Phylogenies support out-of-equilibrium models of biodiversity

Manceau et al. 2015 Phylogenies support out-of-equilibrium models of biodiversity. Ecology Letters 18 (4): 347-356

Overview of speciation underManceau et al.'s model.

Overview of the new Speciation by Genetic Differentation model of Manceau et al.

Will Pearse

It’s been a good few months for Neutral Theory in Ecology Letters (…and so, by extension, PEGE!). In this paper, Manceau et al. put forward an extension of Neutral Theory, including a new model of speciation (Speciation by Genetic Differentation), and relax the dependence upon a static metacommunity. Both are exciting extensions to the theory.

The concept of the meta-community is something that’s always troubled me about Neutral Theory, because it seems a bit much to appeal to something outside the system to keep the system stable. Yet at the same time the only thing I can think of that’s less realistic than a meta-community is not having a meta-community, since clearly no community evolves in isolation. In this model the meta-community can change through time (i.e., it’s not at equilibrium); it’s no longer a deus ex machina, and is instead a part of the ecological theatre (see what I did there? :p).

Equally, the speciation mechanism the authors put forward is a useful development. I’m a fan of protracted speciation models, but my general problem comes from fitting them onto a specific evolutionary process. I don’t doubt they describe pattern and process well, but they don’t seem to be linked to one process in particular. Thus the genetic differentation model the authors suggest is, to me, extremely exciting. As with all these exciting new models, it’s almost a shame that the cleverest bit – the maths – is too complex to present in the body of the paper (I say almost a shame, because I’m certain I wouldn’t understand it!).

To me, the most important concept in this paper is that telling phrase ‘out of equilibrium’. Arguments about whether diversification is or isn’t density-dependent are never going to go away, but there are some who are calling for the debate to happen in the context of recent ecological theory about what carrying capacities in systems look like. Personally, I think that a discussion on density-dependence has to happen with an understanding of species’ abundances, and that means individual-based models. Work like this is an important step towards this.

Lynsey McInnes

Lynsey Bunnefeld

It has indeed been a good couple of months for neutral theory at PEGE. Here, we have another tweak to Hubbell’s original theory to bring phylogenetic tree topologies more in line with empirically observed trees. Specifically, the authors tweak the speciation mechanism from point or random fission speciation (i.e., instantaneous) into ‘speciation with genetic differentiation’ such that new species form only when they have accumulated enough mutations to be distinct genetic ‘types.’ Furthermore, the authors relax the assumption of constant metacommunity size instead allowing size to vary stochastically according to the growth (birth – death) rate of the clade.

I must admit I read this paper far quicker than it merited, so my thoughts are a bit hazy and any qualms might be unfounded. On that note, here goes…

I did appreciate the positivity bouncing around in this paper. The authors were resolutely positive about the capacity of phylogenies and macroevolution in general to inform us on diversity patterns. This was nice to see as many people, myself included, often despair on the ability of phylogenies to tell us anything.

Their two tweaks to neutral theory also sound, on the whole, sensible tweaks that make sense given what we know about species and given that we agree we want to retain the simplicity of the neutral theory while identifying the key assumptions that make it fall down.

First, speciation by genetic differentiation. Indeed, closely related species generally do differ genetically. Whether this difference is just an accumulation of neutral mutations or some kind of adaptive divergence (and which of the two kinds is more common) is another question. I felt like the authors could have discussed this issue more deeply because as a naive reader I was left wondering about the biological reality of such an abstract speciation mechanism. Sure, the model does not claim to be 100% realistic, but a discussion of the different signatures expected depending on the speciation mode would have been nice. The authors talk a lot about future directions and models they would like to compare theirs too (e.g., Pigot’s biogeographic model) and I look forward to hearing about these extensions. They somewhat cryptically refer to some lineages acting like speciation hubs that presumably shoot out new species willy-nilly. What kind of lineages would these be? Large ranged? Sexually selected? Weird mating system? Host shifter?

Second, growing/shrinking metacommunity. I agree with the authors that a constant metacommunity seems unreasonable. But I would have liked to hear more about how a growing/shrinking metacommunity might come about. Are we talking about finer partitioning of a finite area or colonisation of new habitats or competitive exclusion of crappy species, or what? Is a metacommunity the right term to use when we are thinking about the interactions of ENTIRE species. Could populations of the same species occupy different metacommunities? (Meta-metacommunities!! :$).

My hunch is the authors have also thought of all of the above and this is just a first pass attempt, albeit an impressive one that (again) shows that with just a few small tweaks the overall premise of the neutral theory is really useful in understanding general diversity patterns. I remain on the fence whether all this tweaking is destroying the original premise of the neutral theory (as I see it, to provide a conceptually simple null with which we can work out which non-neutral processes really do matter).



