Evolution of dispersal strategies and dispersal syndromes in fragmented landscapes


Cote et al. Evolution of dispersal strategies and dispersal syndromes in fragmented landscapes. Ecography, in press. (Image from http://sarinasunbeam.deviantart.com/art/Seed-Dispersal-Infocomic-606992414)

Lynsey McInnes

Lynsey Bunnefeld

PEGE journal club has morphed into a hybrid in-person/online journal club hosted by the University of Stirling. One half of the PEGE admin has moved to Stirling as a lecturer (me) and is hoping to harness the insights of the department as a whole when discussing matters in the PEGE realm.

We are still straightening out details and may migrate to a new website soon, but in the meantime, a rotating series of bloggers from the Biological & Environmental Sciences department at the University of Stirling will write up a short blog summarising a paper and our discussion every two weeks. As before, we’d be really happy to hear your thoughts on the paper and our interpretation in the comments below. In case you are wondering, Will Pearse is now an assistant prof at Utah State University and we’re even still friends! 

This week, I (Lynsey) chose the paper and committed to writing up our discussion. What follows is my own interpretation of events, apologies if I have misrepresented anything we discussed.


I chose a paper by Cote and colleagues from a recent special issue on fragmentation published in Ecography. I was excited about this paper as it promised to integrate three areas of interest of mine: space (fragmentation), intraspecific trait variation (evolving strategies) and species categorisation (dispersal syndromes). However, these grand promises proved problematic. To summarise our discussion: we came out sceptical of the framework proposed by the authors to integrate these three angles; we deemed it infeasible at best and foolish at worse.

Dispersal is a fiendishly difficult phenomenon to get your head around. Do we mean dispersal capacity or propensity? Is a mean or a kernel adequate to categorise the dispersal ‘ability’ of all members of a species? How much intraspecific variation in dispersal ability exists? Is this variance constant? How does it evolve? The authors acknowledge all of these issues and propose to address them head on. They put forward the idea of dispersal syndromes with covarying traits that either enable, enhance or match – the authors thus do not consider dispersal ability as a trait, but rather an emergent feature that comes about as a result of a bunch of possible traits. So far, so interesting.

Where the paper crumbles (for me) is that they go on to overlay the complexity of categorising dispersal syndromes on top of a fragmented landscape. I’m no expert on the process of fragmentation, but I do know it’s a fiendishly complicated topic too. The authors list four ways in which fragmentation modifies a landscape: it reduces habitat quality, increases number of habitat patches, reduces patch size and increases isolation among patches. Each of these four effects are likely to interact with dispersal capacity AND propensity in non-linear ways. And that’s without even considering these effects as selective pressures promoting the evolution of increased or reduced dispersal.

And so we got stuck. We didn’t feel that we have a good grasp (even for a single snapshot of time) of how to adequately characterise dispersal (although we all agreed it was an interesting problem) and so we were hesitant as to the utility of a framework of predicting how dispersal ability (or the traits that covary with it) are likely to interact with or evolve in response to a fragmenting landscape. A pragmatic solution we came up with was to think about holding some variables constant and looking at the evolution of dispersal strategies in those contexts (for example, varying only one of fragmentation’s four effects, not all four).

To conclude, the authors’ aims were admirable, but we were unsure whether we are really in a position to populate their proposed framework at the moment and, even if we were, we were unsure what generalities could emerge: because dispersal ability is a complex phenomenon we were not convinced a framework could be developed that robustly predicts how it might respond and evolve in species found on fragmented landscapes. Are there not too many unknowns and idiosyncracies of species * landscape? Saying that, we would be happy to be proven wrong!

Next week, John Wilson has chosen a recent paper from Ecology by Menzel et al for us to discuss: Mycorrhizal status helps explain invasion success of alien plant species. Join us!


Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub-Saharan Africa

Fabian et al. (2015). Journal of Evolutionary Biology. Spatially varying selection shapes life history clines among populations of Drosophila melanogaster from sub-Saharan Africa

Various kinds of Drosophila melanogaster mutants. I don't think any of these show clinal variation across Africa!

Various kinds of Drosophila melanogaster mutants. I don’t think any of these show clinal variation across Africa… Taken from D’Avila et al. (2008)

Lynsey McInnes

Lynsey Bunnefeld

I picked this paper on a whim as it looked like it dealt in genetics and ecology, but not in the phylogeographic sense that I am usually drawn to. I liked it a lot, mostly for the approach it outlined rather than any specific results.

In brief, the authors are looking to see if they find evidence for adaptive differentiation in life history traits among tropical populations of Drosophila melanogaster as a function of altitude or longitude, arguing that such clines are seen as a function of latitude, and longitude, and particularly altitude, could be considered parallel gradients in environmental conditions. Indeed, they purport to find evidence for this differentiation.

I had some doubts about aspects of their methodology, particularly the mismatch in the genetic resources they assign to each population (i.e., they do not come from the populations they sampled for life history variation), but I am also happy to believe that irrespective of some potentially dodgy leaps of faith, the results they uncover do reflect reality.

And so, I really enjoyed this paper. My brain is still wired in as a macroecologist and any paper I read that tried to tackle some of the many assumptions of macroecological analyses is an impressive one to me. Here, the authors have taken a small(ish) dataset from a band of tropical populations and measured a ton of stuff in order to test a specific hypothesis on differentiation expected as a function of a geographic cline. Sounds so simple, but is not really that common in macroecology despite its concern with spatial diversity patterns. Oops.

And then you come to the next macroecological qualm. OK, Drosophila melanogaster is a wide-ranging species, so intraspecific variation is to be expected, but so are many other species and it is not so often (although things are definitely improving) that macro scale studies consider this intraspecific variation in life history or ecological or behavioural traits. We need more of this!

