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!



Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk

Johnson et al.. Ecology Letters 15(3): 235-242. Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk

Use of a Billy Joel album cover does not imply any indorsement of Billy Joel by PEGE. Taken from billyjoel.com

Use of a Billy Joel album cover does not imply any indorsement of Billy Joel by PEGE. Taken from billyjoel.com

Jennifer Garbutt

Jennifer Garbutt

I picked this paper because it tackles some of the host-parasite ecology questions that I study (why do some hosts get sick while others stay healthy? How do different life history strategies affect infection risk? Do body size and growth rate matter?), but on an inter specific rather than intraspecific scale. The paper asks whether host “pace-of-life” affects infection risk and the authors’ approach was to compare life-histories and infection outcome across amphibian species.

The pace-of-life idea comes from the eco-immunology hypothesis that mounting an immune response is costly and therefore trades-off against growth and reproduction. Long-lived species should benefit most from defence and invest accordingly, whereas short-lived species should invest instead in growth and reproduction.

The authors infected members of 13 amphibian species with one of my favourite parasites, the developmentally-disruptive trematode Ribeiroia ondatrae. Infected hosts develop malformed, missing or extra limbs. There’s some evidence that these abnormal limbs put the host at greater risk of predation from birds, which is the next host in the trematode’s complex life cycle (Goodman and Johnston, 2011) – so you can see why I think these parasites are pretty cool!

The main finding of the study is that long-lived, slow-developing amphibian species (with a slow pace-of-life) suffered less mortality and abnormality, as well as having a reduced parasite load. The traits that contributed most to infection outcome were size at metamorphosis and time to metamorphosis. A slow pace of life could be beneficial either because slow-paced hosts (i) have a prolonged larval period and so have more time for the repair of parasite-induced damage, or (ii) are larger when inoculated and thus receive a smaller dose of parasite relative to their mass.

I really admire the interspecific comparative approach taken in this paper, but feel that this strategy is inherently problematic because Ribeiroia may have differing evolutionary associations with the amphibian species. The authors say that all the species “likely overlap with Ribeiroia in nature” but it is not easy to be sure that all the species are equally important natural hosts for the parasite. However, any difference in evolutionary host-parasite relationships should cause extra variation in the infection experiments that would, if anything, limit the power of the authors’ analyses, making their inferences conservative. It would be interesting to complement this study with intraspecific experiments in some of the amphibian species to see if variation in life history on this level also affects infection risk (without the confounding effect of host-parasite evolutionary relationships).

I also really liked the study because the most important life history measures to impact infection outcome were early growth characteristics. I like this result because I study the impact on disease of maternal effects, which are normally more pronounced early in life, so this study supports my idea that early life characteristics can be really important in determining infection risk.

Will Pearse

Will Pearse

This is a neat paper; species that live fast are more likely to die of infection, and the authors argue that makes sense because there are better things to worry about (breeding) than looking after yourself if you’re going to die soon anyway. I also think this paper wins the “Understated Methods” award for the rather easy-to-miss statement “experiments were conducted over a 13-year period”!

I was initially surprised that amphibians are this maleable; normally when talking about what I call ‘fire-and-forget’ life history strategies I talk about Drosophila vs. humans, and there are quite a few million years between us to cover all manner of evolution. However, looking at figure 1, I can see that some of these species have most recent common ancestors over 200 million years ago – that’s plenty of time for evolution to kick in. I was also surprised that investment in immunity isn’t more of a discrete trait; it seems there really is an advantage to be ever-so-slightly-more immune in the long-run than another species, which (perhaps based on my fire-and-forget ignorance) I wasn’t expecting.

I’m intrigued by the other pieces of these animals’ life histories, though. Are amphibians that are good at dealing with pathogens also excellent at dealing with environmental stressors? I’d expect extremely mobile (high dispersing) species to have worse immune systems (they’re running faster than their pathogens), and equally they might have much faster life histories because they breed faster to colonise. By that argument, perhaps there could even be a correlation between age of a species and its resistance to pathogens, mixing some taxon cycle ideas with Rickleffs’ pathogen-based speciation ideas. Maybe it really is pathogens all the way down…

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!

