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A visionary scientist with a blind spot

Lynn Margulis as a critic of neo-Darwinism

Acquiring Genomes       Acquiring Genomes. A theory of the origins of species.
by Lynn Margulis and Dorion Sagan
Basic Books, hardback 2002, paperback 2003.
Foreword by Ernst Mayr

reviewed by Gert Korthof, 5 Jun 2005 (updated 20 Jan 2012)


Lynn Margulis died on 22 Nov 2011 at the age of 73 (6,7,8).



Summary of this review
  • Lynn Margulis' symbiosis theory is a proven theory in biology.
  • The claim in Acquiring Genomes that symbiosis is the main mechanism for creating new species in evolution is an unjustified extrapolation from a number of well-documented cases to all domains of life.
  • The claim that the accumulation of mutations do not lead to anything useful is refuted by the facts of molecular and evolutionary genetics.
  • Margulis unambiguously rejects creationism, despite her criticism of the fundamental neo-Darwinistic mechanisms
  • Her alternative theory is a fully naturalistic evolutionary theory.

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Symbiosis is a proven theory in biology

All humans have mitochondria in all of our cells. All animals and plants have mitochondria in their cells. It is largely due to Lynn Margulis that the hypothesis that mitochondria were once free-living bacteria, is now considered a proven scientific theory in biology. The symbiotic origin of mitochondria (1.5 billion years ago) is no longer a controversial theory.

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and is found more frequently in nature than the textbooks show

The authors take one step further. Symbiosis is not a unique historical event that happened 2000 million years ago. They show that symbiosis frequently happened after that event. These claims are generally well documented but are not yet reflected in the evolutionary biology textbooks of today. Two good examples are:
 
Pterotermes occidentis
All termites that are capable of digesting wood
are entirely packed with microbial symbionts.
squid
Glow-in-the-dark squid symbiosis with bacterium
Vibrio fischeri

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Evolution is not always in small steps

According to Darwin evolution occurs by very small steps. But the symbiotic event that created eukaryotes was a big step. Thereafter, many small steps adjusted the mitochondrial genome and the host genome by random mutation and natural selection.

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Symbiosis is not a universal mechanism for the creation of new species

The really controversial claim of Margulis & Sagan is that symbiosis is the main mechanism for creating new species in evolution. This is an unjustified extrapolation from a number of well-documented cases to all domains of life. Ernst Mayr mentions that there is no indication that any of the 10,000 species of birds or the 4,500 species of mammals (including humans) originated by symbiogenesis (1). In my view symbiosis is important in evolution; her new book brings new cases; textbooks must be updated in that respect, but the authors exaggerate the role of symbiosis in the creation of new species. The reason is that symbiosis does not create new genes. That is her blind spot.

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Accumulation of random mutations is crucial for evolution

Three genetic mechanisms cause the creation of new species by reproductive isolation (or hybrid sterility): chromosomal, genetic and endosymbiotic (2, p281). Coyne & Orr conclude that endosymbionts do not represent a common path to animal speciation (p.280). Chromosomal causes of speciation are important in plants. Genetic causes (mutation) are the most common mechanism of new species. Direct molecular evolutionary data now support one of the central tenets of the neoDarwinian view of speciation [creation of new species] - that reproductive isolation results from natural selection within species. This may well represent the most important finding to emerge from the last decade of work on the genetics of speciation (p.319). Furthermore, according to the geneticist W.H. Li "there is now ample evidence that gene duplication is the most important mechanism for generating new genes and new biochemical processes that have facilitated the evolution of complex organisms from primitive ones" (3). Therefore, Margulis' claim that random mutation cannot create new species is untenable.
Furthermore, even Intelligent Design Theorist Michael Behe, admits "We know that single changes to single genes can sometimes elicit a significant beneficial effect" (5).

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Margulis unambiguously rejects creationism

"Anthropocentric writers with a proclivity for the miraculous and a commitment to divine intervention tend to attribute historical appearances like eyes, wings, and speech to "irreducible complexity" (as, for example, Michael Behe does in his book, Darwin's Black Box) or "ingenious design" (in the tradition of William Paley who used the functional organs of animals as proof for the existence of God). Here we feel no need for supernatural hypotheses. Rather, we insist that today, more than ever, it is the growing scientific understanding of how new traits appear, ones even as complex as the vertebrate eye, that has triumphed. What is the news?" (quote from the book, page 202). Ironically, a creationist website rejects endosymbiosis (9).