One could argue that the scale that macroecology operates on means that this kind of variation is not important, that it gets swamped by interspecific variation, but I doubt it. Because, on the flip side, there IS a general consensus that processes acting at multiple scales matter to understand species diversity patterns, so finer (and conversely broader) scales than species-as-unit analyses are relevant.
Don’t worry, I don’t think I am the only person to think this way, I am just still in the beating myself up about how late these things have dawned on me phase.
So, what to do? We probably need more sampling, more genetic resources, more models and better formulation of testable hypotheses. But the hardest thing will be (at least for me) accepting that really interesting insights can be made using model systems or subsets of a taxonomic group, gone is the possibility to use ‘all mammals’, ‘all birds’, etc. (Yes, I am that kind of dirty charismatic vertebrate macro person).  Perhaps general patterns/rules of thumb will emerge quite quickly, along the lines of you need a range of this size to show X and a body size of this size to show Y, or you need to live in environment A to show Z. And then the really interesting part will be piecing together how well intraspecific diversity patterns might predict speciation or extinction probabilities.
Interesting times.

Will Pearse

It’s hard to argue with a paper that does exactly what it says on the tin. This is a nice demonstration of variation within a species across environmental gradients, and an excellent demonstration of how to set up a question and then just go right ahead and answer it.

I was struck by the lack of variation in viability despite the variation in what many people would call life history traits. It’s sobering to consider that there can be this much variation in how a species operates, and yet no general variation in something that’s quite an important component of fitness. Traits play out in their environmental context, and if there can be this much variation within a species we should all be a little more careful when interpreting the importance of very slight differences across species. Of course the authors get at this with their trade-off analysis, but for me (at any rate) it was a nice reminder. I liked that the authors linked all of this variation to climatic variables, but unless I missed something I didn’t see where they explicitly tested climatic factors vs. geographical summaries. I do buy their argument from parsimony that temperature (not altitude + latitude + longitude), and I imagine co-linearities made testing things difficult, but somehow I wanted to see it.

Speaking of variation, staring at the regressions and their oddly high r2 values (I’m becoming a pastiche of myself), I noticed that mixed effects models they used detect a lot of within-line variation. I’m not saying this as a criticism; rather, I think it’s incredible how they were able to partition this out so neatly. It really drives home the importance of variation within species (and populations!), and definitely got me thinking about how biased our measures of trait values are going to be if we can’t grow species in culture like the authors were able to do. I really do just take gene-environment interactions for granted, and completely ignore the micro-processes that Lynsey is now studying. Maybe we do need to start more explicitly linking micro-processes to the macro-ones that I tend to think about.

Dispersal capacity predicts both population genetic structure and species richness in reef fishes

Riginos et al. 2014 Dispersal capacity predicts both population genetic structure and species richness in reef fishes American Naturalist 184:52-64

Distance, distance, everywhere. Figure 2 from

Distance, distance, everywhere. Figure 2 from Rignios et al.

Will Pearse

Will Pearse

This was a strange paper for me to read in some ways, because it harks back to some things that I probably should know something about: fish dispersal (honestly!), diversification, and phylogenetic analyses. The basic idea is that fish that brood their larvae, as opposed to releasing them into the water and letting them do their thing, have more spatial population genetic structure.

It may not come as much surprise to you that species that spray their genetic material with gay abandon have less genetic structure, but this is a pretty comprehensive investigation and is nice for that. It was, however, a surprise (to me) that there isn’t much phylogenetic signal to genetic differentiation. Genetic differentiation is something I would expect to ‘play out’ in the context of a whole host of other ecological factors, all of which will likely exhibit wildly different rates and kinds of evolution. Thus perhaps a single, simple thing like a lambda value isn’t really ever going to capture that level of complexity. Similarly, I feel like there may be another paper coming after this one examining the species richness of the families in more detail. More complex model-fitting exercises might have helped the authors weigh in a little with the Rabosky et al. radiation literature that they reference, but doing so would probably be a lot of work, so I can understand why they might want to leave that for another day!

The authors mention there is likely to be variation in these patterns across space, and I think no one would disagree with that. My personal thought was that this variation should be mapped onto the oceanographic conditions and the timing of reproduction: the currents around reefs are notoriously variable and strong (just ask a diver!) and I would be very surprised if it was easy to account for all of this in a single analysis. Equally, the timing of reproduction could be important since direction and speed of currents change so frequently (and often reliably) throughout the year. Of course, it’s been a very long time since I pretended to know something about the ocean, so I’m likely very wrong about this. All in all… it sounds like it’s a good time to be working on diversification in reef fish!

Lynsey McInnes

Lynsey McInnes

I was really looking forward to this paper. I’m not quite sure what I was hoping for, but I guess I was hoping for big insights underpinning the final line of the abstract: ‘our findings provide a compelling case for the continuity between micro- and macroevolutionary processes of biological diversification and underscore the importance of dispersal-related traits in influencing the mode and tempo of evolution.’

I’m not sure I came away quite satisfied, but that is probably due to my unrealistically high expectations rather than any fault of the authors. In short, they find that reef fishes that hold tight to their eggs have both higher genetic differentiation, or structure, and more species per clade. They infer this is due to less gene flow in benthic guarding species so that populations do not homogenise, instead they can diverge and ultimately speciate.

My disappointment probably stems from reading the wrong paper. I think I was excited to read how they quantified differentiation, but this is lifted from an early paper of the same authors: Effects of geography and life history traits on genetic differentiation in benthic marine fishes published a little while ago in Ecography that I’m definitely going to go read now (and probably should read before posting this post).
I do believe that dispersal-related mechanisms must often underpin diversification patterns and the results documented here do support this idea. I still wonder if we will ever hit upon a more general way to understand the shape of this relationship. For instance, here the fishes possess a handy binary trait that makes classifying them as good and bad dispersers easy. Other analyses have found, using e.g. wing length as a more continuous proxy for dispersal ability, that intermediate dispersers are the most diverse because they move enough to get away from where they were born, but not too well that they constantly homogenise. Is there any way of making this more general? One could argue that Fst/other genetic measures provide this general measure, but what are the species’ traits that actually underpin variation in these measures. Does there need to be a general measure? How general should it be?

