Is dispersal neutral?

Winsor Lowe & Mark McPeek. Trends in Ecology & Evolution 29(8): 444-450. Is dispersal neutral?

Eadweard Muybridge’s "Bird in Flight". He was a pioneer of photography (particularly of animals), and was acquitted of shooting his wife's lover for 'justifiable homicide'. This is all over the Internet and I think past copyright.

Eadweard Muybridge’s “Bird in Flight”. He was a pioneer of photography (particularly of movement), and was acquitted of shooting his wife’s lover for ‘justifiable homicide’. This is all over the Internet and I think past copyright.

Lynsey McInnes

Lynsey Bunnefeld

I picked this paper because I don’t think dispersal is neutral and I had a hunch that the authors didn’t think so either. Perhaps because I already agreed with the main thrust of their argument – that we need to consider how intrinsic traits affect dispersal propensity and movement as well as intra-specific variation in these traits – I came away from the paper a bit disappointed. I know, I know, I am hard to please. Let me explain.

The authors systematically undermine the notion that dispersal might be a neutral process. They note that thinking of it as a neutral process makes it a lot easier to think about and to model as you just need one dispersal parameter that specifies something like average dispersal distance per species (or if you are getting swanky, a parameter to characterise a dispersal kernel for each species). On top of this you can add in dispersal barriers and spatial structure of population patches, but, throughout, you are buying into the idea that all individuals of all populations of a species behave the same way. They go on to outline experimental and field evidence that this is not the case, that individuals vary in their dispersal propensity as a function of intrinsic traits, trade-offs with other traits as well as geographically as a function of intrinsic traits interacting with the extrinsic environment. In short, dispersal is nastily complicated and thinking of it in neutral terms is just too simplistic to be useful.

A few problems with thinking about it more realistically. Data is notoriously hard to come by, and even if you could collect whatever data you wanted, what would you collect? You’d need wide sampling across and within populations, you’d need to account for extrinsic factors and you’d have to have some clear ideas on what traits might influence which bits of dispersal (propensity, distance, establishment).

The authors are most interested in how dispersal affects community assembly, I think by this they mean how does variation in dispersal affect what individual genotypes/phenotypes make it into different communities and is this predictable? This is an interesting question and one that seems to have had only a hazy treatment so far in the literature because, as the authors note, researchers prefer to concentrate on the spatial structure of populations rather than the nature of the individuals in their population set. I agree wholeheartedly with the authors and therefore think this is the point where I felt unsatisfied. I wanted the authors to tell me more about what there expectations were for how non-neutral dispersal might affect community assembly. For instance, will peripheral populations (at continent edges? on islands?) be really different ecologically (services? function?) because only far dispersing phenotypes make it there (far dispersing but rubbish competitors?). Will central populations be more transient than peripheral ones as they have higher flux of different phenotypes coming in and out? Can divergence of one species due to limited dispersal affect divergence of species at another trophic level (who might otherwise have maintain one large range)? And so on, and so on.

OK, maybe I was too harsh to be disappointed and the paper provided ample food for thought without providing a coherent framework for moving forward. Perhaps that will be paper #2 or a result of other researchers picking up the baton and moving forward in this notoriously complicated field.

Will Pearse

Will Pearse

This review really spoke to me. I think it’s hard (if not impossible) to argue that all species have the same dispersal abilities, and almost as hard to argue that variation in dispersal ability shouldn’t interact with other ecological processes. It’s a great essay – go read it. I vote for Lynsey picking all of our papers 😀

It is clearly very hard to get good data on dispersal, and I think it’s clear that there’s unlikely to be a single “dispersal” process to be modelled (long-distance vs. short-distance, etc.). Personally, I also think there’s a continuum between migration and dispersal, and the emphasis on permanent movement isn’t as important as we might think (that’s another rant for another day). Evolutionary biologists have to be very careful with dispersal; larger range sizes make speciation more likely, and if species are dispersing widely across an area I’d argue that makes character displacement a bigger deal for trait evolution. Dispersal on the ecological scale is harder to model in some ways, because it interacts with so many other processes – that’s why I think it’s excellent that the authors have stuck their necks out on the line and made definitive hypotheses about what ecological processes will be linked to dispersal. By finding ways that incorporating it into our models improves their fit, we have a better chance of detecting the influence of dispersal, and determining how, why, and when individuals disperse.

The authors flit across scales (community –> individual), and I wonder if there are two modelling approaches where dispersal could help in each. The first is meta-community modelling: the authors make a good case for how dispersal trades off against other ecological processes, and if this is the case modelling the entire system should simplify things. The source and sink dynamics they describe would simply be an emergent property of the model. The second is agent-based modelling. If individuals are making decisions to disperse based on their surroundings and preferences, then modelling that decision process is the only way to generalise across environments and (potentially) species. Maybe it would be a pain in the neck to do, but it would definitely be useful.


