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Lynn Margulis (wiki)
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In my
previous blogpost
I remarked that Lynn Margulis deserved a Nobel prize for her endosymbiosis
theory. This triggered a comment essentially denying the scientific merits
of Lynn Margulis for evolutionary biology. It was claimed that Margulis was
not the first to propose a symbiosis theory for the origin
of mitochondria and chloroplasts and that she did not provide the DNA
evidence. Here I provide evidence that during the critical 1960s and 70s
mainstream science rejected and ridiculed the endosymbiosis theory and
cytoplasmic heredity, whereas Margulis was defending this. Finally, I
discovered two publications proving that she did publish DNA evidence.
Priorities, predecessors and prejudices
Indeed, there were predecessors of the symbiosis theory. However,
previous publications were not generally known or, when they were noticed
at all, they were ridiculed. For example, American biologist
Ivan Wallin
published in 1927 the book 'Symbionticism and the Origin of Species' proposing his version of the symbiosis theory. Unfortunately, "The
reviews were so scathing that Wallin withdrew from scientific discourse.
(...) To mainstream biologists, Wallin was little better than a crank."
[1]. And according to
wikipedia
"Wallin and his works were largely forgotten, until Lynn Margulis
introduced a more complete endosymbiotic theory with better evidences in
1967." [12].
Further, the Russian biologist
Merezhkovsky
"proposed that the organelles [chloroplasts] are actually cyanobacteria
that took up residence in an early ancestor of plant cells. (...)
That scenario was ignored or flatly rejected." (...) "But in 1966 decisive evidence for the validity of his proposal
about mitochondria came with the discovery that these organelles have
their own DNA." [2].
Additional evidence: the website 'Understanding Evolution'
states: "Biologist Lynn Margulis first made the case for endosymbiosis
in the 1960s,
but for many years other biologists were skeptical. (...) Why
should we think that a mitochondrion used to be a free-living organism
in its own right? (...) Based on decades of accumulated evidence, the
scientific community supports Margulis’ ideas: endosymbiosis is the
best explanation for the evolution of the eukaryotic cell." [3].
Continuing from the same website:
"When one of her [Margulis] professors saw DNA inside chloroplasts,
Margulis was not surprised. After all, that’s just what you’d expect from
a symbiotic partner. Margulis spent much of the rest of the 1960s honing
her argument that symbiosis was an unrecognized but major force in the
evolution of cells. In 1970 she published her argument in the book
The Origin of Eukaryotic Cells." [4].
Three big bangs that made genetics
Next, we need to place Margulis in the context of the history of
genetics.
In 1900 the rediscovery of Mendel made the first big bang in the
biological sciences. The second was no less important: the identification of chromosomes as the physical
location of Mendel's hypothetical factors. At the time this was called the
Boveri–Sutton chromosome theory or the
chromosome theory of inheritance. Nobody knows those name anymore. And it isn't a theory anymore. But it is an essential and necessary step in the construction of genetics
as a science because the theory 1) located the hypothetical Mendelian
factors on chromosomes, 2) showed elegantly that Mendels pairs of
factors corresponded with pairs of chromosomes (homologous chromosomes). Amazingly, Mendel's theory
predicted that we are all
diploid
creatures! Mendel never knew. The third big bang happened a decade before Margulis was trained as a biologist (1960s). That was the
publication of the chemical structure of DNA by Watson and Crick in 1953.
With a big bang molecular genetics became the most successful theory in
the biological sciences. Together these 3 big bangs made genetics the most
successful discipline within the biological sciences. Don't underestimate
the feeling of triumph.
What is the relevance of all this? The relevance of these three
discoveries for my argument is that chromosomes are located in the
nucleus of the cell. In other words: 'genetics' was synonymous with
chromosomal based heredity
or
nuclear heredity. This was the status of biology in the 1960s. Margulis was working in
the shadow of mainstream nuclear genetics. She stubbornly decided
to study
extra-chromosomal inheritance
or 'cytoplasmic heredity'. It is called 'cytoplasmic heredity'
because mitochondria and chloroplasts are located in the cytoplasma of the
cell. It was opposed to mainstream genetics in no less than 3 ways:
non-chromosomal, non-nuclear (outside the nucleus or
extra-nuclear) and non-Mendelian heredity. Cytoplasmic heredity was considered
unimportant or controversial by the majority of geneticists. For example,
Margulis quotes the Drosophila geneticist and Nobel Prize winner
Thomas Hunt Morgan:
"From the point of view of heredity, the cytoplasm of a cell can safely
be ignored." [5]
Margulis commented: "I considered it an arrogant oversimplification." I agree. In general it is 'amusing' and instructive to browse through
old genetics textbooks to get a feeling of the thinking at the time [14].