Really, I imagine that we probably still need to work out what dispersal is, to actually consider intra-specific variation in dispersal ability and the potential for dispersal ability to evolve because we can really get to grips with how it actually influences diversification propensity only if we are all the same page as to what it is.

I also wonder if the current interest in dispersal ability stems from the fact that its a catch-all trait that nicely links ‘nature of the landscape’ extrinsic factors and ‘ability to move across landscape’ intrinsic factors. Perhaps our problem is that dispersal ability is a stupid trait to consider as it means something different and encompasses different things in different taxa. Maybe we need to build up from smaller building blocks (as here with benthic guarding as a trait)?

Speaking as a budding population geneticist, we should probably also work out if the ways we quantify population differentiation are adequate and look closely at that nasty time-scale between a population differentiating and two or more populations being reproductively isolated and happy to be called new species.

As ever, we need more good studies such as this one, combined we better comparative studies across taxa. Lots to do, go go go.

One more thing – Happy New Year! I’m (Will) very sorry that this post is so late – I’m just about to start a new job in a new continent and all of that has made the Christmas period a bit fraught. All of this running around has made me be a nightmare in a lot of ways, and sadly PEGE took an unexpected holiday break while I handled all of that. Sorry for the bother, and thank you for reading!


Do communities exist? Complex patterns of overlapping marine species distributions

Leaper et al. 2014 Do communities exist? Complex patterns of overlapping marine species distributions. Ecology 95:2016–2025


Benthic flatfish and benthopelagic cod on a shore – Jan van Kessel senior, 1626–1679 (Or: what you get when you google ‘demersal fish australia’)

Will Pearse

Will Pearse

I picked this paper because I felt it was a more stats-y/empirical-y way at getting at some old debates in ecology. The methods seem both very complex and very simple at the same time; if you’re interested, skim the Dunstan paper(s) they reference to get a handle on what’s going on. In essence, they’re simultaneously binning species intoarchetypes (groups) and figuring out what predicts where those archetypes are. It’s a binned species distribution model. Speaking as someone who tried (and failed) to do this, I can assure you it’s a hard thing they’ve done a good job of 😀

The authors find archetypes, but do a good job of stressing that this doesn’t mean they’re present all together in the same place all the time. For me, this variation is almost the most interesting thing, because it could reveal competition. Under the archetype approach, things become simpler because you’ve restricted yourself to the species you most expect to be closely-interacting, and so hard-to-find processes should be easier to detect. I’ve spent a lot of time bleating on about how competition can take place within the context of habitat filtering, and how I think phylogeny is a great way to get at this – I think this kind of approach is even better. There should be different traits that determine species ‘ distances from the centroid of their archetype than those that determine how distant each archetype is, because these two things should reflect fundamentally different processes. Goodness only knows what space you’d calculate these distances in, though!

There may be a further temporal and spatial component to these communities. Fish don’t exactly stay still, and a diver conducting a transect is likely to encounter a number of ‘swim-by’ species that are hovering around the area. For species to interact they have to spatially and temporally overlap, and I wonder to what extent all of these species were doing that. I don’t mean this as a criticism: by treating these species as an archetype, we can drill down and explore what each species is doing. How many predators are in a particular archetype, and how many prey species? How frequently were two predators within an archetype seen at the same time (–> whether they compete for prey). Could the method be extended to deal with fuzzy archetypes, such that commonly-encountered predators could affect multiple archetypes? Why is it that, for the whole of this article, I kept wanting to type “habitat type” instead of archetype? Is there a difference? I’m quite excited to find out!

Lynsey McInnes

Lynsey McInnes

This was a funny paper on the back of a suite of PEGE posts commenting on rather grand visions of the future of various subdisciplines of ecology. I think it might have done us good to remember that applying swanky new concepts and frameworks to actual datasets in the first instance involves a lot of work collecting a lot of data and then a degree of frustration interpreting results that don’t fall neatly in one neat quarter of some kind of hypervolume.

So, kudos to Leaper et al. for a well-executed study apparently conducted by people that know their study system well alongside people developing new methodologies. The authors are interested in the nature of communities, whether they are discrete and easily circumscribed or more fluid, with species composition merging into one another across neighbouring communities.

They use the idea of a species ‘archetype’ to get at these questions, this being the quantification of similarity in species’ responses to environment. I.e. rather than seeing which species co-occur in space, the method clusters species based on results of species distribution modelling (i.e. this set of species likes it hot and wet, and so on).

I am on the fence as to whether this idea is a good one. On the one hand I like to cluster and to generalise, on the other I wonder about circularity and the proliferation of too elaborate data transformations. Let alone all the dodginess that comes with SDMs.

The authors find that although they can identify different clusters of species, these species don’t correspond to distinct spatial entities (‘communities’) suggesting that communities, at least of demersal fish or macroinvertebrates off the southern coast of Australia and northern coast of Tasmania, are not highly structured units. Are we surprised?

I think that I, ever the macroecologist, would have liked to have gone one step further and investigated whether there are traits associated with archetype strength (probably things like dispersal ability, philopatry, niche breadth, species richness, the usual) and by extension how ‘closed’ communities generally are. To do this properly, you would of course need a broader dataset spanning a wider range of communities and species. And you get back to the mismatch between burgeoning numbers of frameworks and a limited amount of appropriate data.

The authors note that communities appear to be made up of a selection of species from multiple archetypes that all match bits of the environment found at a site, but that environmentally similar sites are likely to have a different set of species (albeit chosen from the same archetypes). I think this is a neat, but also intuitive, observation that there are assembly rules, that all bases need to be covered, but exact species can be subbed in and out. I like the idea of substitutable species and wonder how true it is in terms of functional redundancy. My bet is species are not really substitutable, but wonder how much variation in this ‘trait’ there might be.

In short, I think we still have a long way before we have a good grasp of how communities are structured and how that structuring changes through time and across space. My hunch is that careful studies such as this one will be important in building enough real world examples of how things work, whether or not the idea of archetypes is crucial or superfluous to the debate.

