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International Journal of Epidemiology, 2015, Vol. 44, No. 4
What we could not discuss in 1995 was information transmission through small non-coding RNAs. This was not recognized until the late 1990s, when the discovery of gene
regulation through RNA interference and the realization that
it provided a powerful research tool gave epigenetics research
an enormous boost. It soon became clear that the small
RNAs that mediate gene silencing can not only be transmitted
to daughter cells, but also move to more distant cells, including germ cells. Thus, another route through which epigenetic
changes can affect future generations was revealed, one that
might have significant effects in all species, including those
with early segregation of the germ line. Weismann’s barrier
was breached in a surprising way, one that was reminiscent
of Darwin’s unaccepted idea that hereditary information is
transmitted from body cells to the reproductive organs
through small molecules called gemmules.10
Today, ‘epigenetic inheritance’ has become an umbrella
term covering the many interacting ways through which
variations that do not depend on DNA differences are transmitted in lineages of cells and organisms. In disciplines as diverse as animal behaviour, plant ecology and epidemiology,
it is recognized that through epigenetic inheritance acquired
variations can have an impact on later generations. Sadly
for us, in our own field of evolutionary biology, with a few
exceptions,11 either the significance of epigenetic inheritance
is down-played or the subject is treated with hostility; many
evolutionary biologists have not bothered to get acquainted
with epigenetic research. We have continued to argue that
epigenetic and other types of non-DNA variations must be
included in evolutionary thinking.12 Our hope is that now
that studies of heredity and development have moved away
from the gene-centric approach that characterized the last
half of the 20th century, the developmental system approach
that is replacing it will lead to more interest in evolutionary
Commentary: A conceptual
revolution limited by
disciplinary division
1105
epigenetic research and to a more widespread acceptance of
the importance in evolution of the inheritance of acquired
epigenetic variations.
Conflict of interest: None declared.
References
1. Jablonka E, Lamb MJ. Meiotic pairing constraints and the activity of sex chromosomes. J Theor Biol 1988;133:23–36.
2. Buss LW. The Evolution of Individuality. Princeton, NJ:
Princeton University Press, 1987.
3. Holliday R. The inheritance of epigenetic defects. Science
1987;238:163–70.
4. Jablonka E, Lamb MJ. The inheritance of acquired epigenetic
variations. J Theor Biol 1989;139:69–83.
5. Silva AJ, White R. Inheritance of allelic blueprints for methylation patterns. Cell 1988;54:145–52.
6. CairnsJ, Overbaugh J, Miller S. The origin of mutants. Nature
1988;335:142–45.
7. Maynard Smith J. Models of a dual inheritance system. J Theor
Biol 1990;143:41–53.
8. Jablonka E, Lachmann M, Lamb MJ. Evidence, mechanisms and
models of the inheritance of acquired characters. J Theor Biol
1992;158:245–68.
9. Jablonka E, Lamb MJ. Epigenetic Inheritance and Evolution:
the Lamarckian Dimension. Oxford,UK: Oxford University
Press, 1995.
10. Darwin C. The Variation of Animals and Plants under
Domestication. Vol 2. London: John Murray, 1868. 2nd edn reprint: Baltimore, MD: John Hopkins University Press,1998.
11. Richards CL, Verhoeven KJF, Bossdorf O. Evolutionary significance of epigenetic variation. In: Wendel JF, Greilhuber J,
Dolezel J et al (eds). Plant Genome Diversity. Vol 1. Vienna:
Springer, 2012.
12. Jablonka E, Lamb MJ. Evolution in Four Dimensions: Genetic,
Epigenetic, Behavioral, and Symbolic Variation in the History of
Life. Revised edn. Cambridge, MA: MIT Press, 2014.
International Journal of Epidemiology, 2015, 1105–1107
doi: 10.1093/ije/dyv021
Advance Access Publication Date: 7 April 2015
Aaron Panofsky
UCLA Institute for Society and Genetics and Department of Public Policy, University of California,
Box 957221 Rolfe Hall 1320, Los Angeles, CA 90095-7221, USA. E-mail: [email protected]
In the past decade or two we have witnessed a remarkable
social sciences. For more than a century it seemed that
thaw in the long chilly relations between the biological and
there was only one basic way the two modes of enquiry
C The Author 2015; all rights reserved. Published by Oxford University Press on behalf of the International Epidemiological Association
V
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could fit together: biology (or genetics or evolutionary
forces) would be fundamental, the basis or bedrock upon
which behaviour and society (or culture or social relations
and structures) are formed. And the relationship would be
basically deterministic, perhaps probabilistic, but certainly
unidirectional. The question would be how biology shapes
society. The social sciences’ best recourse was to assert
their cognitive autonomy, declaring society as sui generis,
and resist and criticize the incursion of biology. In this regime, biologists might one day aspire to colonially dominate their neighbors—E.O. Wilson’s ‘consilience’,1 but most
would prefer to avoid that quagmire and do their work
separately.
