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The Flexible Organism



Ecological Developmental Biology Integrating Epigenetics, Medicine, and Evolution by Scott F. Gilbert and David Epel Sinauer Associates, Sunderland, MA, 2009. 496 pp. $49.95. ISBN 9780878932993. Gilbert and Epel focus on embryonic and larval development of metazoans to explore where "embryology meets the real world."
17 JULY 2009 VOL 325 SCIENCE
I n the last chapter of How and Why Spe-
cies Multiply ( 1), Peter and Rosemary
Grant concluded that “[n]othing in evo-
lutionary biology makes sense
except in the light of ecology.”
In Ecological Developmen-
tal Biology, Scott Gilbert and
David Epel argue that noth-
ing in developmental biology
makes sense except in the light
of ecology either.
Traditionally, ecology—the
study of the relations of organ-
isms to one another and to
their physical surroundings—
has not featured prominently in developmen-
tal biology. Yet, as Gilbert and Epel (devel-
opmental biologists at Swarthmore Col-
lege and Stanford University, respectively)
observe, biologists have known for at least
a century that ecology is an essential partner
in development: In 1909, Danish biologist
Wilhelm Johannsen asserted that an organ-
ism’s appearance, physiology, and behavior
(that is, its phenotype) derive from an inter-
action between its genes and its environment.
Moreover, biologists long ago discovered that
numerous external environmental factors—
such as temperature, diet, physical stress, and
the presence of predators or competitors—
can alter an organism’s development, often
by generating a phenotype that is well suited
for its current environment. For example,
some plants produce large, thin leaves (which
enhance photosynthetic photon harvest) in
low light, and narrow, thicker leaves (which
conserve water) in high light; certain insects
develop wings only if they live in crowded
conditions (and hence are likely to run out of
adequate food in their current location). Such
environmentally contingent development is
so commonplace that it can be regarded as a
universal property of living things.
The emerging eld of ecological devel-
opmental biology (sometimes dubbed “eco-
devo”) explores how organisms develop
and function in “real-world” environments
( 2). Analyzing development among diverse
organisms under different environments is
a departure from how development has pre-
viously been studied. Traditionally, research
has focused on a few species (“model organ-
isms”) in the laboratory ( 3). Because devel-
opment was typically studied in uniform envi-
ronments, past research
fostered the erroneous
view that environmen-
tally contingent develop-
ment is rare or unimport-
ant. However, knowledge
of ecology’s role in devel-
opment is essential for a
complete understanding
of how organisms develop
and evolve. Indeed, accord-
ing to Gilbert and Epel, “in
addition to helping decide the survival of the
ttest, the environment is also important in
formulating the arrival of the fi ttest.
Unraveling ecology’s role in development
is not merely an academic exercise; it is also
vital for matters of public health. Research-
ers have long known that certain environ-
mental agents (including some commonly
used household and agricultural products)
can induce phenotypic variation by altering
gene expression rather than gene nucleotide
sequences. These “epigenetic” changes can
cause diseases such as cancers and diabe-
tes. In addition, because these environmen-
tal modifi cations can be passed stably from
one generation to the next, conditions expe-
rienced by past generations can profoundly
infl uence the health of subsequent genera-
tions. Yet, the descendants experiencing
such health problems may live in a perfectly
benign environment and have no (apparent)
genetic predispositions for the disease. Thus,
by understanding the infl uences on develop-
ment of both present and past environments
we can gain crucial insights into the causes of
disease that we might otherwise miss.
Understanding the connections between
development and ecology is crucial for pre-
serving biodiversity. In a world of increasing
biological invasions, anthropogenic chemi-
cal use, and climate change, many organ-
isms are experiencing unprecedented altera-
tions to their environment. Such changes can
cause unanticipated modifi cations to devel-
opment, which can in turn severely affect
the ecology, and even the survival, of natural
populations. For instance, the pesticide DDT
induces thin eggshells in birds, and atrazine
(the second-largest-selling weed killer in the
world) can cause sex change in many species
of vertebrates ( 4). Ecological developmental
biology is therefore highly relevant to con-
servation biology.
