A Neutral Theory for Interpreting Correlations between Species and Genetic Diversity in Communities

Laroche et al. The American Naturalist 185(1): 59-69. A Neutral Theory for Interpreting Correlations between Species and Genetic Diversity in Communities

Figure 4 from Laroche et al. The Species-Genetic Diversity Correlation plotted against mutation rate (m) and carrying capacity (K). Personally, I (Will) think it looks a bit like a scene from Interstellar if you squint a little. That's not a comment on the science; I just really enjoyed Interstellar.

Figure 4 from Laroche et al. The Species-Genetic Diversity Correlation plotted against mutation rate (m) and carrying capacity (K). Ignore the white splodges; they’re unimportant for our purposes. Hopefully we’ve just nerd-sniped you into reading the paper!

Lynsey McInnes

Lynsey Bunnefeld

Oh the dangers of picking a paper because you like the keywords and finding them cooked in a different way to you had imagined in your head. I have a slow-burning interest in how thinking about intraspecific variation can help explain interspecific patterns of diversity, turnover, etc, and this paper’s keywords fall right into that gap…

Here, the authors are interested in understanding why you often find, or expect to find, positive correlations between genetic diversity of a focal species and species diversity in the same area (i.e., not quite the same thing). They elegantly explain accepted thinking on the effects of local competition and connectivity and size of sites in a metacommunity as being the factors underlying these expected/often observed patterns.

The paper is concerned with adding the omitted factor of mutation ‘regime’ into the mix. If mutation occurs at the same rate as migration among sites, the expected correlation between genetic and species diversity could break down. I’m not going to lie, the way the authors get to this outcome remains somewhat opaque to me. My general understanding is that when mutation rate is high, the impact of migration among sites is less predictable as there will be a greater variance in what amount of diversity is transferred among sites and this leads to unpredictable knock-on effects on genetic diversity-species diversity patterns. How, you might ask, how indeed?

What I did like about this paper, probably because it harks back to what I liked about the keywords is the incorporation of more actual genetics into the model. Mutation regime is a necessary addition to thinking about genetic diversity and, as the authors rightly point out it is going to be easier (and at the same time much more complicated) to deal with as genomic data pours in. We appear to be on the cusp of understanding how these different levels of diversity impact each other and it’s mega exciting! Models such as this one are pretty awesome, and set the stage for the next step which would be incorporating mutation rate heterogeneity, including at selected loci. Population genetics has the machinery to deal with this variation, we just might need a bit more crosstalk with ecologists and theoretical biologists to get to more refined characterisations of patterns (if there are any) at the macro scale.

Will Pearse

Maybe this is off-topic, but I was dreading reading this paper because these sorts of analyses terrify me. I wasn’t familiar with the ‘ODD model‘ of describing biological models, but the authors use it to such excellent effect that my fears were completely unfounded. If you’re a theoretical person, please use this approach!

This is a paper about within-species diversity (community genetics, not community phylogenetics), and so almost by definition they cannot examine speciation processes. However, I was left wondering how speciation would interact with these dynamics; I assume it’s tricky to model because otherwise a ‘smart’ thing for a genotype to do would be to speciate and thus avoid competition with the genotypes it left behind. Perhaps you’d end up moving to a more coalsecent-esque model in which individuals’ competition strengths are a function of time since coalescence – species identity itself would be something a bit arbitrary. I’m interested because I think there are so many parallels with this model and the more Neutral Theory models (and some of the models of fitness we’ve discussed in the past). I wonder what the dynamics would look like if you just shunted some of these dynamics inside a classic Neutral model.

Presumably this sort of literature applies only to neutral alleles – if there is an allele that confers a selective advantage, then natural selection et al. kick in. Which is where I was wondering how competition steps into this framework – I think it’s at the step where new individuals are drawn (please correct me!), in which case I can see how migration and mutation rates would affect what we find. On another side-note, I particularly liked that the authors had worked sampling into their model – it made it a lot easier to draw this back to what would be expected empirically, and helped the authors make sense of how such empirical results seem to disagree with this model at first. More of this as well, please!


