benefit from
taking finer-scale ancestry into consideration.
An important implication of our work is that
multi- and transethnic mapping efforts will
benefit from including individuals of Mexican
ancestry, because the Mexican population har-
bors rich amounts of genetic variation that may
underlie important biomedical phenotypes. A
key question in this regard is whether existing
catalogs of human genome variation capture
the genetic variation present in the samples
analyzed here. We performed targeted SNP tag-
ging and genome-wide haplotype sharing anal-
ysis within 100-kb sliding windows to assess
the degree to which haplotype diversity in the
Mexican mestizo samples could be captured

by existing reference panels [figs. S18 to 20 (9)].
Although Mexican-American samples (MXL) were
included in both the HapMap and 1000 Ge-
nomes catalogs, average haplotype sharing for
the INMEGEN mestizo samples is limited to
81.2 and 90.5% when combined with all conti-
nental HapMap populations. It is only after in-
cluding the Native American samples genotyped
here that nearly 100% of haplotypes are shared,
maximizing the chances of capturing most of the
variation in Mexico.
Much effort has been invested in detecting
common genetic variants associated with com-
plex disease and replicating associations across
populations. However, functional and medically
relevant variation may be rare or population-
specific, requiring studies of diverse human
populations to identify new risk factors (4).

Without detailed knowledge of the geographic
Fig. 3. Subcontinental ancestry of admixed Mexican genomes
and bio-
medical implications. (A) ASPCA of Native American segments
from Mexican
cosmopolitan samples (colored circles) together with 20
indigenous Mexican
populations (population labels). Samples with >10% of non-
native ad-
mixture were excluded from the reference panel, as well as
population
outliers such as Seri, Lacandon, and Tojolabal. (B) Zoomed
detail of the
distribution of the Native American fraction of cosmopolitan
samples
throughout Mexico. Native ancestral populations were used to
define PCA
space (prefixed by NAT) but removed from the background to
highlight the
subcontinental origin of admixed genomes (prefixed by MEX).
Each circle
represents the combined set of haplotypes called Native
American along

the haploid genome of each sample with >25% of Native
American an-
cestry. The inset map shows the geographic origin of
cosmopolitan sam-
ples per state, color-coded by region (9). (C) Coefficients and
95% CIs for
associations between ASPC1 and lung function (FEV1) from
Mexican
participants in the GALA I study, and the MCCAS, as well as
both studies
combined (table S6 and fig. S17) (9). (D) Means and CIs of
predicted
change in FEV1 by state, extrapolated from the model in (C).
SCIENCE
RESEARCH | REPORTS
stratification of genetic variation, negative results
and lack of replication are likely to dominate the
outcome of genetic studies in uncharacterized
populations. Here we have demonstrated a high
degree of fine-scale genomic structure across

Mexico, shaped by pre-Columbian population
dynamics and affecting the present-day genomes
of Mexican mestizos, which is of both anthro-
pological and biomedical relevance. Studies such
as this one are crucial for enabling precision med-
icine, providing novel data resources, empowering
the next generation of genetic studies, and dem-
onstrating the importance of understanding and
measuring fine-scale population structure and
its associations with biomedical traits.
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ACKNOWLEDGMENTS
We thank all volunteers for generously donating DNA samples
and
participating in the study. This project was possible with the
joint
support from multiple Institutions in Mexico and the United
States.
Stanford University supported C.D.B. with funding from the
Department of Genetics. INMEGEN received support from the
Federal Government of Mexico, particularly the Ministry of
Health,
the Mexican Health Foundation (FUNSALUD), and the Gonzalo
Río
Arronte Foundation. State governments and universities of
Durango, Campeche, Guanajuato, Guerrero, Oaxaca, Sonora,
Tamaulipas, Veracruz, Yucatan, and Zacatecas contributed
significantly to this work. This research was also supported by

the
George Rosenkranz Prize for Health Care Research in
Developing
Countries awarded to A.M.-E.; University of California San
Francisco (UCSF) Chancellor’s Research Fellowship,
Dissertation
Year Fellowship, and NIH Training Grants T32GM007175 and
T32HG000044 (to C.R.G.); the Robert Wood Johnson
Foundation
Amos Medical Faculty Development Award; the Sandler
Foundation; the American Asthma Foundation (to E.G.B.);
CONACYT grant 129693 (to H.R.-V.); BBSRC grant
BB/I021213/1
(to A.R.-L.); the National Institutes of Health (NIH) (grants
R01GM090087, R01HG003229, ES015794, GM007546,
GM061390, HL004464, HL078885, HL088133, HL111636,
RR000083, P60MD006902, and ZIA ES49019); and National
Science Foundation award DMS-1201234. This work was
supported
in part by the Intramural Research Program of NIH, National
Institute of Environmental Health Sciences (to S.J.L.). Some

