Professional Documents
Culture Documents
Loison2018 Article LamarckismAndEpigeneticInherit
Loison2018 Article LamarckismAndEpigeneticInherit
https://doi.org/10.1007/s10539-018-9642-2
Laurent Loison1
Received: 27 May 2017 / Accepted: 24 August 2018 / Published online: 27 August 2018
© Springer Nature B.V. 2018
Abstract
Since the 1990s, the terms “Lamarckism” and “Lamarckian” have seen a signifi-
cant resurgence in biological publications. The discovery of new molecular mecha-
nisms (DNA methylation, histone modifications, RNA interference, etc.) have been
interpreted as evidence supporting the reality and efficiency of the inheritance of
acquired characters, and thus the revival of Lamarckism. The present paper aims at
giving a critical evaluation of such interpretations. I argue that two types of argu-
ments allow to draw a clear distinction between the genuine Lamarckian concept
of inheritance of acquired characters and transgenerational epigenetic inheritance.
The first concerns the explanandum of the processes under consideration: molecular
mechanisms of transgenerational epigenetic inheritance are understood as evolved
products of natural selection. This means that the kind of inheritance of acquired
characters they might be responsible for is an obligatory emergent feature of evolu-
tion, whereas traditional Lamarckisms conceived the inheritance of acquired char-
acters as a property inherent in living matter itself. The second argument concerns
the explanans of the inheritance of acquired characters: in light of current knowl-
edge, epigenetic mechanisms are not able to drive adaptive evolution by themselves.
Emergent Lamarckian phenomena would be possible if and only if individual epi-
genetic variation allowed the inheritance of acquired characters to be a factor of
unlimited change. This implies specific requirements for epigenetic variation, which
I explicitly define and expand upon. I then show that given current knowledge, these
requirements are not empirically grounded.
* Laurent Loison
laurentloison@yahoo.fr
1
CNRS, IHPST (UMR 8590, CNRS, Paris 1 Panthéon-Sorbonne, ENS), Paris, France
13
Vol.:(0123456789)
29 Page 2 of 17
L. Loison
Introduction
Over the past 2 decades, arguments supporting the accuracy of the Lamarck-
ian explanation of inheritance and evolution have become more and more com-
mon and explicit. Several scholars claim that Lamarckism is back and that the
Lamarckian concept of evolution through the inheritance of acquired characters
deserves a reappraisal (Gissis and Jablonka 2011; Jablonka and Lamb 1999,
2014; Koonin 2014; Koonin and Wolf 2009; Varmuza 2003; Skinner 2015; Wang
et al. 2017; see also Deichmann 2016a for other examples). The discovery of new
molecular mechanisms of epigenetic inheritance such as DNA methylation, his-
tone modifications and RNA interference has given grist to the mill of the advo-
cates of the Lamarckian revival (Skinner 2015, p. 1296):
Lamarck proposed in 1802 the concept that environment can directly alter
phenotype in a heritable manner. Environmental epigenetics and epigenetic
transgenerational inheritance provide molecular mechanisms for this pro-
cess.
The recent comeback of Lamarckism has inspired some emphatic and pro-
vocative statements like “Lamarck rises from his grave” (Wang et al. 2017, p. 1)
or “Lamarck is back, and perhaps with a vengeance” (Koonin 2014, p. 238). To
what extent are these claims justified? Can epigenetic inheritance be legitimately
thought to vindicate Lamarckism? The present article aims to propose a philo-
sophical examination of these recent defenses of a resurgence of Lamarckism,
which have yet to be consistently questioned (Deichmann 2016a).
First, it must be noted that the supporters of a Lamarckian account of epige-
netic phenomena base their argument on the supposed equivalence between two
concepts: Lamarckism and the inheritance of acquired characters. This is a mis-
leading conflation: the term “inheritance of acquired characters” has long (Nut-
ting 1892) been singled out for its especially vague and inclusive nature, hence
potentially applying to a very wide range of phenomena and mechanisms, only
a few of which might be labelled “Lamarckian”. In other words, the Lamarck-
ian concept of inheritance of acquired characters—which is precisely defined in
the first section of the present article—is only a limited subset of the much more
general concept of inheritance of acquired characters. To describe a phenomenon
in the terms of the inheritance of acquired characters (thereafter IAC) is not suf-
ficient to be able to speak of Lamarckism.