This conceptual framework and the relationships it presupposes are certainly not dead, but they are definitely
on the decline and faced with a raft of competitors. Eva
Jablonka and Marion J Lamb’s ‘The inheritance of
acquired epigenetic variations’2 was early in a series of
publications that were as responsible as anything for
breaking the hold of the prevailing framework. The article
synthesized and codified an emerging research programme
that established epigenetic inheritance as an important
intergenerational and perhaps evolutionary force.
They present the striking image of the ‘gene’s phenotype’—no longer pure information, the gene has a body
too. And that body makes the gene open to the environment. Not once does the article mention ‘society’ or the
‘social’ and, indeed, few social scientists have a particular
interest in evolutionary theory. But the gene’s phenotype
opens the door to social scientists by fracturing the old
biology/society relationship. No longer hierarchical, or at
least not only hierarchical, epigenetics flattens the relationship. For example, in Michael Meaney and Moshe Szyf’s
famous mouse studies of the epigenetic transmission of
maternal care and stress responses, factors such as stress
experience, maternal licking behaviour, cortisol, the glucocorticoid receptor, methylation of the receptor promoter
and DNA sequence all exist as necessary elements in a
complex causal cascade.3 None has ontological priority as
the ‘basic’ or ‘primary’ cause; the concept of environment
has fractured and ramified, and distinctions like social vs
biological are less important than location within the
causal network.
Jablonka and Lamb were eager to establish epigenetics
as a potentially important force in evolution. But the article’s influence, I think, is due less to its evolutionary argument than to the intergenerational logic that drives it.
Everyone acknowledges that environment matters in that,
say, nutritional deprivation during gestation may lead a
body never to develop properly. But once the fetus’s eventual grandchildren or great-grandchildren might be affected, suddenly more seems to be at stake. Where before
International Journal of Epidemiology, 2015, Vol. 44, No. 4
the environment, social forces, etc. might arguably still be
seen as separable from an organism’s or population’s true
(genetic) essence, intergenerational effects, especially those
beyond the offspring, somehow demand different scientific
respect and attention.
These possibilities are leading researchers across the
range of post-genomic life sciences to think of epigenetics
as ‘where environment, society and genetics meet’.4
Epigenetics has offered new ways to take society seriously as
more than extraneous context but less than genetically
determined. It offers a set of mechanisms and frameworks
to talk about gene/environment interaction in ways that are
more than statistical. And thus biological scientists have
begun studying social forces and recognizing the necessity of
an interdisciplinary approach to epigenetically mediated
health conditions such as stress, anxiety and depression.
But here is the thing: biological scientists are talking
about society and social forces without interacting with social scientists. It is incredibly rare for a social scientist to be
listed as a co-author on an epigenetics article—even those
articles ostensibly targeting effects of the ‘social’. With all
due respect to the public health researchers who play the
social science role in this research, potentially crucial social
scientific expertise is largely excluded. At the same time
sociologists, political scientists and economists who have
become emboldened to take biology and genetics seriously,
have overwhelmingly done so using quantitative genetic
family studies or candidate gene association studies to partition genetic and environmental contributions to population variance for socially relevant traits. They have walked
through the door opened by Jablonka and Lamb only to reproduce the old conceit that genes and environment are
distinct and independently measurable causes.
Though Jablonka and Lamb’s work on epigenetics has
helped tear down some of the conceptual walls separating
the biological and social sciences, it has done less to reconfigure disciplinary habits of work. One practical legacy of
the historical chill between the fields is that they have not
yet figured out how to work together. Surely there are
many more stunning advances that will emerge from the
current configuration of epigenetics research. But I would
like to suggest that the next level of advances will depend
as much on changes to science organization and policy as
on conceptual advances. That is, once we figure out how
to incentivize and assemble truly multidisciplinary research
teams in ways that overcome disciplinary divisions of labour (biologists in the laboratory, social scientists measuring the environment), then the truly transdisciplinary
potential of an epigenetic approach to biosocial problems
can be realized.