computations were performed using the UCSF Biostatistics
High
Performance Computing System. We also thank B. Henn,
S. Gravel, and J. Byrnes for helpful discussions; C. Gunter and
M. Carpenter for editing the manuscript; and M. Morales for
informatics and programming support. C.D.B. is on the advisory
board of a project at 23andMe; and on the scientific advisory
boards of Personalis, Inc.; InVitae; Etalon, Inc.; and
Ancestry.com.
The collections and methods for the Population Reference
Sample
(POPRES) are described by Nelson et al. (2008). The POPRES
data
sets used for the analyses described here were obtained from
dbGaP through accession number phs000145.v1.p1. Access to
the
MCCAS data set may be obtained under the terms of a data
transfer
agreement with the National Institute of Environmental Health
Sciences; the contact is S.J.L.. Individual-level genotypes for
new data

presented in this study are available, through a data access
agreement to respect the privacy of the participants for the
transfer
of genetic data, by contacting C.D.B., A.M.-E., and INMEGEN
(http://www.inmegen.gob.mx/).
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/344/6189/1280/suppl/DC1
Materials and Methods
Supplementary Text
Figs. S1 to S20
Tables S1 to S6
References (33–64)
3 February 2014; accepted 21 May 2014
10.1126/science.1251688
TRANSCRIPTION
Interactions between RNA
polymerase and the “core recognition
element” counteract pausing
Irina O. Vvedenskaya,
1
* Hanif Vahedian-Movahed,

2
* Jeremy G. Bird,
1,2
*
Jared G. Knoblauch,
1
Seth R. Goldman,
1
Yu Zhang,
2
Richard H. Ebright,
2
† Bryce E. Nickels
1
†
Transcription elongation is interrupted by sequences that inhibit
nucleotide addition and
cause RNA polymerase (RNAP) to pause. Here, by use of native
elongating transcript
sequencing (NET-seq) and a variant of NET-seq that enables
analysis of mutant RNAP
derivatives in merodiploid cells (mNET-seq), we analyze
transcriptional pausing
genome-wide in vivo in Escherichia coli. We identify a

consensus pause-inducing sequence
element, G–10Y–1G+1 (where –1 corresponds to the position of
the RNA 3′ end). We
demonstrate that sequence-specific interactions between RNAP
core enzyme and a core
recognition element (CRE) that stabilize transcription initiation
complexes also occur in
transcription elongation complexes and facilitate pause read-
through by stabilizing
RNAP in a posttranslocated register. Our findings identify key
sequence determinants of
transcriptional pausing and establish that RNAP-CRE
interactions modulate pausing.
R
egulation of gene expression during tran-
scription elongation often involves sequences
in DNA that cause the transcription elon-
gation complex (TEC) to pause. Pausing
can affect gene expression by facilitat-
ing engagement of regulatory factors, influenc-
ing formation of RNA secondary structures, and
enabling synchronization of transcription and

translation.
Several lines of evidence suggest that pausing
involves specific sequence signals that inhibit
nucleotide addition (1–11). To define key sequence
determinants for pausing, we used native elongat-
ing transcript sequencing (NET-seq), which permits
occupancies of TECs to be mapped genome-wide
with base-pair resolution (12, 13) (fig. S1). The
occupancy of the TEC at a given position is cor-
related with the tendency of the TEC to pause
at the position. Accordingly, NET-seq analysis
enables identification of pause sites. To per-
form NET-seq in Escherichia coli, cells carrying
a chromosomal rpoC-3xFLAG gene, encoding
RNAP b′ subunit with a C-terminal 3xFLAG tag
were grown to midexponential phase; cells were
flash-frozen and lysed; 3xFLAG-tagged TECs were
immunoprecipitated with an antibody against

FLAG; RNAs were extracted from TECs; and RNA
3′ ends were converted to cDNAs and analyzed
using high-throughput sequencing. We defined
pause sites as positions where TEC occupancy
exceeded TEC occupancy at each position 25 base
pairs (bp) upstream and downstream. We iden-
tified 15,553 pause sites, which corresponds to
~19,800 total pause sites, given the estimated
~78% saturation of the analysis (tables S1 to
S7). Alignment of pause-site sequences revealed
a clear consensus pause element (PE): G–10Y–1G+1,
where position –1 corresponds to the position
of the RNA 3′ end (Fig. 1A and fig. S2). Of the
1
Department of Genetics and Waksman Institute, Rutgers
University, Piscataway, NJ 08854, USA.
2
Department of
Chemistry and Waksman Institute, Rutgers University,
Piscataway, NJ 08854, USA.