A new dynamic null model for phylogenetic community structure

Pigot & Eitenne 2015 A new dynamic null model for phylogenetic community structure. Ecology Letters 18(2) 153-163

Figure 2 from Pigot & Etienne. Plots of likelihood of community membership under low (top) and high (bottom) rates of local extinction. Or, if you prefer, a series of variously coloured and not-coloured phylogenies.

Figure 2 from Pigot & Etienne. Plots of likelihood of community membership under low (top) and high (bottom) rates of local extinction.

Will Pearse

As if by magic, the ‘new’ approaches I hoped would appear last post have done so. It’s almost as if I know the posting schedule ahead of time!… Alex Pigot and Rampal Etienne have produced an analytical framework within which we can distingush between speciation, extinction, and colonisation in structuring an assemblage’s phylogenetic structure. Beyond that, they have developed a method that uses phylogeny to its true potential: not a proxy but unique data that helps us estimate evolutionary (speciation and extinction) and ecological (migration) processes of interest.

This is an important contribution because the problem of dispersal is one that has vexed many for some time, yet (with notable exceptions) received relatively little attention. Dispersal from a wider source pool provides an important link between ecological and evolutionary time-scales that we need to model. A species ‘appearing’ can either have an evolutionary (speciation) or ecological (dispersal) origin, and that their DAMOCLES model can at least start getting at that distinction is important. It is of little surprise to anyone who has followed these sorts of studies that phylogenetically overdispersed communities can result from something other than competition, but linking its origin to evolutionary and dispersal events outside a community is interesting.

There are, of course, additional complexities that could be built on top of this model, and I’m not going to bore you by rambling on about traits because I think you all know where we want that to be going. However, I think it’s important to explicitly consider the meta-community (or source pool, if you prefer) from which these species are being drawn. Focusing on one assemblage is useful, but the reality is that speciation and extinction dynamics are happening at biogeographic scales, and we desperately need to link community-scale models such as these with those. Considering multiple assemblages undergoing these kinds of dynamics could be a good place to start. I wonder if the limiting factor may be finding something analytically tractable; while simulating individual communities linked within a wider system is reasonably feasible, doing so analytically (as the authors seem to have started doing) is more difficult.

Lynsey McInnes

Lynsey Bunnefeld

Alex Pigot has a way with null models. He’s already shown that the arc of species’ range size over the course of a species’ lifetime is not necessarily the result of deterministic processes and now he (and Rampal Etienne) have shown that common patterns of community assembly need not be the result of negative biotic interactions if an appropriate null model is used. Wow.

This paper is a great example of a couple of key points that I am most definitely guilty of ignoring. 1. taking time to think whether your null model is biologically as well as statistically null is important. 2. important insights can be made even before your model includes every last contributing factor (see Will’s post above). 3. data examples are important to illustrate your method. Nice.

I’m now going to largely disregard all those things I just said were important and wonder how you might extend this model and wonder what pesky real world effects might topple the null expectation.

I wonder how biotic interactions with non-clade members affect community assembly, i.e., competitors, predators, prey, hosts, etc. I wonder what a null model for this might look like? Should hosts/parasites (for example) evolve in tight coevolution, or not? I wonder what repeat processes of community assembly look like? Always the same, or not (I’m sure this has been treated in microcosms and by Gould). How would phylogenies help with these questions? In the same vein, I wonder how what happens to the new sister species that does not enter the community of his ancestor? I guess I am pondering the effects of space. I have no doubt the authors have too, and would not be surprised if they already have the answers up their sleeve. The authors deal elegantly with variation in a quantitative trait (or traits) meant, I think, the characterise niche. I wonder what happens when you throw in variation in other traits, probably dispersal ability (haha, with all the trauma that goes with defining and measuring that!).

A mean field model for competition: from neutral ecology to the Red Queen

O’Dwyer & Chisholm 2014 A mean field model for competition: from neutral ecology to the Red Queen. Ecology Letters 17: 961-969

I'm reliably informed that this is actually quite simple to understand! Equation 2 from O'Dwyer & Chisholm.

I’m reliably informed that this is actually quite simple to understand! Equation 2 from O’Dwyer & Chisholm.

Will Pearse

To spoil the punch-line, I’m not sure I completely agree that the model in this paper is biological defensible, but I’m quite certain this is a very important contribution. The authors have found a way to incorporate species differences into neutral theory: the most recently speciated species out-competes all others, and as a consequence phylogenetic branching times become more reasonable. Much ink has been spent suggesting Neutral Theory will form the building blocks of models that incorporate species differences, and this (finally!) is an extremely important piece of such work. My main concern is that I think, to be biologically defensible, there has to be some kind of inheritance of fitness from the new species’ ancestor. The only way I can see the youngest species being the best is if the driving force of biology is pathogens – the authors point towards this, and somewhere Ricklefs is jumping for joy – but I just can’t see it. To me, this would require that we change (again) the scope of Neutral models from covering species within the same guild to covering the same ‘pathological guild’. Moreover, I find it hard to believe that each speciation event is coupled with a magic trait that pathogens must evolve, from scratch. Surely a species in a large clade, presumably with an equally large body of pathogens, is even less likely to have such a trait evolve, and we have yet another way for diversity-dependence to rear its head. That said, all is certainly not lost, and this is an (extremely impressive) start. If a similar model could have multiple guilds nested within itself, and allow some degree of exchange between the guilds, I would have little trouble getting behind it. Using diffuse competition to approximate the competitive hierarchy was a wonderful moment in the paper, and it’s fantastic to see an argument used to defend Neutral Theory extending, not defending, it. If we can use these kind of approximations to bring even more niche-based concepts into Neutral Theory, things are looking up!