Phylogenetic approaches for studying diversification



Hélène Morlon. Ecology Letters 17(4):508-525. Phylogenetic approaches for studying diversification

Lynsey McInnes

Lynsey McInnes

We wanted to do a ‘classic’ diversification paper this week, but realised we’d quickly keep referencing the explosion of literature on the subject from the last five years or so, so we cheated a little and decided on Morlon’s review, because here she has summarised it all for us. A difficult paper to critique, so we’ll use it as a jumping off point for our own personal diversification-related pet favourites.

I have a few! First, I am still wavering whether it will ever be possible to have a unified, tractable model of diversification that spans a large chunk of the tree of life. I can’t decide whether it is an honourable aim to go looking for one (with all the necessary heterogeneity of drivers) or whether a better approach would be really trying to look for some objective way to delimit a ‘homogeneous’ clade and then do comparative/meta-analytical analyses on stacks of them (see Aelys Humphreys’ paper for a step in this direction). Models are always simplified versions of what actually happened, so perhaps it is enough to get a ‘good enough’ model that describes diversification and it doesn’t matter to our pattern seeking minds that one pesky species came to be because of a different process to all of its closest relatives. As you can see, I’m still on the fence.

Second, I really think that diversification modelling that incorporates biotic drivers (e.g. among competitors or across trophic levels, etc.) is simply really cool. It is a difficult challenge to (as above) work at a relevant spatial or taxonomic scale and to not overshoot the importance of biotic interactions vs. other drivers, but if we can manage to do this, at least for some clades, I would be satisfied. While the grand aim of incorporating more ecology into diversification analyses is a great one, its really hard to do this in a more than superficial way. I think really unravelling how biotic interactions impact diversification of a focal group will go some way to rectifying this deficit. It is hard as a pattern seeking macro person to incorporate the idiosyncracies of ecological processes, we must try harder!

Lastly, and predictably, I think if we ever want to understand diversification at the broadest scale, treating species as homogeneous units is too simplistic and models that acknowledge that most species consist of multiple populations distributed across a heterogeneous landscape and connected to greater or lesser extents will ultimately provide better insights into how new species form and old species go extinct. But you knew I would say that.

Will Pearse

Will Pearse

This is a fantastic review, and pulls an awful lot of thinking about ecology and evolution into a single paper. Lynsey’s too nice to mention this, but the expressed intention of the paper (“integration of research in ecology and macroevolution“) cites her paper that came out of a symposium she organised with Ally Phillimore; go watch all the videos now please because they’re great and fit with this paper very well.

It’s a testament to how far the evolution of diversity has come that this review has been published in Ecology Letters – many of these models are remarkably ecological, or at the very least they’re trying to be. Morlon points out we have a need for a Holy Grail that links observed ecological mechanism with evolutionary process – this is precisely the kind of thing I’m trying to do right now, and it’s hard. It’s telling that many of the more exciting kinds of models that she describes haven’t been coded up to be tested with empirical data. In many cases that’s because the actual process of model-fitting is too intense, but maybe in others it’s because many of these models ignore what’s going on elsewhere in a phylogeny. Species are often assumed to be interacting only with members of their own clade, and there’s no attempt to take into account what traits other distantly-related species have, presumably because to do so makes everything unidentifiable. Sadly, such situations reflect reality; for my fifty cents, that’s why I think the meta-community models Morlon discusses are our best bet, because they attempt to model groups of species interacting (and are now incorporating trait evolution).

It is tempting to go off on a mini-rant about whether we can actually detect extinction rates from molecular phylogenies. Morlon gives a good summary of this debate, and she’s both more optimistic and knowledgeable than I so I’ll make a more general, phylogenetic comment about all this. I was struck, when going through her types of models, that while some to me seem to me approaches (“look at an LTT plot!”; fig. 2d) and others seem conceptual ideas (“look at how traits change!”; fig. 2c), none of them are mutually exclusive. I don’t think I’m saying anything controversial: each model is an attempt to capture one particular of something that we all know to be important in a way that a particular author thinks they can quantify well. We all agree that ecological differentiation, geographical separation, and every other of these factors determine diversification rates. The problem is, none of them are accounted for when we build the phylogenies which, themselves, go on to determine our estimates of diversification. Until we create an integrated way of building a phylogeny that takes into account where those sequences came from, the geographical history of the clades that determined them, and the traits of those species, we’re sunk. If you can write a model that can do all that (some have started), then I’d love to hear from you!…

Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory

JP Grime. The American Naturalist 111(982): 1169-1194. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory

I find your lack of competitive ability disturbing. Grime's CSR triangle (main), with his estimates of where trees (top-left) and annual herbs (top-right) might lie within it.    Taken from figures 2 and 3 from Grime (1977).

I find your lack of competitive ability disturbing. Grime’s CSR triangle (main), with his estimates of where trees (top-left) and annual herbs (top-right) might lie within it. Taken from figures 2 and 3 from Grime (1977).

Will Pearse

Will Pearse

I’m a zoologist who somehow keeps looking at plants, and this paper is probably the best demonstration of how plant and animal ecologists really do seem to think differently (in my mind, at least). Grime has a section about animals and fungi at the end, but all of this is clearly written by a plant person – and is all the better for that.

There’s a growing feeling in plant trait ecology that plant traits can be grouped together along some economic spectrum (reflecting pay-back of nutritional investment), be that of leaves or wood. Recently, Peter Reich has argued that all of these can be considered as part of the same system, where plants are either fast-adapted or slow-adapted. I don’t want to point out connections between these ideas and Grime’s CSR strategies, but instead draw attention to how plant functional trait studies have somewhat lost their way. Grime makes it quite clear that position along each of his spectra depends on plant traits, but that there’s no one-to-one matching of trait onto CSR strategy. I feel as thought his general message has been lost among papers pointing out how different species have different adaptation to drought, and how SLA or xylem diameter has changed, as if those particular traits defined those species’ niche dimensions. Convergence means that there are many ways to skin a cat, and there are many ways to be ruderal – individual traits that we have decided to measure do not define species.