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!…

Mechanisms of maintenance of species diversity

Peter Chesson. Annual Reviews in Ecology, Evolution, and Systematics 31: 343-366. Mechanisms of maintenance of species diversity

Species' relative abundances fluctuating over time under various models of coexistence. If you just want to think of it as a pretty picture, that's probably OK too. Figure 2 from Chesson (2000).

Species’ relative abundances fluctuating over time under various models of coexistence. If you just want to think of it as a pretty picture, that’s probably OK too; we won’t tell anyone. Figure 2 from Chesson (2000).

Will Pearse

Will Pearse

I’m shocked how many people consider this a classic that “must be read” and yet haven’t read it themselves because it contains “too much math”. I don’t care if you haven’t read this (I’ve not read every paper most people consider a classic), and I think focusing on what people haven’t done is pointless, but I think this is a very readable coverage of what is (otherwise) very difficult math. I do find this field very math-heavy, but with only 9 equations (~1 per 3 pages) this is a really insightful review that for novices like me is helpful.

Chesson very nicely re-phrases coexistence around the ratio of species’ competitive differences and their niche differences; if species are sufficiently different, or compete sufficiently little, they will coexist. This came up an awful lot in the community phylogenetic talks I attended at ESA last year, in part because it torpedoes the assumption made by many that closely related species are more similar to one-another and that’s all that matters for co-existence. I manically circled the idea that species’ niches have an effect (e.g., reducing resources) and a response (e.g., ability to grow given certain resources). Chesson seems desperate for us to stop thinking of a niche as something that is solely a function of a species itself: it’s a function of the context within which we see the species, and that is always shifting. Even when we say a species’ niche involves competing with other species, we’re still missing the key component that the species is using up resources, thus warping the effect-response space that all the species around it experience and themselves modify.

Which sounds a lot like I’m saying the paper is about non-linearities and changes through time; it isn’t, and Chesson very artfully points out that a lot of insight can still be had by setting up simple models in well-considered ways. It is pretty dismissive of Neutral dynamics (…although it was written in 2000!) and the take-home from the section/paragraph “nonequilibrium coexistence” could be paraphrased as “stop using this unhelpful phrase”. I was particularly struck by how Chesson viewed the importance of Neutral Theory for exploring biogeographical dynamics; more than a decade later we’re starting to do this, and we’re even having discussions of how species can evolve, under neutral dynamics, to not be neutral today. This opens a whole can of worms as to what we can usefully call a N/neutral model, but more importantly helps us unify questions at a number of different levels of ecology. Which is a good thing!

Much of what’s in this paper is probably uncontroversial to a community ecologist (right?), but I think remarkably little of it has found its way into the mainstream evolutionary biology literature. I find that interesting because I’m often surprised by how much evolutionary biologists keep track of what ecologists are doing. I can’t think of any serious modelling studies where species’ effect and response traits are seriously modelled across a phylogeny (please correct me!), and I wonder what we would find if we looked.

Lynsey McInnes

Lynsey McInnes

I can’t imagine I am the only PEGE person to have cited this paper on the mechanisms of species’ coexistence without having carefully read it? Its been cited 1694 times! So, choosing it for this week’s PEGE was a great excuse to actually sit down and use some train time to read it through and through.

Now, I have always cited this paper when writing about macroevolution and the idea of equilibrium species numbers and turnover in ‘evolutionary’ time. Oops. Chesson sidelines this view of species’ coexistence early on in his paper and instead focuses throughout on ecological/contemporary notions of species’ coexistence in a – relevantly sized, more or less closed – patch. No matter, I am convinced that most if not all of what he talks about is also relevant or at least interesting for people working at longer timescales.

The problem perhaps is that too many people have jumped on the bandwagon of these ideas being relevant to understanding the build up and maintenance of species diversity that we have become blinkered to the possibility that ecological limits might not be constraining diversity at broad (temporal and spatial) scales. It feels so easy and so neat to extrapolate Chesson’s (and others) equations and explanations of how populations of species manage to stably coexist with each other (a delicate balancing act of getting more intraspecific than interspecific competition, with divergence along at least one relevant niche axis) to how ENTIRE species diversify in the presence of one another until their niche space (in physical or ‘hyper’ space) is full. It is also really easy to obtain patterns, for example in phylogenies, that agree with the idea of diversification slowing as niches fill up.