Lynsey McInnes

Lynsey Bunnefeld

I am still on the fence about this paper. On the one hand, I admire how they have taken neutral theory and changed it a bit in order to produce predictions that more closely match what we see in reality (specifically, they assume new species are fitter than all older species and that leads to more realistic distributions of species ages than the hardcore neutral theory where all individuals are equivalent). This is impressive. On the other hand, this is a bit of a weird tweak to make and doesn’t really seem to be biologically defensible, at least not generally.

I like the idea of neutral theory. I like its simplicity and the fact that it is remarkably good at predicting a lot of recurrent patterns we see in nature. I even like the way it sometimes fails and I really like that it can really irritate people. It is fun to watch people get stressed out about it. I agree that if it is to continue to have relevance, it needs to be continually scrutinised and tweaks applied and tested. This paper provides a remarkably simple and tractable tweak to deal with one of the outstanding issues with neutral theory – that is tends to predict unrealistically long species ages. By making new species fitter than older ones, the authors are able to purge communities of older species more quickly and so reproduce patterns that more closely match those observed in nature. Neat.

But wait? Are new species typically fitter than old ones? The authors’ argument for yes appears to hinge on the new species being free, or at least relatively more free, of nasties that could hold them back. I’m no expert, but my intuition is that not all, or indeed many, new species are ‘free’ in this way. Indeed, don’t most species come about through divergence in geographically or ecologically distinct arenas and might be really quite similar to their close relatives apart from in a key few traits (and not even that sometimes). Indeed, there seems to be mixed evidence at best that you shed the majority of your parasites upon speciation.

OK, but if the assumptions of this model sit uneasily, what other tweaks might be made to neutral theory to reign in unrealistically old species ages? At this is when the authors’ ideas become harder to put down. They have recognised that you need to find something that ‘gets rid’ of older species and their idea seems at least a bit better than species just having an ‘intrinsic’ life span (cycle of life style). An idea that has been bandied about, but with lots of quite robust refutation too. What else might do it? Some kind of slowing down of adaptation to changing environment? Some kind of competitive density effect? Some kind of lag in competitive interactions (your enemies catch up with you and get rid of you?). None of these sound particularly promising.

And so, while I might not agree with the authors’ model I’m pretty happy that people are producing such models and refining and refuting things further. One day we might be able to figure out where these recurrent patterns in biodiversity are coming from and the relative importance of niche and neutral processes. We won’t get there without trying.

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!…

The ecological dynamics of clade diversification and community assembly

Mark McPeek. The American Naturalist 172: E270-E284. The ecological dynamics of clade diversification and community assembly

Blue damselfly; McPeek has studied damselflies extensively. Taken by Umberto Salvagnin (via Wikimedia).

Blue damselfly; McPeek has studied damselflies extensively. Taken by Umberto Salvagnin (via Wikimedia).

Lynsey McInnes

Lynsey McInnes

I picked this paper because I remember reading it when it came out and being taken in by McPeek’s approach. It felt like he had built up a pile of phylogenies with negative gammas (a metric mired in controversy, but that’s for another post) and then he decided he should find out whether more or less feasible processes of ecological or non-ecological divergence generate similar distributions of gamma values.

A short background note: Pybus & Harvey’s gamma purports to detect ‘slowdowns’ in diversification by quantifying the pattern of nodes in a reconstructed phylogeny. In brief, if nodes cluster near the root of the tree, gamma is negative and this indicates that diversification has slowed as we approach the present. Positive gammas could suggest that diversification has sped up as we approach the present, but inference is complicated because of the signal left by extinction, such that a positive gamma does not unambiguously support a particular pattern. Since publication of McPeek’s paper there has been a swath of further papers documenting problems with the metric, probably the no.1 being that you get one gamma value per tree so the results will be dependent on what scope of clade you have chosen as to whether you can detect a clean slowdown or not. Again, this is not a post about the ins and outs of gamma.

Rolling with the assumption that gamma can provide a useful summary of the distribution of nodes in your tree, it can be used, as here, to quantify the different branch lengths attainable under different diversification scenarios. Regular readers will know I have a soft spot for simulation studies, so could anticipate that I liked McPeek’s setup here. Basically, he wanted to find out whether if, he enforced ecological divergence upon speciation, trees are produced that show signs of slowdowns in diversification (as ecological gradients are filled in). And this was indeed what he found. Some might argue that you get out what you put in, and presumably this is true to some extent. But I still found it a neat and tidy finding.

