Coevolution and gene flow
Two species coevolve when changes in either lead to changes in the other. This includes "arms races" between species that compete with each other, but also interactions that benefit both species. "Gene flow" is the movement of genes from one population into another, of the same or related species. For example, some genes in modern cows seem to have come from mating with wild aurochs, before they went extinct. Gene flow often provides new genes; some may be useful to the recipient population. For example, pollen from transgenic sugar beets could transfer herbicide resistance (along with other crop genes) to related weed beets. More often, genes that were useful in the source environment may be harmful to the recipient population. Natural selection will tend to eliminate these, unless gene flow rates are too high. For example, if plants growing on toxic soil around an old mine are outnumbered by neighbors on nontoxic soil nearby, gene flow may swamp natural selection, preventing evolution of tolerance to toxic soil.
This week I'll discuss a review article on coevolution and then an experimental paper showing how gene flow can affect coevolution. The review is "Variable evolution" by Elizabeth Pennisi, published in the May 4 issue of Science. It discusses coevolution of wild parsnip with the webworms that eat them and coevolution of pine trees with birds and squirrels, among other topics.
Like most plants, wild parsnips produce natural insecticides that keep most insects from eating them. 150 years ago, webworms that eat parsnips followed them to America from Europe. Although The Origin of Species was published two years later, nobody at the time was paying attention to how webworms affected the evolution of wild parsnip. But, fortunately, botanists were collecting plant samples and preserving them in herbariums.
Samples of plants, soil, etc. collected over time are really valuable sources of information. They are often used for answering questions that couldn't even have been asked, much less answered, when the samples were collected. The long-term experiments at Rothamsted (UK) have collections of crop and soil samples going back over 150 years. Analyses of soil samples collected there before pH was even defined as a measure of acidity show gradual acidification of the soil with some fertilizers. Similarly, herbarium samples have shown how plants have changed in response to rising CO2.
It's too bad that such collections often get thrown away. That's what had happened to Hans Jenny's old soil samples, when a colleague went looking for them to figure out why cotton yields were decreasing in California. My former department even talked about getting rid of our herbarium, to make room for a new molecular biology lab. It's ironic, because molecular methods have greatly increased the amount of information we can get from old samples. For example, scientists at Rothamsted have used molecular methods to count fungal pathogen spores in wheat samples collected over decades. When I helped set up the UC Davis Long-Term Research on Agricultural Systems experiment, I collected soil samples using sterile sampling methods, so that DNA in the samples could someday be used to study the ecology and evolution of soil microbes in response to agricultural practices. Robert Norris collected and saved weed seeds so that future weed scientists could study their evolution.
But back to webworms. When Arthur Zangerl and May Berenbaum, both of the University of Illinois, analyzed old parsnip samples from herbaria, they found that toxin levels had increased soon (within 20 years) after the webworms arrived. Since then, the webworms have also evolved, so they are now mostly resistant to the parsnip's natural insecticides. Webworms in Europe haven't evolved as much resistance, because there they mostly eat a less toxic plant.
There's a lesson here for those interested in herbal remedies. Many of the chemicals that make plants useful as drugs (caffeine and aspirin, for example) are natural insecticides that tend to evolve rapidly. "Ancient wisdom" about the value of certain herbs in medicine may have been true at the time. But the plants have evolved since then, so they need careful testing again, using statistically valid methods, of course. Furthermore, the same species may have very different chemical properties in different places. Wild parsnips differ between America and Europe, but differences over much shorter distances can also be important.
For example, Pennisi's review discusses how coevolution of pine trees and birds varies across the western US. The birds open pine cones to get the seeds, which they eat. But they also hide a lot of seeds, some of which grow into new trees when the birds forget where they hid them. On balance, this is a good deal for the pines, so they have evolved cones that are easy to open. But not everywhere.
Where squirrels are common, as well as birds, coevolution has led to cones that are harder to open. Maybe squirrels have better memories, and return to eat most of the pine seeds they stash? Whatever the reason, we end up with what John Thompson called a "geographic mosaic of coevolution", a patchwork of areas where coevolution has, or does, vary in rate or even direction.
How does gene flow affect coevolution? That is the subject of a paper in the June issue of The American Naturalist. Samantha Forde, John Thompson, and Brendan Bohannan, of UC Santa Cruz and the University of Oregon, showed that "Gene Flow Reverses an Adaptive Cline in a Coevolving Host-Parasitoid Interaction." Does that sound a little more intimidating than "Variable Evolution"? Well, American Naturalist is a more specialized journal than Science.
We often see trends across landscapes in coevolution between species. These "clines" are hard to interpret. Is some physical factor affecting the evolution of one or both species? Have two parts ("populations") of a species that evolved separately for a while come back into contact as warming climate re-opened a mountain pass? Or is gene flow important, for one or both species?
Forde and colleagues set up an experiment in which these factors could be controlled. They used the gut (and lab) bacterium E. coli and a virus, T7, that infects it. (Although lab strains of E. coli aren't very dangerous, someone needs to find a bacteria that's as easy to work with as E. coli, but can't grow in humans!) The bacteria can evolve resistance to the virus, but then the virus can evolve so that it attacks the "resistant" bacteria, and so on. Both species evolve faster in food-rich environments, because a higher growth rate leads to larger population size. If one in a million is a mutant, then the more bacteria, the more different mutants natural selection will have to select among.
After letting bacteria and viruses evolve together in rich, medium and poor environments (flasks differing in nutrient supply), they tested viruses from the rich environment, to see how well they infected bacteria from the three environments. The bacteria from the low-growth environment hadn't evolved as much resistance as those from the high-growth environment, so they were easier prey for the virus. Imagine a nuclear submarine attacking a WWI battleship.
That was without gene flow. But when they allowed a few of the bacteria and viruses to move between flasks, the trend reversed. With gene flow, viruses from the high-growth environment did worse on bacteria from the low-growth environment than on those from their own environment. Gene flow would have transferred resistance genes to bacteria in the low-growth environment, and apparently the bacteria from that environment had some additional differences to which the high-growth virus was not adapted.
The paper has additional data on the infection success of viruses from the low-growth environment, and on the effects of gene flow among environments that all have the same growth rates.
Can we generalize from these results to coevolution with gene flow in natural landscapes? There may be valid theoretical arguments one way or the other. But I would apply the same criterion proposed in previous posts: I would like to see whether other labs, doing similar experiments but with different species, get similar results. The great thing about microbes is that multigeneration evolution experiments can be done in days or weeks rather than years.