The present article thus proposes a critical enquiry into the relationship of the
categories of epigenetic inheritance and Lamarckian inheritance. My aim is to
show that they are not equivalent subsets of the general concept of IAC. In order
to construct a workable definition of Lamarckian inheritance, my argument will
heavily rely on what history of biology teaches us about Lamarckism in the nine-
teenth and early twentieth century. The first section briefly characterizes some
of the main Lamarckian accounts of IAC, from Lamarck’s (“Lamarck’s zoo-
logical philosophy” section) to those advanced in the late nineteenth and early
twentieth century (“Darwin’s pangenesis” section, “Neo-Lamarckian views”
13
Lamarckism and epigenetic inheritance: a clarification Page 3 of 17 29
It is now known that Lamarck’s biology was part of an elaborate system named “ter-
restrial physics” and that his project was to give a consistent physical account of
“animality” (see especially Burkhardt 1977 and Corsi 1988). In order to explain
physically what an animal is, i.e. how it “works” and how it is formed, Lamarck
devised the very first theory of organic evolution. In 1800, he began conceptualiz-
ing two orthogonal mechanisms: a trend towards complexity and adaptation through
IAC.1 Animals were considered as semi-solid structures in which different types of
fluids flowed (blood, lymph, but also caloric, electricity, etc.). These fluids organ-
ized the plastic body and this organizational improvement sped up flows in return:
1
Note that the exact term “inheritance of acquired characters” was not in use before the death of
Lamarck himself (Gayon 2006).
13
29 Page 4 of 17
L. Loison
Darwin’s pangenesis
13
Lamarckism and epigenetic inheritance: a clarification Page 5 of 17 29
why he emphasized that “any permanent modification” of the body “would act on
the gemmules” (Darwin 1868, p. 382).
Darwin was also explicit about the evolutionary scope of his theory of IAC. For
him, there was no doubt that IAC, by itself—i.e. without any need for natural selec-
tion or other evolutionary factors—was capable of “great changes” in the structure
of the body (see especially Darwin 1868, p. 389). The first part of the chapter is
indeed an impressive list of examples and case-studies that must be explained by
IAC, empirically grounding his pangenesis hypothesis.
How did Darwin explain that living beings are endowed with such physiologi-
cal properties? The issue of the explanandum of IAC is especially significant here
because Darwin was the founder of the selective way of thinking, and, with August
Weismann, one of the best theoreticians working on natural selection at the time.
In the nineteenth century, if someone was to be able to think of IAC as an evolved
mechanism itself resulting from natural selection, it would have to be Darwin. Dar-
win never explicitly addressed this issue in his 1868 book (nor in the second edition
of 1875), but it remains possible to plausibly reconstruct his position. Only at the
very end of Chapter 27 does he give us an indication of it (Darwin 1868, p. 404):
We cannot fathom the marvelous complexity of an organic being; but on the
hypothesis here advanced [pangenesis] this complexity is much increased.
Each living creature must be looked at as a microcosm—a little universe,
formed of a host of self-propagating organisms, inconceivably minute and as
numerous as the stars in heaven.
This passage indisputably echoes the famous last sentences of the Origin of Spe-
cies where Darwin compared natural selection to the “fixed law of gravity” (Darwin
1859, p. 490). In both cases—but more explicitly in 1859 than in 1868—the com-
parison with cosmology and physics strongly suggests that he understood both natu-
ral selection and pangenesis as “laws of nature”, i.e. inherent and obligatory pro-
cesses of life. From an epistemological point of view, the perfect symmetry in the
structure and argumentation of the Origin of Species and The Variation of Animals
and Plants under Domestication greatly reinforces this interpretation. Most likely
then, pangenesis, the mechanism of IAC, was thought to have been efficient since
the origin of life on earth.
Neo‑Lamarckian views
13
29 Page 6 of 17
L. Loison
invertebrate and vertebrate fossils. This is why they laid special emphasis on a vital-
spiritual force that would drive evolution from the inside. This internal force was
supposed to create developmental novelties that always arose in the same definite
direction. Because they were supposed to be cumulated through IAC, these indi-
vidual variations were the cornerstone of the entire phyletic evolution. For example,
Cope emphasized what he called “bathmism”, i.e. the “growth energy” responsible
for both the occurrence of new characters and their subsequent hereditary transmis-
sion (see for example Cope 1896, parts 2 and 3; Bowler 1992, p. 124). Their under-
standing of IAC was thus based on an explicitly vitalist stance. IAC was the nec-
essary consequence of vital forces or energies. As such, IAC was unambiguously
understood as both an inherent attribute of life and a self-sufficient evolutionary
cause.
