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).



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

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

Distance, distance, everywhere. Figure 2 from

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

Will Pearse

Will Pearse

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

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

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

Lynsey McInnes

Lynsey McInnes

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

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

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

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

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

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

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

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


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!…

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.

Ecological character displacement: glass half full or half empty?

Yoel E. Stuart and Jonathan B. Losos. Trends in Ecology and Evolution 28(7): 402-408. DOI:10.1016/j.tree.2013.02.014. Ecological character displacement: glass half full or half empty?

A glass for the eternal optimist - for sale from ThinkGeek

A glass for the eternal optimist – for sale from ThinkGeek

Will Pearse

Will Pearse

I think I’m not the only one with a slight science-crush on Jonathan Losos, and it’s papers like this that do it. Short, sharp, and to the point. The authors argue that tests of ecological character displacement haven’t been as strict as they should have been, and judge case studies according to the criteria the field itself set.

Let’s briefly cover obvious potential gotchas. These six criteria are well-known (>450 citations, and I’d heard of them), but they’re probably not the only criteria and it might be unfair to judge a field by its adherence to one paper’s suggestion. That said, while you might be able to think of some more (please chime in!), I think they’re all pretty fair and I’d be surprised to receive hate-mail about how dreadful the criteria are.

I think it might be worth reflecting on why we’ve been publishing ever-more-exciting sounding examples of character displacement, instead of actually examining whether the examples we have are definitely character displacement. Cynically, I think we all prefer (and fund) nice shiny new example that look great on the cover of Nature, not the boring follow-ups that fill in the (necessary) details. What’s worse, I think we’re all guilty (to some extent) of confirmation bias, and maybe we don’t want to look too carefully at systems that have earned us front-covers of journals in case we find something we don’t want to see.

But back to the biology. There’s a reason figure 3 shows that the least-confirmed criterion is demonstrated competition in nature: it requires ecological data and ecological fieldwork, both things that evolutionary biologists would probably rather not be doing. The last few decades have seen some amazing increases in statistical firepower in evolutionary biology, in part because we have only so much data and we must soak up every ounce of signal we can. However, ecological data isn’t limited in the same way, and I (and others) seem to think that ecological experiments might be an excellent way to improve our understanding of evolution.

Lynsey McInnes

Lynsey McInnes

It’s hard to argue with the conclusions of this paper. Thoughtful, thorough and interesting, it’s a plea to be a bit less lax when purporting to find evidence for instances or the prevalence of ecological character displacement (ECD). ECD -such a satisfying idea, yet difficult to conclusively demonstrate. Schluter and Mcphail’s six criteria provide a comprehensive ticklist to complete, and appear exceedingly difficult to meet (without a shitload of effort).

But what is the appeal of ECD? It’s an exciting phenomenon, bridging ecology and evolution and providing an interesting explanation for divergence. More interesting, say, than adaptation to different abiotic environments or just some other non-adaptive mechanism of divergence.

And yet maybe ECD has been elevated to too high a status. Maybe it is just one interesting mechanism of adaptive divergence, alongside apparent competition or haphazard adaptation to available niches, or some other mechanism and it has been credited with undue (and certainly undemonstrated) importance?

Anoher thing I noticed: studies that meet all six criteria are from well studied systems, sticklebacks, finches, anoles, etc. If other studies had similar amounts of time devoted to them would the other criteria have been met? I didn’t check whether not meeting them equated to them not having been tested for or them actually failing to be met?

The authors highlight the idea that climate change and invasive species are now providing great conditions to witness evolution in real time and thus to test for instances of ECD, as novel communities are brought together providing opportunities or competition for resources and character displacement. Indeed this seems like an opportunity too good to miss, but will nonetheless require careful delineation of what responses are expected and high levels of study to dismiss alternative mechanisms.

I also wonder how ECD fits in with the current trend to look for niche conservatism and/or niche evolution in every clade of organisms. If a clade shows niche conservatism along some environmental axis, do they often also show ECD along some complementary axis? Perhaps we will be understand diversification if researchers in the different camps talked more to one another and there was a better integration of the potential effects of various abiotic and biotic factors.

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!

Molecular evolutionary signatures reveal the role of host ecological dynamics in viral disease emergence and spread

Dule-Sylvester et al., 2013. Philosophical Transactions of the Royal Society B 368 – 1614. DOI:10.1098/rstb.2012.0194. Molecular evolutionary signatures reveal the role of host ecological dynamics in viral disease emergence and spread

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

We covered this paper in a (real, live, in-person) journal club here at the University of Minnesota, so the views below are probably not just mine. So, if you like what’s written below, it’s from the community genetics reading group; if you don’t like what’s written below, it’s all from me.