Everybody knew that heredity was exclusively located in the nucleus of
eukaryotes. It was an established truth. It wasn't even called 'nuclear
genetics' or 'nuclear genes', because everybody knew that the hereditary
material was located in the nucleus!
Illustrative for the status of science is the statement of John Jinks
(1964) in his monograph
Extrachromosomal inheritance:
"There have been increasingly persistent claims that DNA is present in
structures such as plastids and mitochondria." [10].
Please note that 'claims' means not proven ideas.
In A History of Genetics the genetics pioneer A.H. Sturtevant
(1965) wrote:
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Sturtevant 1965
A History of Genetics
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"Quite recently it has been found that there is DNA in
plastids
and at least some mitochondria. ... It may therefore be supposed that
these bodies carry genes of the same nature as those in the chromosomes"
[6].
It must have been a disturbing discovery for those unaware of the symbiosis
theory. See for example what historian of science Jan Sapp wrote:
"The symbiotic theory of eukaryotic organelles attracted criticism from
many sides during the 1970s. Crucial evidence was lacking. ... Leading
cell biologists also argued that theories about eukaryotic cell origins
were unscientific because they could not be proven." (!) [7]. (my
emphasis)
That was how biologists used to think at the time. In 1972 Tribe and
Whittaker wrote in their monograph
Chloroplasts and Mitochondria:
"Up until the last few years, it was generally assumed that the total
information necessary for the synthesis of a cell resided in the DNA of
the nucleus." [8].
Indeed! Remarkably, at the time it was uncertain whether mitochondria and
chloroplasts could divide at all, or whether they were synthesized
de novo (from scratch). It was also a problem how much of the DNA
in mitochondria and chloroplasts was functional at all and, if functional,
what role it played. Furthermore, the authors point out two major
objections to the symbiotic theory [9]. So, my point is that one should
not ignore the status of biology at the time Margulis was
working.
DNA evidence!
The blog commenter also claimed that Margulis did not provide DNA
evidence for the symbiosis theory. This is not correct. I discovered an
ignored publication:
L. Sagan (1961)
Evidence for cytoplasmic DNA in Euglena gracillis [11] in
the Journal of Protozoology.
This publication is not listed in the Lynn Margulis
wikipedia page. Unfortunately, google scholar returns the title only, not the contents,
not even an abstract. However, the title is revealing [12].
The most reliable and exemplary demonstration of DNA in plastids is given
by S. Nass and M.K. Nass (1963) [13].
From the fact that they perform extensive control experiments, it is clear
that they are aware that extraordinary claims require extraordinary
evidence. They wanted to exclude any contamination with nuclear DNA or other false positives. At the time these authors were not interested in evolutionary explanations
and did not interpret the DNA as evidence for symbiosis theory. They were
busy unraveling the structure and function of cellular organelles. No time
for speculation. This shows that the discovery of DNA in mitochondria
occurred independent of the symbiosis theory. On the other hand knowledge of
the symbiosis theory would be an excellent reason to search for DNA in
mitochondria. Nass & Nass came incredibly close to the discovery of an
evolutionary symbiosis theory with this quote : "a structure homologous with
the mitochondrion is the entire bacterial cell." That statement is still not
a symbiosis theory. The most far-reaching conclusion they dared to draw
was:
"In any case, the presence of D N A in mitochondria appears to require
modification and extension of some generally accepted hypotheses of cell
function which consider the nucleus to be the exclusive site of cellular D N
A and genetic information." [13].
Indeed. Clearly, the authors doubted a well established truth. It was the
first step towards a symbiosis theory. Lynn Margulis devoted herself to developing a comprehensive symbiosis
theory.
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Principles of Population Genetics
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'Symbiosis' is still a sensitive subject. A stunning demonstration is the textbook Principles of Population Genetics [15]. Many pages are devoted to describing all genetics aspects of mitochondrial DNA (mtDNA) and chloroplast DNA (cpDNA). And those aspects are without doubt useful for understanding certain
aspects of evolution. However, endo-symbiosis is never mentioned. It is not that mitochondria are absent. It is not that mitochondrial DNA is
absent. No. It is the word 'Symbiosis' that is absent. It doesn't occur in the index. I find that really baffling. Is symbiosis so far beyond the scope of population genetics? It seems
symbiosis does not fit in the theory of population genetics. Could it be that
the origin of mitochondria and chloroplasts can not even be described by the
most advanced mathematical population genetic models? If true, than it clearly shows the limits of population genetics for understanding all the facts of evolution of life on
earth. Symbiosis is not a rarity [19].