At roughly the same time, French biologists opposed this vitalist view and sup-
ported an alternative Neo-Lamarckism (Loison 2011). They argued that the primum
movens of evolution was not a phyletic increase in complexity but adaptation to
local environments. Like the majority of their contemporaries, they thought of the
protoplasm—i.e. “the physical basis of life”, to quote Thomas Huxley’s influential
phrase—as a structure able to accommodate environmental variations in one way
or another. They viewed this kind of adaptive and physiological process as the basis
of all evolutionary changes because of the efficiency of IAC. Among them, Félix Le
Dantec developed a rather elaborate Neo-Lamarckian theory of evolution. His expla-
nation of IAC is of particular interest here. Le Dantec thought of the protoplasm as
a colloidal structure, and it was its colloidal properties that, in his view, allows it
not only to react to its environment but also to secure the new conformation at the
chemical level of the cell (Le Dantec 1907, p. 22, p. 30). In other words, IAC was
not explained by specific vital forces, but—as in Lamarck’s work—because of the
physico-chemical properties classically at work in the organized matter that consti-
tutes living beings.
Outside France, many other biologists tried to produce a physico-chemical
account of IAC. One of the best remembered is Ernst Haeckel’s. In his hypothesis—
the highly speculative “perigenesis of the plastidules” (Haeckel 1876)—undulatory
movements affected the organic molecules of the protoplasm (the “plastidules”).
Heredity was nothing more than the transmission of these vibrations through cell
cycles and from one generation to the next. This means that the evolutionary cau-
sality was strictly individual and physiological in the first place. If the environment
was changing, then the individual organism’s protoplasm was able to adapt and this
change in conformation was recorded and physiologically transmitted by a change
in the vibration pattern of the plastidules. Mario A. Di Gregorio rightly empha-
sized that, for Haeckel, “the universal memory of living matter was handed down
from one generation to another […], it was eternal” (Di Gregorio 2005, p. 225, my
emphasis). This means that in Heackel’s conception, there was no doubt that the
perigenesis of the plastidules, as a necessary outcome of the physical working of the
protoplasm, had existed from the very origin of life.
Despite significant differences, my aim is to show that all these (Neo)Lamarckian
theories were based on two common properties ascribed to IAC. IAC was under-
stood both as (1) an inherent property of living systems (“heredity” in general being
13
Lamarckism and epigenetic inheritance: a clarification Page 7 of 17 29
2
Methyl groups (CH3) are added to the bases of the DNA molecule. Usually, hypermethylation prevents
gene transcription.
3
The term “epimutation”, derived from “mutation”, designates a heritable change in gene expression
that does not affect the actual base pair sequence of the DNA molecule.
13
29 Page 8 of 17
L. Loison
viewpoint, these cases differ from genetic inheritance only regarding the stability of
the alternative character. In contrast to classical genetic mutations, epimutations are
easily reversible, even in the lifetime of an individual. That is why “ripening” sec-
tors in tomato fruits that have a wild-type ripening phenotype are regularly observed
in Cnr organisms (Manning et al. 2006, p. 949). For now, only a few cases of epial-
leles have been reported in natural populations (Weigel and Colot 2012), including
the famous peloric variant of Linaria vulgaris whose flowers exhibit radial symme-
try instead of the typical bilateral one (Cubas et al. 1999).
In animals, epigenetic inheritance exists in some taxa (such as nematodes) but
is much harder to demonstrate in higher vertebrates and especially in mammals
where efficient reprogramming occurs in the early embryo and in the germline. As
Heard and Martienssen emphasize, these “two rounds of epigenetic erasure leave
little chance for inheritance of epigenetic marks, whether programmed, accidental,
or environmentally induced” (Heard and Martienssen 2014, p. 95). Nonetheless,
some allegedly groundbreaking results have recently attracted much attention, espe-
cially those obtained by Dias and Ressler (2014). Their work was devoted to the
possible epigenetic inheritance of behavioral conditioning in mice. They subjected
F0 mice (parental generation) to odor fear conditioning before conception, a treat-
ment that affects their neuroanatomy. They found that subsequently conceived and
unconditioned F1 and F2 generations displayed increased behavioral sensitivity to
the F0-conditioned odor and that their neuroanatomy was also altered in the same
direction as F0s. This pattern of inheritance seems to be decoupled from both paren-
tal effect (i.e. learning) and genetic variation. It was shown instead that a specific
olfactory gene (Olfr 151) was hypomethylated in the sperm of F0 and F1 males.
Dias and Ressler interpreted their own results in an adaptive and evolutionary per-
spective, concluding their article by arguing that what seems to be an experimentally
grounded case shows “how generations can inherit information about the salience of
specific stimuli in ancestral environments so that their behavior and neuroanatomy
are altered to allow for appropriate stimulus-specific responses” (Dias and Ressler
2014, p. 95). Their results immediately gave rise to explicit Lamarckian stances
(Szyf 2014).
