The unselfish genome: the case for cooperating genes

Acquiring Genomes:
A Theory of the Origins of Species
by Lynn Margulis and Dorion Sagan
(Basic Books, 2002; $28.00)

Darwin's Blind Spot:
Evolution Beyond Natural Selection
by Frank Ryan
(Houghton Mifflin, 2002; $25.00)

Ever heard of Demodex folliculorum, a 0.4-millimeter-long mite and a relative of the spiders? Probably not--but if you squint you can get a close-up of one of its preferred habitats. The eyelash mite, as it is more commonly known, lives on almost everybody's face, feeding on dead skin cells and often burrowing into eyelash follicles. And that is not the only creature we share our bodies with. A veritable menagerie of microbes inhabits our various nooks and crannies. Spirochetes live in our gums; staphylococci, micrococci, and a small yeast from the genus Pityrosporon clothe our hides. And then, of course, there's the gut, home to species of bacteria that provide us with, among other things, some of our daily quota of [B.sub.12] and K vitamins. In their most recent book Lynn Margulis, of the University of Massachusetts Amherst, and Dorion Sagan estimate that a staggering 10 percent of our dry weight is made up not of our own cells but of our symbionts.

Acquiring Genomes is full of such marvels of symbiosis. Another good one is the glow-in-the-dark squid Euprymna scolopes. In its belly is a two-lobed spotlight, complete with a translucent muscle covering it and a dark reflector behind. The light (which confuses predators) is emitted by the bacterium Vibrio fischeri, which hatchling squid recruit from seawater with a "welcoming ring" of beating cilia. Without the bacteria the light organs do not mature, and the squid remain unilluminated.

A flamboyant personality, Margulis has never avoided controversy. I once saw her dressed in purple velvet and perched on the edge of the stage at a congress, confronting, with her customary optimistic bravura, a hall full of skeptical bacteriologists. Beginning in the late 1960s, she brought into mainstream biology the idea that cell organelles such as mitochondria and chloroplasts are nothing less than relicts of symbiotic bacteria that were incorporated into the parent cells eons ago. In the ensuing three decades she has been the tireless champion of symbiosis, arguing with some success that other cell components have likewise evolved from bacteria, and that symbiosis is a pervasive and crucial process in evolution. Not surprisingly, then, in Acquiring Genomes Margulis and Sagan once again impress us with the wonders of microbial liaisons.

But their book goes further. The authors maintain that symbiosis is the stuff that evolution is really made of; in their view it should replace random genetic mutation as the main driving force of evolutionary novelty. To put it boldly (and Margulis and Sagan do): it isn't natural selection, but "the unseen beings" that "play the major creative role in the genesis of new species." The changes come about via the fusion of complete genomes, either through integration at the level of the chromosome (like most of the genes in the bacterium that later became our mitochondria) or through their union as joined, co-dependent organisms. The six known species of the single-celled marine organism Euplotidium, for instance, are distinguished from their Euplotes relatives by a band of bumps on their surface, from which defensive ribbons shoot when the Euplotidium are approached by other, predatory protozoans. On close inspection, the bumps turn out to be bacteria that are "body-farmed" by Euplotidium to serve as a defense organ.

Neither Euplotidium nor their bacterial bodyguards can live on their own, and so this life-form clearly evolved when one genome acquired the other.

In spite of such fine examples, however, Margulis and Sagan's argument loses some of its charm when the authors begin to downplay the relevance of natural selection to make way for evolution by symbiosis. Surely the merger of a Euplotes-like ancestor with a live bacterium, giving rise to a new organism, could not have been instantaneous. As with any other close ecological relationship, the merger would have required gradual mutual adaptation (presumably by the natural selection of gene mutations).

But Margulis and Sagan have decided that biology can do away with random mutations, now that a much more powerful originator of evolutionary novelty is available in the form of symbiosis. They maintain that the accumulation of small genetic mutations is virtually always destructive and "does not lead to new species or even to new organs or new tissues." It is a "half-truth whose lack of explicative power is compensated for only by the religious ferocity of its rhetoric"--an assertion that will raise the eyebrows of not a few evolutionary geneticists. And as for natural selection, the authors note that "a staunch resistance to any systematic effort to identify [its causal] agent or agents" persists: a slap in the face at evolutionary ecology.