The Tangled Tree

by David Quammen

  But what made the Ettema work controversial among the mavens of early evolution were two other points. First, Ettema’s group reported evidence that cells such as Lokiarchaeota had begun acquiring complexity before they acquired mitochondria. Important proteins, internal structure, the ability to bend around and gobble a bacterium, perhaps. If so, the Great Mitochondria Capture was an effect, not a cause, of the biggest transition in the history of life. Or, anyway, a later event within a cascade of changes. Certain people, such as Bill Martin, would strongly disagree.

  Second, Ettema’s team placed the origin of Eukarya within the Archaea, not beside it. If correct, that meant we were back to a two-limb tree of life, neither of which is the limb we have long cherished as our own. That meant we ourselves are descended from archaeans, a separate form of life, unimagined before 1977. (There are intricate complications to this scenario, involving horizontal gene transfer of bacterial genes into our archaean ancestors before our lineage even began, so that, yes, bacteria are blended into us too—but the essence is still: woops, we are they!) Certain people, such as Norm Pace, would strongly disagree. Carl Woese would disagree too, but he didn’t live long enough to be aggravated by Ettema’s 2015 paper in Nature.

  On a June morning, in a conference room in Toronto, Thijs Ettema described this work to a roomful of rapt listeners, including Ford Doolittle and a few dozen other researchers, plus me. When I saw him later, Ford said, with his usual wry self-disregard: “I’ve drunk the Kool-Aid.”

  Still later, I sat down with Ettema. We talked about his newest work, at that point still unpublished, which pushes the same implications still further: mitochondria as secondary to the big transition, and human ancestry rooted within the Archaea, on a two-limb tree of life. He was quite aware of the opposing views and of how fervently they would be argued. He said: “I’m really sort of preparing for some wind.”

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  In late spring of 2012, Woese’s health began to fail. He was eighty-three, still going to his office at the Institute for Genomic Biology every day, still with the big questions, uninterested in retirement. On a morning in May, he spoke by phone with his friend Harris Lewin, by then at UC-Davis, congratulating Lewin on his election to the National Academy of Sciences. He warned Lewin to beware of the “shitkickers” in Section 61, the Academy’s section to which Lewin had been elected. Section 61 is Animal, Nutritional, and Applied Microbial Sciences, appropriate to Lewin’s background in agricultural biology. Hard to say whether Woese’s “shitkickers” was a genial allusion to scientists wading in cow manure or reflected his grittier feelings toward applied biology generally. Lewin mentioned the call in his memoir of Woese, then wrote: “Sadly, over the next few months, it seemed that Carl’s physical vigor was waning and his mental state was slipping.” Lewin stayed in touch, as well as he could at a distance.

  In early summer, Woese’s health worsened, involving some sort of intestinal blockage, while he vacationed with his family on Martha’s Vineyard. The family took him to Massachusetts General Hospital in Boston, where imaging diagnostics revealed the problem: pancreatic cancer. It was bad, a tumor wrapped into one of the arteries like a strangler fig. He underwent emergency surgery to relieve the blockage, but surgery couldn’t dice out the tumor, not one so closely entangled with arterial walls. What happened next, his final six months, is best seen through Debbie Piper, the administrative assistant who became his factotum and friend during his years at the Institute for Genomic Biology. She helped Woese die as he preferred to, which was neither amid “heroic measures” nor in Massachusetts.

  Debbie Piper’s bond to Woese had grown like an accidental flower in a vacant lot. He didn’t hire her at the IGB or bring her with him from the old lab. She transferred, from a different job, when the institute opened in 2007, and got assigned to the Biocomplexity program, under Nigel Goldenfeld. “I was just sitting at my desk one day, and here comes this little white-haired guy, carrying a bag of books,” Piper told me. “And I said, ‘Do you need some help?’ And he was like, ‘Sure.’ ” They clicked, and became close. “I think he trusted me because I didn’t want anything from him.”