Now its time to go off on a tangent. Don’t get me wrong, I like this paper and appreciate this kind of study. I really believe that many clades are probably subject to slowdowns as they diversify and this might often be because they have filled some limited set of ecological niches and additional species are formed by geographic isolation without ecological divergence or some other mechanism like sexual selection or filling the niche of a species that has gone extinct. I just wonder how easy or indeed, possible, it is to detect the signal of this diversification trajectory on phylogenies. Perhaps the pattern emergent at the ‘evolutionary’ timescale is rough enough that slowdowns or equilibrial diversity dynamics are detectable and ‘real’ and the more haphazard activities occurring at ecological timescales will always be evened out and undetectable and this is OK. I’m also intrigued by methods that work ‘the other way’ and take massive phylogenies and try to delimit more restricted clades that somehow obey these slowdown patterns. It often seems like taxonomists’ brains have worked in similar ways and genera and families conform to these delimitations. Which is actually pretty cool.

In short, I am mesmerised by broad-scale patterns in phylogenies and often buy into the current trend of assigning ecological explanations to them. In some sense, ecological and evolutionary processes are all part of one continuum so must impact each other, but how often have we made ourselves believe that something more than just random spliting processes are at play. I’ve currently turned my back on macro-scale analyses, but will always have a soft spot for finding out how these crazy, very clearly real, patterns are generated and why.

Will Pearse

Will Pearse

This paper is the scientific equivalent of Samuel L  Jackson in Snakes on a Plane; an old-school “I just sat down and thought” kind of paper, and I like it. It’s probably the best example of how a simulation study can be insightful, starting with some fundamental observations from empirical data, and making a model just complicated enough to derive insight.

McPeek’s reviewer raises a very good point: what does it mean for the fossil record if his simulations shows we get species appearing and then rapidly disappearing? This reminds me strongly of raceme phylogenies, although I think it’s an open question whether these short-lived species would ever be so abundant as to swamp out the main ‘trunk’ of the tree of life. That said, most people would agree speciation is rarely instantaneous, and the shape of the simulated phylogenies would probably be different if a species only became a true species after a delay (à la protracted speciation), even if those proto-species were still ecologically different from one-another.  It makes me wonder the extent to which the diversity on Earth right now is comprised of these side-shoots, and how many of these species (ignore our influence for a moment) will be around in a few million years.

I also enjoyed the discussion of variation in structure among clades. There is no reason to assume that models of evolution are constant across a clade simply because, in the present, a researcher has decided that a particular group forms coherent ecological assemblages. As always, I’m convinced that different ecological processes should be operating in clades that have undergone different kinds of evolutionary processes, but drawing a distinction between ecology and evolution is somewhat arbitrary. The power of McPeek’s approach is that there is no disconnect between the two: in his models, evolution is just ecology over-and-over-again, and examining the two simultaneously must ultimately be the best approach.

There is one caveat to this. Many (and McPeek notes this) are quick to point out that we may never be able to estimate extinction and speciation rates using phylogenies. There are very, very few cases where the fossil record is as rich as we would like, and a molecular phylogeny necessarily misses extinct species. While modelling exercises like this are fantastically useful, I am somewhat skeptical that we can ever reliably fit models this complex to real data; of course that doesn’t mean we shouldn’t try!

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.

Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology

Stefan Hempel et al., 2013. Ecology 94(6): 1389-1399. DOI:10.1890/12-1700.1. Mycorrhizas in the Central European flora: relationships with plant life history traits and ecology

I'm reliably informed there are some mycorrhizae in this photo...

I’m reliably informed there are some mycorrhizae in this photo…

Will Pearse

Aaron David

One of the overarching goals in ecology is to understand the distributions of species and how interacting species shape these distributions. In the world of plant-symbiont interactions, one ongoing question is when is it advantageous to have a symbiont? Hempel et al. compile a dataset of Central European plants and their mycorrhizal associations in order to address several ecological hypotheses. Hempel et al. classify plants as obligate (OM), facultative (FM), or non-mycorrhizal (NM), and ask whether certain types of plants are more associated with various life-history traits (ie. life-form, life-span, pollination, etc.) or environments. The authors find support that different mycorrhizal statuses are over/underrepresented in with different traits and environments. The paper provides strong evidence that mycorrhizal associations may influence plant distributions, and that the benefit of such associations is very much environment dependent. Those such patterns have been shown for individual plant species, Hempel et al. show the generality of this pattern using a large set of plant species.

The authors tackle the exciting question of when it is advantageous to form mycorrhizal associations. For instance, they report that OM plants are found in higher than expected abundance with low soil acidity, while FM plants are found in higher abundance with high soil acidity (NM abundance wasn’t affected by acidity). This result was somewhat puzzling to me, as I would have expected the NM plants to be found with the high soil acidity and the FM to be unaffected. This could suggest that while some plants are able to adjust their associations in different environments, this may not be a general rule for FM plants. The authors define FM plants as those that can form a mycorrhizal association but are not always found with one. Therefore it’s possible that the FM plants as a whole might be composed of NM plants with the occasional mycorrhizal association. It would be interesting to see the FM group split into more definitive categories.