I have a feeling we are on the cusp of entering a new phase of macroevolutionary analyses where we break ranks with trying to match one for one ecological and evolutionary phenomena. I think it is already much more common to think of what units within species evolve (populations/metapopulations depending on gene flow) and also to think of niches as much more labile (e.g., what about niche construction or extent of niche breadth). Similarly, in both macroecology and macroevolution, biotic interactions are moving from postscript to centre stage as more data becomes available to address the effects of biotic interactions on the patterns we can observe and experimental systems are emerging where these effects can be empirically manipulated.

Turns out no matter how hard I try to leave it behind, I am still a macro-scale biologist at heart and it is fun to pull out the macro-scale implications of more or less any paper that I read.

How does ecological disturbance influence genetic diversity?

Banks et al. TREE 28(11): 670-679. How does ecological disturbance influence genetic diversity?

How disturbed are your genetics? From Banks et al.

How disturbed are your genetics? From Banks et al.

Will Pearse

Will Pearse

Disturbance is a topic very close to my heart (that’s meant to be a physiology joke), mostly because I get very annoyed when people don’t define precisely what they mean by it. So I was very heartened to read this review, where the authors discuss the various temporal and spatial scales of disturbance, and also because it’s a very nicely written paper.

Disturbance, within certain conditions, can be part of the background homogeneity of a system, and the authors are keen to stress that in this paper. I was a little surprised to not find mention of the intermediate disturbance hypothesis (even though some find it controversial), since it’s so appropriate in this context. I found figure 1 (partially reproduced above), where the authors go through some case studies of what different kinds of disturbance look like, quite helpful in reminding me that disturbance can be lots of different things, and it can have lots of different effects (not always bad). However, that figure 1 is made up of case studies reflects our lack of a coherent framework to structure how we think about disturbance. Moreover, the right hand side of the figure (which I cropped out, sorry!) talks about two case studies that involve “metapopulation” and “patch dynamics”; this makes a lot of intuitive sense to me, but on reflection I find that kind of weird. Metapopulation theory is a concept humans have generated, it’s not a thing that biological systems recognise, and I think it might be better to categorise systems on the basis of properties they share rather than how we find it easiest to model them.

So what would such a categorisation look like? After reading this paper I think disturbance severity, duration, and extent (bear with me) are three important axes. With ‘extent’ I want to incorporate the ability to temporally and spatially escape a disturbance; spatially means whether the disturbance is everywhere and whether you can move to avoid it, and temporally that means whether the disturbance happens very often or very infrequently and would probably incorporate seed bank effects. I’m sorry ‘extent’ is such a poor descriptor; I’m decaffeinated and would appreciate better suggestions! I’ve very deliberately chosen to put space and time on the same axis; you might prefer to split them. You might also prefer to add predictability as another axis; I don’t, not because I don’t think it’s important, but because I think a system’s history (which, in turn, incorporates predictability) affects quite a lot and the other axes mostly capture what the system has been doing in the past. Not a lot about genetics in this post (sorry!), and instead a framework that almost certainly already exists somewhere and I’ve forgotten I’ve read it. Please do tell me where!

Lynsey McInnes

Lynsey McInnes

I had high hopes for this paper. I’m attracted to any paper that deals with intraspecific variation head-on and am well aware that intraspecfic variation affects and is affected by processes occurring on varying spatial and temporal scales. So, a paper dealing with how disturbance affects genetic diversity seemed right up my street. I was curious about the direction the paper would take as my feeling was genetic diversity is generally quite hard to measure particularly in non-equilibrium populations (such as those that have been disturbed) and assigning particular genetic signatures to historical events (‘disturbances’) is notoriously difficult as not only can a range of different events leave the same genetic signature, the same event can leave different signatures depending on the ecology and population structure of the species involved.

It was good for my ego to find that the authors largely confirmed my suspicions of these issues, but sad for the paper that there seems no easy way out.