These are propitious and exciting times for
integrating the elds of development, ecology,
and evolution. Students and researchers are
fortunate that (in addition to the present vol-
ume) several important books have appeared
recently, including works by Carl Schlichting
and Massimo Pigliucci ( 5), Mary Jane West-
Eberhard ( 6), and Eva Jablonka and Marion
Lamb ( 7). Nevertheless, we have only begun
to construct an integrated framework. Gilbert
and Epel acknowledge the arduous task ahead
and “hope that college students, still relatively
undifferentiated, will come up with their own
connections and syntheses and that they will
see patterns that we haven’t yet imagined.”
Ecological Developmental Biology will serve
as an excellent guide for those interested in
embarking on such a synthesis. More gener-
ally, this lucid and thought-provoking book
should appeal to anyone interested in under-
The Flexible Organism
David W. Pfennig and Cris Ledón-Rettig
The reviewers are at the Department of Biology, Univer-
sity of North Carolina, Chapel Hill, NC 27599, USA. E-mail: (D.W.P.);
Ecological Developmental
Integrating Epigenetics,
Medicine, and Evolution
by Scott F. Gilbert and David Epel
Sinauer Associates, Sunderland,
MA, 2009. 496 pp. $49.95.
ISBN 9780878932993.
Seasonal morphs. Spring Nemoria arizonaria caterpillars resemble oak catkins (left); summer ones,
newly formed twigs (right).
Published by AAAS
W hen I picked up The Age of Entan-
glement, the f irst thing to catch
my eye was a quote on the back
dustjacket, “for a moment I almost thought
I understood quantum mechanics.” I thought,
“Oh boy, this could be trouble.” Recollections
danced in my noggin of uncomfortable con-
versations on crowded airplanes that begin
with “Oh, you are a quantum physicist?—
Then you must have seen What the Bleep Do
We Know!” But proceeding through the book,
my fear was never realized. I instead found a
witty, charming, and accurate
account of the history of that
bugaboo of physics—quan-
tum entanglement.
When I was a graduate stu-
dent in physics, I made the
decision to spurn a respect-
able career in high-energy
physics theory (if nowadays
one can consider superstring
theory to be respectable) and
embraced a future in the foundations of quan-
tum mechanics. As Louisa Gilder repeatedly
points out, in the mid-1980s such a career
move was considered the kiss of death. At
that time a respected professor pointedly told
me, “This foundations of
quantum mechanics is
crackpot stuff—you will
never get at job.” My, how
times have changed.
There are many books
out there on the history
or foundations of quan-
tum mechanics. Some
are more technical, others
more historical, but none
take the unique approach
that Gilder has—to focus
on the quantum weirdness
of entanglement itself as
her book’s unifying theme and to present it
in an inviting and accessible way. The Age of
Entanglement offers neither a technical nor a
biographical account. Rather, as Gilder states
up front, it provides a collection of recon-
structed conversations among some of the
20th century’s greatest physicists. These con-
versations all revolve around the notion of
quantum entanglement: the spooky, action-
at-a-distance effect predicted by quantum the-
ory but only slowly recognized as the theorys
defi ning feature and even more slowly shown
to be experimentally verifi able.
Your opinion of the book will largely
hinge on how you react to these reconstructed
conversations. Concerning one such imag-
ined conversation between Albert Einstein
and Niels Bohr on a streetcar in Copenhagen,
Gilder notes, “We know that the conversation
… happened, because Bohr mentioned it in
an interview …. The content of the conver-
sation is easy to gather from a look at what
the three men were working on … around the
same time.” Rather than provide dry quota-
tions from original sources, Gilder decided
to weave information from these sources
into a series of imagined conversations. The
author offers extensive docu-
mentation for these conver-
sations in the notes, so they
are not flights of fancy. Her
technique leads to text such
as, “ ‘If, however’—and here
[Einstein] looked straight at
Heisenberg, who was leaning
forward in his chair, his pale
hair shining in the dim room—
‘as is obviously the case in
modern atomic physics …. I suppose nei-
ther Einstein, Werner Heisenberg, nor anyone
else recorded that Heisenberg’s pale hair was
shining in the dim room, but it makes for a
good story. For this protocol to work for me, I
had to fi rst execute Coleridge’s “willing sus-
pension of disbelief and then engage Tol-
kien’s “secondary belief.” That done, I was
enthralled and found the
book delightful.