Convergent structure of multitrophic communities over three continents

Segar et al. Ecology Letters 16(12): 1436-1445. Convergent structure of multitrophic communities over three continents

Figs and fig wasps. Taken from the excellent figweb site (c) Simon van Noort (Iziko Museums)

Figs and fig wasps. Taken from the figweb site. (c) Simon van Noort (Iziko Museums)

Will Pearse

Will Pearse

Put simply, this paper is excellent. The authors have amassed an impressive dataset, performed a thoughtful and sophisticated analysis, and then explained the whole thing so clearly that it almost sounds easy. I look forward to trying to play around with some of these ideas in other systems!

It seems like there really has been convergence here: distantly related species are doing the same thing as each other in different places. So how the hell did this happen? While many evolutionary biologists I speak to seem to have a pretty good idea what they think convergence is, I think we’re still lacking a formal mechanistic model that can be tested. Yes, we can isolate parts of a phylogeny that looks convergent, but I don’t think we have a model of trait evolution we can use to model this and I’m not sure what it would even look like (what is the opposite of a Brownian walk?). Perhaps convergence happens when there’s insufficient dispersal for pre-adapted species to move in and occupy a particular niche. Perhaps convergence can only happen when there’s sufficient flexibility in a particular trait, thus labile behavioural traits should show more convergence and things like the Baldwin Effect will become important. Maybe there’s something special about fig wasps, and their emergence and mating on the surface of figs (they do that, right?) that makes them more susceptible to all this. Maybe it’s none of these things.

Perhaps the most important limiting factor would be the evolution of the figs themselves; I wonder if the most important methodological advance would be simultaneous evolution of fig and wasp traits, and simultaneous diversification/extinction of both taxa. Obviously work has been done on this already, but I’m talking about a more explicit derivation where, instead of individuals in a population interacting, there are individuals from two separate populations (figs and wasps) interacting according to some fixed set of rules. Thus a particular trait shift in one population would have to be matched by a complimentary shift in the other. I sense the maths would get quite intractable quite quickly (well, it would for me…), but simulation shouldn’t be impossible.

Lynsey McInnes

Lynsey McInnes

To maintain full disclosure, I am about to start collaborating with senior author, James Cook, so it is in my interests here to be constructive and probably err on the side of positivity. That said, I enjoyed this paper a lot! The fig wasp system is inherently cool and I thought the analyses here were exceedingly ambitious.The authors set out to test the relationships among fig wasp communities across three continents. According to measures of phylogenetic and ecological distance, do they follow the ‘inheritance’ (long term co-diversification, same ecological and phylogenetic diversities), ‘convergence’ (same ecological diversities got through different phylogenetic routes) or ‘constraint’ (ecological roles divergent because of constraints on colonisation and/or niche shifts by resident species (meaning phylogenetic diversity also different among communities) hypotheses. They find most support for fig wasp communities being similarly structured through ecological convergence.There are two sides of the fence on which one could sit with regard to this paper. On the one hand, the authors have built up a perhaps overly-complicated methodology in order to demonstrate ecological convergence when one has the feeling they already knew this result would emerge. These are fig wasp experts after all. For instance, the authors could have put the wasps into their guilds without any analyses at all. Similarly, I still don’t fully understand the ins and outs of the PVR and how that setup is able to decompose the variance into ecological, phylogenetic and joint components. I also worry about the low sample sizes and the power of a 35 species family spanning a ton of other wasp species (these qualms might be unfounded, I imagine Will would know).

BUT…my interest lies in rolling out such a methodology more broadly, perhaps to sets of communities with which one has little expertise. Then, for example, an objective way to delimit guilds is vital. And a step by step framework for analysis (the authors’ figure one) is a great tool. My mind is already ticking over to the time when one could stack various cross-continental analyses of community structure across groups into a big metaanalysis. Is convergence the norm? My feeling is such a meta-analysis is a long way off though.

One can imagine also developing the methodology within the fig wasp system (imagine having the data to do this for each of the 750 fig/fig wasp systems) or, as the authors suggest, looking at the structure in different parts of a single fig tree species’ range. I wonder if there are environmental correlates of the different signals?

I also liked a lot that the authors quantified both richness and relative abundance. I liked a lot that they had explanations for the reasons behind the signal of convergence (weird fig traits, niche shifts). I also liked that the authors distinguish constraint vs. convergence and wonder whether convergence ever follows constraint (and whether you could tell?).

