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 Rignios et al.

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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!

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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.

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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!

 

Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli

Matthew D. Herron and Michael Doebeli. PLoS Biology 11(2): e1001490. DOI:10.1371/journal.pbio.1001490. Parallel evolutionary dynamics of adaptive diversification in Escherichia coli.

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!

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Will Pearse

This is another article that pushed me outside of my comfort zone; I know nothing about bacterial ecology, and probably even less about bacterial evolution. However, this is a very neat demonstration of how bacterial approaches can shed light on questions biologists have been asking for decades: what would happen if we turned back the clock and started evolution afresh?

According to this paper, very similar things. The authors find that bacteria exposed to the same conditions evolved the same kinds of responses, and split into the same kinds of species. Us big-bodied ecologists know that things like this can happen in species like Anolis lizards, but we don’t have the ability to turn back the clock, do the whole thing again, and sequence the genomes of everything while it’s happening. Indeed, while Anolis lizards have radiated into similar niches, I’m not sure there’s evidence that they underwent mutations at exactly the same loci. To be precise, these mutations happened in the same genes, and in the same order, but were not at the exact same points in the genes. This is still amazing, and I guess makes it less likely that we’re just picking up mutations that were previously at too low a frequency to be sequenced.

I wonder what effect gene transfer has on all of this. I’m happy to admit that these are distinct ecotypes, but I’d be surprised if the bacteria weren’t able to share genes. Thus it seems that this is the perfect example of reinforcement driving the generation of these ecotypes – becoming half of one ecotype and half of the other must be maladaptive, and this is something that could be experimentally tested. Thus despite the ability to rapidly ‘hybridise’ and share genes, the bacteria don’t, or rather those that do die out. I imagine it’s the frequency-dependent ‘clonal niche construction’ mechanisms the authors discuss that help this get going to begin with – otherwise the first variant to evolve would dominate the entire assemblage. I wonder to what extent such dynamics are a consequence of constant environmental conditions that allow these biotic interactions to play out.

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Lynsey McInnes

I have a soft spot for experimental evolution. I think it’s because I know, and like, simulation studies and experimental evolution seems like the elusive next step. Elegant, tractable and yet also more ‘valid’ than the clinical world of simulations where, some might say, you get out what you put in. One day, perhaps, I’ll have the guts to team up with these people and step out of my simulated world.

The beauty in these setups include the opportunity to have multiple replicate ‘runs’, for evolution to occur relatively fast and with the possibility to take samples during the run to monitor the trajectory of diversification, to manipulate the ‘environment’ of each run while minimising variation from the outside the system. Mmmm…

Anyways, I digress.

This paper builds on previous work from the Doebeli lab and I think provides a neat addition, capitalizing on advances in sequencing technology to really get at how parallel the dynamics of adaptive diversification can be. I found the conclusions – that the dynamics of diversification follow the same trajectory across populations and that this sometimes involves parallel mutations, sometimes not, really quite cool. That different mutations at the genetic level can lead to the same derived phenotype was also a very neat finding. The authors also make a convincing case that the patterns observed are due to frequency-dependent ecological interactions rather than genetic drift or clonal interference.

The introduction touches upon sympatric speciation and how frequency-dependent selection can cause it; the authors seem to shy away from this still controversial topic in their discussion. This is perhaps fair enough, they make their case briefly and then stick to the study in hand, although the implicit message throughout is that this study is providing further evidence for the feasibility of sympatric diversification.

My following of the literature on sympatric speciation is a bit patchy (although I know Doebeli has made some major contributions) although I have had countless relatively uninformed discussions on its prevalence in macroscopic speciation, me spouting that there is probably some kind of microallopatry going on, my opponent countering that such a setup might still be considered sympatric. Anyways, this paper was one of the first to effectively explain how frequency-dependent selection might lead to ‘sympatric’ speciation. My mind is now whirring as to how this mechanism translates up out of this microcosm setup.

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!

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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?

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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?