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MACROSCOPE

Evolution's Other Narrative

Why science would benefit from a symbiosis-driven history of speciation.

Bradford Harris

2013-11MacroHarrisF1.jpgClick to Enlarge ImageDuring a recent meal with a friend who happens to be a successful engineer, I found myself drawn, as usual, into debate. Although our theological and political views diverge, he and I customarily find common ground in scientific epistemology. However, this time the topic was whether intelligent design should be taught in high schools. When I expressed incredulity at his support for teaching intelligent design, he said, “Brad, just look around us—survival of the fittest can’t be all that’s going on here, and I think it is important to respect people’s sensitivity to that.”

I reminded my friend that, because intelligent design argues for supernatural causes of natural phenomena, teaching it would undermine rational inquiry, together with students’ ability to eventually make the kind of scientific breakthroughs we are enjoying today. I pointed out the U.S. National Institutes of Health’s Human Microbiome Project as an example, which is revealing how human health suffers when the health of the millions of microorganisms with which we’ve coevolved suffers. My friend’s simplistic interpretation of evolution as “survival of the fittest” left him ignorant even of the possibility of projects like this, which are based on evolutionary considerations of symbiosis. Evidently, educators—and certainly evolutionary specialists themselves—must broadcast a more nuanced story of evolutionary theory. Otherwise, future scientists and projects that inform better approaches to human health and global ecology will be sabotaged before they even emerge.

Science education has failed to overcome entrenched cultural ideals rooted not only in religion, but also in political philosophy. For those like my engineer friend trying to comprehend how magnificent structures of life emerge by means of “survival of the fittest,” skepticism is understandable. Popular appreciation for life’s complexity has far outpaced the popular interpretation of the evolutionary source of that complexity, which has remained stuck in 1864, when Herbert Spencer coined the phrase “survival of the fittest.”

When it comes to the story of evolutionary science, people know the name Charles Darwin, but most do not know the names Ivan Wallin or Lynn Margulis—two more recent, groundbreaking evolutionary theorists. Over the past several decades, these and other researchers have revealed that organisms’ cooperation and interdependence contribute more to evolution than competition. Symbiogenesis—the emergence of a new species through the evolutionary interdependence of two or more species—is at least as important in the history of life as survival of the fittest. Such insight has failed to gain traction in American minds—including those of American scientists—because of cultural history traceable back through the popularization of Adam Smith’s individualist philosophy.

Darwinism and Individualism

By the time Darwin published On the Origin of Species in 1859, the Western European and American mind had long been intellectually primed to interpret complexity by reducing perspective to the individual. Adam Smith’s publication of The Wealth of Nations 83 years earlier had set the tone of philosophical and scientific approaches to understanding complex systems. Fundamental to Smith’s philosophy, as economic historian Warren Samuel reminds us, was the notion that large organizations like the economy were to be “comprehended in terms of self-interest or maximization of personal well being.” Smith’s influence on Darwin was as strong as it was on the rest of the reading public.

The appeal of this philosophy was twofold: It morally liberated people to be selfish, and it intellectually liberated them to interpret a range of complicated questions in terms of simpler individual parts. When Darwin presented his theory of evolution in 1859, he stood firmly on the platform of Smith’s individualist philosophy. As the renowned evolutionary biologist Stephen Jay Gould surmised, the essential “Darwinian theory advocates no higher principle beyond individuals pursuing their own self-interest . . . [for] Darwin grafted Adam Smith upon nature to establish his theory of natural selection.” If mid-19th-century readers struggled with the unseen mechanism of evolution, then they could do as Darwin did and conveniently borrow Smith’s economic concept of the “invisible hand.”

For most naturalists and laypeople alike, the logical extension self-interest was endless combat. In the second half of the 19th century, compelling historical reasons existed for this vision. Since Thomas Hobbes published Leviathan in 1651, Western Europeans and later Americans had struggled to reconcile ideals of self-government with social stability, often violently. Humanity’s social institutions might separate it from the violent chaos of nature, but nature’s violent chaos was assumed. The theory of natural selection grew out of and reinforced this assumption, and the most successful circulating English phrases to distill Darwin’s tome depicted violence, not harmony. Nature was understood, through Alfred Lord Tennyson, as “red in tooth and claw.” Similarly, T. H. Huxley tapped the psychological nerve well when he portrayed the history of life as “a continual free fight…the Hobbesian war of each against all.” The English political theorist Herbert Spencer best captured the concept when he defined natural selection as “survival of the fittest.”