Gilder skillfully relates
the early discomfort
physicists felt concern-
ing some of the arcane
predictions of quantum
mechanics; how Einstein,
Erwin Schrödinger, and
others repeatedly distilled
and titrated their misgiv-
ing until they were able
in the 1930s to present the
essence of their fears in
the form of the Einstein-
Rosen-Podolsky paradox; Schrödinger’s cat;
and the now famous notion of quantum entan-
glement—spooky action-at-a-distance that
quantum theory must contain. Much in these
older “discussions” was familiar to me from
other sources. What I found most gratifying
were the studiously documented dialogs of
of later developments: Bell’s inequalities and
the consequent experiments, which proved
that nature is stranger than we can think. The
details of the story of David Bohm and his
trials, after constructing a nonlocal hidden
variable theory, were new to me. The account
of John Clauser and his cohorts in the race
to demonstrate (by testing Bell’s theory) once
and for all that this quantum weirdness did or
did not exist was side-splitting. An old friend
and collaborator, Clauser does in fact curse
like a sailor, as Gilder often has him do. (He
is a sailor, and I wonder whether the cursing
or the sailing came fi rst.) I was spellbound by
the details of the struggles of Clauser and col-
leagues with the massive, punch-tape spew-
ing, “coffi n” contraption clanking away, day
after day, in the bowels of Berkeley. It is tragic
that this apparatus now lies in mothballs in
the attic of LeConte Hall instead of on display
at the Smithsonian.
Gilder wraps up The Age of Entanglement
with conversations among younger quantum
technologists such as Artur Ekert, Nicolas
Gisin, Daniel Greenberger, Michael Horne,
Terrence Rudolph, and Anton Zeilinger. As I
read these pages, I wondered if I should feel
slighted—there is no mention of me. Then
I happened upon this description of a col-
league and friend: “Meanwhile in the Sangre
de Cristo Mountains of New Mexico, Paul
Kwiat, an endearingly birdlike man in glasses
and suspenders with boundless energy and
encyclopedic knowledge, led his team in
attempting various eavesdropping strategies
on their Alice and Bob.” Thank goodness for
small favors, I thought, smiling to myself.
standing how organisms are built, function,
and evolve or how anthropogenic environ-
mental change affects the health of ourselves
and other organisms.
1. P. R. Grant, B. R. Grant, How and Why Species Multiply:
The Radiation of Darwin’s Finches (Princeton Univ. Press,
Princeton, NJ, 2008); reviewed in ( 8).
2. S. E. Sultan, Trends Ecol. Evol. 22, 575 (2007).
3. B. Maher, Nature 458, 695 (2009).
4. T. Hayes et al., Environ. Health Perspect. 111, 568
5. C. D. Schlichting, M. Pigliucci, Phenotypic Evolution: A
Reaction Norm Perspective (Sinauer, Sunderland, MA,
1998); reviewed in ( 9).
6. M. J. West-Eberhard, Developmental Plasticity and Evolu-
tion (Oxford Univ. Press, Oxford, 2003); reviewed in ( 10).
7. E. Jablonka, M. J. Lamb, Evolution in Four Dimensions
(MIT Press, Cambridge, MA, 2005).
8. H. Kokko, Science 319, 1187 (2008).
9. H. A. Orr, Science 285, 343 (1999).
10. J. S. Levinton, Science 301, 767 (2003).
with a Twist
Jonathan P. Dowling
The reviewer is at the Department of Physics and Astronomy,
Louisiana State University, Baton Rouge, LA 70803–4001,
USA. E-mail:
The Age of Entanglement
When Quantum Physics
Was Reborn
by Louisa Gilder
Alfred A. Knopf, New York,
2008. 462 pp. $27.50, C$32.
ISBN 9781400044177.
John S. Bell. Foundational theorizer.
Published by AAAS
... Phenotypic plasticity in locusts is known as phase polyphenism, in which local population density affects the expression of various behavioral, physiological, and morphological traits [4]. In recent years, several regulatory mechanisms related to phenotypic plasticity in pests have been identified, including hormone regulation, differential gene expression, alternative splicing, DNA methylation, etc. [5][6][7][8]. This phase polymorphism phenomenon is a very complex multifactorial process. ...