I wonder if you could ever roll out these studies in some kind of experimental mesocosm? It would be cool to see the genetic underpinning of the various routes to similarity in community structure and how many replicates would get stuck in some setup due to constraint vs. reach the same ‘end’ due to convergence? You could add in the effect of various historical events (climate change! meteorites!), the possibilities are endless.

One final idea, it would also be interesting to look at multitrophic communities much closer together in space and see how movement across communities affects the patterns observed. Although the authors do suggest that their setup would work best for bounded communities. Hm.

So, yes, a very cool project. Thanks James and co 😉

Plus ça change — a model for stasis and evolution in different environments

Peter Sheldon. Palaeogeography, Palaeoclimatology, Palaeoecology 127: 209-227. Plus ça change — a model for stasis and evolution in different environments

Storm of the Bastille - plus ça change? From Wikimedia (unknown artist)

Storm of the Bastille – plus ça change? From Wikimedia (unknown artist)

Lynsey McInnes

Lynsey McInnes

Continuing our choosing-classics strand of PEGE, I chose this paper after reading it years ago and remembering it now as impressively daring. I’ve got a soft spot for discursive papers, where the authors are not scared to be a bit radical and talk their way through an argument, throwing caution and data to the winds.

Rereading the paper this week, I knew I was on to a good thing as Sheldon starts with a quote from Levin about scale:  ‘the problem of relating phenomena across scales
is the central problem in biology.’ And a consideration of scale is one of the issues that has popped up in many PEGE posts this year. Since this paper, there has been tons of literature produced for and against punctuated equilibrium, see the great piece by Pennell et al just published in TREE sorting the whole jumble out, but Sheldon, here, provides, to my mind, a very even handed treatment of what you can, and cannot, hope to ascertain from the extremely patchy fossil record stretching from biases in perception, the links between micro- and macroevolution to emergent macroecological patterns (and much inbetween).

Temporal scale…stating the obvious, we might think patterns are a mix of punctuated bursts and stasis from our contemporary view, but they are actually pretty damn gradual.

Spatial scale…let’s think about the environments lineages are persisting through when deciding whether there is stasis, gradual or bursts of evolution.

I’m realising more and more that I am most grounded in macroecology – however much I ‘want’ to be an evolutionary biologist or a population geneticist. So, I really appreciated Sheldon cutting to the chase on the processes that might generate high tropical diversity (specialist species, easier to speciate, gain some ecological distance and persist as a ‘good’ species, rather than generalists populating (on land) temperate areas, where the generalist ancestral phenotype works best, swallowing up precocious young species trying to match themselves to every last environmental fluctuation (excuse the gross anthropomorphisms). He just states as obvious the expected broad-scale effects of abiotic factors and briefly mentions higher expected impacts of biotic interactions among specialist species and other factors that have been discussed to death in the ensuing two decades of macroecological research. He touches on my pet topic intraspecific variation, although he goes on to suggest (I think) that locally adapted populations responding to broad-scale environmental change could lead to punctuated bursts of evolution (or at least the signal of such), something I’m not too sure about.

I also wonder how his thoughts on the effect of contemporary climate change and evoluationary responses to it were taken at the time of publication. We are so used to these ideas now, but were they radical then? Not sure. I loved that he matter of factedly states that predicting species’ responses is going to be exceedingly difficult.

I’ve written this post in a rush and I’ve realised it’s pretty thin on the ground in terms of actual commentary – my lasting impression of this paper is being awed by Sheldon’s ability to cut to the chase across a range of fields from biases in the fossil record to drivers of species’ diversity. If I had more time, I’d like to go through his conjectures with a fine-toothed comb to see which have stood the test of time and the ravages of ‘proper’ analysis. My hunch is quite a few. Not least the idea that geological timescales are just really long versions of ecological timescales, this can be interpreted in various ways – at the most basic – generalists do better – across timescales – in fluctuating environments.

In short, this paper is well worth a read, if for no other reason that the multitude of brilliant metaphors…pullovers, human rebellion, loud sneezes.

Will Pearse

Will Pearse

There are a number of really cool ideas in here that really spoke to me, and it’s been quite interesting to imagine the impact this paper had on a younger Lynsey! I’m afraid I’m not going to focus on the main thrust of the paper, not because I don’t like it, but because I got wildly over-excited about one aspect of the paper.

