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!…


Mammalian evolution and the Great American Interchange

Marshall et al. Science 215(4538): 1351-1357. Mammalian evolution and the Great American Interchange

Another kind of great American interchange - the ill-fated I-10 Papago Freeway's hellicoil that never was.  Taken from the US Federal Highway Administration.

Another kind of great American interchange – the ill-fated I-10 Papago Freeway’s hellicoil that never was. Taken from the US Federal Highway Administration.

Lynsey McInnes

Lynsey McInnes

Not quite sure where to start this week. What a great story! And a great textbook example of so many biogeographic and macroevolutionary phenomena. Marshall and Co. outline the evidence for the Great American Biotic Interchange (GABI) framed in terms of MacArthur and Wilson’s equilibrium theory of island biogeography and it sounds so neat, so tidy, almost unreal! We’ve got two different dynamic equilibria, we have different sized source faunas, we’ve got tropical and temperate fauna, we’ve got replicated patterns at different taxonomic patterns, we’ve even got an emergent uber trait for the North American fauna that enables them to infiltrate the niches of South American mammals (gotta have something inexplicable, right?).

The above sounds like a highlights summary of any recent macroecology journal. And this paper was published 32 years ago. Ouf. Sure the stats have moved on, but the patterns and conclusions. alongside the inexplicable bits really haven’t, have they?

I had two main thoughts when reading this paper. Number one was that we haven’t moved on much in the insights we are having on broad scale patterns in biodiversity. Which, in some ways, is totally fine, its not like the patterns have changed. We’ve just reinvented the wheel, sliced the cake thinner and topped it with fancy stats.

The second thought was, for me, more frustrating! Over the past couple of years, my intuitive belief in dynamic equilibria and carrying capacities and ecological limits to diversity has been thoroughly shaken. I was coming to the conclusion that these were patterns we were finding in our data because they are neat and tidy and clever and merge beautifully ecological and evolutionary time scales. My opinion was shifting that these patterns might emerge by chance and that regions are not closed enough to reach equilibrium, that biotic interactions mattered more than we gave them credit for and (meta)populations not biogeographic ranges were the appropriate units to look for the processes underlying biogeographic scale patterns, that niche construction mattered, that we were missing tons of important features in our quest to understand biodiversity patterns.

And then a paper like this comes along, and, in theory, it should do nothing to my emerging mindset as all of the above arguments could, more or less, be applied to Marshall and Co’s dataset and reasoning. But somehow the simplicity of the analyses, the merging of masses of paleo data with the explicit linking to M&W’s equilibrial theory has set me back to square one (maybe square two) in buying into equilibria in macroevolution. Wah.

Where to go from here? What data would complement what was already compiled here? What contemporary data could be added? What experiments could be conducted? What stats would we like to apply? What was the elusive North American trait?

Will Pearse

Will Pearse

I was really struck by how few papers tell as a coherent a story as this. It really is almost like a story, with remarkably little in the way of obfuscated statistics and graphs to obscure the general take-home message. In re-reading this, I think I’ve even detected a beginning, middle, and end!

I’m no expert in this field, but I was somewhat surprised how well these methods have stood the test of time. Yes, there are some who would claim rarefaction methods are outdated, but I would hope the signal in these data would overpower methodological quibbles. Equally, the equilibrium models employed here are simplistic – more sophisticated models of carrying capacities I’m sure could now be fit – but their only purpose is to demonstrate that something else is going on, and they do that very well.

What is it about North American species that makes them speciate so much more? The authors seem to come down on the side of some meta-trait, some family-level inheritance of speciation ability. I’m not someone who believes strongly in the concept of taxonomic units as real biological things (although see this, and Aelys does some great work on higher evolutionary units), but it seems there is something about these clades. Perhaps it’s related to how the South American groups have already equilibrated to a particular level of diversity – maybe there’s some kind of genetic inertia and traits associated with dispersal into a new continent give recently-moved species a radiating edge. I’m sure, somewhere, Ricklefs is screaming “parasite load” at the top of his lungs, and maybe there’s something to that. Perhaps it’s because competition is only as fierce as your competitors; the North American lineages had to fight particularly hard (more diversity crammed in? Evolutionary fluke?) and so they won out.

One thing I am certain about is that we need more stories in biogeography and evolution in general. Evolution is an inherently historical science – that doesn’t mean we can’t do comparative analyses, but it does mean that we should be a little more understanding that regressions aren’t everything. Species distributions are not stationary; different processes are operating across different spatial and  temporal scales, and there are far too many idiosyncratic events like the Great American Interchange for us to simply sweep them under the rug. More stories, fewer stats, please. I never thought I’d write that!

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.

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