A second paper of DNA evidence by Lynn Margulis is:
L Sagan, Y Ben-Shaul, HT Epstein, JA Schiff (1965) 'Studies of chloroplast development in Euglena. XI. Radioautographic
localization of chloroplast DNA', Plant physiology 1965 Nov;40(6):1257–1260. (pdf). (Note: at the time Lynn Margulis published under the name L. Sagan
because she was married with Carl Sagan.)
This publication does not occur in
wikipedia
either. The authors conclude that chloroplasts (like mitochondria) contain
DNA and RNA; they are self-duplicating bodies which do not arise de novo;
the DNA represents a multigenic hereditary system which is not derived
from the nucleus and is, in part, responsible for the biochemical
properties of the organelle. In her 1967 paper
On The Origin of Mitosing Cells she made the prediction that all
eukaryotes should contain mitochondrial DNA and all eukaryotic plants
should contain chloroplast DNA. Also in that 1967 paper she refers
to (Sagan, L., 1964, unpublished data) [16].
We should not be surprised that Margulis worked
on DNA evidence! Her thesis was: 'An Unusual Pattern of Thymidine Incorporation in Euglena', 1965 (mentioned in wikipedia). The
abstract
can be found in the The Journal of Protozoology (published under
the name Lynn Sagan). Although the results are confusing and inconclusive,
the thesis shows that she used techniques to detect DNA in the cytoplasm.
(Thymidine is a component of DNA). Interestingly, in the References of her thesis
I found 3 other publications with L. Sagan as author:
- Sagan, L. & Scher, S. 1962. Cytoplasmic incorporation of
H3-thymidine in Euglena gracilis. J. Protozool. 8, Suppl.
20.
- Plaut, W. & Sagan, L. A.*) 1958. H3-thymidine incorporation into the cytoplasm of Amoeba. (pdf) J. Biophys. Biochem. Cytol.**) 4,
843–7.
*) Lynn Petra Alexander Sagan Margulis
(1938-2011)
**) "Content prior to 1962 was published under the
journal name
The Journal of Biophysical and Biochemical Cytology."
- Sagan, L., Ben-Shaul, Y. & Schiff, J. A. 1964.
Radiographic localization of DNA in the chloroplasts of Euglena.
Abstracts of the 4th Annual Meeting of the American Society for Cell
Biology, Cleveland, Ohio.
These three publications do not occur in Wikpedia.The publications prove that Margulis started working on DNA in 1958 or earlier. That is 5 years earlier than Nass & Nass (1963) [18].
Conclusion
The claim that Margulis was not the first to propose a symbiosis theory
is right. However, that is not the point. The point is that the symbiosis theory was disregarded at the time when
Margulis started working on the subject.
The evidence presented here shows that it was risky and unpopular to
study and publish about the symbiosis theory during the 1960s and 1970s.
Margulis (1967,1970) elaborated the theory and provided enough initial
evidence to justify further research into the theory.
Furthermore, I showed that the claim that she did not come up with DNA evidence is wrong.
She produced 5 - 6 publications. The symbiosis theory provided a correct evolutionary explanation for why
there is DNA in mitochondria and chloroplasts.
Now we have reached this conclusion, it is useful to compare Darwin and
Margulis. Darwin did not prove his theory in 1859. Neither was he the
first to propose a theory of evolution.
And his theory was very controversial at the time. But, Darwin provided enough reasons for his contemporaries to take the
theory serious. Subsequent generations of biologists have shown that the
theory was indeed worth investigating and came with abundant evidence. It
is now an accepted theory. The same holds for the endosymbiosis
theory.
I am not the only one with a positive assessment of the contribution of
Lynn Margulis to the theory of evolution. For example Michael Ruse and
Joseph Travis [17] wrote:
"But it was Margulis who took up the idea, now known as the
endosymbiotic theory, offered microscopic evidence, and pushed it (in
her book Origin of Eukaryotic Cells, 1970) until it became
orthodoxy.".
And the architects of the Evolutionary Synthesis wrote:
"The most complete hypothesis is that of Margulis (1970), who has marshalled a great wealth of morphological, biochemical, and paleontological facts ... ". [20].