It seems that the current state of understanding is that we live in an increasingly ‘disturbed’ world . Events such as tsunamis, fires and grazing impact nearby populations, reducing the number of individuals and thus most likely (at least) point estimates of genetic diversity and the challenge is to recognise the types of populations/species that will find recovery from such impacts difficult or impossible (if one is interested in conserving viable populations, otherwise all impacting populations are interesting, for instance, what kinds of species can you bombard with disturbances and they bounce right back to pre-disturbance levels of abundance and genetic diversity?). It seems however, that little research has focussed on the relationship between disturbance and genetic diversity and that there are many outstanding questions.

The second half of this paper gave a helpful overview of these outstanding questions and laid out some helpful ways forward. Namely, and understandably, the integration of multiple sources of data (event type, species’ traits, samples across the range and through time, etc.) will help to unravel the impact, or non impact, of putative disturbances on genetic diversity and, more importantly, what these effects mean for the longer term survival of species and/or communities. In fact, the paper lists FOURTEEN outstanding questions linking disturbance and genetic diversity and all of these are interesting. It would have been nice if these had been dealt with in more detail in the paper, perhaps focussing on a couple and on real routes forward to addressing them.

Maybe I missed this in the paper, but I also felt that what was missing was strong evidence that one expects any general link between disturbance and genetic diversity. As next gen sequencing gets cheaper and more accessible for non-model organisms, it will become trivial to look for these links, but, I feel, we need to know what we are looking for before we go looking for it. The general view is that more genetic diversity per population is better to ensure buffering against a variety of disturbances, but the authors show this is not always the case. Individuals can come from beyond the disturbance centre to make up for lost individuals and/or diversity. To predict this rescue effect one has to have a bigger picture encompassing knowledge of the genetic diversity of multiple populations within and beyond the disturbance centre. Are there enough individuals for recovery and do these individuals possess the desired adaptations? (So, I might differ from Will in thinking metapopulation theory might be helpful here).

I absolutely believe that intraspecific variation within and between populations in terms of genes and ecology must be considered if we hope to understand how populations will cope in the face of point disturbances and longer term environmental fluctuations. This paper drove home to me quite how difficult this endeavour is going to be.

Climatic control of dispersal–ecological specialization trade-offs: a metacommunity process at the heart of the latitudinal diversity gradient?

Jocque et al.. Global Ecology and Biogeography 19(2): 244-252. DOI:10.1111/j.1466-8238.2009.00510.x. Climatic control of dispersal–ecological specialization trade-offs: a metacommunity process at the heart of the latitudinal diversity gradient?

Dispersal's important too, don't'cha'know. From

Dispersal’s important too, don’t’cha’know. From Jocque et al..

Yael Kisel

Yael Kisel

Though it was a nice bonus, I didn’t pick this paper because it says that dispersal (one of my pet topics) is a key process in the creation of global biodiversity patterns. I picked it because it presents an elegant central thesis that I haven’t heard before: that climate variability may modulate species richness indirectly, by deciding whether a region’s species pool will be biased towards ecological generalists that are good at dispersing (and thus have low speciation and extinction rates) or ecological specialists that are poor at dispersing (and thus have high speciation and extinction rates). To me, this idea gives me the “how intuitive and straightforward! why didn’t I ever think about it that way before?” feeling that I associate with true scientific advance and beauty. I just love how it ties together so many key factors – climate, ecological specialization, dispersal, speciation, extinction – and the authors even manage to tie in sex (well, asexual species)! From now on this idea will definitely be a part of my mental framework of how biodiversity probably works.

There are also a few smaller bits and pieces that I quite like in here. I am quite happy with the reasons the authors give for why climate variability should select for increased dispersal. Clif notes: 1) Seasonal weather with some very harsh seasons selects for seasonal migration, which involves a lot of movement and could thus lead to increased dispersal. 2) Environmental variability will likely lead to increased population extinctions, selecting for increased dispersal to recolonize those empty locations when they become habitable again. 3) Occasional harsh environmental conditions favor the evolution of dormant stages, which also make dispersal possible over longer distances. I also really like the idea that climate-driven extinction will disproportionately affect specialized, poor dispersing species. I hadn’t thought about extinction that way before; it makes sense; and it fits into my feeling that diversification over long time periods is characterized by cycles of wide-ranging generalist species budding off lots of small-ranged specialists that don’t do much speciating and eventually die out in big chunks, allowing for another burst of budding from the survivor generalists. Finally, I like how the authors put forward a lot of specific predictions that we should go out and test, like “are tropical species usually poorer dispersers than temperate/polar species?” and “are specialist/poor dispersing species less common during times of faster climate change?” (I wonder if that second question is testable with paleo data though?).