I fee Grime implies that there’s very little difference between being in a nutrient-poor or stressful environment based on the species around you or because the environment is inherently that way. He argues an area can be nutrient-poor because all of your neighbours have soaked up all the nutrients and won’t let go. If (as he argues) some species have evolved to maximise nutrient retention, not rate of absorption, this becomes doubly important. I’m constantly referring to abiotic and biotic drivers, and on second thought there’s really very little reason to distinguish between them if they have the same effect – shade is shade, no matter what the cause.

At times I felt like Grime was implying that much of plant traits come from the environment they’re exposed to – I’m not sure things are always as plastic as some would believe, but I certainly agree plants can change. Most importantly, we shouldn’t be teleological in assuming that observed shifts in species’ traits reflect the thing we’re interested in – what may seem like an adaptation to drought may just be a consequence of altered nutrient turnover rates, and without some kind of breeding experiment I don’t think we could ever disentangle the two.

Lynsey McInnes

Lynsey McInnes

I let Will pick the paper this week, forgetting that he was trying to teach himself about plants. He might be a zoologist learning about plants now and again, but I’m just a bad mathematician/pattern seeker masquerading as a biologist. I found this paper tough going, mostly because I haven’t really thought all that much about the ins and outs of actual individual plants making it in their stressful /disturbed/competitive environments. So, I learnt a lot while reading this and would certainly recommend the paper to budding ecologists interested in a framework for classifying their different plant species based on how they might do in different environments.

Once I got to the end of the paper, I realised it, in fact, did fit into my pattern seeking world view (Grime was trying to squeeze plants into a triangle with three distinct lifestyles at its vertices, after all). But only if you are willing to really work for your patterns. Counting species is easy, but disentangling how many of each kind of species is already one step harder. Especially when, of course, the three strategies form a triangle rather than three distinct boxes.

I am typing as I think here, but I just wonder how macroecology, and its resulting insights, would change if we stopped counting species and really tried to count function. Sure, there have been macroecological studies of functional diversity, genetic diversity, body size, but all still very much tied to species counts. I wonder if we will ever let go of the notion of a species as this magic unit. But perhaps it is a magic unit and function/type/etc. still ultimately harks back to species.

I really don’t know if broad-scale analyses need finer divisions than species counts, but, as Will states above, macro people obsess over the relative importance of biotic and abiotic drivers of diversity patterns and thinking in terms of Grime’s classification, or some other similarly nuanced one,might actually help us spend work out what the biotic drivers might be or rather how they might work.

Ok, this is a real ramble now. In short, I appreciated all that I learnt in this paper and it underlined that we macro people have to get more smart in what we measure if we really mean it when we say we want to know how diversity is ‘generated & maintained’ (& turns over).

Climate envelope modelling reveals intraspecific relationships among flowering phenology, niche breadth and potential range size in Arabidopsis thaliana

Banta et al. Ecology Letters 15(8): 769-777. Climate envelope modelling reveals intraspecific relationships among flowering phenology, niche breadth and potential range size in Arabidopsis thaliana

Easy to forget that Arabidopsis thaliana doesn't just live in laboratories! Via Wikimedia

Easy to forget that Arabidopsis thaliana doesn’t just live in laboratories! Via Wikimedia

Lynsey McInnes

Lynsey McInnes

You guessed it, this was another of my choices. I found it a while back and was intrigued over the approach the authors would take. In brief, the paper looks at whether genotypes underlying (or rather, linked to) flowering time generate significantly different niche models (and by extensions niches) and thus can they (the authors) provide evidence that there are intraspecific differences in niche and niche breadth. A. thaliana is a great species to use to ask this question, it is an exceedingly well-known model organism and has a wide distribution.

The conclusions of the paper are far from surprising, with such a wide distribution and with known flowering time variation, it was inevitable that the authors would find evidence of intraspecific variation in niche dimensions. Nevertheless, this is really important to show! There is a whole market devoted to niche models and projections of range change due to climate change that almost exclusively treat species as a single entity. Oops. This is clearly too simplistic for species beyond a certain range size (and yes people kind of know this already). Papers like this (and the Razgour et al. paper we covered earlier) demonstrate this well. Phew.

Now here comes the issue. This paper was only possible because it builds on a ton of A. thaliana research. For instance, genetic variation in flowering time was already known and the underlying loci already characterised. The authors state themselves that defining coherent populations that might be expected to have significantly different niches to each other is really difficult (they probably could not have emphasised this enough!). Populations are rarely closed entities. They circumvent this problem here by going straight for a crude single locus genotype definition. How would you make your population buckets without this additional data? Can you? Is movement among populations (with their specific local adaptations) something that might save chunks of a species range? Probably.

If niche models don’t die a death completely, their next incarnation is going to be models which incorporate not only intraspecific variation, but also connectivity among these chunks (this is going to have to involve dispersal among spatially discrete chunks and degree of genetic exchange among co-occurring genotypes). For such models to be successful and have ‘conservation relevance’ a lot more crosstalk is going to be needed among (macro)ecologists and landscape geneticists/phylogeographers (yay, that’s me!).

This paper is a great start and I look forward to seeing developments in the field that enable it to be useful for non-model organisms (perhaps with no genetics), using multi-locus genotypes, integrating additional ecological traits, adding depth to our understanding of how populations interact to make up a range and ultimately, one day, far into the future, what a realised niche is relative to a fundamental one?

Will Pearse

Will Pearse

A lot is said about model systems in evolution and ecology, and I think papers like this, where model systems for which we have a lot of information are used to answer questions in related fields, are great.

I wear my love of phylogeny and niche conservatism on my sleeve, but that doesn’t mean I don’t appreciate a good demonstration of intraspecific variation when I see one. Flowering time should be variable in a species that spans so much of Europe, because it’s exposed to such different environmental conditions. Whether ability to adapt to novel conditions, or the general constraints that mean the species has to vary its flowering time, are as variable within the species is a slightly different question. I’ve been spending some time thinking about the inheritance of species’ potential for intraspecific variation, and I’m not entirely sure I can come up with a bullet-proof way of deciding what should, or shouldn’t, show such variation. I’d be interested to know if you can!

