Forum
Has Darwin’s Pangenesis Been
Rediscovered?
YONGSHENG LIU AND XIUJU LI
In order to strengthen his theory of evolution and explain a considerable variety of biological phenomena pertaining to inheritance, variation,
and development, Charles Darwin formulated his hypothesis of Pangenesis with its hereditary molecules, termed gemmules, that are thrown
off by all cells of the body and assemble in the reproductive cells. Darwin’s Pangenesis has been largely thought to be wrong, owing to a lack of
evidence supporting his hypothetical gemmules and a refusal to accept some phenomena that Pangenesis supposedly explains. Now the discovery
of circulating nucleic acids (including small RNAs) and prions provide striking evidence in favor of the chemical existence of gemmules. There
is also a considerable body of experimental evidence for the inheritance of acquired characteristics, graft hybridization, and other “doubtful”
phenomena. The rediscovery of Darwin’s Pangenesis, if and when it is admitted, would, like the rediscovery of Mendel’s work, have a tremendous
impact on genetics, evolution, cell biology, and the history of science.
Keywords: Darwin’s Pangenesis, genetics and evolution, circulating nucleic acids, inheritance of acquired characteristics, graft hybridization
T
he word genetics was coined by William Bateson, a leading exponent of Mendelism. As he grew older, however, he became more and more convinced that an increasing
number of cases of inheritance could not be brought under
the Mendelian laws at all (MacBride 1937). He regarded
Darwin as a pioneer of genetics, because “Darwin made a
more significant and imperishable contribution” (p. 88). (In
this article, our use of Darwin corresponds to Charles, not
Francis, Darwin.) “Not for a few generations, but through
all ages, he should be remembered as the first who showed
clearly that the problems of heredity and variation are
soluble by observation, and laid down the course by which
we must proceed to their solution. Evolution is a process of
variation and heredity. The older writers, though they had
some vague idea that it must be so, did not study variation
and heredity. Darwin did, and so begat not a theory, but a
science” (Bateson 1910, p. 88).
Darwin regarded his (1859) book, On the Origin of
Species as an abstract that contains no molecular basis of the
heritable variations on which natural selection operated. He
fully realized that his theory of evolution must be based on
a sounding understanding of the mechanism of inheritance
and variation. Darwin’s (1868) two-volume work was not
only an attempt to strengthen his theory of natural selection but, more importantly, an attempt to describe the root
cause of variation, because variation is the fountainhead of
evolution. His main contribution was the collection of a tremendous amount of data on inheritance and variation and
an attempt to provide a mechanistic explanation.
Darwin’s Pangenesis as a developmental theory of
heredity
In order to provide a mechanistic explanation for inheritance, variation, and development, Darwin formulated
his Pangenesis hypothesis by postulating the existence of
numerous and minute hereditary molecules, termed gemmules, which were supposed to be thrown off by all cells
of the body, to multiply by self-replication, to be dispersed
through tissues or from cell to cell, to be incorporated into
the reproductive cells, and to be transmitted from parents to
offspring. The essential assumption of Pangenesis is the existence of gemmules and their production by cells, although
Darwin modified the secondary assumption in his late years.
For example, Darwin claimed that he had “never supposed
that gemmules were developed into free cells but that they
penetrated other nascent cells and modified their subsequent development” (Darwin F and Seward 1903, p. 310).