*These authors contributed equally. †Corresponding author. E-
mail:
[email protected] (B.E.N.); [email protected]
edu (R.H.E.)
6189 1285
RESEARCH | REPORTS
DOI: 10.1126/science.1211437
, 1699 (2011);334 Science
, et al.John R. Hutchinson
Evolution of Elephant ''Sixth Toes''
From Flat Foot to Fat Foot: Structure, Ontogeny, Function, and
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registered trademark of AAAS.
is aScience2011 by the American Association for the
Advancement of Science; all rights reserved. The title
CopyrightAmerican Association for the Advancement of
Science, 1200 New York Avenue NW, Washington, DC 20005.
(print ISSN 0036-8075; online ISSN 1095-9203) is published
weekly, except the last week in December, by theScience
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in the Doushantuo fossils [for example, opalinids
are multinuclear (32)]. Only volvocalean em-
bryos show so many rounds of palintomy, but the
resulting blastomeres are connected by a system
of cytoplasmic bridges (35) that are not present
in the fossils. The combination of palintomy with-
in a multilayered cyst wall and peanut-shaped
germination stages as seen in the fossils conforms
to the pattern seen in nonmetazoan holozoans;
nonetheless, there are no discrete characters in the
Doushantuo fossils that are uniquely holozoan.
The “animal embryos” likely represent nonmeta-
zoan holozoans or possibly even more distant
eukaryote branches.
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Acknowledgments: We thank S. Xiao, T. Cavalier-Smith, and
B. Landfald for discussion; T. Hode and Z. Yue for field-work
collaboration; A. Groso for assistance with the srXTM work;
and P. Varvarigos and D. Elliott for the use of fig. S7. The work
was supported by the Swedish Research Council, Natural
Environment Research Council, Ministry of Science and
Technology of China, National Natural Science Foundation of
China, EU FP7, and the Paul Scherrer Institute. Figured or
measured specimens are deposited at the Swedish Museum of
Natural History and the Museum of Earth Science, Chinese
Academy of Geological Sciences. The srXTM investigations
were
conducted at the X04SA and X02DA (TOMCAT) beamlines of
the Swiss Light Source. The data were visualized and analyzed
by using Avizo software. Data are available in the SOM. S.B.
and P.C.J.D. designed the research and wrote the paper; T.H.
found the nucleic structures, prepared the corresponding
visualizations, and wrote the specimen descriptions in the
SOM; J.A.C. found the propagule-like structures and performed
taphonomic analyses and volumetric measurements; C.Y.
and S.B. did the field work; C.Y. provided the additional data
from Hubei; and M.S., F.M., S.B. and P.C.J.D. designed the

srXTM experiments.
Supporting Online Material
www.sciencemag.org/cgi/content/full/334/6063/1696/DC1
SOM Text
Figs. S1 to S7
Table S1
Movies S1 to S5
8 June 2011; accepted 16 November 2011
10.1126/science.1209537
From Flat Foot to Fat Foot: Structure,
Ontogeny, Function, and Evolution
of Elephant “Sixth Toes”
John R. Hutchinson,1 Cyrille Delmer,2 Charlotte E. Miller,1
Thomas Hildebrandt,3
Andrew A. Pitsillides,1 Alan Boyde4
Several groups of tetrapods have expanded sesamoid (small,
tendon-anchoring) bones into
digit-like structures (“predigits”), such as pandas’ “thumbs.”
Elephants similarly have expanded
structures in the fat pads of their fore- and hindfeet, but for
three centuries these have been
overlooked as mere cartilaginous curiosities. We show that
these are indeed massive sesamoids
that employ a patchy mode of ossification of a massive
cartilaginous precursor and that the
predigits act functionally like digits. Further, we reveal clear
osteological correlates of predigit joint
articulation with the carpals/tarsals that are visible in fossils.
Our survey shows that basal

proboscideans were relatively “flat-footed” (plantigrade),
whereas early elephantiforms evolved the
more derived “tip-toed” (subunguligrade) morphology,
including the predigits and fat pad, of
extant elephants. Thus, elephants co-opted sesamoid bones into
a role as false digits and used
them for support as they changed their foot posture.
T
he enlarged radial sesamoid bones of giant
panda forefeet (1, 2) are classic examples
of evolutionary exaptation (3, 4): co-option
of old structures for new functions. It is less
widely recognized that such “sixth toes” or “false
thumbs” have evolved convergently in numerous
tetrapods, such as moles and frogs (5, 6). They
exist in numerous mammals in a less enlarged
state, variably called the prepollex/prehallux (here
called predigits), radial/tibial sesamoids, or other
terms (such as falciform, accessory scaphoid, or
navicular). Whether these sesamoids are ances-
trally or convergently evolved in various tetra-
pod clades remains to be determined. The latter
seems likely, given the absence of similar sesa-
moids in most fossil outgroups, yet a cartilag-
inous nodular precursor cannot be excluded.
Regardless, enlarged sesamoids are quite prom-
inent in both the manus (forefeet) and the pedes
(hindfeet) of elephants, where they have been
mistaken for sixth digits or otherwise presumed
to play a role in foot support (7–9). Indeed, the
recent discovery that moles have developmen-
tally switched their radial sesamoid (prepollex)

