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Symbiosis at the Heart of Change

Photograph: Michael Seljos

So you meet an accomplished genius who spews out visionary yet seemingly unsupported ideas. You try to grasp them, but they seem too expansive, too glittery, too smooth. Still, even as others are muttering that this time she has gone too far, you suspect she might be right. This happened to me when, in the early 1990s, the biologist Lynn Margulis elaborated a sweeping claim: symbiosis lies at the explanatory heart of evolution.

Now I know she was right. Mainstream scientists are starting to accept her insights, although they don’t always give her credit. Charles Darwin thought that a more mechanistic and random process, “descent with modification,” accounted for the origin of species. Populations (e.g., his much-studied barnacles) vary, and natural selection favors some variants over others. With time, variation, and natural selection, new forms arise.

In the first part of the twentieth century, Thomas Hunt Morgan and his collaborators established that genes, which seemed to govern specific traits, were a source of Darwinian variation. Others found that genes change due to a process called mutation. Neo-Darwinists combined the existence of genes and mutations to develop the idea that populations contain genetic variation derived from random mutations. Evolution happens when something changes: the climate gets warmer, thus more heat-tolerant variants reproduce at a higher rate; or pollution darkens tree trunks, making lightly colored moths more visible to hungry birds that eat more of them, leaving darker moths to reproduce. These are well-documented examples of gradual descent with modification. In 1942 Julian Huxley drew together the work on gradual changes of gene frequencies in populations, the random nature of mutations and populations, and other findings in a book called Evolution: The Modern Synthesis. A hallmark of the modern synthesis (often called the new synthesis) is that species originate gradually via small changes in form.

 

We must look to symbiosis to understand a critical aspect of evolution.

 

But in their 2002 book Acquiring Genomes: A Theory of the Origins of Species, Margulis and Dorion Sagan maintain that combining random mutations with natural selection at best explains changes of form only within existing species (more black moths and fewer white). Though the new synthesis continues to generate sophisticated science, Margulis insists that it does not properly account for the appearance of new species. She contends that we must look to symbiosis to understand this critical aspect of evolution.

For more than twenty-five years, Margulis has argued that the wholesale acquisition of new genomes provides the source of inherited variation underlying the evolution of new species. Life forms begin with this symbiosis, cases in which two or more unrelated organisms develop long-term physical associations. Sometimes one is virulently parasitic and kills the other. But in other cases the relationships between parasites and hosts or predators and prey modulate to the point that they need one another to survive.

Imagine a single-celled organism such as an amoeba. It has its own DNA and normally lives by eating bacteria. It might occasionally engulf an alga, a green cell that nourishes itself via photosynthesis. The amoeba ends up with two genomes, its own and that of the alga. The amoeba can now nurture itself in two ways—by engulfing bacteria or via photosynthesis. At first, the amoeba and the alga merely enjoy one another’s company, but over time each of these cells loses the ability to live independently. A new organism, with DNA from very different sources, results. Theorists call such an evolutionary jump in form symbiogenesis.

The examples are fascinating. Consider the green slug, Elysia viridis. Welcome these to your garden because instead of eating plants they capture carbon from the air using chloroplasts, which they permanently acquired from the algae their ancestors used to eat. Likewise admire any of the twenty-five thousand species of lichen, each of which represents the permanent interlinking of a fungus with a green alga or photosynthetic bacterium. This association was demonstrated by Beatrix Potter, revered for her children’s books but neglected as a scientist.

Granted, lichens and green slugs are strange creatures. What about something closer to home, say a large vertebrate such as a cow? With the help of dozens of microbial symbionts in their multi-chambered stomachs, cows and other ruminants, including giraffes, antelopes, and some kangaroos, turn plant cellulose into energy. Mice need bacteria to complete intestinal development. And humans have a permanent partnership with more than 150 species of gut bacteria and maintain a looser relationship with a good 800 additional bacterial groups. The reciprocity can be intricate: a common human gut symbiont, Bacteroides thetaiotaomicron, makes a molecule that promotes new blood vessel development while also killing Listeria, a major competitor bacterium that can also be lethal to humans.

What is more, the mammalian brain may depend on microorganisms and microbial signals to regulate behaviors such as sociality and self-grooming. Right now we are working with clues rather than clear proof, but the glimmers are stunning. Over the past two years, the National Institute of Mental Health has funded seven pilot studies (mostly using model organisms such as fish and mice) to study the microbiome-gut-brain axis. All of the studies aim to elaborate on some things we already know about gut symbionts: gut cells make large amounts of neurotransmitters, which may affect brain function; gut microbes make molecules that promote immune cell activity, which affects neurophysiology; and gut microbes produce cells that can change activity in the blood-brain barrier, a structure that protects the brain against infection and inflammation.

Margulis and others developed what I call their new new synthesis in the shadows of contemporary evolutionary theory, which has dismissed symbiogenesis as a small story about tiny plants and animals. But since 2014 two major statements by well-known evolutionary and developmental biologists have placed the new new synthesis front and center. In a formal debate in the journal Nature, the new new synthesizers argued the urgency of including the latest understandings of ecology, development, multi-genomic inheritance, and more in a transformed account of evolution. In opposition, mainstream evolutionary biologists, while not denying the new information, held that the evolutionary synthesis developed in the 1930s and ’40s can accommodate the evidence brought forth by the challengers. We may be witnessing a moment in science that philosopher Thomas Kuhn called a paradigm shift.

This is very exciting, and yet I note with dismay the near lack of reference to Margulis’s work in these papers. One doesn’t mention her at all, and the other refers only to her early award-winning work on cellular evolution. These two papers erase the fact that since the early 1990s she has made detailed and compelling arguments supporting the symbiogenetic basis for the origin of species. Historian of science Margaret Rossiter (herself under-recognized) wrote about this phenomenon in a piece entitled “The Matthew Matilda Effect.” Renowned sociologist of science Robert Merton coined the term the Matthew Effect (from Matthew 13:12—“for whomsoever hath, to him shall be given . . . but whomsoever hath not, from him shall be taken away”) to describe the over-recognition of scientists at the top of their professions. Merton’s study—ironically using data from his wife Harriet Zuckerman’s dissertation—showed that a well-known person is often given credit for work done by a more junior collaborator. Rossiter used the life and work of suffragist and abolitionist Matilda J. Gage to draw attention to the fact that this often happens to women.

It is thrilling to see the gathering evidence behind Margulis’s ideas, foretelling change and fresh thought in the field of evolutionary biology. Likewise it is amazing to observe a Kuhnian paradigm shift in the making. So it is especially galling to have these pleasures interrupted by the Matilda Effect. May the day come sooner rather than later when such a distraction will be a distant memory.

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