According to Darwin’s Pangenesis, the appearance of the
same characters in a parent and its offspring was made possible by the production of gemmules by all cells of the parent’s body. Cases in which one parent’s specific characters
dominate are due to that parent’s gemmules’ having some
advantage in number, affinity, or vigor over those derived
from the other parent. Thus Pangenesis explains the prepotency associated with Mendelian inheritance (or dominance
inheritance) and Yarrell’s law (which states that, in some
crosses, a parent of an older breed will have more influence
on the character of the offspring than a parent of a younger
breed). If the cells and tissues of the body are modified by
BioScience 64: 1037–1041. © The Author(s) 2014. Published by Oxford University Press on behalf of the American Institute of Biological Sciences. All rights
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doi:10.1093/biosci/biu151
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changes in the environment or by the effects of use and
disuse, they would throw off modified gemmules, which are
transmitted with their acquired traits to the offspring, and,
in this manner, it explains the inheritance of acquired characteristics, or Lamarckian inheritance. Gemmules released
from the stock would be transferred into the scion and
incorporated into buds and reproductive cells, which would
result in heritable changes of the scion and their progenies; thus gemmules provide a mechanistic explanation for
graft hybridization, the subject that later appeared in the
textbook of Michurinian genetics. Reversion is due to the
long-dormant ancestral gemmules’ becoming active after
the transmission of many generations. The regeneration of
lost parts is possible because a reserve of gemmules in the
cells and tissues of rest of the body served for regeneration
in case parts are lost. Gemmules derived from foreign pollen
penetrate the nascent cells of the mother plant and result in
xenia, the effect of foreign pollen on fruits and seeds.
Telegony is a subject of heated scientific controversy. It
means that a previous mating may have an influence on a
female’s offspring by a subsequent mating. According to
Darwin’s Pangenesis, telegony was “intelligible through the
diffusion, retention, and action of the gemmules included
within the spermatozoa of the previous male” (Darwin 1868,
p. 388). In order to explain development, Darwin supposed
that differentiation was a function of the gemmules: “The
organic units, during each stage of development throw off
gemmules, which, multiplying, are transmitted to the offspring. In the offspring, as soon as any particular cell or
unit in the proper order of development becomes partially
developed, it unites with (or, to speak metaphorically, is
fertilized by) the gemmules of the next succeeding cell, and
so onwards” (Darwin 1868, p. 465). Through his Pangenesis,
Darwin tried to account for a considerable variety of biological phenomena and to unite them under a common theory.
Why was Darwin’s Pangenesis considered to be a
great blunder?
Darwin’s Pangenesis is of great importance because of its
inspiring influence on all subsequent theories of heredity,
particularly those of Francis Galton, August Weismann, and
Hugo de Vries. The word gene, coined by Wilhelm Johanssen,
was derived from de Vries’s term pangen, itself a substitute
for the gemmule of Pangenesis. Unfortunately, Darwin’s
Pangenesis has long been excluded from the discipline of
genetics, mainly because of a lack of evidence supporting his
hypothetical gemmules and a refusal to accept some phenomena that Pangenesis supposedly explains.
In scientific research, when we obtain an experimental result
that contradicts a hypothesis, we usually accept the experimental result and abandon the hypothesis, even if the hypothesis
is proposed by a great scientist. In attempts to test Darwin’s
Pangenesis, Galton transfused the blood of one variety of rabbit into the veins of both sexes of another variety and then bred
together the latter. If there are gemmules in the blood, the germ
cells of the recipient rabbits might show the influence of the
1038 BioScience • November 2014 / Vol. 64 No. 11
donor variety. The results of breeding showed no variations of
character in the offspring. From this, Galton (1871) concluded
that there were no gemmules circulating in the blood and that
Pangenesis was incorrect. In addition, Darwin’s Pangenesis
was also severely criticized by many other scientists. It was the
opinion of Beale (1871) that Darwin’s Pangenesis was based
on “the fictions of the fancy.” Now Darwin’s Pangenesis is
regarded as a brilliant blunder (Livio 2013).
Another problem has been that Darwin’s Pangenesis
explains the inheritance of acquired characteristics. In
Thomas Hunt Morgan’s (1926) words, Darwin’s Pangenesis
“was proposed primarily to explain how acquired characteristics are transmitted. If specific changes in the body of the
parent are transmitted to the offspring, some such theory
is required. If the changes in the body are not transmitted,
there is no need of such a theory” (p. 29). Since the earliest
days of evolutionary thought, the subject of the inheritance of acquired characteristics has been a central debate.
