Evolution by natural selection requires three things:
1. A trait shows variation
2. The variation in that trait must be capable of being passed on from parents to offspring (i.e., the variation is “heritable”)
3. The variation in that trait must make a difference in its likelihood of being passed on from parents to offspring. (Usually, but not always, this requires that the trait affect the survival or reproduction of its carrier.)
If all this is true, those forms of a trait that are better at proliferating will gradually increase in a population.
Although these statements are the basis of Richard Dawkins’s book The Selfish Gene, do note that the above characterization doesn’t use the word “gene.” Even if a trait has a nongenetic basis, it will evolve, via a form of natural selection, if it satisfies these conditions. Much of cultural evolution works in this way, although there are profound difference between cultural evolution based on cultural natural selection (or selection among “memes”) and biological evolution based on genes.
A new paper by John Jaenike and his colleagues in Science, however, shows a form of biological evolution by natural selection that isn’t based on changes in genes. It’s based on changes in the presence of symbiotic bacteria that protect a species from parasites.
The species in which the nongenetic evolution has occurred is the mushroom-feeding fruit fly Drosophila neotestacea in North America:
Fig. 1. Drosophila neotestacea
In the eastern U.S., this fly is afflicted by a parasitic nematode, Howardula aoronymphium (we’ll call it “the worm”), that renders females sterile, reduces the mating success of males, and reduces the survival of both sexes. (Fig. 2 gives a pretty disgusting picture of a worm-infected fly.) The nematode enters the fly larva when both are the mushroom, and persists in the adult fly. Females, attempting to lay eggs then pass the nematode into the mushroom, where it mates and enters other fly larvae, completing the lifecycle.
Fig. 2. D. neotestacea female dissected to show reproductive tract and its huge load of parasitic worms. Photo by J. Adam Fenster, University of Rochester
Based on genetic evidence, the nematode appears to have colonized North America from Europe fairly recently (American worms have much less genetic variation than European ones, but represent a genetic subsample of them). But the worm is present in fly populations throughout North America, and in every population about 20% of the flies are infected with worms.
Some flies also carry another organism: the bacterial symbiont Spiroplasma, which is found in many insects. In D. neotestacea, however, the presence of Spiroplasma protects the fly from the sterilizing effects of nematodes. While flies with worms and no Spiroplasma are virtually sterile, the presence of the bacteria confers almost normal fertility on worm-ridden flies. It’s not yet clear how this works, but worms in flies with Spiroplasma are much smaller than those without the bacteria. Presumably the bacteria does something to the worms (or to the flies) that makes the worms grow much more slowly.
So this is a good setup for natural selection. First, there is variation in a trait—some flies have Spiroplasma, others do not. That trait is heritable, for Spiroplasma are transmitted directly from mother to offspring in the egg (there’s no “horizontal” adult-to-adult transmission). And there’s an environmental factor—the parasitic, sterilizing worms—that cause differential reprodution of flies depending on whether or not they carry Spiroplasma. Those flies who carry Spiroplasma can still produce offspring, and hence pass on the Spiroplasma to the next generation; those flies who don’t carry the bacteria don’t get protection from nematodes, and leave no (or very few) offspring. In the presence of worms, then, there’s a huge selective advantage in flies to carrying bacteria.
You’d expect, then, that in the presence of worms, the proportion of flies that carry bacteria would increase over time. This is a form of natural selection, but it’s selection on flies that carry bacteria. Flies with bacteria are the ones who reproduce; they pass those bacteria on to their offspring, and so the proportion of bacteria-carrying flies goes up. There’s no difference in the DNA of flies who reproduce and those who don’t, so the flies’ genomes themselves are not evolving.
Nor do the bacteria seem to be evolving, although there could theoretically have been mutations in the Spiroplasma that make them kill or inhibit nematodes (after all, any bacteria who could do this would leave more offspring). But population-genetic studies of the bacteria suggest that this hasn’t happened. The bacteria seem to confer resistance to nematodes simply through some innate feature of their biology.
What Jaenike et al. found was that the predicted selection occurred, and caused evolutonary change: the proportion of Spiroplasma-infected flies indeed seems to be increasing within populations in the eastern U.S.. Moreover, the bacteria has started to spread from the eastern to the western U.S. in only three decades. Here’s the evidence:
- Museum specimens of flies collected in the eastern U.S. in the early 1980s show no Spiroplasma (you can screen museum specimens for bacterial DNA). But now, in those same populations, the frequency of flies that carry bacteria ranges from 50% to 80%.
- Worm-ridden flies collected in New York in the 1980s were largely sterile, having the same fertility profile as modern flies that are worm-ridden and don’t have the bacteria. But in modern populations, most flies do carry the bacteria and so are fertile even if they have worms.
- There’s a “cline” (a geographical gradient) in the presence of the bacteria from eastern to western North America. As I mentioned above, the proportion of flies with bacteria is high (50-80%) in the east, gets lower (10-25%) across the Great Plains, and is at or near zero in coastal British Columbia. Given the presence of worms in all of these locations, there would be a strong advantage for the western populations of flies to acquire the bacteria too.
- Finally, genetic evidence suggests that flies in western North American haven’t yet reached their equilibrium degree of bacterial infection (it should be about 0.8—it’s not complete at equilibrium because transmission of bacteria from mother fly to her offspring isn’t perfect).
All this suggests that the bacteria are in the process of sweeping from east to west in the flies through a natural selection-like process. All populations of flies have worms, and should thus have bacteria, but the bacteria are just beginning to go west. This is analogous to a new adaptive mutation working its way through a species. And you can make a prediction: in another two or three decades, all western populations of flies should have a high frequency of Spiroplasma.
At the end of their paper, Jaenike et al. note that this example may suggest strategies for wiping out nematode-caused diseases like river blindness and filariasis (which produces the grotesque swelling of limbs called elephantiasis). Those diseases, too, are transmitted by worm-ridden flies, and perhaps deliberate infection of those flies with bacteria like Spiroplasma could reduce the transmission of nematodes and help wipe out these diseases.
Here, then, we see how a species (the fly) has adapted to an environmental challenge not by changing its genes, but by acquiring a whole genome—the Spiroplasma genome. It’s as if the whole bacterium was an adaptive mutation. And we also have a case of selection in action, one that makes testable predictions. Creationists may dismiss it since it’s not “evolution” in the traditional sense, but it shows the principles of natural selection in any meaningful sense.
Jeanike, J., R. Unkless, S. N. Cockburn, L. M. Boelio, S. J. Perlman. 2010. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212-215