Full-text available
The high-density-dependent phase change from solitary to gregarious individuals in locusts is a typical example of phenotypic plasticity. However, the underlying molecular mechanism is not clear. In this study, first, Oedaleus asiaticus were treated with high-density population stress and then analyzed by Illumina sequencing on days 1, 3, 5, and 7 of the body color change to identify the stage-specific differentially expressed genes (DEGs). The KEGG pathway enrichment analysis of the identified DEGs revealed their role in metabolic pathways. Furthermore, the expression patterns of the nine key DEGs were studied in detail; this showed that the material change in locusts began on the third day of the high-density treatment, with the number of DEGs being the largest, indicating the importance of this period in the phase transition. In addition, the phenotypic change involved several key genes of important regulatory pathways, possibly working in a complex network. Phenotypic plasticity in locusts is multifactorial, involving multilevel material network interactions. This study improves the mechanistic understanding of phenotypic variation in insects at the genetic level.
... The sub-national nature of domestic institutions can further support the view of using the sub-national unit as the geographic focal of EMs. First, according to the resource-based view (e.g., Barney, 1991; Baron, 1995; Penrose, 1959) and the environmental contingency argument in biology (Ostrom, 2010; Pfennig & Ledón-Rettig, 2009), organizing systems, like organisms, are initially structured and developed partially as a way to adapt to the available resource endowment of the region. Even when certain formal rules can be designed to apply nationally, the initial institutional framework of informal institutions (e.g., measurement and standards) and enforcement characteristics diverge as different local institutional carriers (e.g., local administrators) confront different problems with different geographic assets (e.g., proximity to raw materials and seaports), different human capital, and different climates (North, 1990). ...
Full-text available
The rise of new global contender MNEs from large emerging markets (EMs) is leading to significant structural transformation of global industries, international institutions, and global power (re)arrangement. Outward FDI undertaken by these EM multinational enterprises (MNEs) is growing fast as they are on a buying spree of assets and companies abroad. The share of EMs in global FDI outflows increased to 19% in 2008 and further to 25% in 2009 (UNCTAD, 2010). Among relatively large EMs, India’s annual compound growth of 176% during 2000-2008 had been unprecedented, ahead of its counterparts such as China (165%), Brazil (123%), and Russia (151%), although from a relatively lower base (UNCTAD, 2010). India’s outward FDI position is much more active than its comparator economy China, which received about $500 billion in inward FDI before its firms began to substantially invest abroad and maintained its inward FDI five times its outward FDI as late as 2007 – substantial inward FDI and outward FDI of India started almost at the same time and India’s total outward FDI (e.g., $25 billion in 2007) is almost as large as total inward FDI (e.g., $17 billion in 2007) (Ramamurti, 2010). These noticeable, interesting observations have triggered a few major special issues and book volumes focusing on Indian MNEs, notably Transnational Corporations Review (Vol. 3, No. 2), Pradhan (2008), and Sauvant and Pradhan (2010). This article takes steps further and examines two myths and potential explanations about Indian outward FDI that lead us to set up a more relevant and nuanced research agenda on EM MNEs.
This excerpt describes the intellectual journey that I have taken the last half-century from when I began graduate studies in the late 1950s. The early efforts to understand the polycentric water industry in California were formative for me. In addition to working with Vincent Ostrom and Charles Tiebout as they formulated the concept of polycentric systems for governing metropolitan areas, I studied the efforts of a large group of private and public water producers facing the problem of an overdrafted groundwater basin on the coast and watching saltwater intrusion threaten the possibility of long-term use. Then, in the 1970s, I participated with colleagues in the study of polycentric police industries serving U.S. metropolitan areas to find that the dominant theory underlying massive reform proposals was incorrect. Metropolitan areas served by a combination of large and small producers could achieve economies of scale in the production of some police services and avoid diseconomies of scale in the production of others.
Elinor Ostrom delivered her Prize Lecture on 8 December 2009 at Aula Magna, Stockholm University. She was introduced by Professor Bertil Holmlund, Chairman of the Economic Sciences Prize Committee.
