Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation

Elena and Lenski (2003). Nature Reviews Genetics 4: 457-469. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation

Local optima can hold back a population from doing the best that they could

Local optima can hold back a population from doing the best that they could. From Elena and Lenski (2003).

Will Pearse

Will Pearse

This paper is more than a little beyond what I usually read, but I always enjoy going to bacterial evolution talks, and I enjoyed this. This is such a rapidly-changing field that I’m certain new things have come out – please do chime in!

I was very struck by the discussion of mutators. The idea that individuals with higher rates of mutation can, in some circumstances, be of benefit to the rest of the population is really cool. It also has a lot of implications for the constant arguments I seem to have with people over what ‘evolvability’ is: as far as I’m concerned, if there’s a thing that increases the rate of adaptation of a population, that’s an increase in evolvability, and mutators seem to be that. We talk a lot in large-organism evolutionary biology and biogeography about the importance of historical accident – that fast rates of mutation only sometimes increase the evolvability of a population, and only sometimes do such individuals come to dominate, is an excellent repeatable and predictable example of the problem. It’s nothing short of amazing that we can do accurate back-of-the-envelope calculations and figure out the odds of a particular outcome in a petri dish.

One thing I want to slightly temper some of this with is the importance of natural history in these populations. It’s all very well studying the evolution of bacteria in stationary phase and discussing how this is different from what we normally find in the lab, but stationary phase is not the normal state of affairs for bacteria. In the wild, bacteria are not transferred into new media when there’s too many of them, and the same goes for large-bodied organisms too. If we want to understand natural evolutionary processes, we need more stationary phase experiments (right? Am I being ignorant?). To paraphase someone else, we also spend a lot of time examining bacteria that cause diseases in particular environments (the human gut, for instance), and modelling their evolution in situ. The problem with this is that this isn’t what those species do for their whole natural history – if you don’t consider how those species got into that environment (water, soil, kitchen sink, etc.), or what some might call a ‘fluctuating environment’ then you’re not going to get the complete picture of the evolution of that species.

Lynsey McInnes

Lynsey McInnes

This is a difficult paper to discuss because I feel like I know that there have been many advances since it came out, not least in our capacity to study mutations and their effects right down to the level of single nucleotide polymorphisms and up again to the level of whole genomes. However, my knowledge of this literature is hazy at best (but see Will’s and my first attempt at discussing experimental evolution here). I’m just going to paste in the abstract below so you know what the paper was actually about (seen as my post barely touches on it…).

Microorganisms have been mutating and evolving on Earth for billions of years. Now, a field of research has developed around the idea of using microorganisms to study evolution in action. Controlled and replicated experiments are using viruses, bacteria and yeast to investigate how their genomes and phenotypic properties evolve over hundreds and even thousands of generations. Here, we examine the dynamics of evolutionary adaptation, the genetic bases of adaptation, tradeoffs and the environmental specificity of adaptation, the origin and evolutionary consequences of mutators, and the process of drift decay in very small populations.

What am I going to write about then? Well, I think going off on a tangent seems like the best idea. My background is heavy on macroecology (patterns! scale!) and my current work centres around exploiting neutral genetic variation among populations to infer demographic history (which I am increasingly realising can get quite close to macroecology when it wants to). So I am not accustomed to thinking about mutations that affect function or adaptation in beneficial or a deleterious ways. Selected genes are in fact the bane of my data. Although I remain unconvinced that we are ever confident that a locus is ever completely neutral.

In fact, I am quite jealous of experimental evolutionary biologists. It seems unfair that they are able to watch things (really, anything!) happen in real time whereas macro-scale analyses (macroevolution, macroecology, phylogeography, biogeography) rely on sometimes shaky sets of assumptions, occasional blind leaps of faith and (more often than not) bundling a lot of unexplained variation into historical contingency. I am a big fan of comparative and meta-analytical approaches (which I’ve advocated on many a PEGE post) where generalities can emerge on diverse topics such as prevalence of niche conservatism, latitudinal richness gradients, modes of trait evolution, even of community assembly, but there is always the niggling doubt that contingency gets in the way and overrides any signal. Wouldn’t it be great if we had five Caribbeans and could throw on five identical Anolis clones and watch what happened? Bacterial experiments can do this! So jealous!