Such enthusiastic interpretations need to be viewed sceptically. This kind of work
suffers from at least three serious limitations. The first is its statistical weakness. As
shown by Francis, samples sizes are far too low to avoid severe biases that explain
why published results show “too much success” (Francis 2014). The second con-
cerns the possible mechanism that would allow such an inheritance to occur. The
criticism here is essentially the same that Weismann put forth more than a century
ago: how could we conceive that a tissue-localized modification retroacts (other-
wise it would only be parallel induction) on the germ line in producing epigenetic
marks that must later be themselves able to causally produce, through ontogenesis
and several mitotic cycles, a neuroanatomical and behavioral phenotype equivalent
to the one initially induced? Similar criticisms have been made even by biologists
in favour of these series of experiments (Szyf 2014, p. 3). The third limitation is
related to the so-called transgenerational dimension of this case of epigenetic inher-
itance. The behavioral pattern induced in F0 is inherited only in F1 and F2, i.e. for
two generations. If the authors are right when they claim that the F2 mice “are full
13
Lamarckism and epigenetic inheritance: a clarification Page 9 of 17 29
and complete generation removed from the environmental perturbation” (Dias and
Ressler 2014, p. 94), the fact remains that such a weak intergenerational inheritance
could hardly be termed “transgenerational”.
While recent findings in epigenetics support the reality of this mode of biologi-
cal inheritance in multicellular organisms, we must note that highly different cases
are reported in the scientific literature. On the one hand, robust results are available
in various taxa (mostly plants, nematodes and insects) where it is shown that epige-
netic inheritance could sometimes mimic genetic inheritance in a less stable fashion.
But these cases show no clear evidence of a possible causal role of the environment
in the production of epigenetic marks and, above all, variations are not intrinsically
adaptive; on the contrary, they are random regarding the issue of adaptation (see
“Epigenetic inheritance as a self-sufficient evolutionary cause?” section for a more
detailed discussion). On the other hand, a handful of cases of adaptive epigenetic
inheritance have been experimentally explored in multicellular organisms, but they
remain to be ascertained and show a very weak form of biological inheritance, last-
ing only two generations at best.
13
29 Page 10 of 17
L. Loison
This rules out conclusively the possibility that this type of IAC might have been
primitive (i.e. efficient since the very beginning of life). IAC has to be explained by
natural selection and cannot be taken for granted. This settles an irreducible epis-
temological difference regarding the explanandum of IAC between current knowl-
edge and what standard Lamarckism was in the history of science. In other words,
because IAC can no longer be conceived as an inherent property of living systems,
Lamarckism is definitely not back.
Moreover, this difference regarding the explanandum also has a direct and obliga-
tory consequence on the explanans because it prevents IAC from working as a valid
explanation of the first stages of organic evolution. If real, the possible Lamarckian
dimension of evolution—as was rightly noted by Koonin and Wolf—could only be
emergent in the history of life. This point reinforces the demarcation between the
standard Lamarckian understanding of IAC and epigenetic inheritance.
13
Lamarckism and epigenetic inheritance: a clarification Page 11 of 17 29
it must be noted here that one cannot find statements as explicit as those quoted
above in Evolution in Four Dimensions). Again, Jablonka and Lamb are interested
in IAC as emergent causal processes in organic evolution, without denying their
Darwinian origin. While the origin criterion is pertinent to draw an epistemologi-
cal line between the traditional Lamarckian concept of IAC and transgenerational
epigenetic inheritance (cf. “Epigenetic inheritance as a necessary evolved feature
of organisms” section), this criterion is irrelevant to tackle the issue of the causal
role of epigenetic inheritance in subsequent evolution.
My interest here is not in discussing the evolutionary scope of epigenetic
inheritance in general (i.e. the possible insufficiency of the Modern Synthesis),
but only in examining whether this role can rigorously be said to be responsible
for an emergent Lamarckian evolution.
As we have seen in “Classical Lamarckian accounts of IAC” section, the
Lamarckian concept of IAC requires IAC to be a self-sufficient evolutionary
cause, by itself able to causally produce adaptive trajectories at the phyletic
level. To be consistently labeled “Lamarckian”, epigenetic mechanisms must be
endowed with such evolutionary consequences. This requirement was to some
extent heeded by some supporters of the Lamarckian account when they endorsed
the view that transgenerational epigenetic inheritance has become a self-suffi-
cient evolutionary cause. At least on a few occasions, they have proposed that
epigenetic mechanisms are now powerful enough to potentially drive evolution
by themselves, without the need for the genetic hereditary system to be involved
and even—at least sometimes—natural selection. For instance, in Evolution in
Four Dimensions, Jablonka and Lamb devote several pages to a thought exper-
iment: a case of true evolution solely based on epigenetic inheritance and that
would have occurred on planet Jaynus (Jablonka and Lamb 2014, pp. 112–117).