As a fungal ecologist, I found this paper provided interesting insights towards questions of fungal distributions. One of the burgeoning areas in fungal ecology is understanding the distributions of mycorrhizal associations (see the work of Peter Kennedy). Hempel et al.’s results suggest to me that these limitations to mycorrhizae distributions could arise from local environmental conditions or host plant distributions. Of course as the author’s note, it’s not necessarily clear which symbiont is limiting the other. One way to test this idea would be to overlay maps of mycorrhizae distributions with those of plant distributions. Environmental sampling of soil can be used to get a broader picture of mycorrhizae distributions, since many may live as saprobes in addition to being symbionts, though it’s likely the authors could generate a similar distribution map using their available data. Understanding both sides of symbiont distribution would more fully address how species are limited.

Will Pearse

Will Pearse

I’m no mycologist (for what it’s worth I love eating them), but I still thought this was an interesting paper. Literature reviews like this, where massive databases that are going to be of use to future scientists are just thrown out for all to enjoy, are exactly what science should be about. Hurrah.

I think the conclusions of this paper are sound, but I’m going to draw attention to two things just to be picky. Firstly, I have been brought up to think that the phylogenetic corrections employed here should be avoided (listen to Rob Freckleton please). This is a very touchy subject (I’ve heard of people bursting into tears over it!), but in brief the authors create eigenvectors that represent the phylogeny, and then by including them in their analyses hope to correct for phylogeny. A similar approach is used in spatial analyses, but for both it’s hard to know how many eigenvectors is ‘sufficient’, and it’s always unclear to me why you wouldn’t just other methods that directly incorporate the phylogenetic variance-covariance matrix you’re making eigenvectors to describe. Phew. Got that off my chest. Secondly, I wonder what effect the publication bias (that the authors find) will have on these results, particularly as the results are in agreement with what we might expect.

However, as I say, I think the results are pretty sound, and so I wonder whether we could model the co-evolution of plant and fungi. Indeed, there are some very neat new methods (we covered one recently) that examine these questions. More specifically, I wonder if the evolution of a tight association with mycorrhizae would allow a clade to break away from its close relatives and suddenly radiate out into as-yet unexplored habitats and niches. Equally, there could be links between mycorrhizal diversity and plant associations, although I’m almost certain this has already been looked at, and defining fungal species is hard (I think!). I’d quite like to hear from more fungus people!

Is regional species diversity bounded or unbounded?

Howard V. Cornell, 2013. Biological Reviews 88(1): 140-165. DOI:10.1111/j.1469-185X.2012.00245.x. Is regional species diversity bounded or unbounded?

This post is PEGE’s contribution to the first PEGE/EvoBio journal clubs crossover. Add your comments to the bottom of this post and then come and join us with the guys over at EB-JC ( next Monday (May 13th, 4:30p ET) to discuss things further over video chat.

EB-JC works a bit differently from us so we are keen to join forces and see what happens.

Is speciation rate bounded, unbounded, or... sort of both?

Is speciation rate bounded, unbounded, or… sort of both? (from Cornell 2013)

Will Pearse

Will Pearse

This paper is a brave attempt to reconcile the debate over what limits diversity through evolutionary time. Cornell’s ‘damped increase hypothesis’ is a compromise between a constant (unbounded) rate of speciation and one where clades have a (bounded) carrying capacity determined by ecological interactions. He acknowledges that diversity tends to increase through time, but this increase can be tempered by ecology; those looking for fireworks should look elsewhere (go read ‘that’ Wiens paper), because this is an attempt to reconcile and move forward.

It’s easy(ish) to derive models of evolutionary diversification, the problem is finding reliable data to validate them. You can’t sequence what isn’t here, so molecular phylogenies can’t incorporate extinct species, while the fossil record has biased sampling and makes it difficult to distinguish among species and higher taxonomic groups. Moreover, distinguishing between a clade becoming more diverse because of increased speciation or decreased extinction would be hard even with perfect data. Despite a number of really cool methods (I like these), I sometimes worry we may never be able to sort this mess out.

Much of this paper hinges on whether niche space ever gets filled. If species can fill up niche space, then it’s reasonable to expect that competitive effects would limit diversification, and Cornell’s first conclusion is that we need more experimental tests of whether these kinds of competitive effects exist. That’s not to say we need more research on competition – we have decades of that in ecology – but we need more explicit tests in extant clades that biogeographers are examining. We can’t turn back the clock, but we can validate the assumptions of our models in the present where we’re not data-limited. Now that is eco-evolutionary modelling!

