What do you think is the biggest recent conceptual advance in ecology?

What new idea has emerged recently that is likely to revolutionize ecology?

Of course, it depends in part on how you define “recent”. I’ll intentionally leave that vague here. I’d say that the concept of trait-mediated effects has already revolutionized ecology, but I don’t know that it counts as recent. The Werner and Peacor review of TMIIs is from 2003, so this idea isn’t new enough to count as recent in my book.

Instead, I think my answer to this question would be the idea the microbes associated with larger organisms (that is, the microbiome) are what’s really driving much of what we observe out in nature. A series of papers on aphids and their parasitoids provides a good example, I think. As a beginning grad student, I read this 1995 paper by Henter and Via showing differences between aphid genotypes in their susceptibility to a parasitoid wasp. It was a really neat result, and showed clear differences between aphid genotypes. But then, when I was finishing up grad school, this 2005 paper by Oliver et al. came out showing that that variation in susceptibility was actually due to bacterial symbionts carried by the aphids. Whoa! That was neat. The hosts weren’t really in charge; their microbes were instead. And then it got even crazier (in a good sort of way) when it was later shown (in this 2009 paper by Oliver et al.) that, actually, those bacteria weren’t in charge, either – what was really controlling resistance were phage carried by the bacteria. So, in the end, the susceptibility of an aphid to attack by a wasp is determined by whether its gut microbes carry a phage. How cool is that?

The finding that susceptibility to parasites is controlled by microbes has been found in other systems, too (e.g., bumble bees, frogs). How general is it? It’s too early to know, but people now routinely think about the role of commensal microbes in determining disease susceptibility and tolerance, which is a pretty huge shift. This includes in humans, too. The human gut microbiome affects all sorts of things: two great, accessible reviews are this NY Times piece by Michael Pollan and this one for National Geographic’s Phenomena site by Carl Zimmer.* This knowledge is affecting how we treat people (fecal transplants are a very effective treatment for people suffering from recurrent C. difficile infections) and I think is probably one of the most promising avenues for trying to get people to stop overusing antibiotics. If you knew that taking a course of antibiotics increased your risk of debilitating diarrhea or might favor obesity (antibiotics are used as a “growth promoter” in agriculture), you’d think twice before taking them, right?

People who work on plants have been focusing on the role of mycorrhizal fungi for a while now, but, even there, fundamental breakthroughs are still occurring. A prominent recent example is this recent paper by Averill et al., which found that the type of mycorrhizal fungi that dominate an ecosystem determines soil carbon storage, with very important consequences for the global carbon cycle. There’s also a lot of interesting recent work being done on how soil microbes that are associated with plants influence a plant’s ability to tolerate heat and drought (as reviewed here).

Even behavior can be controlled by microbes, as reviewed in this recent Ezenwa et al. article (which also lays out a lot of interesting avenues for future research on the microbiome and animal behavior). As one example, Drosophila mating behavior was influenced by commensal bacteria, as shown in this Sharon et al. study. There’s evidence that human behaviors and mental health are also influenced by the gut microbiome, which has the potential to influence how we treat things like anxiety and depression.

All of which is to say: I think the role of the microbiome in mediating ecological processes and interactions is the recent advance that is in the process of revolutionizing our field. I also think the links between the human microbiome and health are fascinating and have the potential to strongly influence how we treat infections and chronic diseases.**

What about you? What do you think is the biggest recent conceptual advance in ecology?

Postscript: After putting this in the queue, Jeremy, Brian, and I had a brief email exchange related to what counts as a ‘conceptual’ advance. You could argue (as Jeremy originally did) that a ‘conceptual’ advance would be something that is rooted in theory, which this isn’t. But, while I agree that that might often be the case, I think the microbiome is something that, while empirically based, has fundamentally changed how we view the natural world. That, to me, is a major conceptual advance; we think about the world differently now that we know about the microbiome.

* Both of those focus primarily on the gut microbiome, but there’s also work on the lung microbiome (including asking whether it might influence the risk of asthma), the vaginal microbiome (which seems to influence the risk of preterm birth, HIV, and HPV), and the skin microbiome.

**I’m teaching a class this semester on how ecology and evolution are relevant to human health and disease, so this is a topic I’ve been thinking about a lot.

29 thoughts on “What do you think is the biggest recent conceptual advance in ecology?

  1. I am fascinated by all the areas we are finding the microbiome to be important for mediating ecological dynamics. As far as conceptual advances, I am partial to the relatively recent applications of the idea that ecology and evolution can play out on comparable timescales.