to a digit-like identity (10) intimates that ele-
phants and other species may have done the same.
Here, we report a multidisciplinary anatomical, his-
tological, functional, and phylogenetic analysis (11)
of the predigits in elephant feet. We hoped this
would illuminate how elephants evolved their char-
acteristic subunguligrade (nearly “tip-toed,” with
only distal toes contacting the ground) foot posture
and function, as compared with the plesiomorphic
plantigrade (“flat-footed,” with wrists/ankles con-
tacting the ground) foot posture in many other
tetrapods.
In 1710, Blair (7) provided the first detailed
osteological description of elephants, conclud-
ing that they have six toes. The “sixth toes”
(medialmost position; corresponding to digit zero)
were later identified as the enigmatic prepollex
1Department of Veterinary Basic Sciences and Structure and
Motion Laboratory, The Royal Veterinary College, Hatfield
AL9
7TA and London NW1 0TU, UK. 2Department of
Palaeontology,
The Natural History Museum, Cromwell Road, London SW7
5BD, UK. 3Leibniz Institute for Zoo and Wildlife Research,
im Forschungsverbund Berlin e.V., Postfach 601103, Berlin
D-10252, Germany. 4Dental Physical Sciences, Barts and The
London School of Medicine and Dentistry, Queen Mary Uni-
versity of London, Mile End Road, London E1 4NS, UK.
www.sciencemag.org SCIENCE VOL 334 23 DECEMBER 2011
1699
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and prehallux (8, 9, 12) (figs. S1 to S4). Three
centuries of sporadic discussion about the iden-
tities of predigits in tetrapods have ensued (8, 9),
sometimes returning to the question of whether
they are actually atavistic digits (9, 13). Consid-
ering the characteristic variability (8) and apparent
mineralization late in the ontogeny of sesamoids
(14), as well as their articulations (15) with meta-
carpal I/tarsal I and metatarsal I (Fig. 1 and movie
S1), the prepollex/prehallux of elephants must
correspond to the radial/tibial sesamoids of other
tetrapods. The late mineralization and confounded
scientific history of predigits have tended to pre-
vent their preservation, discovery, scholarly descrip-

tion, and even museum exhibition. The vexing
issue of the homology of elephant predigits re-
mains unresolved, complicated by the specializa-
tion of paenungulate outgroups (such as Sirenia
and Hyracoidea).
Despite early studies, it remains unclear
whether elephant predigits are never more than
cartilaginous rods, as current literature assumes
(8, 9, 12), or whether they become true bones at
some point in ontogeny. We used a combination
(11) of dissection, computed x-ray tomography
(CT) scans, histology, and backscattered elec-
tron scanning electron microscopy (BSE SEM)
to address this question (Fig. 2 and figs. S5 to
S13). Using this combination of methods, we
found that elephant predigits initially form as
massive, purely cartilaginous rods and that these
can become further stiffened through a slow con-
version to bone (that is, forming endochondrally)
by an unusual ossification mechanism. Histolog-
ical examination showed that this initial hyaline
cartilage element lacks a preferential orientation
of chondrocytes or growth-plate–like stratification
(fig. S13). Imaging with BSE SEM and CT in
addition to histology revealed that patches of this
cartilage calcify and are resorbed and replaced
by bone that subsequently models to a foam- or
honeycomb-like cancellous (spongy bone) struc-
ture. The advancing mineralizing fronts and the
thickness of the calcified cartilage layers resem-
ble those seen in mature articular cartilage.
Together, our analyses not only show that the
cartilaginous predigits are slowly replaced by
bone during late ontogeny, but that this bone is

unusual in its development [Fig. 2, supporting
online material (SOM) text, and figs. S5 to S13].
Ossification typically begins years after other ses-
amoids have become well mineralized (for ex-
ample, the proximal digital sesamoids, at ~3 to
7 years of age), and it occurs in a large cartilage
structure surrounded by a fat pad rather than by
tendon or ligament. Such ossification can remain
incomplete [in 10 out of 37 (10/37) feet exam-
ined] or even uninitiated (11/37 feet) in some adult
(~20+ years old) individuals (figs. S4 to S6). This
singular mode of ossification is endochondral, ex-
tending from several seemingly haphazardly po-
sitioned centers within the massive cartilaginous
precursor. Furthermore, BSE SEM and CT indi-
cate that the resultant cancellous (spongy) bone,
unlike others in the appendicular skeleton, does
not seem oriented to match any predominant load-
ing direction and lacks compact cortices, which
could confergreater longitudinal bending stiffness.
This indicates an unusually flexible ossified struc-
ture that nevertheless is stiffer than the surrounding
fat pad or cartilage, although even cartilaginous
enlarged predigits should provide some support.
We used an indirect approach to solve the
difficult question of how elephant predigits func-
tion. Elephant predigits are deeply embedded in
the digital cushions or fat pads of the feet, thus
their positions and motions are obscured. The
thick keratinized skin of elephant feet prevents
ultrasound or x-ray imaging at safe intensities,
thus preventing in vivo investigation. We pre-
viously speculated that elephant predigits might
function as strut-like weight supports, because

they grow with strong positive allometry simi-
lar to that of the metapodials (16). This function
would be expected to involve a static orientation
of the predigits during loading. Alternatively, pre-
digits might function as dynamic levers (more
like mobile digits) if they reoriented when loaded,
rotating about their joint(s). Animals variably em-
ploy similar functions with their true digits (17).
We tested these hypotheses by statically
loading cadaveric elephant feet ex vivo and CT-
scanning them to examine the effects of applied
loads on their orientation (11). Predigits behav-
ing in a weight-supporting role should maintain
a constant orientation, whereas predigits acting
as dynamic levers should display joint mobility
(movie S2) that reorients them with increasing
load. Our reconstructions (Fig. 3) reveal that the
prepollex and prehallux act differently when
loaded: The prepollex does not move apprecia-
bly even though its proximal joint allows some
mobility, whereas the prehallux rotates caudo-
dorsally. Internal motion contributing to this ro-
tation is apparent for the prehallux which, once
ossified at least, is consistently split into prox-
imal (fixed to the first metatarsal and tarsal) and
distal (free to move) segments (evident in 8/8
individuals with well-ossified prehalluces; movie
Fig. 1. Foot anatomy in
humans and elephants,
with sesamoids shown in
white. (Top) Diagram of
human manus and pes
(for comparison). Dotted

