NB: I don’t suppose anyone will want to read this on the first day of the new year, but I’m a typical academic…obsessed and burning the midnight oil reading papers on coevolution, haha.
I have a manuscript that has been rejected a
couple few times. (Okay, so ALL of my manuscripts have been rejected a few times at this point.) It is a manuscript that is very important to me, and I’m very a teensy bit frustrated, so I thought I’d go back to its origins and think about coevolution: what it is, what it means, and how we might provide evidence for or against it in plant-pollinator systems. Excuse me if I think out loud in this forum and feel free to provide thoughts (or ignore this post altogether…it’s crazy long). I kind of need to feel free to write without worrying about word limits or jargon.
The most fundamental definition of coevolution is reciprocal changes in populations of interacting organisms. Or in the words of Janzen (1980): “an evolutionary change in a trait of the individuals of one population in response to a trait of the individuals of a second population, followed by an evolutionary change in the second population in response to the first.”
Much of the research on coevolution has been done in host-parasite systems, where there is an arms race of adaptations (see for example Schulte et al 2010 and Decaestecker et al 2007). The host improves its defenses and the parasite improves its attacks in a way that keeps them in balance (this is referred to as the Red Queen Hypothesis, but I won’t go into it here). The patterns resulting from this arms race are visible in the patterns of evolutionary history and association.
The original (i.e Darwin’s) idea of coevolution is based on pairwise or specific coevolution. This type of coevolution requires a tight and specialized interaction. One great example is the interaction between Darwin’s moth and orchid. There are other examples of these specialized interactions (for example, Rediviva and Diascia, Steiner and Whitehead 1991), but they tend to be the exception rather than the rule in plant-pollinator systems, which are highly generalized and asymmetric. Thus, on a pairwise basis, plant-pollinator systems should rarely exhibit coevolution.
However, there is also a notion of diffuse coevolution, where groups of species can coevolve together. From what I can tell, Janzen introduced this idea, again in his landmark 1980 paper: “Diffuse coevolution occurs when either or both populations in the above definition are represented by an array of populations that generate selective pressure as a group.”
By one definition, the presence of an additional species changes the interactions between the others in such a way as to influence their co-adaptation (Iwao and Rauscher 1997). To me, the idea that diffuse coevolution could exist on a broad scale in plant-pollinator systems is intuitive, though its lack of use in the literature since then shows either a lack of consensus of a need for a more thorough theory with testable hypotheses. The idea is that a bee does not need to know exactly what a rose is, but what a flower in general is, and how to get food from it.
The problem with diffuse coevolution, as expressed by John Thompson in his book, “The Coevolutionary Process”, is that there needs to be a limit to it. Otherwise, we could end up with some “Gaia like extreme of oxygen-producing plants and oxygen-consuming animals.”
The geographic mosaic of coevolution is a theory put forth by Thompson (2005), which addresses the fact that populations, and thus the interactions between populations, are spatially variable. If that is so, then the coevolution between species must also vary across geographic distances. There is pretty strong evidence that this can happen in plant-pollinator systems (Anderson and Johnson 2007). But again, this focuses on only two species coevolving.
Outside of a laboratory, or a field study with a very restricted number of species, how can we look at broad patterns of coevolution? The only way is to look at broad patterns within the evolutionary history of interacting organisms. What kinds of patterns would we expect to see in the presence or absence of coevolution? One popular idea has been that coevolving species should have correlated phylogenies, or branching patterns in their evolutionary history.
This method of supplying evidence of coevolution has recently come under fire, however. Recent work shows that correlated phylogenies are neither necessary nor sufficient to show that coevolution is at work (see Nuismer et al 2010 among others).
So the question is this: if plant-pollinator systems are generalized and full of diffuse interactions, how could coevolution be acting and how could we provide evidence to support it? The answer I try to provide is that we need to look at many interactions in a broad range of taxa in order to see the signal. As Thompson (1997) says, “Interaction commonly grow through the accumulation of new taxa.” We also need to account for the alternative hypotheses put forth by Althoff et al 2013, two of which are relevant to my system (i.e. plant-pollinator interactions).
1) Habitat filtering: one possible explanation for correlated phylogenetic histories is that selection acted simultaneously on both interacting partners from abiotic or external sources. For example, they have similar branching patterns because they are filtered by similar habitats. In my mind, we can address this alternative hypothesis by looking only within one particular habitat. Branching within that habitat type must then be due to some other factor. Webb et al (2002) also elucidated similar concepts, distinguishing scales at which ecological factors ruled, and those where geographical factors were dominant. By sticking to smaller spatial scales, we might hope to avoid the noise due to habitat filtering.
2) Phylogenetic tracking: another possibility is that, instead of reciprocal selection, the correlated phylogenies are a result of one species tracking the other. This could be true of many plant-pollinator interactions. Indeed, asymmetry is common in these kinds of interactions. For example, Ramirez et al (2011) showed asynchronous diversification in the highly specialized Euglossine bee-orchid symbiosis. We can address this by identifying cases where there is an asymmetry in the correlation between interaction structure of one taxa and its phylogeny relative to its partner. In other words, the interaction may be more important to one partner than the other.Addressing this alternative hypothesis is challenging.
Most of all, I hope to open up the discussion as to what might constitute evidence for diffuse coevolution in plant-pollinator communities, and whether phylogenetic patterns can provide clues to the mechanisms that formed the interactions between plants and pollinators…because, at this scale, at the scale of WHOLE COMMUNITIES, we can’t do pairwise experiments where we remove or add a single species. And I’ll finish this long rant with another Thompson quote (and pretend that he’s my bestie):
The diversity of species cannot make sense unless we also understand the diversity of interactions among them. ~Thompson 1997