    • I certainly agree that the idea that ecology and evolution can play out on the same timescale is fundamentally important!

  2. Sorry to jump into the thread early, but I’m about to leave the office for the day and I couldn’t wait to comment on such a great post!

    Your answer surprised me Meg. I agree the microbiome is a hugely important recent advance, but I tend to think of it as an empirical advance, not a conceptual one. My own snap answer to your question was modern coexistence theory, and I could imagine others stumping for things like MaxEnt or neutral theory or metabolic theory. And thinking back to this old post:

    And the most-cited ecology papers from the 70s, 80s, and 90s are… (UPDATEDx6)

    I recall several commenters lamenting that the many conceptual advances of the 1960s and 70s since like a one-off, that these days our advances are of a different sort. But then, maybe I and others who’d stump for things like coexistence theory or MaxEnt just have an overly-narrow view of what constitutes a “conceptual” advance?

    So without wanting to get too abstract and philosophical, what’s a *conceptual* advance, as opposed to an empirical advance?

    • To me, a conceptual advance in ecology is something that changes the way we think about the natural world. That is often rooted in theory, but it doesn’t have to be. So, it seems that my definition is broader than yours.

      Darwin was clearly strongly influenced by his observations of the natural world when forming his theory of natural selection. Does that mean it wasn’t a conceptual advance?

      • “To me, a conceptual advance in ecology is something that changes the way we think about the natural world.”

        That’s basically the response I was anticipating, and I wouldn’t necessarily disagree. Empirical data certainly can reveal that we’re living in a very different world than the one we thought we were living in.

        Re: Darwin, yes, of course his ideas were a conceptual advance! I’d merely add that that advance sprang from a complicated mix of sources. Very much including, but very much *not* limited to, observations of nature. There was also reading of Malthus, observations of artificial selection, his many, many manipulative experiments…

  3. So, there is a student who’s committee I am on who works with microbes. She’s proposing a chapter on a BEF experiment based on some observations from her field work. So for her quals, I asked her to address how BEF theory works or doesn’t in microbial systems. Her answer was fascinating. She pretty convincingly showed how many of the ideas we view as theoretical foundational either don’t work or only work in weird ways, once you consider real-world microbial systems. If anything, it’s convinced me that, if ecological theory is to have generality, there is some massive rethinking we need to do. And if anything, this will open up new vistas in thinking about microorganismal ecology.

    • Very interesting! I run an aquatic ecology journal club here, and last week we discussed a paper that was looking at species-area relationships in microbes. There was a really interesting discussion of how microbes alter what you might expect to see, in part because using sequencing-based methods means you’re capturing lots of things that are dormant, too. So, I agree that thinking about how to add microbes in can really stretch our thinking about ecology in general (and that that’s a good thing).

    • Indeed, and this is not to mention that much of modern evolutionary theory does not apply in a straightforward manner to microbes, because it has largely been based on sexual organisms or completely clonal organisms, whereas microbes are somewhere in between. Lateral Gene Transfer has fascinating implications for evolution, and I wonder what cool effects it has on ecology too. My favourite recent thought experiment inspired by microbial lifestyles is the public good model of evolution (http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3179745/). So I agree, understanding the ubiquity and importance of microbes definitely has and will continue to shake up our view of life, and not just in ecology. Can’t wait to see what comes of it!

  4. A fellow grad student and I had an interesting discussion on this topic recently. We basically came to the conclusion that ecology hasn’t had a conceptual (theoretical) advancement since Fisher. Of course we have come a long way in re-defining classical theories, and adding a few conceptual notes and modifications, but almost everything that we study is based on theory from the early to mid 20th century.

    Microbial ecologists who are mostly looking at gut microbiomes and plant-soil microbe feedbacks, are really just doing mid 20th century ecology. They are defining species concepts, advancing detection methods, addressing species occurrences, defining coexistence and competition in microbes, and just trying to understand what mechanisms affect patterns of diversity and species turnover. Unfortunately, many of the data collected by microbial ecologists seriously lacks replication. Often, studies of gut microbiomes use just one or a few individuals, since the process of getting gnotobiotic mice is expensive and takes a lot of time.

    I agree with Meg, microbes will allow us to refine theories and better understand mechanisms that affect diversity, and other ecological patterns (that’s not new theory, however). There will also need to be much discussion about how an OTU relates to a species concept in plants/animals. Species concepts aren’t perfect, but the concept of an OTU has some really troubling assumptions.