Lamarck, Darwin, and several of the greatest figures in
biology accepted it as an established fact, but many geneticists refused to accept its reality. A well-known example
is Weismann’s intent in docking the tails of mice to reject
the inheritance of acquired characters, and his doctrine of
the continuity of the germ plasm as opposed to Darwin’s
Pangenesis (Romanes 1893, Weismann 1904). This situation had persisted into the twentieth century, accompanied
by two unfortunate episodes (Fine 1979). The first was the
apparent falsification, by Kammerer, of evidence purporting
to demonstrate that the acquired pigmented thumb pads
of midwife toads could be inherited (McLaren 1999). The
second was the heated scientific controversy led by Trofim
Denisovich Lysenko, who regarded Mendelian genetics as
“bourgeois science” and “psedoscience,” and forced Soviet
geneticists to accept Lamarckian ideas. It should be noted
that among 30 of the most widely used college textbooks of
genetics during 1960s and 1980s, none indicated that actual
examples of inheritance of acquired characters had been
found (Landman 1991).
Darwin was the first to put forward the concept of graft
hybridization and considered this phenomenon as striking
evidence in favor of his Pangenesis. In attempts to prove this
fact, George Romans devoted an immense amount of time
to patient experimentation, but his grafting experiments
yielded, for the most part, negative results (Schafer 1896).
In 1950s, there were about 500 papers on graft hybridization published in the Soviet Union. But these were largely
thought to be fraudulent results, and Lysenko, a keen supporter of it, was regarded as a fraud (Hagemann 2002). With
regard to the case of telegony, it was dismissed as “another
breeder’s myth” (Morgan 1907) and was offered to the student as objects of ridicule.
Striking evidence for the chemical existence of
Darwin’s hypothetical gemmules
“History may be circular, but the history of science is helical: It
repeats itself, but each time at a deeper level” (McLaren 1999).
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As was stated above, Galton failed to induce heritable
changes in his blood transfusion experiment. In the early
1950s, however, Sopikov demonstrated that repeated injections of the blood of Australorp roosters (black feathers)
into white leghorn hens and the subsequent mating of these
hens with roosters of the same breed (white leghorn) yielded
progeny of a modified inheritance (Sopikov 1954). His work
has been followed by a long series of confirmatory reports in
domestic poultry (Liu 2008). It is worth noting that Sopikov’s
(1954) procedure involved long-term intravenous or intraperitoneal injections of whole blood (accumulate dosage of
approximately 150–400 milliliters) at a frequency of twice
per week in the course of a 3–6-month injection period,
which was different from Galton’s blood transfusion method.
During the 1950s and the 1970s, there was a considerable
body of experimental evidence for genetic changes induced
by blood transfusion. Among the 50 reports we collected,
45 indicated positive results, and only 5 indicated negative
results (Liu 2008).
Does the blood carry Darwin’s supposed gemmules?
Mandel and Metais (1948) described the presence of cellfree nucleic acids in human blood, providing direct evidence
for the chemical existence of Darwin’s hypothetical gemmules. Lo and colleagues (1997) demonstrated that fetal
DNA was present in peripheral maternal blood, shedding
new light on telegony (Liu 2011). Over the past several
decades, a growing body of evidence has accumulated indicating that nucleic acids are released and circulate in the
blood, either because of apoptosis or necrosis or because of
a new mechanism of active release (Gahan 2013). In plants,
nucleic acids were first detected in the phloem translocation stream in the 1960s. Later application of heterografting
and molecular techniques provided compelling evidence
that RNA molecules are not only transported through the
vascular system but that they also travel between plant cells
(Xoconostle-Cazarers et al. 1999, Liu 2004).
Darwin (1875) imagined that gemmules were “inconceivably minute and numerous as the stars in heaven” and
that “many thousand gemmules must be thrown off from
the various parts of the body at each stage of development”
(p. 399). Today, we know that small RNAs, particularly
microRNAs, can be secreted from mammalian cells and
circulate in blood and other body fluids. They are also
capable of moving between plant cells and through the
vasculature and play important roles in gene regulation,
diverse cellular and developmental processes (Chitwood and
Timmermans 2010). In recent years, thousands of different
RNAs have been identified in mammalian sperm, which
supports Darwin’s idea that “almost infinitely numerous and
minute gemmules are contained within each bud, ovule,
spermatozoon, and pollen grain” (Darwin 1875, p. 397).
