Do plants and pollinators coevolve?

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

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32 thoughts on “Do plants and pollinators coevolve?

  1. Really nice, thought-provoking post – a perfect start to the New Year 🙂 Here’s some initial thoughts that have popped into my slightly hung-over brain:

    1. The obvious answer to your over-arching question is yes, sometimes, but not always. I think we do have some compelling examples of co-evolution sensu stricto in p-p interactions. They tend to be found in regions which have been relatively stable over the past few million years, e.g. tropical rainforests, South African biomes, etc. But….

    2….the two examples you gave, of Darwin’s moth and its orchid, and Rediviva bees and Diascia, plus others I could list such as long tongued flies in South Africa, etc., are certainly examples of co-evolution s.s. But they are not, I would argue, examples of “tight and specialized interactions” in the way we define for host-parasite systems. Rediviva bees collect oil, pollen and nectar from, and pollinate, a range of other plants, not just Diascia; likewise Xanthopan morgani, the pollinator of Darwin’s orchid, takes nectar (and probably pollinates) other types of flowers (in fact it’s a widespread species, also occurring on mainland Africa. So these interactions are also asymmetric and to some extent generalized, at least within a community context. In that respect they are different to the few truly obligate p-p relationships, such as fig-fig wasp interactions.

    3. Diffuse coevolution at a community scale is really hard to determine, as you appreciate. But one broad line of evidence might be the overall requirement of most flowers for animal pollination, and in turn pollinators show some kinds of adaptations to obtaining resources from flowers. That may be as much as we can hope for.

    4. Don’t be too down hearted at the rejection of your manuscripts; it happens to us all!

    Best wishes for 2014,

    Jeff

    • Wow, thank you so much for reading and commenting…it is great to have an expert opinion at my finger tips! In the paper, I have argued that broad scale patterns of correlated phylogenies in interacting plants and their insect visitors might be a signal of diffuse coevolution, such that, by studying the correlation between the interaction structure and the phylogeny of each interacting taxa, and then by comparing the structure of the phylogenies to each other, we might gain insight into where the interactions are asymmetric (for example, when an insect taxa has a correlated interaction structure and phylogeny), and where they are symmetric (ie. where the insect taxa and plant taxa have correlated phylogenies). I have had difficulty explaining it in a persuasive way and have gotten very mixed reviews, some very positive and some very negative. I do believe my results are consistent with the idea of diffuse coevolution, but I have tried to make the manuscript less controversial by just talking about the patterns of phylogenetic structuring…at which point it gets rejected for not being “novel enough.” So I’m not sure whether to return to my coevolution story and make it more convincing or to try and back off, which seems to make the paper boring in the eyes of the reviewers!

      • My initial response would be that you stick with the diffuse co-evolution story, that’s the interesting part as far as I’m concerned. But your conclusion depends on the level of specialisation between the two phylogenies, and almost by definition any congruence between the phylogenies is going to require there to be an assumption about the level of mutual obligation within the relationship. Difficult for me to comment further without knowing which systems you’re analysing though.

  2. Nature is so complex and it seems for all of this to make for certainty, weather, more specifically, global warming, would speed up or alter this process. But could plants and insects/animals evolve as quickly as weather is making changes worldwide? It seems weather is throwing off any and all the interactions in the plants that evolved to satisfy a pollinating or hungry insect. Even just a bit by plants blooming before the arrival of their pollinating insects. I would wonder if even a week matters? Just my thoughts. Your post is very thought provoking and the science compelling.

    • Thank you! I thought it was too long for anyone to actually read it! I appreciate your comments…yes, climate change has altered interactions, but in plant-pollinator systems anyway, they seem to be pretty labile. Even a shift in the flowering time of the plants relative to the bees doesn’t seem to have too much of an impact (yet) because the bees and plants are mostly generalists. Only time will tell, though.

    • As standingoutinmyfield said, most plant-pollinator relationships are fairly flexible and resistant to such shifts, at least in the short term. I have some unpublished data for two plant species where the same populations flowered a month later or earlier in consecutive years. It made no difference to the reproductive success of the plants because there were sufficient pollinators available for those plants and they had either responded to the weather in the same way as the plants, in one example (a bee pollinated generalist), or would naturally be active throughout the flowering period in the other (a fly pollinated specialist). Must publish that some day.

      • My smiley face was replying to the wrong comment….blame the hangover! What I wanted to say was that I admire your ambition, “five orders of insects and 27 orders of plants, and over 13,000 unique interactions”. But how are you assessing this? As a single analysis? Or analysing phylogeny-pair by phylogeny-pair?

      • I have two different analyses…I first look for correlations using jaccard distance matrices of interactions and taxonomic distance matrices as a proxy for phylogeny…I can compare within a given taxa using the Mantel test. This basically tells me whether closely related organisms interact with similar partners. Then I use a fourth corner algorithm to directly search for correlations between the taxonomic distance matrices of plants and the insects that visit them. So all of the analyses are done using linear algebra. I look at the whole community first, then subsets of the community determined by taxa (i.e. within hymenoptera, coleoptera, etc).

      • That’s ok, I’ll respect it! I’ve done a lot of editing and reviewing in 2013 so I’m going to try to cut down on it this year. So I may turn it down anyway!

      • Thank you for your response. I live within walking distance to Ontario Canada in Niagara Falls, NY. It is really cold here most years, but in the last six years the weather has been bordering on Spring-like conditions with little snow. This year seems to be a ‘normal’ year, but with temps going to -4F on Friday, maybe it is still abnormal. I have been noticing the pollinators late to their flowers, but as you say there are many native bees and many seem to be generalists. We have also had springs with frost or excessive rain where farmers could not plant certain crops. I know observation by laymen is not science in any way, but it does seem like we are getting insects and birds not common to our area on a more frequent basis.

      • Regarding the comment that “observation by laymen is not science in any way”, I strongly disagree! “Amateur” observations have been the backbone of phenological surveys for many decades, and anecdotal information can be hugely valuable in suggesting hypotheses to test. Keep up the good work!

      • I’m with Jeff on this one…phenological records are crucial to our understanding and we need more people like you, especially if you record your observations. Do you know about the NPN? Here’s a link…you can sign up and record phenological things as they happen: first bloom, leaf fall, etc. https://www.usanpn.org/

  3. Definitely not too long to read – in fact it makes a very nice change to all the Happy New Year/Resolutions posts in my feed at the moment. 🙂

    As for the science, the idea of diffuse co-evolution makes intuitive sense, so it is ‘just’ a (difficult) case of working out how to test for it. Good luck with re-jigging the manuscript to get it accepted.

  4. Thanks for the great post, and I wish you luck with your manuscript! If you haven’t already read it, Dyer et al. (2012) Proc R Soc B 279:3606-3615 is a great paper discussing parallel evolution of angiosperms and Hymenopterans – it’s from the angle of insect vision and flower colour, but it could be worth a read.

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