About will.pearse
Ecology / evolutionary biologist

12 Responses to Is dispersal neutral?

  1. I skimmed this paper when it came out, and your post brought back a point that confused me at that time – intraspecific variability, geographic variability etc. may be important to consider, but how do they make dispersal non-neutral?

    That dispersal is non-neutral means (at least for me) that dispersal parameters depend on the relative frequency of a species in its community; or at least that they lead to frequency-dependent fitness. It’s not immediately clear to me how intraspecific variability, e.g., would achieve that effect.

    • will.pearse says:

      It’s a good question, and you’ve reminded me of something I really wanted to mention in my post but forgot! I think they mean that by assuming you can just have ‘more dispersal’ from a particular species/population, you’re assuming that individuals are identical/exchangable in their properties (i.e., neutral). By saying “as long as I add more of these individuals, I’m increasing dispersal”, you’re implicitly saying that all individuals can disperse equally well.

      I think that also extends to what you’re talking about – there should be inter- and intra-specific variation in the rate at which individuals disperse. Does that make any sense?

      • Hmm, not 100% convinced. Identical is sufficient, but not necessary for neutral dynamics. Necessary is that all traits / species / phenotypes have the same fitness, regardless of their relative frequency in the community. E.g. Zhang, D.-Y.; Zhang, B.-Y.; Lin, K.; Jiang, X.; Tao, Y.; Hubbell, S.; He, F. & Ostling, A. (2012) Demographic trade-offs determine species abundance and diversity. Journal of Plant Ecology, 5, 82-88.

        I don’t see how differences in dispersal necessarily lead to frequency-dependence, specially if we speak about non-heritable intraspecific variability.

      • will.pearse says:

        …apparently comments don’t nest enough for this, sorry…

        I agree that it’s sufficient but not necessary (or, to be more precise, I don’t think I’m qualified to argue! :D). I think they’re generally arguing that dispersal abilities interact with other processes that vary at the inter- and intra-specific level.

        On a side-note, I’m not sure it’s productive to obsess about whether models are neutral, Neutral, or none of the above – I think it’s better to consider what kinds of processes those models capture. I think it’s fair to say there is a class of process that we can’t capture if we assume all species have equal dispersal abilities. There are neutral models where species vary in terms of their traits (neutral trait evolution leading to unequal trait variation in the present) – I don’t think it’s helpful to talk about whether these models are neutral or not, they’re just interesting!

      • Fair enough, but it’s in the title after all, and so one would like to know they mean by “non-neutral”. Specially because, at least for me, non-neutral suggests stabilizing and therefore diversity-enhancing, so I would have been interested if they mean that.

        However, I found in the meantime that the abstract states that “Neutral theory assumes that dispersal is stochastic and equivalent among species. This assumption can be rejected on principle, but common research approaches tacitly support the ‘neutral dispersal’ assumption.”

        As said above, I don’t really agree that that equivalent is strictly necessary for neutrality, but if we accept the statement then I guess it makes sense to follow that dispersal is non-neutral when its either non-stochastic (=under selection?) or variable within/between? species ….

      • will.pearse says:

        You make a good point… I think they are arguing for the non-equivalency/under selection thing. Maybe we should do some more neutral papers, I’ll poke Lynsey about this…

  2. lynsey83 says:

    Hm, team. Head explosion! My take on non-neutral was that individuals within a species vary in their dispersal propensities and that this variation might have, for instance, geographic variation or co-vary with some other traits or aspects of the external environment. Further, dispersal ability could be selected for or against. Which to me makes a lot of sense and sounds non-neutral enough.

    However, I have to omit I am not clear on the strict definitions of neutral or Neutral traits. And tend not to think of frequency dependency at all. Florian, are you saying that even with selection and/or intraspecific variability it may still be valid to treat the trait ‘dispersal ability’ as an emergent species level trait that can be considered neutral? Or are you talking about how differences in dispersal ability or change through time within a species needs to be able to alter the relative frequency of a species (in a community, say) for it to be non-neutral. Or am I barking up the wrong tree(s).

    I’m still thinking about this…

    Thanks for taking the time to comment!

  3. Jeremy Fox says:

    I don’t know where anyone ever got the idea that dispersal (or dispersal limitation) is a “neutral” process in the first place. I don’t even know what that’s supposed to mean:

  4. Jeremy Fox says:

    And while we’re at it, “neutral” doesn’t mean “stochastic” either:

    • will.pearse says:

      I agree with you. I think one of the more interesting parts of the paper (and one I should have emphasised in my post) is the idea that dispersal ability varies, and that we tend to ignore that. I feel like calling for the incorporation of species-level differences in dispersal ability is different from conflating dispersal and neutrality. Perhaps you disagree!…

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