Simple and cleanly fused with the entrenched political ideal of individualism, Darwinian natural selection totally dominated the Western perspective on evolution for more than a century. But even before the end of the 19th century, some Western naturalists began interpreting evolutionary principles differently, looking beyond competition to the role of cooperation.

These investigators studied the many “individual” species that resembled a composition of autonomous species or specie parts somehow working in association—for example, lichens, giant green anemones, and termites. In the 1880s, for example, the Scottish biologist Patrick Geddes interpreted the biological relationship between the algal and animal cells in giant green anemones as a special form of speciation. He reasoned that green algal cells were infused into the animal flesh of the anemone cooperatively. Geddes’s chief interest was the evolution of this relationship. In 1882 he published in Nature under the title “Symbiosis of Alga and Animals,” in which he argued that the giant green anemone, which outnumbered competing anemones that lacked algal cells, represented evolutionary adaptation outside the conceptual framework of Darwinism.

Geddes was not the first to use the term symbiosis, but he was among the first to discuss it in terms of evolution. He appreciated that symbiotic associations between “species” could become so integral to their biology that their individual species identity had little meaning outside of the relationship. Although admired briefly by his cohort, however, “Symbiosis of Alga and Animals” was buried beneath his work in other disciplines, such as urban planning. Apparently constrained by his culture’s prevailing individualist perspective, Geddes never fully articulated a theory of symbiotic-driven speciation, nor did any other Western European or American scientists for another two generations.

If an evolutionary theory featuring symbiotic-driven speciation was to emerge, then it would likely do so outside Western Europe and North America. In fact, by 1910 Russian biologists had raced ahead with the idea of symbiotic-driven speciation. In that year enough relevant evidence had accumulated in the Russian scientific community for the botanist Constantin Merezhkowsky to create a new evolutionary term: symbiogenesis. He declared that the term aptly described “the origin of organisms by the combination or by the association of two or several beings which enter into symbiosis.”

The Russians were not merely unswayed by the Western European and American cultural ideal of individualism; many of them were explicitly hostile to it. The well-known Russian naturalist, evolutionary theorist, and political philosopher Peter Kropotkin was highly critical, especially of Huxley’s “Hobbesian war of each against all.” In his travels across Siberia, Kropotkin was impressed by the cooperation he observed among people and animals. Saddled with his own cultural biases tilting toward socialism, Kropotkin was most interested in how the intra- and interspecies relationships of people, reindeer, birds, fish, ants, and numerous other organisms enabled them to survive the harsh Siberian winters.

Outside of their ecological associations, Kropotkin believed, individual organisms were not worth studying from an evolutionary perspective, because isolated individuals were not biologically viable in the unforgiving Siberian environment. In his most popular work, Mutual Aid (1902), Kropotkin wrote that “mutual aid is as much a law of animal life as mutual struggle, but . . . as a factor of evolution, it most probably has a far greater importance.” He explained that “it favors the development of such habits and characters as insure the maintenance and further development of the species.”

According to science historian Liya Nikolaevna Khakhina, Russian evolutionary theorists did not discount Darwinian natural selection, but they did conceive of it differently. By the 1920s, many Russian scientists had come to believe that “symbiosis was the source of evolutionary novelty but natural selection . . . acted on emerging and tightening symbiotic associations.” In other words, according to Khakhina’s notion of speciation, if “symbiosis is the author, natural selection is the editor.”