  Piper met me at a coffee shop in Urbana, just down the block from Timpone’s restaurant. She was fiftyish, with graying hair scooped down around her face, and a soft voice, and a firm manner. “He told me once, he said, ‘You know what, Debbie, we’re like family.’ ” But almost better than family, he added, because “we don’t have all that mess.”

  She spoke about how Woese had reacted to his own renown, back in the late 1970s, after he had his fifteen minutes of Warholian fame, in the New York Times and elsewhere, and then suffered what he took as rejection and backlash by the community of his colleagues. “I wasn’t there at that time, but we talked about it a lot.” Thirty years on, Woese’s aggrievement remained. “He had made this amazing discovery,” as she took it from him, “and either people didn’t think it was significant, or they didn’t think it was real.”

  But it was the work, not himself, in Debbie Piper’s impression, for which he still craved renown. He detested (or professed to detest) what he called “the cult of personality” in science. Darwin had been canonized by it. Woese didn’t want that—at least, so he persuaded Piper, who knew him well. Others, who had known him longer and as a scientific colleague, disagree; but she, supportive and forgiving, was there at the end. “He didn’t want his work to be about him,” she told me. “He thought the work should stand by itself.” During the later years, the years of her protectorate, other academics visiting campus would want to meet him, the famous Carl Woese, regardless of their own research fields, their comprehension or incomprehension of his work. Sometimes he told her, “I am not a dancing bear.” He didn’t want to meet people, to bask in adoration. He didn’t want to travel. “He just wanted to be left alone to think.” Piper’s own role at the IGB evolved, with the full blessing of Goldenfeld, toward being Woese’s personal assistant. Whatever he wanted came first. It was odd, she said, because at the beginning, she had no idea who he was, what he did, the extent of his reputation.

  “He was just this guy with the white hair,” I suggested.

  “Just this lone wolf professor with white hair, yeah,” she agreed, “in the office across from me.” As they got acquainted, she had learned he was funny. He was kind. He was private. He was the most intelligent person she ever met, though on quotidian matters, he could be clueless. His mind roamed, who knew where. He was one of the best friends Debbie Piper ever had, and she still missed him terribly. Unpretentious? I wondered. Yes, unpretentious. Then she qualified that.

  “He was not pretentious at all. He was really pretty humble. But then he would say, ‘I have a lot to be humble about.’ ” She laughed.

  A few minutes later, we turned to the hard part. Woese got his cancer diagnosis at the very beginning of July 2012. He had the emergency surgery on July 3, she recalled. “He called me and asked me if I would come out there.” On July 4 she flew into Boston.

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  Among the essential points of the upheaval that Carl Woese helped initiate, and of this book in which I try to sketch that upheaval, are three counterintuitive insights, three challenges to categorical thinking about aspects of life on Earth. The categoricals are these: species, individual, tree.

  Species: it’s a collective entity but a discrete one, like a club with a fixed membership list. The lines between this species and that one don’t blur.

  Individual: an organism is also discrete, with a unitary identity. There’s a brown dog named Rufus, there’s an elephant with extraordinary tusks, there’s a human known as Charles Robert Darwin.

  Tree: inheritance flows always vertically from ancestor to descendant, always branching and diverging, never converging. So the history of life is shaped like a tree.

  Now we know that each of those three categoricals is wrong.

  Biologists have argued for a long time, long before molecular phylogenetics began complicating matters
, about how to define species. The concept dates back at least to Linnaeus and, in looser forms, to Aristotle. Him again! But never mind the deep philosophical and etymological history. As used by Linnaeus in his classification system, during the eighteenth century, a species was an entity (an aggregation of creatures, but still an entity) that had constancy and essence. Darwin in the nineteenth century, with help from Wallace and others, dismissed that sort of idealism, persuading people that species change, species originate and depart, species consist of individuals that vary from one another, sharing a certain degree of similarity but no ineradicable common essence. In the twentieth century, a clarified definition of species was offered by Ernst Mayr, whom I mentioned earlier as one of the founding neo-Darwinists. Mayr’s view carried weight because, besides being an eminent evolutionary theorist, he authored books on the history of biology, often writing himself into the saga in respectful third-person singular. Mayr’s famous 1942 definition was: “Species are groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups.” You know enough by now to see two problems with that definition.