Conflict of interest: None declared.
International Journal of Epidemiology, 2015, Vol. 44, No. 4
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3. Weaver ICG, Cervoni N, Champagne FA et al. Epigenetic programming by maternal behavior. Nature Neuroscience 2004;7:
847–54.
4. Majnik AV, Lane RH. Epigenetics: Where environment, society
and genetics meet. Epigenomics 2014:6:1–4.
References
1. Wilson EO. Consilience: The Unity of Knowledge. New York,
NY: Random House, 1999.
2. Jablonka E, Lamb MJ. The inheritance of acquired epigenetic
variations. J Theor Biol 1989;139:69–83. Reprinted Int J
Epidemiol 2015;44:1094–103.
International Journal of Epidemiology, 2015, 1107–1108
doi: 10.1093/ije/dyv022
Commentary: The
information of conformation
Advance Access Publication Date: 7 April 2015
Hannah Landecker
Institute for Society and Genetics, Department of Sociology, University of California Los Angeles,
Box 957221, 1320 Rolfe Hall, Los Angeles, CA 90095-7221, CA, USA. E-mail: [email protected]
A deeply staining substance known as chromatin
(Flemming),1 is the nuclear substance par excellence,
for in many cases it appears to be the only element of
the nucleus that is directly handed on by division from
cell to cell, and it seems to have the power to produce
all the other elements.2
In the 1870s, intensive microscopical work to analyse
the dynamics of cell division produced a new entity for the
cell: chromatin, so named by Walter Flemming because it
readily took up histological dyes. The word means coloured substance. Thus it is a rather arbitrary word, more
to do with the technique of visualization than a descriptor
of the thing. Nonetheless, before the ascendance of the
gene concept, the powers of heredity were ascribed to chromatin. As EB Wilson put it in 1900, chromatin ‘seems to
have the power to produce all the other elements’ of the
nucleus.2 With the rise of the gene in the 20th century,
chromosomes were seen as gene-carriers; with the identification of DNA as the hereditary material, the importance
of ‘chromatin as the physical basis of inheritance’—as
it was frequently described in the first half of the 20th
century—receded still further.3 This conceptual separation
between DNA as the locus of information and its transmission, and chromatin as a mere scaffold was as arbitrary as
the initial naming of chromatin: after all, chromatin is,
by definition, the complex of DNA and proteins
constituting the contents of the nucleus (and one wonders
today if the definition of chromatin should not include
RNA).
A key point of Jablonka and Lamb’s now classic ‘The
inheritance of acquired epigenetic variations’4 is to insist
that DNA never comes alone: chromatin structure and
conformation are redescribed as ‘the gene’s phenotype’.
Italicized in the original to draw attention to the importance and perhaps anti-intuitive nature of the phrase, chromatin is highlighted here as the animate body of the gene.
For this reader, it is a description that evokes both ideas of
chromatin before DNA—such as De Vries’ notion of chromatin as a living colony of invisible biophores5—as well as
the future that would come after 1989, a renaissance in
chromatin biology. Today, the complex architecture and
topography of chromatin, as well as its temporal dynamism, is at the centre of research in gene regulation and
epigenetics. Chromatin has become an ‘integration and
storage platform’ for signals coming into the cell,6 the
‘physiological template of all eukaryotic genetic information’,7 the nuclear ‘landscape’ of pluripotency and senescence8 and ‘the physiological form of our genome’.9
Indeed, if the 20th century was the century of the gene, as
historian Evelyn Fox Keller puts it, the 21st may well turn
out to be the century of chromatin.10
It is instructive, therefore, to return to the role of chromatin in this seminal theorization of epigenetic inheritance.
Chromatin structure and conformation were proposed as
the gene’s phenotype, that which ‘determines its functional
state’.1 Evidence was offered from studies with nuclease
enzymes, which were useful because they could only cut
the DNA strand if the enzyme could get at it, implying an
open conformation of chromatin. More important than the
experimental evidence brought to bear on the question of
chromatin conformation is the rhetorical construction of
chromatin as an impressionable physical material. It was
pliable enough to take the imprint of an environmental or
developmental event, but stable enough to then hold that
C The Author 2015; all rights reserved. Published by Oxford University Press on behalf of the International Epidemiological Association
V