They postulate that all living beings on Jaynus, which exhibit very different mor-
phologies, have exactly the same DNA sequences. Hence, the entire evolution-
ary process has only been grounded on non-genetic variations. On this point, the
authors seem to move back and forth between two rather different explanations.
First, they present evolution on Jaynus in Darwinian terms, i.e. stable hereditary
variations adaptively accumulated through natural selection. The only difference
with classical Darwinism is that these variations are conceived as epigenetic, not
genetic. Nonetheless, they are stable enough that “natural selection led to [their]
accumulation” (Jablonka and Lamb 2014, p. 114). This is exactly what could hap-
pened if selection is applied to epialleles described above in “Two possible cases
of transgenerational epigenetic inheritance in multicellular organisms” section.
This is of course pure Darwinism.
But Jablonka and Lamb also suggest a substantially different picture when they
write “that the role of directed or interpretive variation had been much larger on
Jaynus than on Earth” (Jablonka and Lamb 2014, p. 114). This seems to indicate
that they endorse the possibility of a somewhat emergent evolution, decoupled both
from genetic variation but also, at least to some extent, natural selection. In such
presentations, IAC is conceived as a self-sufficient evolutionary cause which is the
only theoretical positioning consistent with the explanans of traditional Lamarckian
theories.
13
29 Page 12 of 17
L. Loison
Thus, we now have to consider the conditions that epigenetic variation must
fulfill to be able to autonomously drive adaptive evolution. Some of these—espe-
cially the first three (see below)—have already been mentioned, but without much
explanation and clarification (see for example Charlesworth et al. 2017; Deichmann
2016b, p. 253). My aim is to render them completely explicit in order to discuss
their plausibility in light of current scientific knowledge. My claim is that IAC could
be a self-sufficient evolutionary cause if and only if the individual (now epigenetic)
variation is: (a) adaptive, (b) hereditarily stable, (c) frequent and (d) open-ended.
Only under these four conditions would IAC be able to causally produce adaptive
evolution. Altogether, these conditions are the theoretical requirements for the pos-
sibility of an emergent Lamarckian evolution.
13
Lamarckism and epigenetic inheritance: a clarification Page 13 of 17 29
vidual variations must also consist, at least to some extent, in starting points of
true evolutionary innovations.
If this argument is valid, the next question is: given current knowledge about
transgenerational epigenetic inheritance, are these four requirements fulfilled? The
answer to this question, I insist, is dependent on the scientific knowledge available,
and in the end must be decided by scientists themselves. Yet, given what is known
today about transgenerational epigenetic inheritance, the answer seems to be nega-
tive. This might be the case at least for the first two properties, adaptiveness and
hereditary stability. Regarding adaptiveness in particular, crucially, it remains dif-
ficult to find even a single piece of evidence of ascertained hereditary meiotic trans-
mission of adaptive epigenetic variation in the literature (Charlesworth et al. 2017;
Deichmann 2016b, p. 253; Heard and Martienssen 2014, p. 105), as supporters of
the so-called Lamarckian account themselves acknowledge (Jablonka and Lamb
2014, p. 151; Wang et al. 2017, p. 23). The issue of the hereditary stability of epige-
netic variation also seems settled: compared to the stability of genetic variation, it is
considerably lower. At best, these variations could be passed on through only a very
small number of meiotic events (Charlesworth et al. 2017; Heard and Martienssen
2014). As we have seen for the epiallele responsible for the Cnr phenotype (“Two
possible cases of transgenerational epigenetic inheritance in multicellular organ-
isms” section), reversion is frequent in natural conditions. The frequency of the Cnr
phenotype in tomato populations (the same is true for the peloric phenotype of Lin-
aria) is thus not so much the consequence of its faithful hereditary transmission as
of the intrinsic epimutability of its DNA locus, for reasons so far unknown.