  First problem: it’s inapplicable to bacteria and archaea, which don’t “interbreed” in anything like the way implied by Mayr. Second problem: How can “reproductively isolated” be an absolute standard if genes are continually transferred horizontally (by viral infection and other mechanisms) and if, furthermore, members of one species sometimes breed with members of another, producing new lineages of hybrid offspring? (Such hybridizing happens often among plants and sometimes among animals.) Answer: reproductive isolation is a useful and intuitive standard, yes, but not an absolute one.

  Take Homo sapiens, the species most dear to our hearts. In the era of DNA sequencing, scientists have recognized that the human genome contains evidence of hybridizing events. Homo neanderthalensis, Neanderthal man (and woman), was discovered in 1856, named in 1864, and for many decades considered a discrete species, closely related to us within the hominid family, but distinct. Some experts now consider the Neanderthals to have been a subspecies of Homo sapiens, more properly called Homo sapiens neanderthalensis, but others argue that Homo neanderthalensis is still the right label, representing the group as a full species. In any case, our lineage diverged from their lineage sometime between about three hundred thousand and six hundred thousand years ago, maybe more, when pioneers left Africa and colonized Eurasia. From those pioneers would descend several non-African species, including Homo neanderthalensis. Our own lineage, known as “modern humans,” sent another wave of dispersers out of Africa and colonized Europe again, but much later, around fifty thousand years ago. Then, for one reason or another, the Neanderthals disappeared.

  Paleoanthropologists have long speculated that either our ancestors killed off the Neanderthals, by direct aggression, or forced them to go extinct, by competition, or else absorbed them to some degree, by interbreeding. But there was no conclusive proof. Nowadays, since the recovery and sequencing of Neanderthal DNA by a team including the Swedish biologist Svante Pääbo, analyses indicate that hybrid matings did occur between Neanderthals and modern humans. The human genome, especially as found among non-African peoples descended from those hybrid matings, now contains about 1 percent to 3 percent Neanderthal DNA.

  And it’s not just Neanderthals in our genome. The human lineage diverged from the chimpanzee lineage seven million, or ten million, or maybe thirteen million years ago—nobody knows the timing with any precision. But recent genomic analysis suggests that, sometime well after the big split, hominid ancestors and chimp ancestors came back together for hybrid matings, and that those hybrid matings have left genuine chimpanzee genes (not just close human equivalents) in parts of our genome. The imprecise dating of the full divergence, in fact, may owe to the ratcheting stages by which it happened. As a consequence, some parts of our genome even today look more chimp than human. This knowledge tends to blur our prideful and categorical confidence that Homo sapiens is a discrete entity, produced through gradual evolutionary processes but now standing alone in space and time. We’re not so discrete, not so alone. Svante Pääbo calls our genome a mosaic. He wasn’t the first to use that metaphor in the realm of genomics, as I’ve noted, but when applied to us, it carries a peculiarly strong challenge to selfhood.

  Of course, the presence of chimpanzee genes, or Neanderthal genes, isn’t the half of it. There’s also that viral DNA—including syncytin-2, a gene co-opted from a retrovirus, repurposed to enable human pregnancy. The fact that endogenous retroviruses constitute 8 percent of the human genome certainly complicates our sense of Homo sapiens as a species of primate.

  It complicates our sense of human individuality even more. So does the recognition that each of us contains, as a necessity for health and digestion and other aspects of our physiology, some hundred trillion bacterial cells, representing thousands of different bacterial “species.” And so does the realization that within every one of our human cells reside captured bacteria, long since transmogrified into mitochondria, without which we couldn’t exist.