    I think the best information that will come from current microbial ecology is a complete breakdown of how we view competition and coexistence mechanisms in higher-order taxa. We often underplay the importance of pathogens and diseases in regulating the outcome of competition between species (especially for plants), but new data suggest that competition for resources may be less important than the effects of microbes (both beneficial and harmful).

  5. And indeed, once again Lynn Margulis might have been right when everybody was dismissing her.

    She said that symbiosis might be more important than natural selection in adaptation and diversification. Considering how much we’ve learned about the role that microbes are playing in so many ecological and evolutionary interactions, I wouldn’t wholly rule this out, yet.

    • Hmm, that’s kind of a bridge too far for me, Terry. “Microbes are more important than we thought” is a *very* different claim than the much more specific claim that symbiosis is more important than evolution by natural selection. Heck, when I was a grad student, I saw Margulis give a talk at Rutgers in which she actually made even much stronger claims than that…

      • It’s also a bridge too far for me, at the moment. But I’m leaving the door open for the possibility. Given what we still don’t know, there is a nonzero chance that she could be right. I think it’s unlikely, but she was well ahead of us on the microbiome. Of course, much of what she said is even more wacky, as you point out.

  6. If we’re thinking about conceptual advances (as opposed to formal theory) and we’re defining “ecology” very broadly, then a significant advance of the last 15 years or so has been in the form of valuation of ecosystem services. Now, we can debate whether or not specific valuation is at all accurate (or even desirable) but there’s no doubt that such valuations have made governments and business sit up and take notice of the intrinsic value of the natural world in ways that they never previously did. Whether that is a good or bad thing remains to be seen…..

  7. My vote is for phylogenetic approaches to testing hypotheses.
    See, e.g. Harvey & Pagel 1991. The Comparative Method in Evolutionary Biology. OUP.
    Is that too old to be “recent”?

    • That works for me! I think it would be interesting to see how people define ‘recent’, and to see if it correlates with age/career stage. I’m guessing grad students will tend to have a narrower range of things they would consider ‘recent’, but that’s just a guess.

      • Thanks. Indeed the challenge here is to define “conceptual advance” and “recent”!
        I like the microbiome summary: this stuff is indeed fascinating and important but I am not sure it is really “one concept” but rather results from our improving view of a rich vista of different things as our methods improve. For example, we have known for a good while that we depend on prokaryotes (cobalamin, nitrogen fixing, etc). The degree to which parasites may manipulate their hosts is certainly remarkable but I’m not sure how new that is either (though we now see many more examples). Certainly exciting stuff whether or not it is recent or conceptual.

  8. What a great post, and I entirely agree with the excitement over microbes, that’s why I work with them :-). I do think it will leave its mark conceptually, because macro-micro interactions may differ fundamentally from macro-macro interactions because of the different generation times: ecological timescale for one is a evolutionary timescale to the other, as well as the “one to many” aspect of the interaction that is orders of magnitude higher than at the macro-scale.

    For me some of the most important recent findings is that soil nutrient cycling and carbon storage are controlled in totally different ways than was always presumed. Or at least what I always understood from simplified textbooks. Examples are this http://www.ncbi.nlm.nih.gov/pubmed/21979045 and this http://doi.wiley.com/10.1111/gcb.12113 .
    This probably doesn’t count as it is not core ecology and mostly complicates rather than simplifies our views, I do find it amazing how little we understand from these important processes.

    I just can’t come up with one that really applies. I think I am just generally more excited over less “world-changing” ideas and findings, that i just find cool.

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  10. This is a really tough one. I’d certainly agree above on maximum entropy, symbiosis, and maybe neutral ecology. I’d also like to suggest (1) facilitation (non-competitive interactions) and (2) network theory.

    (1) can tie in with the theme of symbiosis, but I think that it has advanced a good deal of work and opened the doors for other lines of theory. These works span Regan Callaway’s positive interactions between plants, some of John Thompson’s coevolutionary framework, and works cited in Bruno et al. (http://www.sciencedirect.com/science/article/pii/S0169534702000459). Some advancements on positive interactions are diametrically opposed to and challenge more traditional lines of thinking (e.g., http://www.nature.com/nature/journal/v458/n7241/full/nature07950.html).

    (2) originated out of pure mathematics and, like maximum entropy, for instance, has been adopted by ecology. I suggested (2) not only because it is somewhat of a quantitative paradigm shift, but because it’s a conceptual extension of ecology that has pervaded other fields. Off the top of my head, I can’t think of many other areas of ecology that have been able to do that.

    Thanks for the post.

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