A racemose phylogeny (look here if you’re not a plant person) is a  phylogeny with lots of bristly, transient off-shoots that die out quite quickly (it’s attributed to Williams), and it immediately brings to my mind that first phylogeny Darwin drew. People get very excited at the idea that particular sub-populations of a species can act so differently; if we all talked about raceme phylogenies and how our definition of species is somewhat arbitrary a little more explicitly (and not just when we’re leading that Biology 101 class), I think we wouldn’t be so surprised. Species are collections of populations, always budding off one-another and then re-joining the main body. This got me thinking: what would our expectations of trait evolution look like if we accepted a raceme where species are constantly being born and die, and each separate raceme spike has a slightly different trait? Remember that these tiny, off-shoot branches are probably never truly lost, and maybe they just act as repositories of genetic diversity that get pulled back into the main population.

I have never been sure what an evolutionary response over geological time looks like. I think of evolution as the outcome of lots of ecology over lots of time, and as such I have always found it hard to imagine the outcome of evolution as anything more than the emergent property of ecology. But when coordinated with the raceme ideas above, I think I finally see it. Geological time is like the mother of all ecological storage effects – perhaps species and traits that are (maybe only slightly) mal-adaptive now can survive over longer periods of time (perhaps in the tips of these racemes…) until they are useful later, and then those traits come to dominate. Thus the species survives through these stored pools of variation, in a constant state of flux, and yet somehow appearing the same. Plus ça change.

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.’

Heat freezes niche evolution

Araújo, Ferri-Yañez et al. Heat freezes niche evolution. Ecology Letters, early view.


Some pretty exciting datasets used in this study (above)

Will Pearse

Will Pearse

I’m sorry everyone, because a number of work commitments (including preparing for ESA) mean I haven’t been able to spend the time I would normally devote to PEGE this week. I’m particularly annoyed, because this paper has a story, and stories require sitting in a quiet room with a beer and thinking, which I really don’t have right now.

Let’s assume that the tropical origin theories are right, and that the tropics are a huge source of diversity. If so, I completely buy more variability in cold tolerance – that’s what allowing species to spread towards the poles, and that’s what’s allowing species to radiate out into new niches. We should expect variation, because it’s that variation that’s driving speciation / it’s speciation that’s driving that variation.

When I look at the evolution of species traits, I assume I can measure them fairly accurately, and describe them with a single value. Well, this paper (and in particular figure 7a) really makes me think I should stop doing that, because tolerances seem to be things that are described by distributions with long (or at least variable) tails, and quite strong asymmetries. Perhaps even some kind of linkage with the traits that underly cold tolerance, and how those work physiologically, might help. So, maybe it’s time to crack out that dusty old physiology textbook!

Lynsey McInnes

Lynsey McInnes

Oops, I’ve managed to pick a paper that merits more consideration than either Will and I have had time to give it this week. But in the spirit of publishing PEGE more or less on time each week (less this week given Latvian wifi collapse), here are some initial thoughts on this paper.

Well, it looks like we are finally beginning the next generation of niche conservatism type analyses and that physiology is about to take centre stage. For a while now, we have been bandying about the notion that we can’t really look at niches by summarising the different climates found within species’ range polygons, that really niches relate to physiology and that we need to address physiological mechanisms head on. However, physiological traits are way harder to measure! The authors here do a great job of collating all available date on physiological tolerances and asking some interesting questions with this dataset (as an aside, I am extremely fond of papers that dare to use data from variety of sources and measuring slightly different things, rather than restricting themselves to more ‘perfect’ homogeneous datasets).

They conclude that upper thermal limits are much less variable than lower ones and that this indicates that upper limits are much more conserved. This in turn suggests that species living in regions close to these limits are most likely to be most screwed in the face of increasing temperatures. I really need more time to think about this, but on first glance, this sounds pretty reasonable and sits well with similar assessments of latitudinal gradients of climate change risk that have not used real physiological data.

I really appreciated that authors tackled head on what their results mean for all those studies (mine included) that make loose handwavey gestures that realised niches should be correlated in some nicely linear way with fundamental niches. I also liked the way they highlight how their findings deal (another) blow to using bioclimatic modelling to make robust assessments of species likely responses/range movements in the face of climate change.

Some thoughts that popped into my head…

How are these results affected by there just not being higher temperatures around at the moment? And by there being more species in the tropics, with smaller ranges? Is there any conflation going on?

Are there any experimental evolution studies around that have selected for increased temperature tolerance/looked at the genetic mechanisms behind this? (I expect yes!)