This study links an epidemiological model of how rabies spreads among raccoons to the structure of the genealogy that the rabies would have given present-day sequence data. I really like the modeling framework this paper presents. Inferring ecological patterns directly from a genealogy is a brave thing to try and do, and while others have done similar work this is probably the most explicit model I’ve seen someone trying to fit. This is also the paper’s greatest weakness: I’m not sure that these models could ever be fit successfully to real data. Taking figure 3 as an example, the authors state that they can detect the influence of long-distance dispersal because the exponential growth model fits their data better; I don’t think we would ever get such neat graphs with real data, and the predictions of their linear and exponential models look too similar (to me) to distinguish between in the presence of experimental noise. Indeed, while the authors use parameters derived from real data, they don’t actually attempt to fit their models to real genetic data; I wonder if they would be able to do so.

Moving past those rather snarky comments, this paper interested me because they’re attempting to model the ecological processes that might produce a particular genealogical (phylogenetic) structure. By looking for what kinds of signals long-distance dispersal leaves in the genome of rabies, they’re able to make useful predictions about what the rabies is doing right now – that’s presumably a lot of help if you’re trying to control an epidemic. I’d never really thought about how perfect a system diseases are for eco-phylogeneticists – they jump from host-to-host, making lineages nice and separate, and they evolve really quickly. Let’s just ignore multiple infections and DNA saturation for a moment, and think about the opportunities for fitting these kinds of complex models. Maybe we can all start linking phylogenetic (whoops – genealogical) structure to explicit models of evolution that incorporate ecology, and in the process help better-understand disease dynamics. As an eco-phylogeneticist, that kind of excites me!

Lynsey McInnes

Lynsey McInnes

First, apologies for the delay to this week’s post – I got caught up in Easter Monday laziness and what follows is largely random thoughts that popped into my mind as I read this paper on the train into work this morning.

I really enjoyed the idea behind this paper. I haven’t read much of the literature around the eco-evolutionary dynamics of virus evolution, but it sounds like crazy fun. I have read A LOT of the literature around models of spatially-explicit diversification and this paper definitely made me want to see more cross-talk between these two research areas (neatly incorporating my new field of statistical phylogeography/population genetics).

(I think) just like Will, I was excited by the possibilities that the authors outline, impressed by their modelling framework, but dubious about some of their outcomes and the likelihood that such a detailed model could often be used for predictive inference. I’d be happy to proven wrong however, and have very little feeling for how much data is really need/exists for such models to be powerful for, e.g. public health decision making. I’m also not convinced by figure 2 – is there not a ton of pseudoreplication going on in there – should there not be only five data points (as in figure 1b). Dare I say it – how about a mixed effects model?

Although the authors did perform sensitivity analyses and spend time discussing the effects of landscape heterogeneity and demographic stochasticity on their ability to infer process, I would have liked to see have seen more exploration of the effect of missing or biased data (for example how noisy can the data be before signal becomes distorted/lost?). I concede I have not checked the supplementary information and this information might be in there…

As a side project, I’ve been thinking about the effects of dispersal on macroevolutionary diversification and it was refreshing in this paper to see local and long distance dispersal so simply made distinct. I think this clarity of distinction is lacking from macroevolutionary analyses (so that when people look for the effects of dispersal on diversification they get conflicting results depending on whether they are looking inside a restricted area or beyond it (to cut a long story short)). Here, the authors have clear hypotheses on the differences expected whether or not the host moves beyond its immediate neighbourhood. One imagines that there isn’t really two distinct categories, but there is certainly more than one. So, hooray.

This comment might have come across as overly negative. I did not mean it to. I really enjoyed reading this paper, it was extremely well-written and thought-provoking (such that someone with no real background in disease dynamics could understand both the rationale and methods). I am going to check out the other articles in the special issue of Phil Trans that this article came from and look forward both to seeing how these types of models develop and hopefully to pilfering some of these ideas across into macroevolutionary diversification (that is similarly affected by processing acting on ecological time-scales (always good to end on a blatant note of self-citation).

Macroevolutionary perspectives to environmental change

Condamine et al. 2013. Ecology Letters: early view. DOI:10.1111/ele.12062. Macroevolutionary perspectives to environmental change.

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!

Lynsey McInnes

Lynsey McInnes

For our second post, we picked a monster by accident. This is a mammoth perspective paper on the potential of macroevolution to provide insights into expected environmental change. It’s good, it’s comprehensive, it’s kinda hard to get through in one reading. I commend anyone that did.

So, my commentary is going to be a bit haphazard and mostly just the thoughts that came to mind after my fourth skim. It should also be prefaced with the info that I’ve just turned my back a bit on macro-scale approaches because I’d become frustrated with all the patchings-over and arm waving necessary to get from pattern to process with data at this scale. Having said that, smarter people than me can probably make that leap and it be meaningful (i.e., a lot of the recent research cited here: note the prevalence of refs from 2011 and 2012 – this field is moving fast!).