Most recently, Gapp and colleagues (2014) demonstrated
that stress in early life alters the production of microRNAs in
the sperm of mice, which results in depressive behaviors in
subsequent generations. Szyf (2014) proposed that microRNAs derived from the brains of mice that had undergone
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stressful experiences could make their way into the reproductive organ through the circulatory system and could then
target the specific gene in sperm. Obviously, this proposal is
consistent with Darwin’s Pangenesis.
According to Darwin’s Pangenesis, a reserve of gemmules
in the cells and tissues of the rest of the body serves in
regeneration in case parts are lost. For example, if the leg of a
salamander has been removed, the leg gemmules, which are
present in the body, can migrate to the cut surface, unite with
the cells of the cut surface and develop into a new limb, identical to the old one. Interestingly, microRNAs have recently
been shown to have a large impact on regeneration. For
example, Jayawardena and colleagues (2012) showed that the
transdifferentiation of neonatal and adult cardiac fibroblasts
to cardiomyocytes could be achieved by using a combination of microRNAs (miR1, miR-133, miR-208, and miR-499)
and a chemical Janus kinase inhibitor. They further demonstrated that miR-1 alone was sufficient to induce the cardiac
phenotype. Later, Eulalio and colleagues (2012) performed
a large-scale screen for microRNAs that could specifically
enhance the proliferation of neonatal rodent cardiomyocytes
in vitro, and they identified 204 microRNAs that could independently trigger cardiomyocyte mitosis. Several of these
microRNAs increased cardiomyocyte proliferation not only
in adult cells in cell culture but also in vivo when they were
injected into the heart or expressed by means of viral vectors
in mice. Furthermore, they showed that forced independent
expression of two microRNAs resulted in robust cardiomyocyte regeneration and an improvement of cardiac function
in a mouse model of cardiac ischemia. These findings are
notable because they not only show that microRNAs can
modulate cell regeneration in the heart, which may lead to
promising new therapies, but also provide striking evidence
in favor of Darwinian’s Pangenesis.
In a host of neurodegenerative diseases, specific proteins
misfold and aggregate into seeds that structurally alter similar
proteins, causing them, in turn, to aggregate and form pathogenic assemblies (Jucker and Walker 2013). These proteinaceous seeds, generically known as prions, are also reminiscent
of Darwin’s gemmules. Now we know that the self-propagating
prions are released by cells and have been detected in the
blood (Saa et al. 2006). They are also able to transmit prion
disease through blood transfusion (Houston et al. 2000).
Further evidence for the “doubtful” phenomena that
Pangenesis supposedly explains
Throughout his career, Darwin consistently attributed the
causes of hereditary variation to changes in the environment
(Darwin 1881). He clearly stated, “There can be no doubt
that the evil effects of the long-continued exposure of the
parent to injurious conditions are sometimes transmitted to
the offspring” (Darwin 1875, p. 57). In a letter to Nature, he
claimed that many special fears in animals, which might be
acquired through habit and the utility in, for example, predator avoidance, could be strictly inherited (Darwin 1873).
His claim has now been confirmed by Dias and Ressler (2014),
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who examined the inheritance of parental traumatic exposure and showed that an olfactory experience could be
passed onto the progeny.
The great Russian physiologist, Ivan Pavlov, accepted the
possibility of the inheritance of acquired habit and believed
that some of the conditioned newly formed reflexes eventually became transformed into unconditioned ones through
heredity. Later, he reported the results of his experiments,
showing that the conditioned reflexes—that is, the highest
nervous activity—were inherited (Pavlov 1923). McDougall
(1938) demonstrated that, when rats were forced by unpleasant experience to acquire a habit, they gave birth to offspring
that acquired the habit more readily than did their parents.