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Margulis is not always credited for her contribution to evolutionary theory

For example, Margulis is not credited for the discovery of the eukaryotic merger by Mark Ridley (2004) in his third edition of Evolution: "Mitochondira and chloroplasts almost certainly originated by symbiosis (Section 10.4.3, p.265). Their symbiosis was first suggested by the morphological similarity of the organelles to bacteria. The theory has since been strongly supported by molecular evidence." (page 533). Furthermore, Margulis is neither present in the References nor in the Index. In the section 10.4.3 Margulis is not mentioned either. Furthermore, Ridley claims that symbiosis does not violate Darwinism: "Evolution by symbiosis, or combining several genes into new composite genes, can violate the letter, but not the spirit, of Darwinian gradualism. (...) However, no deep principle in Darwinism has been violated because the adaptive information within each ancestral cell was built up in gradual stages." (page 266). It is remarkable that Ridley knows that the eukaryotic merger is of profound importance for life on earth, because it created all eukaryotes on this planet, but at the same time tries to play down its importance (4).
Furthermore, Margulis is not in the index of two recent evolution textbooks: Nicholas Barton et al (2007) 'Evolution' and Scott Freeman and Jon Herron (2007) 'Evolutionary Analysis' (4th ed.). Compare this with a full-page interview with Margulis in Strickberger (2000) 'Evolution' (third edition, p.179).. In the most recent evolution textbook Graham Bell (2014) The Evolution of Life, 'Margulis' is absent, but 'endosymbiosis' is present (10).

On the other hand, Margulis is not ignored in works of John Maynard Smith. In his The Theory of Evolution (third edition 1997) Margulis and symbiosis are present. More than that: "I am again indebted to many collegues. Dr. Lynn Margulis has read Chapter 6." (p. xxii). Furthermore, symbiosis and cooperation play an important role in the major transitions in the history of life on earth (11).



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Notes

  1. Ernst Mayr in the Foreword of the book (page xiii).
  2. Jerry A. Coyne & H. Allen Orr (2004) Speciation. Sinauer Associates, 545 pages.
  3. quoted by Jerry Coyne in Nature, 435, 1029-1030, 23 June 2005
  4. "All subsequent complex life has been shaped by the eukaryotic revolution" (p.165) and "mergers have contributed only a few of our genes" (p.164) in Mendel's Demon. His estimate of 5% is based on an outdated estimate of 60,000 human genes. Today, the estimate is 20,000 - 25,000 genes, so a correct estimate would be 13%.
  5. Michael Behe (2007) The Edge of Evolution, page 101. And: the mutations conferring chloroquine resistance on the malaria parasite are an example of random beneficial mutations (page 74 and further). Another mutation, a single amino acid change makes malaria one hundred times more resistant to the new drug pyrimethamine. "The classic example, taught in virtually all biology textbooks, is that of sickle cell hemoglobin, where a change of one amino acid confers resistance to malaria, saving many children from premature deaths." (p.101)
  6. Lynn Margulis, Evolution Theorist, Dies at 73, The New York Times, November 24, 2011.
  7. James A. Lake 'Lynn Margulis (1938–2011)', Nature, 480, 458 (22 December 2011)
  8. Moselio Schaechter (2010) Retrospective Lynn Margulis (1938–2011) Science 20 January 2012
  9. The Endosymbiosis Hypothesis and Its Invalidity (Harun Yahya International © 2005).
  10. Graham Bell (2014) 'The Evolution of Life', Oxford University Press, 496 pages. Of course, this does not mean the textbook is bad! Endosymbiosis is discussed in Chapter 8 and 17 but apparently Margulis has nothing to do with it.
  11. John Maynard Smith & Eörs Szathmáry: "The Origins of Life. From the Birth of Life to the Origin of Language", Oxford University Press, 1999.