What is the relationship between upper and lower thermal limits and the absolute range of thermal tolerance for each species? (Not sure what I mean here, but I think I mean what about the physiology analogue of the effect of range size/intraspecific variation?).

How would these results change if studied in an explicitly phylogenetic context (harping back to my musings on what is niche conservatism without the ‘phylogenetic’ bit?).

Given the apparent complexity in species’ (thermal) niches is there any real hope that we are able to make accurate predictions of species’ likely responses to climate change (and then go on to use these predictions to take useful conservation decisions)? The typical trio – move, evolve, perish – still stand but how much progress have we made in working out what is more likely (my feeling is most species will have a bit of all three in different/overlapping parts of the range). Pragmatically, maybe we need to give up on these species by species assessments and instead look at emergent community/ecosystem assessments to insure healthy ecosystems (whatever that might mean) rather than persistence of individual species. I.e. go more macro instead of less?

Alternatively, if our aim is not necessarily to conserve, but just to understand what on earth is going on and how niches ‘work’, it looks like we are going to have heat up a lot more organisms on hot plates and digitise a few less maps…

Functional extinction of birds drives rapid evolutionary changes in seed size

Galetti et al. Science 340(6136): 1086-1090. DOI:0.1126/science.1233774. Functional extinction of birds drives rapid evolutionary changes in seed size

Birds only disperse what they can carry! From Galetti et al.

Birds only disperse what they can carry! From Galetti et al.

Will Pearse

Will Pearse

Wam-bam, this is a paper I would have loved to put in my undergrad essays. Plants need birds to disperse their seeds, and so when large birds go locally-extinct, plants evolve smaller seeds that smaller birds can carry. This happens really, really fast (within the last 75/100 years!) and so is a great example of rapid evolution.

A nastier man than I would point out that this is somewhat inferred; with no data on what seed size was like 100 years ago there’s a fair bit of supposition going on here. However, their variance decomposition (34% due to birds in forest, 0.1% differences among sites) is really quite striking, so I’m quite happy to go along with this. There’s such a clear link between seed size and probability of being dispersed (figure 2b) that I’m quite happy to accept the smoking gun of a huge selective pressure and observable differences.

Which leaves me with a slight problem, because I always assume that we can ignore both intraspecific variation and rapid evolution when doing ecosystem service work. If trait can evolve this rapidly, treating species’ ecosystem services and traits as fixed is no longer acceptable. Indeed, the situation is doubly problematic because there are going to be a lot of downstream effects of changing seed size, not just on the plant species itself (it’s now shifted on the simplified on the r vs. k selection spectrum), but also other species that interact with that plant. There is a huge literature on how phenology shifts are worse in tri-trophic interaction networks because not every component of the system can keep up with change – I see no reason for this not to be a concern here.

Lynsey McInnes

Lynsey McInnes

This is to all intents and purposes a very neat demonstration of purported rapid evolutionary change in the face of a new selective pressure brough about by human-mediated loss of large-gaped frugivores from forest fragments. One could quibble on whether the frugivore loss is driving the contraction in seed size variation, or whether fragmentation caused the frugivore loss, and so on, but the authors do a thorough job of dismissing other possible correlates….environmental differences among sites, checking the time needed for such a response, and I’m pretty convinced the relationship holds.

This is bad news! It suggests many of those stacks of papers predicting responses to climate change or habitat fragmentation that brush evolutionary responses under the carpet are probably missing key elements of the response game, Similarly, how does this two trophic level result cascade to additional trophic levels. Without big palm seeds and thus big healthy palms, what grows in their place? What effect do these newly dominant plant species have on other pieces of the forest ecosystem.  Ah, its frightening.

What is the next step? Can we rejoin the forest fragments and get the large-gaped frugivores back? Is there enough genetic variation left to get back the large seeds?

This must have been a time-consuming study and its just not feasible to initiate tons of new studies at similar scales to ascertain how pervasive such rapid evolutionary responses are. I would naively guess that it might be better to continue with this system and see if we can work out this change’s effect on additional chunks of the forest ecosystem. Perhaps the authors are already working in that.