I thought the authors did a great job of provided a measured perspective on the potential for macroevolution to provide practical insights into the effects of contemporary environmental change. They highlight that today our environment is changing extremely rapidly, potentially way more rapidly than in the past (although this may just be because we can’t resolve time to such narrow intervals in the past). They take great pains to highlight how dodgy extinction rate estimates from reconstructed phylogenies are (but indicate the sorts of conditions where estimates might be more reliable). They emphasise that extinction risk today might have different correlates to in the past (and outline neat ways to test for this). They collate and summarise a ton of (mostly very recent) paleo- and phylo- research in an accessible and intelligent way.

A tiny rant – so much on whales! Which demonstrates a point that I think the authors would also agree with: data availability remains an issue. The most robust contributions from macroevolution seem to be ones consisting of a mix of good paleo- and phylo- (here, reconstructed phylogenies of extant lineages) data. And this data is patchy or absent for most groups – except whales… How much are our inferences curtailed by lack of data versus lack of signal of past events in that data?

Cross-talk. One thing I did think the authors could have mentioned (in an otherwise comprehensive overview) is the potential lack of communication with researchers generating the data and researchers developing methods to analyse this data. Although there are (probably quite a few) exceptions, my view is that there is a small band of researchers developing ever more complex models that are then applied by another set of researchers on their painstakingly built phylogenetic dataset. A more fruitful method might be for more cross-talk between methodsy and data people so that data is collected and compiled explicitly to answer interesting questions with powerful methods. For instance, the authors end with a brief discussion of the impact of interaction networks and ecological traits on species’ responses to environmental change. What data would be most useful to start modelling these questions and who is best placed to generate it? THAT development would be exciting!

A random selection of other thoughts that came to mind:

Would macroevolutionary perspectives be most useful in conjunction with microevolutionary ones? As global change is so rapid, microevolutionary/ecological responses are the ones we are going to be able to measure. How do these translate into macroevolutionary change (i.e., what types of short-term responses are retained to be detected at the macro-scale – if we knew that, we could (maybe) look for such signals in existing phylogenies)?

Will we ever be able to confidently identify clades nested in larger phylogenies that have been diversifying according to some homogeneous process (or rather will we ever be able to identify higher-level units a la Barraclough 2010)? It seems like if we can do this we’ll be in a much stronger position to infer how past environmental change or past biotic interactions have influenced clade dynamics.

More generally, are we approaching the point where we’ve extracted all the information we can from macro-scale data, or are we just waiting on more sophisticated models/methods?

Finally, in 10 or 100 or 1000 years time, what will the tree of life look like?

Lynsey McInnes

Lynsey McInnes

Everything Lynsey said about this being a big paper is correct, but I think we’d both recommend you stick with it because it covers so much ground. One of the best things a paper can do is make you think, and I really enjoyed reading this paper with a beer in hand to fuel my thoughts!

Lynsey mentioned data availability, and while the authors mention foraminifera quite a few times, they only briefly mention Ezard et al. I like this paper for two reasons: firstly, it has some of my friends on it (…), and secondly, they assess extinction rates using a dataset where we can be almost certain that we caught most of the extinction and speciation events that mattered. Estimating extinction rates from molecular phylogenies is hard (the authors discuss this) – and sometimes it’s really hard to do. Should we (/could we) be shifting our efforts to systems like foraminifera where we have more precise data? This naturally leads me to wonder to what degree taxa differ in their extinction and speciation rates, and what impact this could have on the field…

I think there’s a weird disconnect between conservation biologists and evolutionary biologists, and (as someone who works on eco-evolutionary stuff) I really enjoyed their discussion of how conservation biologists could focus on areas that generate phylogenetic diversity. I think things like the EDGE list are a really good way of helping the general public place evolutionary dynamics in the wider context of conservation biology, but maybe we could do more to link these two areas. Conserving particular areas because they are evolutionary sources of biodiversity is one way, but could we start using information about the way in which species originated to help us better model how they are likely to respond in the future? For example, maybe species that radiated in ‘favourable’ conditions are more likely to go extinct when faced with difficult environmental conditions – a bit like cichlid species being lost when Lake Victoria becomes more polluted. Perhaps that’s stupid, but aren’t there other (fairly tractable) examples we could use?

A few small (probably increasingly silly) questions to finish off. There’s a lot of debate in ecology about spatial scaling, and the extent to which processes at the local (micro) scale apply at the global (macro) ecological scale. If conservation actions are more micro-scale in their application (we can’t make a protected area the size of Brazil, for example), does this reduce the utility of these kinds of historical analyses when trying to understand present-day change? Land-use change is distributed across the planet different to many previous drivers of extinction – does this matter for these kinds of studies?

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