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Reviews

  1. Acquiring Genomes is reviewed by Axel Meyer: Viewing life as cooperation in Nature 18 July 2002.

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Further Reading

  • Michael Shermer (2005) "The Woodstock of Evolution" in: Scientific American, June 27. Lynn margulis is quoted saying "It was like confessing a murder when I discovered I was not a neo-Darwinist".
  • Lynn Margulis and René Fester (1991) Symbiosis as a Source of Evolutionary Innovation. Speciation and Morphogenesis. The MIT Press (publisher's info). (with a contribution of John Maynard Smith). (Out of Print in 2013)
  • Lynn Margulis, Clifford Matthews, Aaron Haselton (Editors) (2000) Environmental Evolution - 2nd Edition: Effects of the Origin and Evolution of Life on Planet Earth. (Paperback). In this book fifteen distinguished scientists discuss the effects of life--past and present--on planet Earth. It provides a unique synthesis of atmospheric, biological, and geological hypotheses that explain the present condition of the biosphere. Info.
  • Richard A. Watson (2006) Compositional Evolution : The Impact of Sex, Symbiosis, and Modularity on the Gradualist Framework of Evolution (Vienna Series in Theoretical Biology) (Hardcover) The MIT Press (February 17, 2006)
    • From Amazon: " In Compositional Evolution, Richard Watson uses the tools of computer science and computational biology to show that certain mechanisms of genetic variation (such as sex, gene transfer, and symbiosis) allowing the combination of preadapted genetic material enable an evolutionary process, compositional evolution, that is algorithmically distinct from the Darwinian gradualist framework."
  • Christian de Duve (2007) The origin of eukaryotes: a reappraisal, Nature Reviews Genetics 8, 395-403 (May 2007)
    • "Ever since the elucidation of the main structural and functional features of eukaryotic cells and subsequent discovery of the endosymbiotic origin of mitochondria and plastids, two opposing hypotheses have been proposed to account for the origin of eukaryotic cells. One hypothesis postulates that the main features of these cells, including their ability to capture food by endocytosis and to digest it intracellularly, were developed first, and later had a key role in the adoption of endosymbionts; the other proposes that the transformation was triggered by an interaction between two typical prokaryotic cells, one of which became the host and the other the endosymbiont. Re-examination of this question in the light of cell-biological and phylogenetic data leads to the conclusion that the first model is more likely to be the correct one."
  • Nancy A. Moran (2007) 'Symbiosis as an adaptive process and source of phenotypic complexity', PNAS published online May 9, 2007 (Free Access).
    • "The literature on symbiosis is vast and growing quickly, largely because of the insights based in genomics. Although symbiosis was once discounted as an important evolutionary phenomenon, the evidence is now overwhelming that obligate associations among microorganisms and between microorganisms and multicellular hosts have been crucial in many landmark events in evolution, in the generation of phenotypic diversity, and in the origin of complex phenotypes able to colonize new environments."
  • Anthony Poole & David Penny (2007) 'Eukaryote evolution: Engulfed by speculation', Nature 447, 913 (21 June 2007).
    • "One thing at least is agreed: the mitochondrion, powerhouse of the eukaryote cell, evolved from an engulfed bacterium. The question is 'who' did the engulfing. Did an archaeon engulf a bacterium? Did a bacterium, bacterial consortium, or RNA cell engulf first an archaeon (which became the nucleus) and then the mitochondrial ancestor? Perhaps nuclei emerged in a virus-infected archaeon, which then engulfed mitochondria. Which, if any of these, is right?"
  • Yaacov Davidov & Edouard Jurkevitch (2007) 'How incompatibilities may have led to eukaryotic cell', Nature, 448, 130 (12 July 2007).
  • Julie C. Dunning Hotopp et al (2007) 'Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes', Science 21 September 2007: 1753-1756.
    • "Unexpectedly, the symbiont Wolbachia can transfer segments of DNA consisting of individual genes or almost its entire genome to its insect or nematode hosts."
  • Harmit S Malik (2007) 'Genes get diabolical', Nature Genetics 39, 577 (2007) is a review of 'Genes in Conflict: the Biology of Selfish Genetic Elements', Austin Burt and Robert Trivers (2006).