The Story of Symbiogenesis

2013-11MacroHarrisF2.jpgClick to Enlarge ImageThroughout the first half of the 20th century in Western Europe and America, even as scientists reduced their investigations on evolution down to the microscopic level of the cell, the individualist school of thought continued to dominate. Researchers assumed that the genes inside the cell nucleus contained all the information determining an individual’s functions, traits, and health, and therefore the individual’s evolutionary prospects. The new preoccupation with genetic competition only extended the appeal of interpreting evolution as survival of the fittest. Nonetheless, struggling against this reinforced structure, a minority of investigators maintained interest in symbiotic interpretations of biological adaptation. For these scientists, nuclear genetics told only part of the evolutionary story.

One of the most important of these symbiotic thinkers was Ivan Wallin of the University of Colorado, Boulder. During the 1920s he set out to investigate the history of the eukaryotic cell organelles called mitochondria—the globular structures outside the nucleus that produce the cell’s energy. Wallin proposed a radical hypothesis: Mitochondria did not evolve endogenously through a long history of random nuclear genetic mutation; instead, mitochondrial organelles inside our cells descended from bacteria that had formed cooperative associations with our cells—with us. This idea contradicted combative survival of the fittest.

In 1927 Wallin published Symbionticism and the Origin of Species, in which he pointed out that mitochondria’s possession of their own, distinct genes showed their independent bacterial ancestry. This was the first direct genetic evidence presented to the western European and American scientific community that supported the theory of symbiogenetic evolution.

Wallin should have caused a sensation, but Western scientists failed to take note. Symbiogenetic insights remained overshadowed by the preoccupation with cell nuclei. Especially after the resurrection of Gregor Mendel’s work, most scientists believed that any genetic material that might be found outside the cell nucleus was unimportant to evolution.

The public, meanwhile, was less interested in esoteric variations in evolutionary theory among experts than they were with the creationism-evolution debate during the 1925 State of Tennessee v. Scopes trial. Whether evolution was real—not how it proceeded—was the popular drama. When Scopes was a fading memory in the 1950s, James Watson’s and Francis Crick’s revelation of the double-helical structure of DNA subsumed symbiogenesis under a whole new generation of enthusiasm for nuclear genetics. Yet another generation passed before the evolutionary biologist Lynn Margulis succeeded in revivifying the insights of Wallin and the earlier Russian symbiogeneticists.

Lynn Margulis’s Legacy

According to Margulis, the evolving relationships between microscopic organisms and other micro- and macroscopic organisms are the essence of the history of life. Despite scientists’ mid-century focus on eukaryotic life (organisms with larger cells featuring a bounded nucleus and organelles), the most prolific type of organism on Earth, bacteria, is prokaryotic (an organism without a bounded nucleus). Virtually all eukaryotic forms of life have adapted symbiotic associations with prokaryotic bacteria. Margulis was among the first Western scientists to attempt to popularize this fact. She spent virtually her entire career laboring to bring this mostly microscopic form of evolution to the macroscopic focus of her readers.

Margulis’s research in microbiology equipped her to verify and expand on Wallin’s symbiosis-centered theory. In 1966 she attempted to publish a summary of her perspectives on the evolution of complex life forms in “The Origin of Mitosing Eukaryotic Cells,” only to be rejected by more than a dozen scientific journals. When her article was finally published by the Journal of Theoretical Biology, criticism ensued. Nonetheless, the further Margulis pushed her symbiotic evolutionary theory, the more convinced she became that the emergence of eukaryotic cells a billion and a half years ago—a major evolutionary transition in the history of life—was the result of symbiogenesis.

In Margulis’s view, out of prokaryotic–prokaryotic symbiosis emerged eukaryotes. Out of prokaryotic–eukaryotic symbiosis emerged more competitive eukaryotes. And out of eukaryotic–eukaryotic symbiosis emerged multicellular life. The classic image of evolution, the tree of life, almost always exclusively shows diverging branches; however, a banyan tree, with diverging and converging branches is best. To this day, many scientists and most laypeople remain ignorant of this way of imagining evolution, which profoundly constricts how they imagine themselves.

Most of the mass of our DNA is “ours” because there are many more cells making up our body than there are composing the microorganisms living in and on our body. Nonetheless, most of the genetic diversity in and on our body is not ours. Rather, it is found in the microscopic organisms with which our body interacts to maintain optimal health. Eyelash mites, skin fungi, gut bacteria, and more all work in harmony with us. “Each one of us is a massive colony of microorganisms,” Margulis explained. “Former protists are now eloquently orchestrated animals with fancy tissues and organs.”