The issue of the frequency of these forms of hereditary transmission in natural
conditions is still under discussion. As indicated in “Two possible cases of transgen-
erational epigenetic inheritance in multicellular organisms” section., an emerging
consensus is that it probably depends on the kind of organism biologists are inter-
ested in: transgenerational epigenetic inheritance might be relatively frequent in
groups like plants and especially unicellular organisms but much rarer in higher
vertebrates where efficient reprogramming systems have been selected (Heard and
Martienssen 2014; Whitelaw 2015). Nonetheless, in comparison to allelic variation,
epiallelic variation is very rare in nature and seems to concern only a few epimuta-
ble genes in the whole genome (Quadrana and Colot 2016, p. 469).
The last requirement—the open-endedness of the variation—is also still to
be decided. While it seems indisputable that the informational density of DNA is
greater by many orders of magnitude than that of epigenetic mechanisms (Haig
2007, p. 422), the storage possibilities of these hereditary systems might nonetheless
be sufficient to allow for substantial exploration of the evolutionary space. Here the
work performed by Colot’s group at the ENS in Paris might be useful. In the labora-
tory, they managed to create inbred lines of the plant Arabidopsis thaliana that are
genetically equivalent and differ only regarding their methylome (Roux et al. 2011).
These “epiRILs” (epigenetic recombinant inbred lines) show phenotypic diversity
that could be hereditarily transmitted for at least eight generations (Quadrana and
Colot 2016, p. 475). Nonetheless, the phenotypic variation observed remains “of
smaller amplitude than that found in classical RILs” (Quadrana and Colot 2016, p.
13
29 Page 14 of 17
L. Loison
480), suggesting that the phenotypic range of epigenetic variation is not comparable
to that of classical genetic variation.
From these considerations, it follows that typical epigenetic hereditary systems
like mechanisms of DNA methylation, histone modifications or of RNA interference
are not self-sufficient evolutionary causes in the sense defined in the present article,
i.e. that they cannot be responsible for an emergent Lamarckian evolution. The use
of Lamarckian terms, already debatable regarding the explanandum of IAC, is thus
also unjustified on the grounds of the characterization of the explanans of epigenetic
inheritance systems.
Conclusion
In this article, I have presented two main arguments against the so-called Lamarck-
ian interpretation of transgenerational epigenetic processes. The first argument is
based on the analysis of IAC as an explanandum. Whereas in traditional Lamarckian
theories IAC was thought as the consequence of physical or vital forces acting at
the level of living matter, nowadays biologists unambiguously understand epigenetic
mechanisms as evolved molecular systems built by natural selection. This means
that IAC is no longer seen as an intrinsic property of living things and therefore that
it is now definitely impossible to think of Lamarckism as a general theory of organic
evolution able to explain the entire evolutionary process (as was the case around
1900, during the golden age of Lamarckism).
The second argument is based on the analysis of IAC as an explanans. Regardless
of the origin of the mechanisms of transgenerational epigenetic inheritance, support-
ers of the Lamarckian account are primarily interested in their evolutionary scope.
I have shown that, according to the history of science, IAC must then be a self-
sufficient evolutionary cause producing unlimited change. Given current knowledge,
transgenerational epigenetic mechanisms are not self-sufficient evolutionary causes
because variation is not at the same time (a) adaptive, (b) hereditarily stable, (c) fre-
quent and (d) open-ended. This implies that epigenetic mechanisms are not respon-
sible for an emergent Lamarckian evolution either.
Thus, from the perspectives of both the explanandum and the explanans of IAC,
I contest the validity and accuracy of the Lamarckian discourse that has been flour-
ishing since the 1990s in connection with the emergence of the field of epigenetic
inheritance. Not only are these claims inaccurate, but they might also be counter-
productive. Constantly bringing Lamarckism and Lamarck back in modern biol-
ogy considerably blurs what is really at stake in epigenetic inheritance. However
one defines it precisely, epigenetics brings to light interesting unknown processes
about gene regulation that might enrich our modern concept of biological heredity.
To label them in Lamarckian terms unnecessarily exacerbates the debates regarding
their scope. Because of that, discussions are too often reduced to an over-simplis-
tic alternative: whether epigenetic inheritance vindicates Lamarckism or the Mod-
ern Synthesis remains unchanged (see for example Charlesworth et al. 2017, p. 7).
This alternative is neither grounded nor useful. Arguing that epigenetic inheritance
should not be seen as a revival of Lamarckism is not tantamount to claiming that this
13
Lamarckism and epigenetic inheritance: a clarification Page 15 of 17 29
form of inheritance could have no impact on the structure of the Modern Synthesis.