lines for the prepollex
and prehallux show rough
approximations of where
these structures would lie
in humans, but they are
normally absent. These
predigits are not to be
confused with the paired
digital sesamoids, which
elephants and humans
have more distally in their
digits—the so-called “tib-
ial sesamoid” in humans
is one of these. (Middle
and bottom) Elephant
foot anatomy in medial
view of right feet. The
manus is on the left [pre-
pollex (dark) and meta-
carpal I shown below];
the pes is on the right
[prehallux (dark) and me-
tatarsal I shown below].
Bottom-row images are
from CT scan reconstruc-
tions of specimen no. 4
(table S1). See movie S2
for representative mobil-
ity of a predigit. Osteo-
logical terms are from
(25, 26). Labels are as fol-
lows: ac, accessorium (pi-
siform); ca, calcaneus;
D3, third digit; ds, digi-
tal sesamoid(s); mc1,
metacarpal I; mt, meta-

tarsal I; ph, prehallux;
pp, prepollex.
50mm50mm
20mm20mm
50 mm
ca
ca
ac
pp
ph
ph
pp
ph
pp
ds
ds
mc1 mt1
mc1
mt1
ac
mc1

mt1
ds ds
D3
D3
D3
D3
23 DECEMBER 2011 VOL 334 SCIENCE
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S1). The prehallux thus has a proximal portion
that statically transfers load to the tarsus (anal-
ogous to the whole prepollex), and a distal, mo-
bile, lever-like portion. Such segmentation was
not apparent in any of our prepollex specimens,
which behaved as simple struts. This difference
in prepollex and prehallux mobility and function
may relate to the more upright manus and more
horizontal pes bone orientations (Fig. 1). Both
types of predigits, however, are particularly well
suited to stiffen the highly compliant fat pad
against excessive deformation. Furthermore, the
predigits’ tight syndesmotic articulations with
the carpus and tarsus indicate that they also are
able to transfer loading proximally from the sole
of the fat pad to those bones, partly bypassing
the digits. Therefore, the enlarged predigits render
elephant feet functionally plantigrade while the
true digits remain in subunguligrade orientations.
Indeed, the predigits may allow elephants to ef-
fectively reduce the degrees of freedom in their
Fig. 2. Histology of elephant predigit, from speci-
men no. 2 (table S1) prepollex. (A) Toluidine blue
histology of bone:cartilage interface [proximal slab
4 (fig. S6); cartilage, dark blue, bone, pale blue, bone
marrow space, white; width = 1200 mm]; see also fig.
S13. (B) BSE SEM macerated slab 1 (width = 34 mm).
The large space in the right central area (see also fig.
S9) was occupied by cartilage and shows the
endochondral mineralization front [higher magnifi-
cation in (C), width = 1204 mm]. (D) BSE SEM of

polymethylmethacrylate-embedded slab 0 (width =
28 mm; see also fig. S7) with a pseudocolor look-
up table. The lowest backscattering coefficient
(top) is level from the monobrominated standard
and highest at 255 from the monoiodinated di-
methacrylate standard (27); the densest phase is
calcified cartilage. (E) Higher-magnification gray
image of the calcified cartilage:bone interface
(width = 900 mm). Enlarged versions of images (B)
to (E) are in figs. S8 and S10 to S12.
A
B C
D E
Fig. 3. Passive motion of elephant predigits under
loading. Right cadaveric manus (top row) and pes
(bottom row) specimens under minimal (left) and
maximal (right) loads are shown. In the manus, the
prepollex does not move noticeably relative to the
vertical, whereas the metacarpal dorsiflexes up to
13° at maximal load. In the pes, the distal segment
of the prehallux rotates around the static proximal
segment, dorsiflexing up to 17° as the metatarsal
dorsiflexes up to 10°. Bones (Fig. 1) are colored to
match movies S1, S3, and S4. Predigits are aqua-
marine color. Specimen numbers from table S1
are no. 3 (manus) and no. 5 (pes). Labels are as fol-
lows: MC3, metacarpal 3; MT3, metatarsal 3; ph,
prehallux; pp, prepollex.
50mm 50mm
50mm50mm

ph ph
pp
pp
MT3MT3
MC3MC3
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feet, by providing a more passive stabilizing sup-
port that reduces need for more active and mas-
sive muscular tissues, analogous to the reduction
of toes in other ungulate groups (18). Yet the
persistence of musculotendinous structures an-
chored to these sesamoids [such as the abductor
pollicis (9)] indicates some retained ability to
control their position or caudolateral motion, so
the predigits are not entirely passive structures.
There is a smooth ridge on the caudomedial
surface of metacarpal I with which the prepollex
articulates, as well as a mobile ball-and-socket–
like joint on the distal end of tarsal I and a ridge
on the caudomedial side of metatarsal I that both
articulate with the prehallux (15). These features,
found even in juvenile elephants that lack ossified
predigits, are thus osteological correlates of the
presence of predigits (Fig. 1) that might be iden-
tifiable in fossils. Their presence in any skeletal
specimen would corroborate the existence of en-
larged predigits (cartilaginous or ossified).
Our survey of the fossil record of the clade
Proboscidea revealed some evidence of predigits
in extinct forms (11), which also clarifies how
elephant foot posture and function evolved. Un-
fortunately the most basal proboscideans (such
as Barytherium and Numidotherium) lack suffi-
ciently well-preserved metapodials (and thus po-
tential evidence of predigit articulations) to more
directly test whether they had large predigits.
However, their preserved proximal carpal and