There are many examples, now often included under
the blanket term transgenerational epigenetic inheritance,
of altered environmental conditions’ resulting in heritable
changes in gene expression that occur without a change in
DNA sequence (McLaren 1999, Anway et al. 2005, Jablonka
and Raz 2009). However, one cannot easily distinguish whether
a phenotype is due to genetic or epigenetic variation without
a detailed molecular analysis (Grossniklaus et al. 2013).
Other possible mechanisms include prion inheritance, RNAmediated inheritance, and horizontal gene transfer (Landman
1991, Steele et al. 1998, Liu 2004, 2007), which seems to be
consistent with Darwin’s Pangenesis. For example, prion diseases can be classified as sporadic, inherited, or acquired. The
acquired forms are caused by the transmission of infection
between different individuals or species. The introduction of
an infectious prion molecule into different individuals or species could result in the formation of new prions in the second
individual or species, in which the normal protein acquires
altered conformational characteristics. Therefore, the propagation of prion molecules in different hosts can be regarded
as evidence of the inheritance of acquired characteristics
(Edmunds and Yool 1997, Halfmann and Lindquist 2010).
Although there has been a refusal to accept the concept
of graft hybridization, the existence of graft hybrids has now
been confirmed by several independent groups of scientists.
For example, Shinoto, the former president of the Genetics
Society of Japan, successfully obtained graft hybrids of eggplants (Shinoto 1955). Lindegren (1966) regarded Shinoto’s
(1955) result as an adequate confirmation of graft hybridization by an unbiased experimenter of great skill and integrity.
Moreover, Ohta and Chuong (1975) also demonstrated that
genes for fruit color and fruit position could be transferred
by grafting. Commenting on Ohta and Chuong’s (1975)
study, Pandey (1985) claimed that “the work is thoroughly
documented, and there is absolutely no cause to doubt the
genuineness of the results” (p. 235). Now there is increasing
evidence for heritable changes induced by plant grafting
(Taller et al. 1998, Liu 2006, Zhou et al. 2013).
The rediscovery of Darwin’s Pangenesis: An
important step in biology?
After the publication of Darwin’s (1868) two-volume work,
he was concerned with how the readers would react to
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his Pangenesis. In 1867, Darwin wrote to Lyell, “This is
my case with Pangenesis (which is 26 or 27 years old),
but I am inclined to think that if it be admitted as a
probable hypothesis, it will be a somewhat important
step in biology” (Darwin F 1888, p. 72). To Lankester,
he wrote, “I was pleased to see you refer to my much
despised child, ‘Pangenesis’, who I think will someday, under
some better nurse, turn out a fine stripling” (Darwin F
1888, p. 120). To Romanes, he wrote, “as you are interested
in Pangenesis, and will someday, I hope, convert an ‘airy
nothing’ into a substantial theory” (Schafer 1896, p. 481).
In the history of biology, neglecting certain discoveries is
not uncommon. It is well known that Mendel’s experiment
on plant hybridization was ignored for decades. For nearly
150 years after the formulation of Darwin’s Pangenesis, it
has been resolutely excluded from the pale of biological
science and is now only of historical interest. However, we
can affirm that Darwin’s idea that pangenetic gemmules are
the molecular carriers of hereditary characters and that they
are diffused through the tissues or from cell to cell has been
removed from the position of a provisional hypothesis to
that of a well-founded theory. It is supported by the discovery of circulating nucleic acids in human blood and plant sap
and the results of experimental work in inducing hereditary
changes through blood transfusion in animals and through
grafting in plants. The rediscovery of Darwin’s Pangenesis, if
and when it happens, would, like the rediscovery of Mendel’s
work, have a tremendous impact on genetics, evolution, cell
biology, and the history of science.
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Yongsheng Liu ([email protected]) and Xiuju Li ([email protected]) are
researchers at Henan Institute of Science and Technology, in Xinxiang, China,
and in the Department of Biochemistry at the University of Alberta, in
Edmonton, Alberta, Canada.
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