The macroecologist in me also ponders the feasibility and merits of expanding the scope of such studies. Perhaps to a mesoscale at least. I am reminded of Phillimore et al‘s very slick mesoscale studies on variation in phenological responses across space in British frogs. Here, the authors were looking to distinguish local adaptation vs. plasticity governing the spatial variation that they saw in order to predict how populations would cope in the face of climate change that will alter the timing of temperature cues. In short, the authors conclude climate change is expected to outpace the frogs’ ability to respond. However, they ignored the potential for microevolutionary change, as the timescales they were thinking of were so short. The challenge now seems to be to incorporate this possible response? Admittedly, easier said than done…

Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes?

Michael Crisp and Lyn Cook, 2012. New Phytologist 196(3): 681-694. DOI:10.1111/j.1469-8137.2012.04298.x. Phylogenetic niche conservatism: what are the underlying evolutionary and ecological causes?

The multi-coloured world of phylogenetic niche conservatism (from Crisp and Cook)

The multi-coloured world of phylogenetic niche conservatism (from Crisp and Cook)

Jan Schnitzler

Jan Schnitzler

Much has been written about phylogenetic niche conservatism (PNC) over the past few years (e.g. Revell 2008, Losos 2008, Cooper et al. 2010, Wiens et al. 2010), so one might wonder what another review can add? Given that PNC still seems to be both a ‘hot’ topic, but also one of considerable disagreement, a conceptual paper might ideally help to clarify some open questions and suggest directions that research should take in the future. In my opinion, this is exactly what Crisp and Cook have done here.

Starting with the more general part, the paper provides a nice discussion of PNC, how different researchers have defined it, and how it compares to ‘niche conservatism’ and ‘phylogenetic signal’ (and continuing the discussion of whether it is a pattern or process – I admit that I tend to agree with Crisp and Cook here…). I get the impression that there is still quite a bit of uncertainty (understandably) regarding the use of these concepts in the scientific literature, so I believe this is a very good overview.

In the next part of the paper, they highlight a number of key processes and discuss how these may lead to PNC. One that caught my attention in particular was extinction, which that could lead to a pattern of PNC as an artefact. Even if the evolution of a niche-related trait is not constrained in the first place, higher extinction rates in a particular state (rainforest vs. scleophyll biomes in their example, but it could of course also be a continuous trait like body size) may result in a pattern of PNC. I think indirect processes (like extinction) have not really received much attention in the past. Also, this is a reminder again that molecular phylogenies of extant species might give a somewhat biased picture of the evolutionary history of a clade. The growing number of ‘total-evidence’ phylogenies will hopefully contribute to an improved (unbiased) understanding of trait evolution.

Another interesting section highlights the different tests that could be used to evaluate the degree of PNC. Blomberg’s K and Pagel’s λ are well known and widely used tests for phylogenetic signal, but as other studies have shown before, Crisp and Cook point out that the relationship between phylogenetic signal and phylogenetic niche conservatism is not always straightforward (especially if evolutionary dynamics diverge from the simple Brownian motion model).

Towards the end, the authors bring up some intriguing challenges for studying patterns of PNC. For example, we need to consider that transition rates between traits might be unequal, and that different traits might be linked to differential rates of speciation and/or extinction. Finally, I did like the outlook on the possibilities that incorporating genomics offers (yes, everything nowadays is done using genomics). If we do get a better understanding of how genomic processes influence phenotypic evolution, we will be a lot closer to understanding why some specific niche-related traits are conserved in some groups, but not in others.

In summary, I really enjoyed the paper, in particular the focus on identifying the underlying processes rather than just documenting the patterns of PNC. However, given the uncertainty about the best way to quantify PNC and the potentially confounding effects of different processes, I wonder how close we really are to achieving this.

Will Pearse

Will Pearse

Crisp and Cook have written a very thorough review of what can cause different levels of phylogenetic niche conservatism (PNC), and I find it hard to think of anything they haven’t covered. So, seeing as how I work on eco-phylogenetics and am always being accused of blindly accepting PNC without giving it any thought, I’m going to play devil’s advocate and try to argue that PNC isn’t that interesting, in the hope that someone will take issue with everything below and put me in my place!