When I saw figure 4, which shows that earlier-flowering genotypes have larger potential ranges, I was very happily sold. I’m often somewhat nervous when I read a paper involving niche modelling or species distribution models, simply because the things seem so damn hard to get right. Therefore that the authors found any kind of relationship (albeit one with some scatter) is extremely impressive, and indicates they’ve really found something cool. The extremely tight relationship between niche breadth and potential range size is less surprising to me, both from existing theory (that the paper cites), and from the definition of niche breadth itself. A species has a higher niche breadth if “different habitats are equally suitable” (p. 772) based on the MaxEnt suitability scores for each cell, and the potential range is also defined from the MaxEnt predictions which, presumably, incorporate habitat suitability. Thus I’m not so surprised that the relationship between these two things are so strong, because I think they’re related to one-another; that doesn’t make the conclusions any less valid, but it did leave me hoping (as the authors themselves mention) that someone will be able to quantify observed range occupancy for these genotypes. If I’ve missed something obvious about the above, please do let me know – I’m no niche modeller for sure!

Niche syndromes, species extinction risks, and management under climate change

DF Sax, R Early, and J Bellamare. Trends in Ecology and Evolution 28(9): 517-523. doi:10.1016/j.tree.2013.05.010. Niche syndromes, species extinction risks, and management under climate change

Do you have a niche syndrome? You can get a cream for that you know... From Sax et al. (joke from Sarah!)

Do you have a niche syndrome? You can get a cream for that you know… From Sax et al. (joke from Sarah!)

Sarah Whitmee

Sarah Whitmee

I chose this paper before I knew that Lynsey and Will were to review a very similar one just two weeks earlier, coincidence or something more sinister? Actually, I don’t think either of those things, but is in fact due to a new phase in the field of species distribution modelling (SDM), one in which concepts are clarified and the assumptions of models are questioned and tested. Well that’s my hope anyway…. Nevertheless, it is becoming increasingly clear that a big assumption made by those practicing the dark art of SDM, namely a linear relationship between the realised niche (the area of environmental space actually occupied by a species) and the true environmental tolerance limits of a species does not exist, at least not for most species. This was illustrated in the Araujo et al study discussed here, where it was neatly demonstrated that lower thermal tolerances varied widely across species while upper tolerances were much more conserved. Happily, I think this study complements the earlier paper, phew!

The authors start in true TREE style with a nice overview of the current state of the field and the definitions of key terms. While often this is just restating the obvious it’s actually a pretty useful exercise for anyone working in SDM to go through, varying definitions of the fundamental, realized and potential niche plague the discipline and formally stating them for yourself can help later down the line when trying to interpret and understand models.

They then get down to the business end of the paper, the introduction of a new concept: the ‘tolerance niche’. The tolerance niche is defined as “the set of physical conditions and resources that allow individuals to live and grow, but preclude a species from establishing self-sustaining populations”. While I’m not convinced that the field of species distribution modelling needs more jargon I can see the usefulness of this concept in theory, specifically in relation to predicting the impacts of climate change on species persistence. The idea is that while a species cannot thrive in these tolerance zones they can persist temporarily in them, for example during dispersal to reach new suitable climates or to outlast temporary climate fluctuations. The introduced concept is then used to illustrate a number of niche syndromes, or ways we might want to think about species responses under climate change. They choose horticultural plants as a key group for illustrating how you could formulate hypotheses for these niche syndromes and also how you might work out a species tolerance niche, from evidence of specimens in botanic gardens outside a species native distribution.

Overall I like this paper, its clear and well thought through. I buy into the idea of the tolerance niche and think it’s a good step towards more dynamic species distribution models, rather than the time-slice approach employed in earlier analyses. Being a macroecologist I have a problem with this paper that I often encounter with the more fine scale SDM work. While the concept or model works well for a single species or a particularly well studied ecosystem (its no coincidence that a large proportion of SDM studies are all about the South African fynbos you know) these concepts fall down due to a lack of data when you try to scale up for multi-species predictions. The example species given in the paper works beautifully for the concept they are proposing but I wonder how many other species show such clear relationships. So I would have like to have seen more real world examples to convince me that the tolerance niche can truly be estimated. I know very little about plants (outside the ones in my garden) but I’m nervous about the idea of inferring tolerance simply from presence in a botanic garden outside the native distribution with a better understanding of how the plant is managed in situ for example it might be protected against winter frost or supplemented with food or key nutrients. I guess for species of key conservation concern such an approach might pay dividends.

I did like the idea of managed relocation for slow growing species, putting them in an area that they can tolerate in the short-term but which will eventually become climatically suitable for growth and reproduction. It’s a risky business though and I would want a much higher confidence in my climate models before attempting such a bold step.

To sum up the tolerance niche is a neat concept but how applicable it will be in the long term, I’m not sure. I’m a fan of these authors though so perhaps other will have a different view.

Will Pearse

Will Pearse

Like Sarah, I like these authors (and I know Lynsey does too!), so perhaps this is going to be a bit of a biased PEGE. I view the essential idea of this paper as defining the idea of a tolerance niche: conditions where a species can just-about survive, but can’t form a self-sustaining population. I buy it, and think it’s a nice idea and a great paper.

Indeed, I think similar ideas have been floating around in population biology for some time. We have source populations, that fire off propagules into the meta-community, and sink populations, where propagules arrive, individuals persist, but there’s a net loss of individuals and so that population can’t sustain itself. These concepts have really helped population biologists think about meta-community dynamics, and as we try to link macroecology more intimately with local-scale abundance changes and interactions, it seems sensible to conceptually link these concepts.

