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Chapter Eighteen



A beehive is a collaborative enterprise on far more levels than first appears. —Matt Ridley


You may be under the impression that you have a single set of genes, arrayed along chromosomes in the nucleus of each cell. A common misconception. The nucleus is just one of many little subcellular bodies called organelles. And one kind of organelle the mitochondrion, which processes energy—has its own genes, passed down separately from the genes in your nucleus. Whereas your nuclear genes were drawn equally from your mother and father, all your mitochondrial genes came from your mother. And if you are male, you have no chance of passing them to future generations.

Why on earth would each cell have two sets of DNA? The answer, now generally acknowledged after decades of resistance, is this: Once upon a time, before there were multicelled organisms, the distant ancestor of your mitochondria was a free-living, self-sufficient cell, something like a simple bacterium; and the distant ancestor of the cells the mitochondria now inhabit—your nucleated cells—was also a free-living, self-sufficient cell. Then the two free-living cells merged; the mitochondrion specialized in processing energy, and the larger cell handled other matters, such as locomotion. The two lived happily ever after in blissful division of labor.

I'm such a romantic—always stressing mutual benefit. Some biologists would say that the story as I've rendered it glosses over ugly details. According to the Nobel laureate Renato Dulbecco, the once-autonomous mitochondria are now "subservient to the needs of the cells in which they reside." According to John Maynard Smith and Eors Szathmary, authors of The Major Transitions in Evolution, mitochondria are "encapsulated slaves," subject to ruthless "metabolic exploitation. "

As we'll see, one can argue with such cynical interpretations of the mitochondria's plight, but for now the point is just that biologists actually talk this way—as if a mitochondrion,, a dinky blob presumably lacking sentience, had a plight. What do they mean? In what sense could an organelle be a "slave" that gets "exploited"? You would think, to hear this kind of talk, that a mitochondrion, like a person, has interests that are either served or not served. Is there any sense in which that's true?

Yes, in a Darwinian sense. In Darwinian terms, living things are "designed"—by natural selection—to get their genes into subsequent generations. To serve their "interests" is to aid this genetic proliferation. To frustrate their interests—to "exploit" them, for example is to reduce their genetic legacy.

With this vocabulary in hand, we can apply game theory to biological evolution. When two organic entities can enhance each other's prospects for survival and reproduction, they face a non-zero-sum situation; to the extent that their interests are at odds, the dynamic is zero-sum. In this light we will see that biological evolution, like cultural evolution, can be viewed as the ongoing elaboration of non-zero-sum dynamics. From alpha to omega, from the first primordial chromosome on up to the first human beings, natural selection has smiled on the expansion of non-zero-sumness...



One of the greatest thresholds was the coming of the "eukaryotic" cell. For much of the early history of life, the most complex being was the prokaryotic cell, which persists today in such forms as bacteria. Prokaryotes are a bit slovenly. For example, their DNA is bloblike, constituting a chromosome only in the loose sense. The eukaryotic cell, which went on to be the building block for plants and animals, is more tidy and bureaucratic. Its DNA is arrayed neatly along distinct chromosomes and housed in a nucleus, whence it issues commands that are shuttled forth. The eukaryote has much division of labor, thanks to its many organelles. These include the mitochondria, mentioned above; and, in plants, the green bodies called chloroplasts, which handle photosynthesis and which, like the mitochondria, descended from a free-living ancestor that fatefully merged with another cell.

Back when many biologists doubted the autonomous origins of mitochondria and chloroplasts, the foremost proponent of the scenario was the biologist Lynn Margulis. Margulis contends that various other organelles, too, had free-living ancestors. The nucleus itself may even be an example. Most mainstream biologists doubt that Margulis is right, but then again, not so long ago they were doubting her story about mitochondria and chloroplasts.

Why all the mainstream skepticism? Margulis, for one, believes that biologists (who tend to be male) have a bias in favor of competition, and against cooperation, as the formative force in evolution. She might plausibly use the scientists quoted above, talking about "exploitation" and "subservience," as Exhibit A in her indictment. Though they accept her thesis that mitochondria came about by merger, they still insist that mitochondria are brutally subjugated by dominant partners. Or, to put their claim in the language of biology: they accept that two distinct entities came together through "symbiosis"—which just means "living together"—but insist that the symbiosis is parasitic, not "mutualistic." Or, to put the claim in the language of game theory: yes, it all started with a relationship between two sovereign beings, but the central dynamic has been zero-sum, not nonzero-sum.