The authors go to some pains to point out that PNC is both a pattern and a process, because while some processes generate PNC (and thus it is a pattern), PNC itself generates other patterns (and thus it is a process). I don’t like this argument; increased algae in a pond is caused by putting fertiliser in that pond (and thus it is a pattern), but increased algae has implications for other species in the pond (and thus it is a process). Making predictions using algae is probably fine, but if we want to understand the system we should model the cause of algae population levels – the fertiliser. In the same way, to understand the patterns generated by the PNC, I think it makes more sense to skip the middle-man and model the process that generated the PNC itself. Perhaps the only situation in which you would care only about observed PNC is when inferring something about the present-day ecology of those species, when past evolutionary dynamics matter only in the sense that they affect species today. However, in such cases why not just use the trait data used to derive PNC and cut out the phylogenetic middle-man (regular readers know I’ve been repeating this idea like a worn-out record).

To my mind, PNC is useful to evolutionary biologists in exactly the same way that diversity measures are useful to ecologists. Diversity measures are something we can measure about a system, and help us understand the mechanisms driving that system. The authors describe how PNC has helped us understand Darwin’s ‘abominable mystery’ (the sudden radiation of the angiosperms), but in reality it is only by making models to explain PNC that we have understood it. That’s not to say that measuring PNC is not important, but understanding the origin of what we have measured is also key!

Lynsey McInnes

Lynsey McInnes

Phylogenetic niche conservatism has come up in a bunch of our posts so far, and I’m glad Jan chose this paper this week so we could tackle PNC head on. I really enjoyed reading this paper, I thought it was a well-written, balanced, but still clearly an opinionated piece that does make a useful contribution to the already overflowing literature on PNC. I thought the authors managed to cut through a lot of the confusion and controversy, but still did not sit on the fence regarding their own stance. They unreservedly come down on the side of PNC is a pattern caused by a set of processes, and the interest lies in determining what these processes are and how they do or do not generate PNC. I also appreciated their repeated emphasis that the most fruitful avenue of research is a relative approach (e.g., is this niche-related trait more conserved than this one?) rather than an absolute one.

The authors also emphasise that niche conservatism is intimately related to spatial patterns of diversity and community assembly. I feel that it is often overlooked that niches, more or less, are inherently spatial entities (this is probably debatable but most papers that purport to have looked at PNC so far are looking at conservatism in traits that have a spatial dimension like maximum climate found within a species’ range, rather than the physiological traits that actually mediate an organism being able to cope with such a temperature). Until it is easier to measure physiological traits across broad sets of taxa, these spatial proxies for niche-related traits will remain popular (and useful) so (I think) its good to explicitly realise their geographic dimension.

Clearly, you can’t cover everything in a single article, but I was surprised by some omissions/elements that were skimmed over. First, what is a niche? This was restricted to boxed text and I think the paper could have been stronger with a lengthier introduction into what a niche is, especially to get straight a definition that has relevance across clades. But perhaps this discussion has been done to death, so it was fine to keep it short and sweet. I also wonder what the authors’ views are on the difference between phylogenetic niche conservatism and niche conservatism (without the phylogenetic bit). Is there a difference? Does the concept only have meaning in the context of a phylogeny? I’m really not sure.

The authors were quite concerned with temporal scale, and the idea that some niche traits are conserved over very very long timescales and broad swaths of taxa (all angiosperms for example). There was less focus on spatial scale. I do wonder if PNC might also be interesting to study at very limited spatial scales…we often talk about tropical niche conservatism and the inability of tropical lineages to colonise temperate latitudes. But what about within tropical or temperate latitudes? There are quite some niches in both – how are they divided/shared among lineages? Are the processes that determine PNC patterns at these scales the same as those are broader spatial scales?

The authors do highlight, as did Jan, that the advent of genomic datasets might be helpful in this regard. What genes/mutations/phenotypes/selection pressures/genetic backgrounds are responsible for the patterns that we see? How does the genetic basis differ depending on the process that produces the pattern? Perhaps the only way we are going to clear up the confusion and controversy surrounding PNC is to get down to the genetic basis of the ACTUAL traits that produce these patterns? Perhaps not…?

And, I have to say it, I am really interested in the insights we might gain from looking at niche conservatism below the species level. Niche conservatism is often looked at in traits emergent at the species’ level (e.g., mean temperature across the species’ range). What can we learn if we look at geographical variation in temperatures found within in the range? Are populations within the range located adapted to temperatures they are exposed to? This is directly related to the recent paper we discussed on cosmopolitan taxa – how do they get to be/stay cosmopolitan? But probably also has relevance for species with even moderate range sizes. How does niche variation/conservatism within a species relate to conservatism among species?