I wonder if we can go a step further, and stop treating different parts of the niche (fundamental, realised, tolerance, etc.) as discrete boundaries, and instead be up-front in acknowledging that we know species do better in certain parts of their niche than others, and maybe try to quantify that. Essentially, just have some value (why not fitness) that changes throughout niche space, and acknowledge that, in some parts of niche space, fitness will be so low that a population won’t be sustaining. Indeed, such an approach (borrowing heavily from Chesson) would let us handle realised vs. fundamental in a much more intuitive way, because we could distinguish between niche differences and fitness differences when trying to understand whether species can coexist. Because, as I’m sure we can all agree, parameterising a fitness function across niche space would be really, really tractable and easy to do :p

Hopefully the above makes sense; I have a very serious case of man flu!

Lynsey McInnes

Lynsey McInnes

This paper touches on plenty of topics that we have covered in different guises here at PEGE, with a perhaps more applied angle than most. In essence, the authors seem to be drawing attention to the potential importance of a kind of buffer zone of conditions that species could survive in beyond their current distributional limits (the tolerance niche) and how this zone might be extremely important in mitigating climate change induced species’ disasters.

The idea seems pretty reasonable and meshes well with experimental studies that find that translated populations can make it in conditions not found anywhere within their range. The authors also showcase a brilliant dataset of naturalised and garden centre/botanical garden populations of a plant species in the eastern US. The inclusion of this data lifts the paper from one based on loose concepts to one with real results; that was nice!

However, I do still worry how ‘useful’ the concept of a tolerance niche is going to be beyond these plant examples. In effect, the authors are creating an additional category of niche that in most cases is going to be quite difficult to identify? I would have liked to have seen one additional step to go the figure one and that would be to investigate traits that predict the extent and/or location of this tolerance niche. For instance, the authors draw attention to the distinction between short- and long-lived species, but are there any other distinguishing features? These could be along the lines perhaps of large range (probably also has a bit of tolerance niche), restricted range endemic (probably doesn’t), is part of a complicated food web (probably doesn’t have much of a tolerance niche), most kinds of generalist (probably do have tolerance niches). The next step, as the authors emphasise, is where is the tolerance niche located in relation to the realised niche and how easy is it to get to?

The above just gave me the nagging feeling that the tolerance niche concept might be quite difficult to implement as, like everything macro- it seems (I’m having a down on general patterns week), these things depend on so many other things: landscape structure, biotic interactions, the usual suspects. So, while the concept of the tolerance niche could provide US with a kind of buffer so that we can worry less about species’ survival (they can probably tolerate a bit more heat, drought, what have you) than they currently do, it seems like a difficult concept to draw strong or helpful conclusions from across broad taxonomic or spatial scales.

In conclusion, this was a well-written, thoughtful paper, but I am not convinced that the new concept and piece of jargon are robust or flexible (can something actually ever be robust and flexible?) enough to be rolled out very widely. As always, its a data problem…

The shaping of genetic variation in edge-of-range populations under past and future climate change

Razgour et al.. Ecology Letters (early view). DOI: 10.1111/ele.12158. The shaping of genetic variation in edge-of-range populations under past and future climate change

Plecotus austriacus; photo by Branko Karapandža

Plecotus austriacus; photo by Branko Karapandža (via EuroBats)

Will Pearse

Will Pearse

This is an extremely impressive set of analyses that did make me think. The authors examine the genetic structure of these bats, find that glacial refugia contain a lot of its genetic diversity, and then show that under climate change a lot of this diversity will be lost.

It had never occurred to me that hiding from glaciers and hiding from climate change involve species moving in opposite directions, and so what was a refuge before is now a death-trap with nowhere to run to. We know that species’ traits can vary (often adaptively) within their ranges, and we know that species’ past selective pressures can leave an imprint on species today (phylogenetic signal/inertia) and can cause sub-optimal phenotypes. Thus I think it’s entirely plausible that the progeny of the colonists that survived the last great climate-shift on Earth are the ones that will be worst-hit by the next, and so might do badly in it. Of course, you could invert this and say that the descendants of those who dispersed after glaciation are now in the safest spot, and so maybe we’ll be OK. Anyway, my point is to expose my own ignorance, and to wonder whether this could help us figure out a null expectation for what intraspecific variation should look like when looking at lots of species, and improve the fit of species distribution models. Perhaps this has already been done, in which case please let me know!

I like bats (I worked with them one summer as work experience), and while I’m no expert, I feel safe saying they’re very sociable animals. I wonder what effect this will have on their ability to disperse in the face of climate change, because while they are quite choosy in where they roost, they (surely) choose a new roost as a group and as such they’re more likely to find a suitable habitat. Indeed, they must also be less sensitive to allee effects because an entire group is moving at once, and in species where males roost together they’re always having to hunt around for females anyway. I must emphasise I know very little about bats, and so if any/all of the above is nonsense please call me on it right now!

A final thought: I like this paper very much, and love the story it tells, but what will the consequences be of losing these populations of diversity? Are these differences all just drift, or are there adaptations? In other words, what would we be losing? I imagine the authors know the answer to these questions, but I’d quite like to know what they are!

Lynsey McInnes

Lynsey McInnes

Wow, this paper has a bit of everything,and, weirdly, incorporates elements of most of my interests in one, pretty impressive, whole! Niche conservatism, rane shifts, climate change, barriers to movement and my persistent pet interest genetic diversity within the range and the need to consider intraspecific variation and not just treat the range as one big, homogeneous whole. Neat.

The authors do a fine job of integrating the results from a whole host of analyses to suggest that this bat species is most genetically diverse in Iberia (the site of one of its refugia in the LGM) and is showing signs of movement north westerly into England where there is evidence of decreasing population size despite conditions here seemingly spot on for population persistence. The authors emphasise that such results underline the need to conserve edge of the range populations (Iberia for diversity, England for suitable conditions for driving forth any range shift necessitated through shifting climates). Sounds reasonable.

