Independent populations that colonize similar environments and then evolve similar traits provide strong evidence for a deterministic response to natural selection. The resulting pattern has been variously called “parallel” or “convergent” depending on similarity among the starting populations and on one’s preferred definition.*
As parallel evolution provides some of the most convincing evidence for the power of natural selection, finding it has become a rite of passage for evolutionary biologists working in any given natural system, and it is a common stamp of approval for authors publishing on adaptation. Over the years, I have probably seen more than a hundred papers that examine phenotypes from multiple populations in two or more environments. Some statistical model is applied to the data and the main effect of “habitat type” is examined with great expectation. When this effect is significant, the paper trumpets its success in documenting the power of natural selection in shaping the diversity of life.
What often strikes me about such papers, however, is that the population means of the different habitat types often overlap considerably. That is, some populations in one habitat type have larger traits values and some have smaller trait values than populations in the other habitat type. This pattern implies to me that the coarse classification of habitat type is, in reality, not very predictive of phenotype and that many other factors must also be involved. Sadly, investigators rarely embrace and explore – or even acknowledge – this unexplained variation. We recently published a paper* that does so, and I was prompted to make a blog entry about it as a result of my seminar visit last week to the University of Connecticut.
Parallel/convergent evolution was a common theme in discussions with many UConn folks. Some labs studied situations where different organisms occupy similar environments and so would be expected to evolve similar traits (Schlutz lab: adaptation to the osmoregulatory challenges of fresh versus salt water by stickleback and alewives). Other labs studied situations where similar body forms evolved independently and so one would expect similar selective pressures to have been the cause (Jockush lab: large and small bodied skinks of different lineages in California). In South Africa, the plant genus Pelargonium is highly variable in leaf shape and growth form (Schlichting and Holsinger labs). So variable, in fact, that I (as a non-plant person) would never have imagined that they would all be in the same genus. Presumably all of these different shapes and forms in Pelargonium are the result of adaptation to different environments, and yet species with very different growth forms can be found side-by-side in the same environment. (OK, I only saw them in a greenhouse but I am told this is true in nature.) If adaptation is the cause of this group’s radiation, then why are two plant types of very different form found in the same environment? This dramatic non-parallelism is just the sort of thing I am talking about.
To investigate non-parallelism, Renaud Kaeuffer, Dan Bolnick, Katie Peichel, and I quantified ecological (diet), morphological (body shape, trophic traits, armor traits), and genetic (neutral and QTL-linked microsatellites) variation in each of six independent lake and stream population pairs of threespine stickleback*. Some traits were remarkably parallel. For example, all lake populations had stickleback with shallower average body depths than did all stream populations (no overlap in the population means). Other traits, however, were decidedly non-parallel. For example, the main effect of habitat type (lake or stream) explained essentially none of the variation in armor traits. So what is the cause of this variation in parallelism? By relating divergence in morphological traits to the degree of ecological divergence, we were able to show that deviations from non-parallelism are mostly likely the result of variation in selection. That is, variation in parallelism is caused by selective factors that do not map so cleanly onto the coarse habitat type classifications that we (and possibly other investigators) typically use. We are not the first group to find this, of course, but we certainly have fun embracing it.
The pressing question to my mind is just how common and strong are these effects? How similar will be the physiological adaptation of alewives and stickleback? To what extent is the variation in skink body shape the result of adaptation to particular environments – as opposed to some other effect? Is the variation in growth form in Pelargonium the result of variation in microhabitats with a general location – or is it the result of some other historical contingency? To what extent does variation in gene flow cause deviations from parallel evolution. We previously found this last effect to be strong in lake and stream stickleback, and it also seems critical in Mark Urban’s salamanders.
Just how parallel is parallel evolution – and why?
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