Cornell spends a good deal of time discussing the importance of migration on clade dynamics, and species moving into an area and occupying niches is a rather thorny problem. However, I’m just not sure we’re ever going to be able to handle this; after decades of work, we’re only just beginning to understand how we can model species’ distributions in the present day, and attempting to do that using only biased fossil distributions for all of evolutionary time sounds like an incredibly tall order. Perhaps one thing we could do is look for correlated extinctions/speciations in the fossil record. Imagine a new species has just evolved that occupies a new kind of niche; if we assume it spreads essentially instantaneously in evolutionary time, any slow-down in other clades’ diversification rates should be immediately detectable.

Lynsey McInnes

Lynsey McInnes

This paper has been in my to read pile since I spotted it sometime last year. It probably remained there because it’s long, dense and comprehensive and takes more than a commuter train ride to get through. So when Rafael Maia over at Evo Bio journal club challenged Will and I to find a super cool paper on the geography of speciation, we decided to go with this one as it more or less covers ALL super cool papers on the geography of speciation ever published. So, thanks Howard Cornell for summarized this research field for us and providing us with plenty of food for thought for our first EB/PEGE journal club crossover.

For those of you who know me/have read my posts here at the site, you can guess that I chose this one and that it appeals to my interest in understanding the spatial nature of diversification. First, a note about the style of the paper. I really enjoyed reading it, and managed the whole thing in a single sitting and I think that is down to Cornell’s extremely clear writing style and his total command of the subject he is writing about. Wow. I was also impressed with his ability to navigate through a field that has become quite contentious in recent years; he managed to extract relevant points from a suite of Rabosky & Wiens papers without explicitly acknowledging the animosity apparent between these two camps. In fact, he elegantly concludes that regional diversity is, in effect, both bounded and unbounded and puts forward the damped increase hypothesis to cover this inclusive idea. Hoorah.

Enough rambling, what has Cornell left us to talk about?

First, I really liked his repeated emphasis on taxonomic scale. By this, he meant the conclusions we reach on the diversification of a clade will dependent on the breadth of diversity found within the clade (i.e., a subclade of mammals, a clade restricted to a single region, a clade found in a region with ecologically-similar species from different clades, a clade that has newly-colonised an area, and vice versa). I think this is an underappreciated point within macroevolution and one that deserves more explicit treatment in the future. If we are using a phylogeny to understand diversification of a group, we want to use a well-defined monophyletic clade, maybe we even want to compare two or more than two monophyletic clades. This is fine and admirable, but when doing so, we have to remember that the clade does not exist in isolation (ecologically-(dis)similar species probably occupy the same area, the clade probably included additional taxa that have now gone extinct, the size and nature of the area it currently occupies have probably changed substantially since the origin of the clade, and so and so on). If we really, really want to understand how clades diversify, we have to try really, really hard to account for at least some of the above. At the very least we have to circumscribe what we are trying to understand (How an area became populated? How a clade diversified? How extrinsic/intrinsic traits shape diversity/diversification?)

Years ago, I remember Joaquin Hortal – community ecologist extraordinaire – scoff in the face of the idea of ecological limits to diversity. His reasoning was that he knew of no system that was totally full, there was always scope to squeeze in new species if only the new species could be transported to the area in question. I kinda believed him, but somehow decided that he was talking at some kind of narrower scale than me, that at the continental scale or global scale of entire clade (what is an entire clade?!?!), limits could be reached. I think Cornell’s paper is the first I have read that both implicitly recognises and reconciles these multiple scales that I had in mind. I do wonder if we will ever work out a way to identify the optimal spatial and taxonomic scale to look at how diversity is generated or even if such an optimum exists?

To conclude a bit of a rambley post, I really appreciated this paper. It summarized the weight of evidence for two hypotheses that had somehow recently become quite polarized in the literature and emerged with a happier medium incorporating the best bits of both. Cornell also sets out his vision for making progress in this field and this involves taking a more thoughtful approach to improving our understanding of regional diversity patterns: collect more and better data, incorporate multiple types of data in any analysis, analyse it properly, and perhaps most importantly think about the SCALE of your analysis before you set out and as you interpret your results. Onwards and upwards!

Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes

Banks-Leite et al. 2013. Ecology 93(12) 2560-2569. DOI:10.1890/11-2054.1. Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes

Below, we give our first impressions of this article. Please comment below, or tweet Will or Lynsey (maybe use #pegejc). Think of this as a journal club discussion group!

We both wrote our responses quite rapidly this week, but decided to post them anyway and hopefully start a discussion with our readers. Both of us found this paper thought-provoking and hope to have more coherent thoughts to add later in the week…

Will Pearse

Will Pearse

I picked this paper almost entirely on the basis of figure 1b – the fit looked so good I had to read the paper to find out what it meant. The central claim of this paper is that SAR curves miss changes in species composition when fragmentation takes place, meaning there is a disconnect between species richness and the local extinction of species. The quality of the analysis and the size of the dataset make this a particularly pleasant paper to read, and it reminded me of things (like SLOSS, see below) I haven’t thought about for some time.