What I’d like to see is more engagement between experimental evolutionary biologists and macro-people. How close can we get to equivalent situations? Can we apply our macro approaches to bacterial setups and see what we find? What is and is not transferable? How much does asexuality mess things up? How much does single cellularity mess things up? I am quite sure that there must be some theoretical exploration of these ideas, but I’d like to see more cross-talk among empiricists. Especially now that we can sequence anything (especially easily bacteria), let’s find out more about how comparable these systems are and what the next stage might be?


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.

Functional extinction of birds drives rapid evolutionary changes in seed size

Galetti et al. Science 340(6136): 1086-1090. DOI:0.1126/science.1233774. Functional extinction of birds drives rapid evolutionary changes in seed size

Birds only disperse what they can carry! From Galetti et al.

Birds only disperse what they can carry! From Galetti et al.

Will Pearse

Will Pearse

Wam-bam, this is a paper I would have loved to put in my undergrad essays. Plants need birds to disperse their seeds, and so when large birds go locally-extinct, plants evolve smaller seeds that smaller birds can carry. This happens really, really fast (within the last 75/100 years!) and so is a great example of rapid evolution.

A nastier man than I would point out that this is somewhat inferred; with no data on what seed size was like 100 years ago there’s a fair bit of supposition going on here. However, their variance decomposition (34% due to birds in forest, 0.1% differences among sites) is really quite striking, so I’m quite happy to go along with this. There’s such a clear link between seed size and probability of being dispersed (figure 2b) that I’m quite happy to accept the smoking gun of a huge selective pressure and observable differences.

Which leaves me with a slight problem, because I always assume that we can ignore both intraspecific variation and rapid evolution when doing ecosystem service work. If trait can evolve this rapidly, treating species’ ecosystem services and traits as fixed is no longer acceptable. Indeed, the situation is doubly problematic because there are going to be a lot of downstream effects of changing seed size, not just on the plant species itself (it’s now shifted on the simplified on the r vs. k selection spectrum), but also other species that interact with that plant. There is a huge literature on how phenology shifts are worse in tri-trophic interaction networks because not every component of the system can keep up with change – I see no reason for this not to be a concern here.

Lynsey McInnes

Lynsey McInnes

This is to all intents and purposes a very neat demonstration of purported rapid evolutionary change in the face of a new selective pressure brough about by human-mediated loss of large-gaped frugivores from forest fragments. One could quibble on whether the frugivore loss is driving the contraction in seed size variation, or whether fragmentation caused the frugivore loss, and so on, but the authors do a thorough job of dismissing other possible correlates….environmental differences among sites, checking the time needed for such a response, and I’m pretty convinced the relationship holds.

This is bad news! It suggests many of those stacks of papers predicting responses to climate change or habitat fragmentation that brush evolutionary responses under the carpet are probably missing key elements of the response game, Similarly, how does this two trophic level result cascade to additional trophic levels. Without big palm seeds and thus big healthy palms, what grows in their place? What effect do these newly dominant plant species have on other pieces of the forest ecosystem.  Ah, its frightening.

What is the next step? Can we rejoin the forest fragments and get the large-gaped frugivores back? Is there enough genetic variation left to get back the large seeds?

This must have been a time-consuming study and its just not feasible to initiate tons of new studies at similar scales to ascertain how pervasive such rapid evolutionary responses are. I would naively guess that it might be better to continue with this system and see if we can work out this change’s effect on additional chunks of the forest ecosystem. Perhaps the authors are already working in that.