tarsal elements show that the feet were quite
plantigrade, leaving little space for an expanded
digital cushion or predigits (Fig. 4, movies S3
and S4, and SOM text). Furthermore, the artic-
ulations of more distal foot bones indicate the
presence of relatively dorsiflexed and more splayed
(abducted) toes; not as adducted as in later Pro-
boscidea and consistent with a more amphibious
lifestyle. Hence we infer that basal proboscideans,
like many of their amphibious or wholly aquatic
tethytherian outgroups [Sirenia and Embrithopoda
(19)] were more plantigrade than extant elephants,
as is ancestral for tetrapods.
We therefore hypothesize that the evolution of
more subunguligrade toes in elephants is linked
with the expansion of the manual and pedal digital
cushions and their supporting predigits. In this
scenario, the predigits increasingly adopted the
supportive roles that were played by the carpals
(e.g., pisiform) and tarsals (e.g., calcaneus) in more
plantigrade basal Proboscidea. Representative
elephantiform and deinothere taxa along the phy-
logeny (Fig. 4) before Elephantidae support this
hypothesis (SOM text, figs.S14 to S16, and movies
S3 and S4): All well-preserved taxa exhibit smaller
proximal carpal/tarsal bones and foot bone articu-
lations that are more consistent with increased
dorsiflexion of the toes, and thus a more subunguli-
grade toe posture relative to the ancestral condition
for Proboscidea. All of these taxa display osteolog-
ical correlates for the articulation of predigits in the
manus and pes. Thus, we conclude that the pre-
digits have served to stiffen the expanded fat pad
and maintain a plantigrade-like foot function, trans-

ferring loads from the substrate to the carpus/tarsus,
since early in elephantiform evolution.
Extant elephants have remarkable feet that
combine advantages of plantigrady [such as the
potential for damping impacts at heelstrike (20),
larger foot surface area and thus moderated
pressures (21), large translations of the center of
pressure during the stance phase involving pro-
nounced heelstrike, dynamic gearing, and toe-
off dynamics (17)] with those of digitigrady or
subunguligrady [such as reasonable mechanical
advantage of the toes to keep supportive tissue
stresses at safe levels (22), or even potential ben-
efits to metabolic economy from elastic energy
storage (23)]. These changes occurred while early
elephantiforms attained gigantism (>2000 kg
of body mass or shoulder height >2 m) in the
Eocene epoch (~40 million years ago, Fig. 4) and
occupied a wider range of terrestrial habitats, be-
coming less amphibious around the node joining
Deinotheriinae and Elephantiformes (Fig. 4).
Hence, there is probably a link between the in-
Fig. 4. Evolution of pro-
boscidean foot posture.
A stratigraphically time-
calibrated axis is shown
at top, using the phyloge-
netic tree from (28–30),
with clades Proboscidea,
Elephantiformes, and El-
ephantoidea labeled at
nodes; the Sirenia (sea-
cows; manatees and du-
gongs) extant outgroup

is shown. Manus (on left)
and pes (on right) speci-
mens are shown in ap-
proximate osteologically
neutral poses in lateral
view (more explanation
and images are in the
SOM text and figs. S14 to
S16). Movies S3 and S4
show three-dimensional
foot reconstructions and
predigit articular surfaces
(where present). A shift
from a relatively more
plantigrade manus and
pes in Numidotherium
and Barytherium to more
subunguligrade feet in
later taxa is evident, es-
pecially when articular
surfaces are compared.
Shoulder heights (top of
scapula) for each genus are roughly estimated in parentheses, as
a proxy for body size changes. Representative skeletons of
Barytherium (top) and Deinotherium
(bottom) are shown with approximate relative size differences.
PLIOPaleP
Sirenia
Erytherium
Numidotherium
(1m)

Barytherium
(2m)
Phiomia
(<2m)
Deinotheriinae
(3m)
Mammut
americanum
(3m)
Gomphotherium
(3m)
Elephantidae
(3m)
60 my 50 my 40 my 30 my 20 my 10 my
Paleocene Oligocene Miocene Plio IVEocene
Proboscidea
Elephantiformes
Elephantoidea
Increasing
terrestriality
& gigantism
(>2m)
23 DECEMBER 2011 VOL 334 SCIENCE
www.sciencemag.org1702

