The rise and fall of parallel evolution: dispatches from Belgium and Texas.

Evolutionary biology has traditionally sought support for the power of natural selection through evidence that similar phenotypes evolve in similar environments: flying animals all have wings, cave organisms predictably lose their eyes and pigments, and birds on small islands often lose their wings! If similar traits evolve in similar environments despite independent origins, then surely natural selection is overwhelmingly powerful in shaping the deterministic evolution of organisms. This pattern is generally called “parallel” when it occurs from similar ancestors and “convergent” when it occurs from different ancestors. (Although some interpretations focus more on whether similar [parallel] or different [convergent] genetic changes are involved.) In this vein, countless studies have reported parallel or convergent evolution and thereby provided overwhelming evidence for the power of natural selection.

I will here argue that parallel evolution is – or should be – on the wane. I don’t mean this in the simple semantic sense that evolution is never parallel but is instead convergent; as has been recently argued by a number of authors. I instead mean it in the more subtle, but probably more important, sense that parallel (and convergent) evolution is much less parallel (and convergent) than is normally promulgated – and that evolutionary biologists are increasingly realizing this fact. My inspiration to revisit this topic (see the earlier post) stems from meetings I recently attended in Leuven, Belgium, and Austin, Texas.

The typical approach in studies of parallel or convergent evolution is to test whether independent populations that have evolved in similar environments (or habitats or food types) are more similar than independent populations that have evolved in different environments. If a statistically significant effect of “environment type” is found across such populations, then parallel evolution is invoked. The trouble with using this result to invoke parallel evolution is that independent populations in similar environments, although often superficially similar, do show many subtle (or even obvious) differences. Wings look extremely different for pterosaurs, bats, birds, and insects! Not all cave organisms lose their eyes!  Not all birds on small islands lose their wings! Has our need to invoke the power of selection blinded us to the fact that evolution is not very predictable? Or, in short, how parallel (or convergent) is parallel (or convergent) evolution, really?

Several talks at the Leuven meeting invoked parallelism (or convergence): spiders in Hawaii, spiders in Galapagos, beetles in salt marshes, stickleback in freshwater, and many others. In most cases, however, examination of the data made clear that although all evolution generally occurred in roughly similar directions, the independent populations colonizing similar environments were never the same either morphologically or genetically. That is, they might share some phenotypic or genetic similarity but the differences among different populations in similar habitats were often, to my eye, as striking as the similarities. A couple of talks near the end of the meeting brought this to the idea to the front of my brain and thus precipitated this post. First, Joop Ouborg showed that the genetic basis for inbreeding depression was almost entirely non-overlapping between different plant species. Second, Freddy Chain showed that lake-stream stickleback divergence in five independent watersheds was almost entirely non-parallel at the genetic level. In short, the fact that evolution is generally non-parallel (or non-convergent) is remarkably parallel (or convergent).

Of course, these are just my interpretations and I have to confess that I have been wrong before – even quite recently. Take grappa, for instance; that crazy Italian drink made by fermenting the leftovers from the pressing of grapes to make wine. Distinctively musty, this drink is quintessentially Italian and is wonderful when drunk for the first time late at night in downtown Napoli surrounded by locals cheering their football team against Barcelona. Or is grappa really that good? Maybe I just liked it because of the context and novelty. Indeed, subsequent consumptions of grappa have further separated the drink from the context and somewhat decreased my enthusiasm. Well, I told the above sad tale at dinner to Nelson Hairson, Luc De Meester, and Isabelle Olivieri right after Nelson ordered grappa. Bah, says Nelson, grappa is good even outside of the context. Ok, then, I challenged him, name three mainstream drinks worse than grappa. And then Isabelle had a brilliant idea – Nelson should pick one drink on the menu that was worse that grappa. That will get him, I figured. So Nelson takes a careful academic look at the menu and pronounces that “Spiriteux de poivre” would be worse. So we ordered this drink and passed it around the other end of the table, where they had not heard our argument and didn’t know what the drinks were: a single-blind experiment if you will. And the verdict: grappa was not very good – but Spiriteux de poivre was infinitely worse.

The Texas gunslinger re-envisioned

Back to parallel evolution. The idea that (even) parallel evolution is often non-parallel was the focus of the meeting that I had in Austin with Dan Bolnick, Yoel Stuart, Dieta Hanson, Rowan Barrett, and Katie Peichel. We had recently received money from the NSF to quantify the non-parallel and parallel contributions to lake-stream stickleback divergence. We will use 16 independent lake-stream pairs to quantify parallelism at the ecological level, the morphological level, and the genetic level. We will then ask to what extent parallelism and non-parallelism at each level can be explained by parallelism and non-parallelism at the other levels. This meeting was set up to plan our first real field season. But, in reality, that was really just the excuse because my main memories involve eating outstanding tacos and barbeque, drinking copious amounts of beverages from Texas, California, and Scotland, and climbing, both in Dan’s backyard “cave” and at Reimer’s Ranch. (If you are at the NSF, I am just kidding.) To push a metaphor perhaps too far, all climbing routes go in an overall parallel direction (up!) but each one follows its own idiosyncratic route and often ends up in a different place.

Parallel?

Multitasking par excellence- or "why McGill hired Dr. Barrett"