The first comprehensive synthesis on development and evolution: it applies to all aspects of development, at all levels of organization and in all organisms, taking advantage of modern findings on behavior, genetics, endocrinology, molecular biology, evolutionary theory and phylogenetics to show the connections between developmental mechanisms and evolutionary change. This book solves key problems that have impeded a definitive synthesis in the past. It uses new concepts and specific examples to show how to relate environmentally sensitive development to the genetic theory of adaptive evolution and to explain major patterns of change. In this book development includes not only embryology and the ontogeny of morphology, sometimes portrayed inadequately as governed by "regulatory genes," but also behavioral development and physiological adaptation, where plasticity is mediated by genetically complex mechanisms like hormones and learning. The book shows how the universal qualities of phenotypes--modular organization and plasticity--facilitate both integration and change. Here you will learn why it is wrong to describe organisms as genetically programmed; why environmental induction is likely to be more important in evolution than random mutation; and why it is crucial to consider both selection and developmental mechanism in explanations of adaptive evolution. This book satisfies the need for a truly general book on development, plasticity and evolution that applies to living organisms in all of their life stages and environments. Using an immense compendium of examples on many kinds of organisms, from viruses and bacteria to higher plants and animals, it shows how the phenotype is reorganized during evolution to produce novelties, and how alternative phenotypes occupy a pivotal role as a phase of evolution that fosters diversification and speeds change. The arguments of this book call for a new view of the major themes of evolutionary biology, as shown in chapters on gradualism, homology, environmental induction, speciation, radiation, macroevolution, punctuation, and the maintenance of sex. No other treatment of development and evolution since Darwin's offers such a comprehensive and critical discussion of the relevant issues. Developmental Plasticity and Evolution is designed for biologists interested in the development and evolution of behavior, life-history patterns, ecology, physiology, morphology and speciation. It will also appeal to evolutionary paleontologists, anthropologists, psychologists, and teachers of general biology.
How and Why Species Multiply. The Radiation of Darwin's Finches. By Peter R. Grant and B. Rosemary Grant. Princeton University Press, Princeton, NJ, 2008. 272 pp. $35, £19.95. ISBN 9780691133607. Princeton Series in Evolutionary Biology. Drawing on decades of research in the Galapagos (especially their own work), the authors offer a comprehensive introduction to Darwin's finches and to evolutionary radiations on islands.
Phenotypic Evolution A Reaction Norm Perspective. Carl D. Schlichting and Massimo Pigliucci. Sinauer Associates, Sunderland, MA, 1998. 400 pp. Paper, $38.95. ISBN 0-87893-799-4. Schlichting and Pigliucci argue for the evolutionary importance of the "developmental reaction norm," a concept that combines adaptive plasticity, development, and allometry.
Developmental Plasticity and Evolution. by Mary Jane West-Eberhard. Oxford University Press, New York, 2003. 814 pp. $100, £79.50. ISBN 0-19-512234-8. Paper, $49.95, £31.99. ISBN 0-19-512235-6. Discussing a wide range of ideas and empirical studies that support them, West-Eberhard focuses on showing what recent findings in development, physiology, and behavior suggest about the origins of evolutionary novelties.
Developmental Plasticity and Evolution
Atrazine is the most commonly used herbicide in the United States and probably the world. Atrazine contamination is widespread and can be present in excess of 1.0 ppb even in precipitation and in areas where it is not used. In the current study, we showed that atrazine exposure (> or = to 0.1 ppb) resulted in retarded gonadal development (gonadal dysgenesis) and testicular oogenesis (hermaphroditism) in leopard frogs (Rana pipiens). Slower developing males even experienced oocyte growth (vitellogenesis). Furthermore, we observed gonadal dysgenesis and hermaphroditism in animals collected from atrazine-contaminated sites across the United States. These coordinated laboratory and field studies revealed the potential biological impact of atrazine contamination in the environment. Combined with reported similar effects in Xenopus laevis, the current data raise concern about the effects of atrazine on amphibians in general and the potential role of atrazine and other endocrine-disrupting pesticides in amphibian declines.