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creasing demands of supporting and moving
greater weight on land and the benefits of having
more upright toe bones but directing some loads
away from the toes with the predigits and fat
pad, which resulted in the peculiar compromise
that persists in the feet of extant elephants.
The recognition of elephant predigits as en-
larged sesamoids that perform digit-like functions
fuels inspiration for examining the evolution of
foot function, terrestriality, and gigantism in other

lineages. Sauropod dinosaurs had expansive foot
pads, particularly in their pedes (24); however,
no evidence of predigits has been found. Con-
sidering that the predigits form on the medial
border of the feet, they would tend to be lost if
digit I is lost or reduced, as it was in early peris-
sodactyls and artiodactyls. This loss might limit
foot pad expansion and thereby explain why
rhinos and hippos seem to lack predigits [but see
(18) for a possible rudimentary pollex in hippos]
and have less expanded foot pads than elephants
do (8). Regardless, the previously misunderstood
and neglected predigits of elephants now deserve
recognition as a remarkable case of evolutionary
exaptation (4), revealing how elephants evolved
their specialized foot form and function.
References and Notes
1. D. D. Davis, Fieldiana 3, 1 (1964).
2. H. Endo et al., J. Anat. 195, 295 (1999).
3. S. J. Gould, Nat. Hist. 87, 20 (1978).
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6. M. R. Sánchez-Villagra, P. R. Menke, Zoology 108, 3
(2005).
7. P. Blair, Philos. Trans. 27, 53 (1710).
8. H. Neuville, Arch. Mus. Natl. Hist. Nat. Paris 13, 6e Serie,
111 (1935).
9. K. von Bardeleben, Proc. Zool. Soc. 1894, 354
(1894).
10. C. Mitgutsch et al. Biol. Lett., 10.1098/rsbl.2011.0494

(2011).
11. Materials and methods are available as supporting
material on Science Online.
12. G. E. Weissengruber et al., J. Anat. 209, 781 (2006).
13. F. Galis, J. J. M. van Alphen, J. A. J. Metz, Trends Ecol.
Evol. 16, 637 (2001).
14. J. Prochel, P. Vogel, M. R. Sánchez-Villagra, J. Anat. 205,
99 (2004).
15. J. R. Hutchinson, C. E. Miller, G. Fritsch, T. Hildebrandt,
in Anatomical Imaging: Towards a New Morphology,
R. Frey, H. Endo, Eds. (Springer, Berlin, 2009),
pp. 23–38.
16. C. E. Miller, C. Basu, G. Fritsch, T. Hildebrandt,
J. R. Hutchinson, J. R. Soc. Interface 5, 465 (2008).
17. D. R. Carrier, N. C. Heglund, K. D. Earls, Science 265,
651 (1994).
18. A. B. Clifford, J. Vertebr. Paleontol. 30, 1827 (2010).
19. N. Court, Palaeontogr. Abt. A 226, 125 (1993).
20. D. E. Lieberman et al., Nature 463, 531 (2010).
21. F. Michilsens, P. Aerts, R. Van Damme, K. D’Août,
J. Zool. (London) 279, 236 (2009).
22. A. A. Biewener, Science 250, 1097 (1990).
23. M. N. Scholz, M. F. Bobbert, A. J. van Soest, J. R. Clark,
J. van Heerden, J. Exp. Biol. 211, 3266 (2008).
24. M. F. Bonnan, in Thunder-Lizards: the Sauropodomorph
Dinosaurs, K. Carpenter, V. Tidwell, Eds. (Indiana Univ.

Press, Bloomington, IN, 2005), pp. 346–380.
25. M. M. Smuts, A. J. Bezuidenhout, Onderstepoort J. Vet.
Res.
60, 1 (1993).
26. M. M. Smuts, A. J. Bezuidenhout, Onderstepoort J. Vet.
Res.
61, 51 (1994).
27. A. Boyde, R. Travers, F. H. Glorieux, S. J. Jones,
Calcif. Tissue Int. 64, 185 (1999).
28. C. Delmer, Acta Palaeontol. Pol. 54, 561 (2009).
29. E. Gheerbrant, Proc. Natl. Acad. Sci. U.S.A. 106, 10717
(2009).
30. E. Gheerbrant, P. Tassy, C. R. Palevol. 8, 281 (2009).
Acknowledgments: We thank the staff of the Structure
and Motion Laboratory of the Royal Veterinary College for
assistance and three anonymous reviewers for constructive
criticism. Many individuals assisted with the collection of
the cadaveric data; we particularly thank the European-based
zoos that provided the specimens and G. Fritsch for CT
scans done in Germany. O. Cosar, R. Weller, A. Wilson, and
K. Jespers assisted with the ex vivo loading experiments.
J. Molnar assisted with Figs. 1 to 4 and the movies. This project
was funded by the Biotechnology and Biological Sciences
Research
Council (BBSRC) (grants BB/C516844/1 and BB/H002782/1
to J.R.H.). Additionally, A.A.P. appreciates funding from
Arthritis Research UK and the BBSRC, and A.B. was supported
by the Veterinary Advisory Committee of the UK Horserace
Betting Levy Board. The data reported in this paper are
tabulated in the SOM. The authors declare no conflicts