For example, the possible links between epigenetic inheritance and the efficiency of
the Baldwin effect or genetic assimilation are indeed stimulating prospects, which
might expand our conception of the evolutionary causality involved in micro-evolu-
tionary processes (for a recent example, see Fanti et al. 2017; see also Wilkins 2011,
p. 392). In other words, the fact that the Lamarckian concept of IAC is not back does
not mean that other concepts of IAC, like Waddington’s or Schmalhausen’s, could
not, given current knowledge about epigenetic inheritance, represent genuine and
stimulating challenges for the standard Modern Synthesis gene-centered view (Fab-
ris 2018; Loison 2018).
Acknowledgements Some of the ideas presented here were first discussed on October 2014 at the IHPST
(Paris-1/CNRS) in Paris during the international workshop “How can we redefine inheritance beyond
the gene-centered approach?”. I would like to thank Francesca Merlin and Gaëlle Pontarotti for their
invitation and all the workshop participants for their insightful questions and comments. I would like also
to thank Vincent Colot, Michel Morange, and Adam S. Wilkins for their helpful remarks on successive
versions of this paper. During the last stages, my argument benefited from exchanges within other mem-
bers of an informal discussion group on the boundaries of the concept of biological heredity: Guillaume
Achaz, Francesca Merlin, Gaëlle Pontarotti and Livio Riboli-Sasco. I am also deeply in debt to the anon-
ymous reviewers (especially “Reviewer 3”) and Maureen O’Malley, who patiently helped me to improve
the present article. Last but not least, the final version was edited by Jean-Yves Bart.
References
Bowler P (1992) The eclipse of Darwinism. The Johns Hopkins University Press, Baltimore
Burkhardt RW (1977) The spirit of system: Lamarck and evolutionary biology. Harvard University Press,
Cambridge
Burkhardt RW (2013) Lamarck, evolution, and the inheritance of acquired characters. Genetics
194(4):793–800
Charlesworth D, Barton NH, Charlesworth B (2017) The sources of adaptive variation. Proc R Soc B
284:20162864
Cope ED (1896) The primary factors of organic evolution. The Open Court Publishing Company,
Chicago
Corsi P (1988) The age of Lamarck, evolutionary theories in France, 1790–1830. University of California
Press, Berkeley
Corsi P (2011) Jean-Baptiste Lamarck: from myth to history. In: Gissis SB, Jablonka E (eds) Transforma-
tions of Lamarckism, from subtle fluids to molecular biology. MIT Press, Cambridge, pp 77–102
Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral
symmetry. Nature 401(6749):157–161
Darwin C (1859) On the origin of species by means of natural selection, or the preservation of favoured
races in the struggle for life. John Murray, London
Darwin C (1868) The variation of animals and plants under domestication. John Murray, London
Deans C, Maggert K (2015) What do you mean, “epigenetic”? Genetics 199(4):887–896
Deichmann U (2016a) Why epigenetics is not a vindication of Lamarckism—and why that matters. Stud
Hist Philos Biol Biomed Sci 57:80–82
Deichmann U (2016b) Epigenetics: the origins and evolution of a fashionable topic. Dev Biol
416(1):249–254
Di Gregorio MA (2005) From here to eternity. Ernst Haeckel and Scientific Faith. Vandenhoeck &
Ruprecht, Göttingen
Dias BG, Ressler KJ (2014) Parental olfactory experience influences behavior and neural structure in
subsequent generations. Nat Neurosci 17(1):89–96
Dickins TE, Rahman Q (2012) The extended evolutionary synthesis and the role of soft inheritance in
evolution. Proc R Soc B 279:2913–2921
13
29 Page 16 of 17
L. Loison
Fabris F (2018) Waddington’s processual epigenetics and the debate over cryptic variability. In: Nichol-
son DJ, Dupré J (eds) Everything flows, towards a processual philosophy of biology. Oxford Univer-
sity Press, Oxford, pp 246–263
Fanti L, Piacentini L, Cappucci U, Casale AM, Pimpinelli S (2017) Canalization by selection of De
Novo-induced mutations. Genetics 206(4):1995–2006
Felsenfeld G (2014) The evolution of epigenetics. Perspect Biol Med 57(1):132–148
Francis G (2014) Too much success for recent groundbreaking epigenetic experiments. Genetics
198(2):449–451
Gayon J (2006) Hérédité des caractères acquis. In: Corsi P, Gayon J, Gohau G, Tirard S (eds) Lamarck,
Philosophe de la nature. PUF, Paris, pp 105–163
Gissis SB, Jablonka E (eds) (2011) Transformations of Lamarckism, from subtle fluids to molecular biol-
ogy. MIT Press, Cambridge
Gliboff S (2011) The golden age of Lamarckism, 1866–1926. In: Gissis SB, Jablonka E (eds) Transfor-
mations of Lamarckism, from subtle fluids to molecular biology. MIT Press, Cambridge, pp 45–55
Haeckel E (1876) Die Perigenesis der Plastidule oder die Wellenerzugung der Lebenstheilchen. Reimer,
Berlin
Haig D (2007) Weismann rules! Ok? Epigenetics and the Lamarckian temptation. Biol Philos
22(3):415–428
Heard E, Martienssen RA (2014) Transgenerational epigenetic inheritance: myths and mechanisms. Cell
157(1):95–109
Henikoff S (2005) Histone modifications: combinatorial complexity or cumulative simplicity? Proc Natl
Acad Sci USA 102(15):5308–5309
Jablonka E, Lamb MJ (1999) Epigenetic inheritance and evolution. The Lamarckian dimension, 2nd edn.