The macroecologist in me also ponders the feasibility and merits of expanding the scope of such studies. Perhaps to a mesoscale at least. I am reminded of Phillimore et al‘s very slick mesoscale studies on variation in phenological responses across space in British frogs. Here, the authors were looking to distinguish local adaptation vs. plasticity governing the spatial variation that they saw in order to predict how populations would cope in the face of climate change that will alter the timing of temperature cues. In short, the authors conclude climate change is expected to outpace the frogs’ ability to respond. However, they ignored the potential for microevolutionary change, as the timescales they were thinking of were so short. The challenge now seems to be to incorporate this possible response? Admittedly, easier said than done…

Convergence, adaptation, and constraint

Jonathan B. Losos. Evolution 65(7): 1827-1840. DOI:10.1111/j.1558-5646.2011.01289.x. Convergence, adaptation, and constraint

Are these Anolis dewdaps constrained? Maybe more than you’d think… (PLoS One; click for source)

Will Pearse

Will Pearse

We’ve covered too many data papers recently (that’s not a joke, but it does read like one), and so I picked this paper to help us step back a little and think. I’m pleased with the result: this is an excellent essay, that really made me think about what convergent evolution actually is. I’m particularly keen to hear what you all think of my comments about history!

Losos argues convergence is scale-dependent: there are many ways to evolve a long beak, and while there may be divergent evolution of the actual genes involved, the resulting phenotype (a long beak) is convergent. We’ve covered convergent evolution in bacteria, where the same genes (but different regions of those genes) mutated in parallel in separate lineages. I like this scale-dependency – it allows us to define convergence so that it’s amenable to study at all levels from phenotype to genetic mechanism.

I think we can push this framework further, and compare very different systems in meaningful ways. For instance, maybe examining constraints to evolution in responses to predation in Daphnia is easier when you consider what constrains their tolerance of the abiotic environment. Maybe seeing particular stressors and evolved responses as analogous to one another allows us to better compare evolution among clades, and view constraints to evolution in a more holistic way..

Apparently, there are some who take the view that evolutionary changes are incomparable historical events, and so the whole idea of convergence is a nonsense. I think this is rather peculiar; while there is a debate in history as to whether the field is a science (I think it is, but I’m not a historian!), every historian I know compares periods and events in history, with the precise aim of drawing parallels among periods. Thus I think the argument that evolution is the study of history, and therefore will not allow us to compare events, is not one even a historian would agree with!

Lynsey McInnes

Lynsey McInnes

Commenting on a Losos paper is always going to be tricky, as this is a man who knows his evolutionary biology! You can tell this in two ways, first simply by the breadth of examples he draws on and second by his daring to question the be all and end all of phylogenetically-informed analyses, another recent examplesof his critique of such analyses can be found here.

Like Will, I appreciated having a week off from data bashing and am currently juggling all the different issues that Losos brings up on what is and is not convergence, parallelism, adaptation, exaptation, etc. The biggest take home message I got from the essay was that, as always, scale matters. Birds and bats both have wings that let them fly, are these convergent traits? Depends on your scale of comparison. It seems like identifying instances of convergent evolution would be simplified immeasurably if the researcher concerned just set out the scale across which he is looking and perhaps also mentions whether he is worried about the trait being the ‘same’ at the genetic, phenotypic, morphological and/or morphological level. Hey presto, confusion and agro could be gotten rid of.

I can’t help comparing the issues brought up here to the ones Losos, and plenty of others, have attempted to deal with concerning identifying instances of niche conservatism. Again, it all depends on scale. Cooper et al. provide an excellent roadmap for conducting analyses on nice conservatism, I’d like to see a companion piece to this essay detailing the practical approaches to sensible analyses of putative instances of convergent evolution.

I’ve recently shifted the scale of my own analyses to incorporate (currently to deal exclusively with) intraspecific variation. In practice, this has meant starting to think about different models of mutation (infinite site, infinite allele, shitty recombination raising its ugly head begging to be dealt with) so I find my scale of analysis shifting to the genetic level, wanting to see mutations in same genes, indeed at the same sites to qualify as parallel evolution. For this reason, I really appreciated this essay as it forced me to address my newfound genetics-only bias and realise that interesting, valid and evolutionarily important convergent changes at the functional (or even just phenotypic) level need not be produced from identical genetic changes.

The recent bacteria study that we discussed here at PEGE was a brilliant example of a standalone set-up for studying evolution across these different levels (genetic, phenotypic, etc.), the next step, as always, is to devise a set-up that facilitates similar inference in systems where access to all these levels might be patchy. Losos’ essay will undoubtedly be helpful in this regard.

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