To be cynical, I’m actually not sure how novel such advice is. In a world where extensive range shifts to track climate are predicted (and have been observed), it seems intuitive to focus on range edges as these are the populations that are most likely to lead the movements. To be less cynical, the authors try to show this really is the case. Similarly, a whole host of studies have shown that genetic diversity is often greatest in glacial refugia, if, for no other reason, because these populations are the oldest. Nevertheless, this study is still one of the few that sample range wide populations to show this, and also find that not all refugia are similarly diverse.

The authors also take a pragmatic approach to finding evidence for niche conservatism, arguing that their ecological niche models probably are capturing the fundamental niche and not the realised niche such that their observation of temporal continuity is valid because the species already exists in sympatry with members of its genus (ie not limited by species interactions) and is absent from more arid regions adjacent to its range despite the ability to get there (if it wanted to). While these arguments seem reasonable and are better elaborated than many similar studies, I do wonder whether there are any more conclusive ways to test this assumption. Probably heating the bat on hot plates would be one way forward (dessicating it as well to test further niche axes perhaps).

I remain on the fence over the validity of ABC analyses, but really appreciated the thought that went into defining populations and models to test. I just worry a lot about the sheer amount of simulations necessary to implement such analyses. In this case, the conclusions wrought were interesting and seemed reasonable. Just out of curiousity, I wonder at what stage the ABC analysis was implemented and how much the authors had a feeling for the results already…

I’ll end this with a plea of – watch this space – our lab is working on ways to obtain analytical solutions to similar questions of demographic history and phylogeography such that there will be no need for the simulation quagmire of ABC.

In short, I was really impressed with this study, bringing together a lot of data and analyses to underline the necessary route forward to successful protection of a species. How do we now make this macro- and roll it out for more species, either across a whole clade or a whole community? Exciting times.

Will plant movements keep up with climate change?

Richard T. Corlett and David A. Westcott. Trends in Ecology and Evolution 28(8): 482-488. DOI:10.1016/j.tree.2013.04.003. Will plant movements keep up with climate change?

It's a plant moving. Look, do you have any idea how hard it is to find a picture every week?

This plant can move fast enough… From Wikipedia

Will Pearse

Will Pearse

I picked this paper (out of Lynsey’s selection) because I had a long chat with someone about this at ESA. We concluded then that we didn’t really know whether plants could move fast enough, and to be honest that’s pretty much the conclusion I came to at the end of this review.

Box 4 of the review lists outstanding problems that include “ignorance of the factors that currently limit species ranges”, “largely unknown to what extent plants can acclimate to climate change”, and a number of other factors. The section “can plants track climate change?” lasts only two paragraphs – we apparently have no idea whether plants can track climate change or not. The authors give a number of (for what it’s worth, quite reasonable) reasons they probably can’t, but I think they’d agree that we don’t actually know. Frankly, I’m slightly shocked that we don’t know more about this.

I’m not convinced that animal-dispersed species are necessarily going to fare much better in the face of climate change. This assumes that animals with larger territories are going to move more easily (not necessarily true), particularly given we don’t fully understand the mechanisms by which species would shift their ranges. An animal that eats fruits that moves when it’s hungry is not going to disperse that fruit polewards, because it’s hungry and hasn’t eaten that fruit!

Long-distance dispersal as a mechanism by which individuals trapped in a sea of bad habitat can save the species is an interesting idea. I think this would benefit from a simulation study, but I sense it would require species to be able to colonise in the face of a quite severe numerical disadvantage (small number of immigrants, lots of incumbents). Still, this is a nice idea I’d like to think about for longer…

Lynsey McInnes

Lynsey McInnes

This is a funny paper. On the one hand, a very useful, succinct review of the different factors involved in thinking about how plants might respond to climate change and why this is of interest to ecologists/conservation scientists/mankind and on the other hand, a frustratingly on-the-fence expose of plant movement research to date and its likely next steps.

The authors undoubtedly do a great job in summarizing many recent studies (check out the reference list, its stacked with refs from post 2010). This subject is most definitely timely and popular. And yet it seems we don’t know much. For example, conclusive answers are absent for questions such as what determines a plant species’ current range? How much more range could a species occupy with unlimited dispersal/removing other species/new climates? Is this period of climate change different to past ones (cities in the way, etc.)? The author’s box 4 neatly summarizes the extent of our lack of knowledge!

I got to the end of the paper and found myself wondering (a bit like last week), should we worry? Or should we worry in a more focused way? Does the identity of individual plant species matter as long as the ecosystem is still functioning healthily? If you are a ‘rubbish’ species, has your time come? Perversely, I do just find the outstanding questions listed in box 4 of interest in and of themselves, but firmly, firmly believe that for conservation purposes, they are not the correct ones to be focusing on. I’m not a conservation scientist so I’m allowed (have allowed myself) to ponder these questions, but if wanted to be practical, I reckon we need to think more about functional types (mentioned in box 1), more about corridors to facilitate movement, more about redundancy, more about … ?

Can we ever know – ‘Will plant movements keep up with climate change?’ Seems like this is not a yes or no question. It will depend on the specific set of traits the plant species has/the environment it is found in/the interactions with other species (plants, dispersers, pollinators) it has now and could have in the future? Different camps want an answer for different reasons. Generalities seem to be in place already (and are well-summarised in the paper). However, if we want to conserve species or functions, we need more than these generalities, it seems. If want to use this broad question to learn some fundamentals on the biology of plants, my suggestion would be we need more of everything: more field studies, more theory and perhaps most importantly more of a recognition and exploration of interacting forces: a bit of evolution, a few influential abiotic factors, one or two key biotic interactions, a whole host of more minor ones, across and within trophic levels, some anthropogenic effects, short- and long-distance dispersal and this whole shebang playing out against a shifting climate.

I think the paper left me unsatisfied as it was pitched too broad and thus felt too shallow. What are these authors interested in? What piece of the puzzle will they tackle? Ja, perhaps that’s unfair to ask of from a review, but I’m curious anyway.

Finally – I did very much appreciate this line from the paper: ‘The involvement of government agencies, nongovernmental organizations, and citizen-science networks will be essential, given the focus of academic science on novelty.’

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