Oxford University Press, Oxford
Jablonka E, Lamb MJ (2014) Evolution in four dimensions, 2nd edn. MIT Press, Cambridge
Koonin EV (2014) Calorie Restriction à Lamarck. Cell 158(2):237–238
Koonin EV, Wolf YI (2009) Is evolution Darwinian or/and Lamarckian? Biol Direct. https://doi.
org/10.1186/1745-6150-4-42
Lamarck JBM (1801) Système des animaux sans vertèbres. Déterville, Paris
Lamarck JBM (1802) Recherches sur l’organisation des corps vivans. Maillard, Paris
Lamarck JBM (1809) Philosophie zoologique. Dentu, Paris
Le Dantec F (1907) Eléments de Philosophie biologique. Alcan, Paris
Loison L (2011) French roots of French neo-Lamarckisms, 1879–1985. J Hist Biol 44(4):713–744
Loison L (2018) Canalization and genetic assimilation: reassessing the radicality of the Waddingtonian
concept of inheritance of acquired characters. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcd
b.2018.05.009
Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB (2006) A
naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits
tomato fruit ripening. Nat Genet 38(8):948–952
Mayr E (1961) Cause and effect in biology. Science 134(3489):1501–1506
Nutting CC (1892) What is an “acquired character?”. Am Nat 26(312):1009–1013
Pfeifer E (1965) The genesis of American Neo-Lamarckism. Isis 56(2):156–167
Probst AV, Dunleavy E, Almouzni G (2009) Epigenetic inheritance during the cell cycle. Nat Rev Mol
Cell Biol 10(3):192–206
Ptashne M (2013) Epigenetics: core misconcept. Proc Natl Acad Sci USA 110(18):7101–7103
Quadrana L, Colot V (2016) Plant transgenerational epigenetics. Annu Rev Genet 50:467–491
Riggs AD, Russo VEA, Martienssen RA (1996) Epigenetic mechanisms of gene regulation. Cold Spring
Harbor Laboratory Press, Plainview
Roux F, Colomé-Tatché M, Edelist C, Wardenaar R, Guerche P, Hospital F, Colot V, Jansen RC, Johannes
F (2011) Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in
nature. Genetics 188(4):1015–1017
Skinner MR (2015) Environmental epigenetics and a unified theory of the molecular aspects of evolu-
tion: a Neo-Lamarckian concept that facilitates Neo-Darwinian evolution. Genome Biol Evolut
7(5):1296–1302
Szyf M (2014) Lamarck revisited: epigenetic inheritance of ancestral odor fear conditioning. Nat Neuro-
sci 17(1):2–4
Varmuza S (2003) Epigenetics and the renaissance of heresy. Genome 46(6):963–967
13
Lamarckism and epigenetic inheritance: a clarification Page 17 of 17 29
Wang Y, Liu H, Sun Z (2017) Lamarck rises from his grave: parental environment-induced epigenetic
inheritance in model organisms and humans. Biol Rev. https://doi.org/10.1111/brv.12322
Weider LJ, Pijanowska J (1993) Plasticity of Daphnia life histories in response to chemical cues from
predators. Oikos 67(3):385–392
Weigel D, Colot V (2012) Epialleles in plant evolution. Genome Biol 13:249. https://doi.org/10.1186/
gb-2012-13-10-249
Whitelaw E (2015) Disputing Lamarckian epigenetic inheritance in mammals. Genome Biol 16:60. https
://doi.org/10.1186/s13059-015-0626-0
Wilkins A (2011) Epigenetic inheritance: where does the field stand today? What do we still need to
know? In: Gissis SB, Jablonka E (eds) Transformations of Lamarckism, from subtle fluids to molec-
ular biology. MIT Press, Cambridge, pp 389–393
13