    • "The result is a powerful resource in evolutionary genetics that will help influence many skeptics who would (still) rather think of selfish genes as simply rare deviants in a largely symbiotic network of genetic interactions."
  • James O. McInerney and Davide Pisani (2007) 'Paradigm for Life', Science, 30 Nov 2007.
    • "The role of horizontal gene transfer in evolution has raised fierce debate about the relevance of the Tree of Life, a long-accepted representation of the interrelatedness of living things through evolutionary time, based primarily on the sequence of the genes that encode the small subunit of ribosomal RNA. The question is whether this depiction should be replaced with a network, or Web of Life".
  • Graham Lawton: Why Darwin was wrong about the tree of life, New Scientist 21 January 2009.
  • Kenneth M. Weiss, Anne V. Buchanan (2009) The Mermaid's Tale. Four Billion Years of Cooperation in the Making of Living Things, Harvard University Press.
    Info. "Even after 150 years, Darwin's theory of evolution by natural selection is irresistibly compelling. But how can this idea -in which competition prevails- be consistent with all that we know about the thoroughly cooperative nature of life at the genetic and cellular level? This book reconciles these discrepancies." "Although relentless competitive natural selection is widely assumed to be the primary mover of evolutionary change, The Mermaid's Tale shows how life more generally works on the basis of cooperation."
  • A beautiful example of symbiosis: "The best studied solar-powered slug is Elysia chlorotica, which eats only the alga Vaucheria litorea. These molluscs are some of the most fascinating creatures in the world, eating algae and harvesting chloroplasts through specialized epithelial cells in the gut. Once phagocytosed, the chloroplasts are maintained within the animal's cells for months at a time, during which the slug gains energy directly from photosynthesis. Nature 459, 207-212 (14 May 2009)
  • Scientists have stumbled across the first example of a photosynthetic organism living inside a vertebrate's cells: Anna Petherick (2010) 'Salamander's egg surprise. Algae enjoy symbiotic relationship with embryos', Published online 4 August 2010 Nature 466, 675 (2010).
  • Dorion Sagan, Ed. (2012) Lynn Margulis. The Life and Legacy of a Scientific Rebel, Chelsea Green, White River Junction, VT, 2012 Hardback: 215 pp.
  • Bruce A. Curtis et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs, Nature, Published online 28 November.
    • Cryptophyte and chlorarachniophyte algae are transitional forms in the widespread secondary endosymbiotic acquisition of photosynthesis by engulfment of eukaryotic algae.
  • Erik F. Y. Hom, Andrew W. Murray (2014) Niche engineering demonstrates a latent capacity for fungal-algal mutualism, Science 4 July 2014. See also Perspective article: The birth of cooperation by Duur K. Aanen, Ton Bisseling in the same issue.
  • Elizabeth Pennisi (2014) Modern symbionts inside cells mimic organelle evolution, Science 31 October 2014. (tertiary endosymbiosis, The smallest mitochondrial genome 6000 bases; human mitochondrial DNA 16,000 bases, the biggest known 11 million bases; similarities between endosymbionts and organelles).
  • Symbiotic Earth, This is a demonstration of our upcoming documentary: Symbiotic Earth: How Lynn Margulis rocked the boat and started a scientific revolution – a film by John Feldman, presented and owned by hummingbirdfilms.com.
  • E. Toby Kiers, Stuart A. West (2015) Evolving new organisms via symbiosis, Science 24 Apr 2015. (insightful overview of when and why new organisms evolve via symbiosis and when and why they do not enter symbiosis).
    • "The elegance of the major transitions framework [Maynard Smith and Szathmáry] is its simplicity. It argues that the same problem–how to overcome the selfish interests of individuals to form mutually dependent cooperative groups–has arisen and been solved at several crucial moments in history across all orders of life. At the same time, it recognizes that transitions in individuality are rare and require strict conditions: Partner interests need to be aligned and the benefits of more integrated cooperation must lead to mutual dependence."
  • Elizabeth Pennisi (2015) Leaf bacteria fertilize trees, researchers claim. Science 22 May 2015.
    • bacteria between leaf cells of poplars and limber pines are transforming nitrogen from the air into a form the tree needs to sustain rapid growth.

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Copyright ©G. Korthof 2005 First published: 5 Jun 2005 Updated: 22 May 2015 N/F.R.: 22 May 2015