The 1970s were a good time to be a conservation biologist: you could still fly to conferences without feeling too bad, and debate was raging about whether to have a Single Large Or Several Small (SLOSS) conservation reserve. This paper is a perfect example of why this debate was never fully resolved: larger fragments may have a higher species richness, but they don’t necessarily contain the same species as smaller fragments. To my mind, this is the clearest demonstration of this effect to date; figure 3d shows more species in larger fragments, but (crucially) there are species present in larger fragments that are absent from smaller fragments, and vice-versa. Going further, a fragment’s surroundings matter too: small fragments in pristine forest resemble larger fragments in near-pristine forest, but are nothing like the smaller fragments in heavily deforested surroundings. Hence all of the figures in this paper are sorted by surrounding forest cover, and then fragment size. Let me say this again: I don’t think I’ve ever seen such neat graphs. Ever.

Which is perhaps something to do with individuals’ range size. I’m no field biologist, but some birds fly quite a long way during the day, and others don’t. This means that different spatial scales of habitat damage are going to be relevant for different birds, and extreme logging of forests might be expected to affect wide-ranging birds first irrespective of the size of individual fragments. Could these kinds of traits, which reflect the use of the surroundings (matrix) by birds, be incorporated into further analyses? Perhaps similar things could be found when comparing among taxa – would insects that disperse only a few meters in their entire lifespan produce as nice graphs as these?

According to the supplementary materials, these fragments are ~40-60 years old, so (in my opinion) these are fairly mature fragments – we’re certainly not seeing the immediate after-effects of fragmentation. Which makes me wonder what those species that specialise in smaller habitat patches represent – what kind of Amazonian species is pre-adapted to small fragments of forest in a sea of deforestation? If they’re not that well-adapted to Amazonian living, and have only come in with deforestation, are they definitely using the forest fragments, and not just passing through? Is it possible to quantify the extent to which particular birds are using a resource? I’ll end on that – if anyone knows how this can be done with mist net data, please let me know. I’ve only done a tiny bit of mist-netting and pit-fall trapping in my time (I was dreadful!) and I often wonder how we’re meant to handle transient passers-by.

Lynsey McInnes

Lynsey McInnes

Typically, I shrike at reading ‘Ecology’ papers – I’m not an ecologist I say to myself. Since joining a department more or less full with population geneticists, it turns out I AM an ecologist, albeit somewhat by accident. Needless to state, Will picked this paper and I went along with it because I like species-area relationships…

That was the first concept to be knocked down, turns out SARs suck at characterising community responses to habitat fragmentation! Ooops.

I found this paper really neat. Very cool, very precise question, amazing data, very sexy, very understandable simulations! I really have to stop myself going to have a play with the R code that does the simulations (also neat that this is provided!).

The rationale for the study and the conclusions they come up with seem robust to me, I am just now wondering whether there are any comparably good datasets where these questions could be asked again? Is such a comprehensive dataset necessary? (Probably yes, right?)

I’ve been a bit lazy and not read the J Appl Ecol. paper where the authors test a bunch of metrics to come up with an adequate one for community composition so I was a bit disappointed that the rationale/robustness/power of the measure chosen wasn’t better explained here. Is it biased in anyway? Does it miss anything?

With my macro-hat on, I wonder if this setup could be used to look at turnover/composition on broader temporal and spatial scales. For example, debate is still raging on ecological limits to diversity, lots of signals point to the diversity-dependence of cladogenesis and this is typically explained by niche filling (diversification slows down as niches get filled), lineages competing for limited resources/niche space. However, how does this really work on broad spatial scales where few lineages within a radiation will actually ever come into physical contact, let alone interact. And perhaps more relevant here, the region in which they diversify is not just one homogeneous blob, but a matrix of different sized habitable units more or less connected to each other. I’m rambling a little, but I think incorporating landscape features in models of spatially-explicit diversification may help in explaining the patterns that we see (I have to think more about this though).

Two more things:

  1. I guess (and Will’s the expert here), on broader scales similar studies have been undertaken under the umbrella of community phylogenetics. I’m still getting a handle on how this study fits with the latter…Also, what would happen if we added a phylogenetic take on compositional turnover? Would it simplify things? Box out traits relevant to persistence in the different fragments?
  2. What does this mean in terms of practical conservation guidelines now that we cannot fall back on the faithful SAR? It sounds to me like we need to get our hands on way more elaborate datasets of species identity and move from there into the traits that the different species bring to the fragments they can persist in. This sounds difficult. Are there any easy work-arounds?

Apologies for a very rambley, not well-thought out response to this article. In short, I really enjoyed it, it made me quite fearful for all those conservation decisions based on species numbers and made me thoughtful on whether these insights and setup could bring clarity to questions typically asked at different scales. Watch this space…


Founder takes all: density-dependent processes structure biodiversity

Waters et al. 2013. Trends in Ecology and Evolution 28(2) 78-85. DOI:10.1016/j.tree.2012.08.024. Founder takes all: density-dependent processes structure biodiversity

Below, we give our first impressions of this article. Please comment below, or tweet Will or Lynsey (maybe use #pegejc). Think of this as a journal club discussion group!

