Under the mistletoe, coevolution is about s and m

Plants and plant products, from sprigs of holly to pine boughs, have been traditional winter holiday decorations since before Christmas became Christmas. Nowadays, if we don't resort to plastic imitations, we deck our halls with garlands from a nursery and a tree from a farm. But seasonal decorations have natural histories apart from mantelpieces and door frames—ecological roles and, yes, coevolutionary interactions with other species.

Mistletoe. Photo by Ken-ichi.

One good example is mistletoe, whose white berries contrast nicely with holly's red ones, and whose traditional association with kissing is probably responsible for more holiday party awkwardness than anything short of rum-spiked eggnog. Mistletoes are parasites, rooting in the branches of trees and shrubs to make a living at the expense of those hosts.

This sort of intimate interaction might be expected to result in coevolutionary natural selection between mistletoe and its hosts, potentially creating very specific pairings in which individual mistletoe species are only able to infect one or a few host plants with particular immune responses and defense chemistry. Yet mistletoe is dispersed by birds, which like to eat mistletoe berries, or can carry mistletoe seeds in their feathers—so seeds from a single plant might end up on a wide range of hosts. This means the specificity of mistletoe's host associations is determined in a tug-of-war between selection from individual hosts and gene flow created by wide-ranging seed dispersal.

In population genetics models, we usually use s to represent selection, and m to represent gene flow, or migration. If s from an individual host species or the local climate is stronger than m, it creates local adaptation to those conditions. But even relatively small m from populations experiencing different conditions can wipe out that local adaptation. So in the case of mistletoe, does s win out, or does m?

One approach to answer this question would be to experimentally infect a range of host plants with a particular mistletoe, and compare their success. But with long-lived host plants, this method would be slow and expensive. Conveniently, local adaptation of mistletoe to individual host species should mean that mistletoe collected from different hosts is more genetically differentiated than mistletoe samples from the same host. And that's quite a bit easier to test.

A 2002 study [PDF] of one North American mistletoe species found exactly this pattern. Coauthors Cheryl Jerome and Bruce Ford sampled dwarf mistletoe, Arceuthobium americanum from several host trees—Jack pine, ponderosa pine, Jeffrey pine, and two subspecies of lodgepole pine—growing across North America. They found that almost a third of the genetic variation they found in A. americanum was distributed among hosts—that is, it could differentiate dwarf mistletoes collected on one host from dwarf mistletoes collected from another.

A lodgepole pine branch supporting dwarf mistletoe in the Uinta Mountains, Utah. Photo by Fool-On-The-Hill.

Within these "host races," geographic distance did have an isolating effect, but the effect was not as strong as that attributable to host differences. When Jerome and Ford examined the population genetics of the three principal A. americanum host trees—Jack pine and the two lodgepole pine subspecies—they found less differentiation than in mistletoe from the same populations [$a]. That suggests that, although coevolution with the trees strongly shapes mistletoe's genetics, mistletoe infection is only one of many selective pressures acting on the host trees.

Although this approach is frequently used to test for coevolution, it isn't entirely conclusive. The observed pattern of genetic differentiation in dwarf mistletoe on different host species could also arise if the A. americanum host races have climactic requirements that closely mirror the distribution of their respective hosts, or if birds carrying mistletoe seeds tend not to move the seeds between host species. Other indirect approaches exist to test these alternatives, but (so far as I can find) they haven't been applied to dwarf mistletoe.

References

Jerome, C., & Ford, B. (2002). The discovery of three genetic races of the dwarf mistletoe Arceuthobium americanum (Viscaceae) provides insight into the evolution of parasitic angiosperms. Molecular Ecology, 11 (3), 387-405 DOI: 10.1046/j.0962-1083.2002.01463.x

Jerome, C., & Ford, B. (2002). Comparative population structure and genetic diversity of Arceuthobium americanum (Viscaceae) and its Pinus host species: insight into host-parasite evolution in parasitic angiosperms. Molecular Ecology, 11 (3), 407-20 DOI: 10.1046/j.0962-1083.2002.01462.x