Notes
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Lynn Margulis, Dorion Sagan (1997) Slanted Truths chapter 4,
page 50.
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Lynn Margulis, Dorion Sagan (1997) Slanted Truths, chapter 3,
page 38.
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Website
Understanding Evolution
page 'Evidence for endosymbiosis' of the Berkeley museum of
paleontology. (by the way, very good website!)
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The full title:
Origin of eukaryotic cells;: Evidence and research implications for a
theory of the origin and evolution of microbial, plant, and animal
cells on the Precambrian earth
(1970) Yale University Press. (still available at amazon). See also: the
website
Understanding Evolution
page
Endosymbiosis: Lynn Margulis
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Lynn Margulis (1998) The Symbiotic Planet.
A new look at evolution, hardback, page 22.
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A.H. Sturtevant (1965) A History of Genetics page 125 chapter 19
'Maternal Effects'. Sturtevant refers to: Gibor and Granick (1964)
Science 145: 890-897. This publication is also referred to by
Margulis (1967).
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Jan Sapp (2003) Genesis. The Evolution of Biology. page
246.
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Michael Tribe, Peter Whittaker (1972)
Chloroplasts and Mitochondria. page 54.
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idem page 57.
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John L. Jinks (1964) Extrachromosomal inheritance.
Prentice-Hall. p.89.
Dutch: John L. Jinks (1968) Extrachromosomale erfelijkheid. Het
Spectrum. paperback, pagina 132. He did not refer to publications.
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Sagan, L,
Evidence for cytoplasmic DNA in Euglena gracillis, Journal of Protozoology 8 4: 20 (1961). Euglena is a
single-celled eukaryote.
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I found the publication via the references in Lynn Sagan (1967)
On the origin of mitosing cells
(her first publication. It is a large, complex, wide-ranging
publication). She writes: "A plethora of recent studies elegantly
reviewed by Gibor & Granick": A. Gibor and S. Granick (1964)
Plastids and Mitochondria: Inheritable Systems: Do plastids and
mitochondria contain a chromosome which controls their multiplication
and development?
Science 28 Aug 1964. Only the Abstract is available, but,
amazingly, I discovered in the References of G&G: "L. Sagan (1961)"
[11].
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S. Nass and M.K. Nass (1963) Intramitochondrial fibers with DNA characteristics. II. Enzymatic and
Other Hydrolytic Treatments. J Cell Biol 1963 Dec 1;19(3):613–629. A pdf is available.
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For example the genetics textbook Srb, Owen, Edgar (1965)
General Genetics, Second edition, hardback, which I still have on
my bookshelf, contains a chapter 'Extrachromosomal and Epigenetic
Systems'. That is great. But browsing through the pages reveals that the
most important criterion for extrachromosomal inheritance is simply that
it does not obey the laws of Mendel and must be located in the cytoplasma.
Mitochondria and chloroplasts are mentioned, but at the time it was
impossible to prove that these organelles contain DNA. It was an open
question whether extrachromosomal heredity relies on 'coded information'.
"Extrachromosomal heredity has reality, and manifests itself in almost
bewildering variety." (p.345). There is no mention of '(endo)symbiosis'.
How amusing and useful a little time travel can be!
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Hartl & Clark (1997) Principles of Population Genetics, third
edition. Sinauer Associates. hardback.
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"This is quite analogous to the presence of two distinct DNA bands of
nearly equal size found in CsCl density gradient runs on DNA isolated from
Paramecium bursaria (Sagan, L., 1964, unpublished
data).
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Michael Ruse, Joseph Travis (2009)
Evolution. The First Four Billion Years, Harvard University
Press, hardback, 979 pages. page 712-713. This is just one example. The
influential evolutionary biologist John Maynard Smith recognized her
contribution to science; see
my review of Lynn Margulis.
- This paragraph was added 14 Mar 2025. See for a summary of the first attempts to demonstrate cytoplasmic DNA: William A Wells (2005) There's DNA in those organelles J Cell Biol. 2005 Mar 14.
- Nancy A. Moran (2025) 'Symbiosis. A Very Short Introduction', Oxford University Press. 192 pages. "The majority of evolutionary biologists continue to regard symbiosis as a marginal process that can mostly be disregarded." 15 Mar 2025
- Dobzhanksy, F.J. Ayala, G.L. Stebbins, J. Valentine (1977) 'Evolution', W H Freeman and Company. hardback. page 383–389. The book is a comprehensive overview of the theory of evolution as it was at that time. 17 Mar 2025