Will Pearse

Will Pearse

This week’s paper is a whistle-stop tour of how diversity-dependence drives a lot of ecological patterns, and I found it pretty damn hard to disagree with anything they wrote. Essentially, the authors argue that once a species has established in a particular area, it stops other (similar) species invading by virtue of numerical superiority – density dependence drives everything.

I’m not a bacterial ecologist, so ‘microbial sectoring’ was entirely new to me. In it, bacteria spread through an agar plate and competitively exclude different genotypes as they do so, creating wedge-shaped patterns of genetic diversity once the colonies have matured. The authors (rightly, I think) view this as a sort of postglacial colonisation in miniature, and suggest that ecologically equivalent marine species are excluded through similar processes, even in the absence of dispersal limitation. However, I’m not sure I agree with their definition of ecologically equivalent; in most neutral models, ecologically equivalent species intermingle and successfully coexist because there’s no way to tell those species apart. I think density-dependent processes like allelopathy might drive these kinds of patterns, since without some kind of selectivity conspecifics wouldn’t be able to recruit either. There are (a number!) of counter-arguments to what I’ve just said, and I’m just pedantically splitting hairs since I’m invoking a different kind of density-dependence to explain these patterns!

I think invasive species are another exciting area where we can see differences among advancing species. There’re a few examples of invading populations that have different traits and genetic compositions to native populations, and it makes good intuitive sense that individuals able to survive dispersal by humans should be well-adapted to slightly different conditions to the rest of their source populations. Equally, individuals on the leading edge of an expanding range might be better-adapted to dispersal, or have higher reproductive rates to enable rapid colonisation, like human colonists expanding along a river in Quebec seemed to bring a number of genes for female fertility with them. However, before I get too teleological, the authors stress that sometimes genes are just piggybacking on advancing waves – they’re just allelic surfers.

Lynsey McInnes

Lynsey McInnes

Hm. This was a weird article! I started off thinking – wow, profound – and quickly segued into – wow, trivial? I’m basically not sure I got the point. I certainly don’t disagree that density-dependent processes are important and that they operate at a variety of temporal and spatial scales. But I don’t think I’ve gained any deeper understanding of general biological processes by having these across-scale processes highlighted to me.

The authors also skirt around the genetic underpinnings of the processes they talk about, making it unclear whether they are actually the same at microcosm to continental scales. I guess computer simulations have shown, e.g., how deleterious mutations can surf on an invasion front, and how newly-established populations (e.g., following postglacial reconstruction) can exhibit less genetic diversity than “older” populations.  I’m biased because I’ve just started thinking of the underlying genetics of macro-scale processes myself, but the paper did make me wonder what’s going on with the genetics of all these events.

So far, I’ve mostly thought of density-dependent processes in the context of cladogenesis (following the past couple of years flurry of publications reporting evidence of declines in diversification rates widely thought to be due to the operation of ecological limits/filling of niche space), i.e., the density- (or diversity-) dependence of cladogenesis. The authors touch on this idea, but don’t go into much detail. On the one hand, it’s perhaps a little off-topic, the authors seem most pre-occupied by density-dependent processes operating as a kind of barrier to the influx of further genetic diversity after an initial colonisation event, while, within the diversification/cladogenesis literature, density-dependence has largely been invoked in relation to something like a closed system where all members (lineages) are equally affected and the niche/range/genetic diversity of the initial colonizer would be similarly reduced to accommodate additional lineages. But perhaps this outcome is just one step further along from what the authors concern themselves with and so is relevant to the discussion. I.e., does the founder advantage (or our ability to detect it) drop off through time?

Data. I know this is a review, but it would have been great to see some kind of more or less formal meta-analysis of the existing data across scales to innumerate instances of founder takes all events (versus instances where there wasn’t evidence for this – stronger competitors arriving later? This must happen sometimes – surely?). Alternatively, some kind of ‘simple’ simulations exploring a broad parameter space to see when founder takes all is expected versus when it might break down (A REALLY strong competitor coming later? Some kinds of poor trait x environment combinations? Incredibly slow dispersal rates? A highly stochastic environment?)

One other thing, there is not much discussion on what makes a founder? Are there traits associated with being first in line? Are these shared/analogous across taxa?

But perhaps I’m trying to sketch out a set of companion papers, and I should be less demanding!

To end on a more positive note – first, if nothing else, the paper has put me a bit on edge – why is it bothering me so much? So, in the end, it has ticked the thought-provoking box. Second, I did appreciate the breadth of examples the authors drew upon (simulations, microcosms, terrestrial and marine ecosystems, human dispersal & human impact) and I will go away now and think some more on the connections they have highlighted.

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