  Biologists and philosophers of science have struggled for a long time, and continue struggling, to define and clarify the concept of an “individual” in biological terms. Some have argued that it’s crucial to have such a definition, because the logic of evolution by natural selection—Darwin’s core principle—depends on the differential survival and reproduction of . . . individuals. If so, what is an individual? Is a single bacterium an individual? Carl Woese and Nigel Goldenfeld teased at that question in their 2007 paper “Biology’s Next Revolution.” Sorin Sonea, the Romanian who argued that all earthly bacteria constitute a single “superorganism,” a single interconnected genetic entity, would say no, bacteria considered one by one are not individuals. Is a worker ant, incapable of reproducing itself, living its life to maximize the reproductive output of the queen ant, an individual? Or is the ant colony itself an individual? Is it another “superorganism”?

  What about a Portuguese man-o’-war, that peculiar relative of jellyfish, floating the ocean surface like a swim bladder with stinging tentacles? An individual? It seems so, but biologists who study these things tell us that, no, a Portuguese man-o’-war is not. It too, like an ant hill or a termite community, is a colony of individual creatures (in this case, small multicellular forms known as zooids), aggregated for a common purpose and variously performing specialized functions. Likewise that very strange thing known as a cellular slime mold, which during one phase of its existence looks and behaves like a garden slug, but at another phase reveals itself to be a fine-tuned team of individual amoebae. When food is scarce, the amoebae aggregate into the slug, unified in their effort to crawl toward better habitat, raise a stalk atop which sits a fruitlike body, and, when that opens, disperse spores. If the spores land in a place where food particles (bacteria) are available, they awaken as new amoebae.

  Likewise again with aspen trees in a grove. They may look like individuals, but, in fact, aspens grow as clonal eruptions from underground rootstock, all interconnected, all sharing the same genome, sometimes including hundreds of trees across a wide area. The grove is the individual. By one accounting, the largest organism on Earth may be a single aspen clone composed of thousands of trees spread across more than a hundred acres in Utah’s Fishlake National Forest. It weighs about thirteen million pounds, this aspen individual, and is roughly eighty thousand years old.

  These cases and others illustrate what the philosophers of science confront in their erudite papers: The meaning of “individual” is hard to define, except on a case-by-case basis, and not so easy even then. Coral might be ambiguous. Lichens might be ambiguous. Everyone agrees that puppies are individuals, owls are individuals, humans are individuals, until you consider the disquieting molecular facts. We are mosaics, as Pääbo noted, as Bill Martin said, not individuals.

  And then there’s that third challenged categorical; the tree of life. You’ve read
here the reasons why it doesn’t, in fact, look like an oak. Why it doesn’t look like a Lombardy poplar. Even aspens in a grove make an unsuitable metaphor because, though interconnected underground, they don’t reconnect above. Their roots form a network, but their limbs and branches only diverge, growing away from one another, seeking open space in which their leaves may harvest light. They don’t converge, they don’t inosculate, not in the wild—not like John Krubsack’s grafted box elders or Axel Erlandson’s grafted sycamores. The tree of life is not a true categorical because the history of life just doesn’t resemble a tree.

  Carl Woese knew that, though it wasn’t among his highest priorities to say so. He interested himself in big limbs, not small branches. And of big limbs, in his view, considering the past four billion years, there were three: Bacteria, Eukarya, Archaea. Those three diverged from the last universal common ancestor of all life as we know it—life on Earth, life using one common genetic code, life that began with the RNA-world and then yielded cells and passed through the Darwinian Threshold and became very complex. One of the ironies of Carl Woese’s career, it seems to me, is that although profoundly interested in complexity and how it arose—infatuated with complexity theory and emergent properties late in his life, when he collaborated with Nigel Goldenfeld—he was also deeply entranced by simplicity. Three living domains, from which all else results: that’s simplicity. His holy trinity. It’s almost religious.