Some of Margulis’s most vivid contributions to a richer understanding of evolution appear in her books Symbiotic Planet: A New Look at Evolution (1999) and Acquiring Genomes: A Theory of the Origins of Species (2002). In Acquiring Genomes Margulis describes, for example, the evolutionary integration of genetically distinct bacteria onto the surface of a genus of ciliated saltwater microorganisms called Euplotidium. All six species of Euplotidium bear surface bacteria that act like archers defending the royal Euplotidium castle. When Euplotidium species sense approaching predators, their surface bacteria react by shooting out ribbons of protein, like little micron-sized crossbows. The ciliated Euplotidium cannot survive without these protective bacteria, nor do these particular extracellular bacterial organelles appear to exist anywhere except on the surface of the six known Euplotidium species.

Laboratory experiments to cultivate these bacteria removed from Euplotidium have failed; without the association between the two entities, neither could exist. The association that evolved between the ancestors of Euplotidium and its surface bacteria catalyzed the origin of this genus. This kind of symbiogenetic speciation typifies the role that prokaryotes play in the evolutionary history of eukaryotic life. Wherever biologists now look in nature, they find examples of unicellular and multicellular eukaryotes that exist in association with bacteria and algae possessing distinct genomes.

Despite Margulis’s legacy, early 20th-century concepts of “survival of the fittest” continue to determine how evolution is taught and, therefore, how it is understood even by most scientists. Beyond the popular discourse, relatively advanced textbooks devoted entirely to the study of evolution omit the concept of symbiogenesis. The fourth edition of a leading undergraduate textbook of evolution, Evolutionary Analysis (2008), still devotes entire sections to “combat,” “competition,” and “conflict,” neglecting symbiosis. Most high school graduates are taught the term symbiosis, but it is typically presented to mean little more than mutually beneficial cooperation. Students learn how symbiosis benefits individuals, but not how symbiotic relationships themselves often constitute emergent organisms that display their own evolutionary histories. Only evolutionary specialists have universally adopted an appreciation for symbiogenesis.

Recovering the story of evolution goes a long way toward understanding how to maintain the integrity of a living organism. Wherever symbiotic ideas spread, they lead to important new practical insights. Some of the potentially most therapeutic applications of symbiogenetic science today are being directed toward problems of chronic disease. Many medical scientists are drawing inspiration from Margulis’s and others’ symbiogenetic research to reorient approaches to human health, as it becomes clearer that microbes that have evolved symbiotically with humans are integral to our well-being. The dramatic rise in rates of allergies, eczema, ulcerative colitis, and other chronic health problems are increasingly believed to involve a perturbation in the human–microbe relationship, leading in 2008 to the Human Microbiome Project.

Exploring the history of scientists’ attempts to understand evolution reveals neglected insights into the associations between individuals, associations at least as meaningful as the individuals themselves. Now, thanks to Margulis, these insights are finally beginning to percolate from the realm of the lone expert to that of the wider scientific community, the classroom, and even the dinner table. Supporting this trend will benefit our stewardship of human and global ecology. As we disentangle some of our political discursive traditions from our scientific ones, the story of evolution may itself evolve.

Bibliography

  • Huxley, T. H. 1888. The struggle for existence in human society. Nineteenth Century 23:195–236.
  • Khakhina, L. N. 1992. Concepts of Symbiogenesis: A Historical and Critical Study of the Research of Russian Botanists. New Haven, CT: Yale University Press.
  • Kropotkin, P. 1904. Mutual Aid: A Factor of Evolution. Reprint. Hong Kong: Forgotten Books.
  • Margulis, L. 2002. Acquiring Genomes: A Theory of the Origins of Species. New York: Basic Books.
  • Sapp, J. 2002. Symbiogenesis: The hidden face of Constantin Merezhkowsky. History and Philosophy of the Life Sciences 24:413–440.


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