of interest.
Supporting Online Material
www.sciencemag.org/cgi/content/full/334/6063/1699/DC1
SOM Text
Figs. S1 to S16
Tables S1 to S3
Movies S1 to S4
20 July 2011; accepted 8 November 2011
10.1126/science.1211437
Global Seabird Response to Forage
Fish Depletion—One-Third for the Birds
Philippe M. Cury,1* Ian L. Boyd,2* Sylvain Bonhommeau,3
Tycho Anker-Nilssen,4
Robert J. M. Crawford,5 Robert W. Furness,6 James A. Mills,7
Eugene J. Murphy,8
Henrik Österblom,9 Michelle Paleczny,10 John F. Piatt,11 Jean-
Paul Roux,12,13
Lynne Shannon,14 William J. Sydeman15
Determining the form of key predator-prey relationships is
critical for understanding marine
ecosystem dynamics. Using a comprehensive global database,
we quantified the effect of
fluctuations in food abundance on seabird breeding success. We
identified a threshold in prey
(fish and krill, termed “forage fish”) abundance below which
seabirds experience consistently
reduced and more variable productivity. This response was

common to all seven ecosystems and
14 bird species examined within the Atlantic, Pacific, and
Southern Oceans. The threshold
approximated one-third of the maximum prey biomass observed
in long-term studies. This
provides an indicator of the minimal forage fish biomass needed
to sustain seabird
productivity over the long term.
P
ublic and scientific appreciation for the
role of top predators in marine ecosystems
has grown considerably, yet many upper
trophic level (UTL) species, including seabirds,
marine mammals, and large predatory fish, re-
main depleted owing to human activities (1–4).
Fisheries impacts include direct mortality of ex-
ploited species and the more subtle effects of
altering trophic pathways and the functioning of
marine ecosystems (5). Specifically, fisheries for
lower trophic level (LTL) species, primarily small
coastal pelagic fish (e.g., anchovies and sar-
dines), euphausiid crustaceans (krill), and squid
(hereafter referred to as “forage fish”), threaten
the future sustainability of UTL predators in
marine ecosystems (6, 7). An increasing global
demand for protein and marine oils contributes
pressure to catch more LTL species (8). Thus,
fisheries for LTL species are likely to increase
even though the consequences of such activity
remain largely unknown at the ecosystem level. It
remains challenging, however, to assess fishing
impacts on food webs because numerical re-

lationships between predators and prey are often
unknown, even for commercially valuable fish
(9, 10). Ecosystem models and ecosystem-based
fisheries management, for which maintaining
1Institut de Recherche pour le Développement, UMR EME-212,
Centre de Recherche Halieutique Méditerranéenne et Tropi-
cale, Avenue Jean Monnet, BP 171, 34203 Sète Cedex, France.
2Scottish Oceans Institute, University of St Andrews, St
Andrews
KY16 8LB, UK. 3Ifremer, UMR EME 212, Centre de Recherche
HalieutiqueMéditerranéenneetTropicale,AvenueJeanMonnet,
BP 171, 34203 Sète Cedex, France. 4Norwegian Institute for
Nature Research, Post Office Box 5685 Sluppen, NO-7485
Trondheim, Norway. 5Branch Oceans and Coasts, Department
of
Environmental Affairs, Private Bag X2, Rogge Bay 8012, South
Africa. 6College of Medical, Veterinary and Life Sciences, Uni-
versity of Glasgow, Glasgow G12 8QQ, UK. 710527 A Skyline
Drive, Corning, NY 14830, USA. 8British Antarctic Survey,
High
Cross, Madingley Road, Cambridge CB3 0ET, UK. 9Baltic Nest
Institute, Stockholm Resilience Centre, Stockholm University,
SE-106 91 Stockholm, Sweden. 10Fisheries Centre, Aquatic
Ecosystems Research Laboratory (AERL), 2202 Main Mall, The
University of British Columbia, Vancouver, BC, Canada V6T
1Z4.
11U.S. Geological Survey, Alaska Science Center, 4210 Uni-
versity Drive, Anchorage, AK 99508, USA. 12Ecosystem
Analysis
Section, Ministry of Fisheries and Marine Resources, Lüderitz
Marine Research, Post Office Box 394, Lüderitz, Namibia.
13Animal Demography Unit, Zoology Department, University
of
Cape Town, Private Bag X3, Rondebosch, Cape Town 7701,
South Africa. 14Marine Research Institute and Zoology Depart-

ment, University of Cape Town, Private Bag X3, Rondebosch,
Cape Town 7701, South Africa. 15Farallon Institute for
Advanced
Ecosystem Research, Post Office Box 750756 Petaluma, CA
94952, USA.
*To whom correspondence should be addressed. E-mail:
[email protected] (P.M.C.); [email protected] (I.L.B.)
1703
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ORG561
Examining Modern Leadership Toolkit 1.0
Use this toolkit for quick access to resources that may be used
to support skill and knowledge development related
to leadership study. Tools listed here are associated in some
way with discussions and assignments in ORG561.
Gather additional resources for your kit and share with others in
the classroom. Together you may just build an
even more robust, reusable kit; you might even call the updated
version Leadership Toolkit 2.0.
Professional
Writing
General
Analytic
Essay
Writing the analytic essay
https://www.kibin.com/essay-writing-blog/analytical-essay-
outline/
Business
documents
Design procedure for routine business documents

headings, information access, typography, space (HATS)
Includes section on graphics
https://owl.english.purdue.edu/owl/resource/632/1/
Outlines-
alphanumeri
c and full-
sentence
Tone Tone in business writing
Workplace
writing
Effective workplace writing
Presentatio
n
Slide
presentatio
n
developmen
t
10 tips to build slide presentations

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