All that said, there’s also a lot that disappointed me in this paper, and I wouldn’t immediately recommend you to read it thoroughly. I felt the authors were trying too hard to sell their idea, I didn’t understand why they needed to discuss “metacommunities” and “continuity of habitat availability in time and space” so much instead of using simpler language, and there were many specific points in their reasoning that I didn’t agree with or couldn’t follow (for instance, I don’t agree that ecological specialization and competitive ability are interchangeable). I also think the central figure is a bit sloppy – it’s unclear to me why ecological specialization should itself limit gene flow, and it’s unclear whether “isolation” refers to reproductive isolation or geographic isolation – a big distinction. I also wish that they had used the latitudinal diversity gradient as one example of a possible application of their theory, rather than the main topic, as for me that focus both limited and confused the paper. Finally, just to vent for a second about typos, I found it lame that the annoying word eurytopic was spelled wrong the one time it was used!

Moving on, I think this theory deserves to be tested properly and I see some cool ways to do that. Of course, as I said, the authors lay out a number of rather specific predictions and those should be tackled (are any students reading this that need a research project for their degree?). I also had a few more ideas while reading through. First, assuming that invasive species are generally rather generalists that thrive in disturbed areas and disperse well (correct me if I’m wrong!), this would suggest that invasive species should generally come from more climatically variable regions. Is that true? Second, though the authors really focus on tropical vs. polar species/communities, what about other gradients in climate variability, for instance between coastal regions and continental interiors? Do these gradients also show the expected patterns of variation in dispersal propensity, species richness, speciation and extinction rates, etc?

I don’t have any other big thoughts about the paper to conclude with, so instead I’ll conclude with an appeal for PEGE readers to consider doing more research that would produce results useful to me. Study dispersal! Especially with comparative population genetics or new databases of dispersal related traits! It’s fascinating, I promise!

Will Pearse

Will Pearse

I’m not a dispersal person, and I’m not much of a macroecologist, so if I say something stupid below please correct me in the comments. I liked this paper; they put their heads above the parapet, whacked out some testable hypotheses, and that enables me to be constructive in my criticism (I hope) because they’ve given me something concrete to aim at.

Dispersal is complex, and I’m pretty sure it’s not just one thing. Long-distance dispersal, in my mind, is this rare process that moves individuals very long distances. Rafts carrying seeds or stems of plants across oceans are an example of it. I don’t disagree with much of what these authors say, but I think they need to be more clear about the kind of dispersal they’re considering, and I can’t actually find much of a definition of dispersal in the paper. Is long-distance dispersal relevant when talking about regional co-existence? Probably not. Is long-distance dispersal relevant when talking about the latitudinal diversity gradient and whether the tropics are cradles or graves of diversity? Probably. I think mixing in community ecological definitions of dispersal and then using them to explore long-term evolutionary trends is a bit iffy, and (I never thought I’d say this) I’d almost like to see some kind of theoretical analysis of how some of this might work. More explicit and complex incorporation of dispersal into evolutionary processes is a good thing, but we need to know what we’re putting in.

Much of what the authors suggest comes from an intrinsic trade-off between ecological specialisation and dispersal ability. As the authors acknowledge, community ecologists have known about these sorts of trade-offs for a while, and have made them more complicated, but I buy the concept for a regional approach with the authors’ proviso that suitable habitat has to be hard to find. If you’re specialised, and your habitat is hard to find, it makes little sense to move. But that also means it makes no sense whatsoever to move, which means you’re going to be stuck as a very local-scale endemic species, unless there’s some king of long-distance dispersal process (…) that occasionally shunts you out of your local area. So, if there are rare, hard-to-find habitats, why is it that such small-ranged endemics are so rare, perhaps except for the tropics where many invoke Neutral Theory to explain how so many similar (and so not really specialised!) things are able to coexist?

Much of the above rests on my whole ‘different kinds of dispersal’ argument, and I’d be interested to hear what you all think about that. I sense I could be missing something very important!

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