Eco-evolutionary supermodels

Eight years ago in Alaska, Joe Travis gave a plenary address as president of the American Society of Naturalists. He began by posing the whimsical and implausible scenario where the program officer at the US National Science Foundation called you on the phone and said “We have a million dollars for you to spend on whatever research question you want.” Joe then asked the audience if they would take the offer. The answer was dead obvious until then he gave the hitch. You had to work on the organism that NSF specified. You could thus have 100% control of the research question but 0% control of the research organism. Hmmm. Now everyone was thinking, “well what organism is it?” Believe it or not, many people – myself included – were thinking they might say no to a million dollars depending on the research organism.

So Joe gave us an organism. NSF, he said, has decided the million dollars must be spent on research using the pirate perch, Aphredoderus sayanus. A fish, I thought, cool, I can do something with that – but what? Joe then read the species description. “The pirate perch, Aphredoderus sayanus, is a freshwater fish of the Percopsiformes order. This small fish (up to 14 centimetres (5.5 in) TL) is native to the eastern half of North America. It is dark brown, sometimes with a darker band near the base tail.” OK, nothing special – just a typical run of the mill small fish. Then Joe continues “A unique feature of this fish is the forward placement of its cloaca, under the head, anterior to the pelvic fins.” Ah, OK, now I know what to study: why in the hell would a fish poop beside its mouth.*

Besides the pirate perch, the point I most remember from Joe’s talk – and the resulting paper – was that some folks are organism people and other folks are question people. Organism people work on one taxonomic group and study tons of questions in that one group – think Peter and Rosemary Grant working on Darwin’s finches or Jonathan Losos working on Anolis lizards. Question people, by contrast, work on a whole host of taxonomic groups but use each to address the same general question. Of course, an organism focus and a question focus are really two independent axes and so you can also have folks that work on many questions in many taxonomic groups – the dilettantes – and folks that work on a single question in a single taxonomic group – the professionals (apparently this is the official antonym of dilettante).

Taking the organism focus to extremes, we have the so-called “model” organisms: the flies, mice, worms, and Arabadopsises (Arabadopses?) of biology that are well characterized developmentally and genetically, having full genome sequences, transcriptomes, clonal lines, transgenic strains, and the like. This historically exclusive club has recently exploded to the point that we now have lots of “model” organisms. As one example, the threespine stickleback is now a recognized model organism – and one of the few that also have been well characterized ecologically. This explosion of model organisms has led to the desire to somehow elevate some models over others – supermodel organisms, if you like.

So what would be (or could be) an eco-evolutionary supermodel? Last week I was visiting Nancy Emery at Purdue University to give the Karling Lecture, and we had a spirited dinner conversation with her lab on the topic. One of Nancy’s students (Elizabeth Larue) was planning her research topic – cast very generally as the role of adaptation to climate change in shaping eco-evolutionary dynamics. Cool question – but what organism to use? Nancy’s lab works on plants, so Elizabeth has spent some time thinking of various eco-evolutionary model organisms, maybe the evening primrose, maybe goldenrod, or maybe even (if all else fails) Arabadopsis. But, if we are really to pick from scratch the best organism for eco-evolutionary studies, would it be a plant – and what would be the other candidates?

Conversations like this usually don’t get very far before someone brings up Daphnia – in fact, they don’t get beyond hello if Luc De Meester, Nelson Hairston, or David Post are present. Daphnia show very rapid evolution, they are short lived and small (which eases experiments and laboratory work), they are “strong interactors” in the community, they can be propagated clonally, and – most amazingly – they can be resurrected from resting eggs in sediments to directly compare the genotypes from the present to various times in the past. (My favorite is the 2008 Nature paper of Ellen Decaestecker where Daphnia and their parasites were resurrected from several times in the past and cross-infected to show that parasites from a given time period were better adapted to Daphnia from that time period than they were to Daphnia from the past and the future.) Who could ask for anything more of an eco-evolutionary supermodel? And so we decided right then and there that Elizabeth’s thesis should be on Daphnia. And why stop there, perhaps Nancy should give up on plants and just switch to Daphnia for all her work.  

The Emery Lab - Daphnia here we come!

If Daphnia are the true eco-evolutionary supermodel, then perhaps we should all work on them. Not so fast, you might say, we need to study many organisms to determine the generality of any given phenomena. OK, true enough, but that is a cop out – it is like saying that Daphnia really are the best but some other poor sucker should study alewives or guppies or stickleback or cottonwood trees or aphids or evening primrose. The hard question is – are Daphnia really that perfect? Perhaps not. First – and as the plant people are presumably thinking at this point – plants have many of the same properties as Daphnia, including the possibility of resurrecting genotypes from the past. Second, Daphnia are so small that no one can study the fate and success of individuals in nature, whereas one can (sometimes with difficulty) for all of the above organisms. Third, much (but not all) of the evolution studied in Daphnia on short time scales is clonal selection, which is equivalent to studying different species.

But then supermodels aren’t perfect anyway – they just look good, at least to most folks. So maybe Daphnia really is the ultimate eco-evolutionary supermodel, it just has the usual flaws of human supermodels, such as binging and purging, bulimia, bad boyfriend choices, drug abuse, and a limited shelf-life. But then again, we don’t have just one human supermodel – we have a bunch of them that we can pick and choose among to suit our current ad campaign (i.e., Nature submission) or our budget or the flavor of the month. The same should be true for eco-evolutionary models and supermodels and, yes, Daphnia can be one of them – but so too can be alewives and guppies and stickleback and cottonwood trees and aphids and evening primrose. I can’t wait for the eco-evolutionary supermodel swim suit issues in Evolution and Ecology.

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*This species description is from Wikipedia, which then continues: “This placement allows the females to place their eggs more precisely into root masses.” I am skeptical. Why wouldn't other fish do this? And why does having your bum under your chin help you be more precise? Did someone experimentally manipulate anus position and test egg laying precision? The question is definitely worth a million dollars of research.