Are these stereotypically male biologists right? Not demonstrably. Consider Dulbecco's contention that the "needs" of mitochondria are "subservient" to the needs of the larger eukaryotic cell. It rests entirely on his observation that the actions of the mitochondria are governed mostly by genes in the larger cell's nucleus; the big shots in the nucleus give the orders, and the mitochondrion obediently follows them—the very definition of servitude.

It's true that many instructions governing mitochondria issue from the nucleus. Indeed, as other biologists have noted, some genes that were initially in the mitochondrion, and controlled it from there, seem to have migrated to the nucleus, where they exercise remote control. But, as some of those biologists have also noted, this transfer may have been favored by natural selection because it raised the efficiency of the overall cell. If so, then the transfer brightened prospects for the DNA remaining in the mitochondrion as much as for the DNA in the nucleus—since the overall cell is, after all, the boat in which both kinds of DNA find themselves.

Dulbecco is anthropomorphizing mitochondria. Human beings like autonomy, and often resist control. But there's no evidence that mitochondria have a strong opinion about autonomy one way or the other. The only sense in which they can be said to have "needs" or "interests" is in a Darwinian sense. And in Darwinian terms, they are just as interested in the efficiency of the larger cell as is the nuclear DNA. For both of them, the larger cell is home. The two are locked into a highly non-zero-sum relationship.

The jaundiced view of Maynard Smith and Szathmary also has anthropomorphic overtones, but of a different sort. To back up their view of mitochondria as slaves, they theorize that long ago, at the beginning of the symbiosis, nuclear cells kept mitochondria around "as humans keep pigs: for controlled exploitation." That is: they would let the mitochondria reproduce in captivity, then eat a few, then let them reproduce some more. In this scenario, the cell's current handling of mitochondria—inserting "tapping proteins" to extract energy, rather than eating the whole mitochondrion—is just a higher-tech version of the original enslavement; it is a "more elaborate metabolic exploitation."

But, even granting that mitochondria started out as the subcellular equivalent of pigs, would this really be exploitation? Don't get me wrong. I'd rather be a person than a pig, and I do believe that pigs get the raw end of the pig-person relationship. But that's because when I think about human benefit—and, in a way, even when I think about pig benefit—I think about happiness; and in both species (presumably) a certain amount of freedom furthers happiness. But when we talk about nuclei and organelles, we're talking only about Darwinian benefit, about genetic proliferation. And in Darwinian terms, domesticated species do very well, thank you. There is today a lot more pig DNA around than its undomesticated kin, wild boar DNA. In that sense in the Darwinian sense—getting eaten is the best thing that ever happened to pork. Analogously, the "controlled exploitation" of those proto-organelles may well have boosted their legacy, in which case it wasn't exploitation. Certainly they have lots of descendants today—billions in every sizable animal on earth.

In harping on intra-cellular non-zero-sumness, I don't mean to say that the interests of organelle DNA and nuclear DNA entirely coincide. Though the two spend most of their life in the same boat, they do take separate boats to the next generation. Since a mitochondrion's DNA is passed down only via mothers, its Darwinian interests might be served by biasing reproduction in favor of females, so that daughters were the norm and sons the exception. Even if this sexual imbalance cut down a bit on the reproductive success of the overall organism, the trade-off could still be worthwhile from the mitochondrion's point of view. But the nucleus would take a different view, since it gains nothing by a surplus of daughters.

Hypothetical as this logic may sound, it has actually found incarnation—in plants at least. In various plant species, mitochondria have genes that cause the (male) pollen to abort, biasing reproduction in favor of (female) seeds. That this works against the nuclear DNA's interests is evident in the countermeasures it takes. In some cases, nuclear "restorer" genes have evolved to neutralize the bias by boosting the supply of pollen.

This is a reminder that non-zero-sum relationships almost always have their natural tension, their purely zero-sum dimension. It is also a reminder that biologists such as Dulbecco are not wrong to say that tension can exist between mitochondria and nuclei. But they are sometimes wrong in what they see as evidence of tension, and in leaping to the conclusion that tension is pervasive, when in fact it is a small part of the overall picture...


An excerpt from Nonzero: The Logic of Human Destiny, By Robert Wright, published by Pantheon Books. Copyright 2000 by Robert Wright.