I concede that this has become a bit of a ramble on thoughts in my head about PNC in general rather than related to the paper itself. Sorry about that. But thank you to paper for provoking all these, perhaps tangential, things to think about. I do wonder quite why the study of PNC has taken off in quite the way it has. It’s related to data availability for sure and bandwagons, is there anything else? The authors note that the concept was already thought about by Tansley, I wonder where its next steps are?

Convergence, adaptation, and constraint

Jonathan B. Losos. Evolution 65(7): 1827-1840. DOI:10.1111/j.1558-5646.2011.01289.x. Convergence, adaptation, and constraint

Are these Anolis dewdaps constrained? Maybe more than you’d think… (PLoS One; click for source)

Will Pearse

Will Pearse

We’ve covered too many data papers recently (that’s not a joke, but it does read like one), and so I picked this paper to help us step back a little and think. I’m pleased with the result: this is an excellent essay, that really made me think about what convergent evolution actually is. I’m particularly keen to hear what you all think of my comments about history!

Losos argues convergence is scale-dependent: there are many ways to evolve a long beak, and while there may be divergent evolution of the actual genes involved, the resulting phenotype (a long beak) is convergent. We’ve covered convergent evolution in bacteria, where the same genes (but different regions of those genes) mutated in parallel in separate lineages. I like this scale-dependency – it allows us to define convergence so that it’s amenable to study at all levels from phenotype to genetic mechanism.

I think we can push this framework further, and compare very different systems in meaningful ways. For instance, maybe examining constraints to evolution in responses to predation in Daphnia is easier when you consider what constrains their tolerance of the abiotic environment. Maybe seeing particular stressors and evolved responses as analogous to one another allows us to better compare evolution among clades, and view constraints to evolution in a more holistic way..

Apparently, there are some who take the view that evolutionary changes are incomparable historical events, and so the whole idea of convergence is a nonsense. I think this is rather peculiar; while there is a debate in history as to whether the field is a science (I think it is, but I’m not a historian!), every historian I know compares periods and events in history, with the precise aim of drawing parallels among periods. Thus I think the argument that evolution is the study of history, and therefore will not allow us to compare events, is not one even a historian would agree with!

Lynsey McInnes

Lynsey McInnes

Commenting on a Losos paper is always going to be tricky, as this is a man who knows his evolutionary biology! You can tell this in two ways, first simply by the breadth of examples he draws on and second by his daring to question the be all and end all of phylogenetically-informed analyses, another recent examplesof his critique of such analyses can be found here.

Like Will, I appreciated having a week off from data bashing and am currently juggling all the different issues that Losos brings up on what is and is not convergence, parallelism, adaptation, exaptation, etc. The biggest take home message I got from the essay was that, as always, scale matters. Birds and bats both have wings that let them fly, are these convergent traits? Depends on your scale of comparison. It seems like identifying instances of convergent evolution would be simplified immeasurably if the researcher concerned just set out the scale across which he is looking and perhaps also mentions whether he is worried about the trait being the ‘same’ at the genetic, phenotypic, morphological and/or morphological level. Hey presto, confusion and agro could be gotten rid of.

I can’t help comparing the issues brought up here to the ones Losos, and plenty of others, have attempted to deal with concerning identifying instances of niche conservatism. Again, it all depends on scale. Cooper et al. provide an excellent roadmap for conducting analyses on nice conservatism, I’d like to see a companion piece to this essay detailing the practical approaches to sensible analyses of putative instances of convergent evolution.

I’ve recently shifted the scale of my own analyses to incorporate (currently to deal exclusively with) intraspecific variation. In practice, this has meant starting to think about different models of mutation (infinite site, infinite allele, shitty recombination raising its ugly head begging to be dealt with) so I find my scale of analysis shifting to the genetic level, wanting to see mutations in same genes, indeed at the same sites to qualify as parallel evolution. For this reason, I really appreciated this essay as it forced me to address my newfound genetics-only bias and realise that interesting, valid and evolutionarily important convergent changes at the functional (or even just phenotypic) level need not be produced from identical genetic changes.

The recent bacteria study that we discussed here at PEGE was a brilliant example of a standalone set-up for studying evolution across these different levels (genetic, phenotypic, etc.), the next step, as always, is to devise a set-up that facilitates similar inference in systems where access to all these levels might be patchy. Losos’ essay will undoubtedly be helpful in this regard.

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