Eco-evolutionary modeling north of the Arctic circle

In early March I headed up to Abisko, Sweden, for a "winter school" on eco-evolutionary modeling of speciation.  The school was offered by FroSpects, which been hosting some great workshops, conferences, and schools lately, including the Speciation 2010 conference in Austria last December that Andrew wrote a post about (and by the way, videos are now posted for all the talks at Speciation 2010).

Abisko is easily the most remote place I've ever been.  It's a bit north of the Arctic circle, so when they called this a "winter school" they meant it.  We got lucky, though; the week before the school, temperatures were -35°C and the road to Abisko was closed by snow (by an avalanche, in fact, I think), but the week I was there was relatively clement, and we even got several clear nights when we could see the Aurora borealis:

Abisko was a stunningly beautiful place, in a very stark, barren way:

Those who want to see more photos and such can check out my travel blog, but from here on in I'll focus on the science.  We had talks by (in order of appearance) Ulf Dieckmann, Åke Brännström, Eva Kisdi, Rupert Mazzucco, Akira Sasaki, Katja Enberg, Sander van Doorn, and Ole Seehausen.  We also had some discussions and student presentations, but most of our time was spent in lectures.  I think there were twenty students in all, with about a 50-50 mix between modelers and empirical biologists; model systems particularly well-represented at the school included sticklebacks, Heliconius butterflies, and African cichlid fish, but we also had students studying phytoplankton, parasitoid wasps, mice, Wolbachia bacteria in grasshoppers, potato blight, and bacteriophage ecology, among others.  Most of us were PhD students, but we had one precocious undergrad, one postdoc, and one university lecturer, if I got my count right.


A myriad of models

For me, probably the most striking thing about the school was the breadth of modeling techniques discussed.  It was nice to see all of these in one big tent, as it the expression goes; all of these methods have their place.

Eva Kisdi and Sander van Doorn discussed mostly adaptive dynamics models.  These models handle evolutionary branching and speciation particularly well, because they go beyond a study of equilibrium to look at how a population evolves over time, and because they can accommodate a population that branches into distinct phenotypes, unlike approaches that model only the mean and variance of a population and can thus only accommodate unimodal phenotypic distributions.  This type of modeling is not my field, so I was surprised to see how broadly applicable it can be; adaptive dynamics models were discussed for sexual organisms, for example, and for genetically explicit organisms with properties such as dominance (Peischl & Schneider 2009). Åke Brännström also gave a quick talk about using an adaptive dynamics approach to model the evolution of food webs and the process of ecological diversification.

Rupert Mazzucco discussed individual-based models, mostly from a broad philosophical perspective.  These models are ideal for cases where one has reason to believe that a bottom-up approach is best, because individual variation in genetics, behavior, and so forth matter to the emergent high-level pattern of evolution, or because individual-level phenomena such as demographic stochasticity are likely to be important.  Rupert also discussed some implementation issues related to continuous-time individual-based models, such as an event-scheduling technique (Allen & Dytham 2009) that will speed up some of my models considerably.

Katja Enberg talked about "eco-genetic models," which use an individual-based approach combined with empirically parameterized ecological and life-history traits to create unusually realistic models incorporating density-dependent and frequency-dependent ecological feedbacks, phenotypic plasticity, explicit genetics, and other factors.  These models can yield realistic population dynamics and predictions of multi-trait evolutionary rates and sequences, and can even predict evolutionary responses to human influences. The models she discussed were of Atlantic cod (e.g. Enberg et al. 2009), which have been drastically overfished and have evolved (and crashed) in response to that fishing pressure; but this technique seems very promising for other systems as well.

Akira Sasaki presented traditional analytical models (i.e. based on differential equations) of species packing, beginning with the classic models of MacArthur and May from the 1970s, and then showed some of his own work that connects these concepts to spatial distributions of species and heterogeneous distributions of resources (Sasaki 1997).  The connection to speciation may not be immediately apparent, but in fact this was rather mind-blowing for me because it finally explained for me the reasons for the spatial patterns observed in classic individual-based models of competition and speciation such as Doebeli & Dieckmann (2003).  If reproductive isolation often begins with isolation by distance, then spatial patterns may be very important to speciation.

Finally, Ole Seehausen gave a broad, historical perspective on speciation, and presented some of his empirical work on speciation in African cichlids (e.g. Seehausen et al. 2008). He and Sander van Doorn discussed the sensory drive speciation model from both an empirical and a theoretical perspective, and they led a quick workshop that tried to integrate all of these ideas together to show how empirical work is related to theoretical modeling, and how each can benefit from the other.  For me, this was the most challenging part of the school; both the empirical findings and the models were quite complicated, and then the conceptual work of integrating the two perspectives together proved quite difficult!


Hot concepts

As at Speciation 2010, one hot topic during the school was the idea of "magic traits".  There was much discussion, and little agreement, about what is or is not a magic trait, how common they are in nature, how important they are to speciation, and even whether or not it's a term that we ought to use.  It is apparent that the ideas in this area are important; but there is a pressing need for greater clarity, both terminological and conceptual, so we can avoid endless semantic tail-chasing.

Beyond that, probably the most prevalent theme of the school was the future of speciation work, both empirical and theoretical.  There certainly seems to be a growing consensus that the old paradigm of dividing speciation into allopatric and sympatric (and then categorically stating that sympatric speciation doesn't exist :->) is dead.  But what exactly is going to replace it?  There needs to be, it seems, more of a focus on the details of process.  It's highly unlikely that every speciation unfolds in the same way; instead, there appear to be many ways that it can be affected by natural selection and by sexual selection, by ecology and by the environment.  Allopatry and sympatry are limiting cases, but different degrees of parapatry may be the rule. Speciation can be talked about in both sexual and asexual organisms, but the processes are likely very different; and of course there are shades of gray here, too, with facultative selfing in plants, lateral gene transfer in bacteria, and so forth. Different forces may operate at different stages of the speciation process, and the rate of the process may vary dramatically over time — or even reverse.  Genetic details can matter a lot to all of this, as can individual-level behaviors such as mate choice and dispersal behavior.  And speciation will itself interact with other evolutionary processes; one interesting question raised during the school was whether magic traits might be selected for, and thus tend to be available to trigger later speciation.  Speciation is a bottomless cornucopia of beautiful complexity; it will keep us all busy for a long time to come.

One thing we all agreed on, though, is that if progress is to be made it will be essential for theorists and empiricists to communicate more, but it seemed difficult to elucidate concrete ideas to promote this.  One idea that someone proposed is a sort of theorist/empiricist "dating service," a website, presumably, where theoreticians looking for particular sorts of empirical systems to model could get matched up with empiricists looking for modelers with particular skill sets and interests.  Anybody out there want to set this up?  For me, though, the simplest way forward was exemplified by the school itself: get theorists and empiricists together in one room, and let them talk to each other.


Conclusions

I'll leave you with a group photo of (most of) the students and instructors at the school:

Thanks to FroSpects, and more specifically to Ulf and Åke, for organizing this school, and thanks to the instructors, who volunteered their time and their enthusiasm.  Thanks also to my fellow students, who were both brilliant and fun to hang with.  This school embodied, for me, the best of the spirit of science.  I'm already looking forward to the next FroSpects event I'm going to attend, the Niche Theory and Speciation workshop in Hungary this fall, and they've got many more upcoming events that you might want to keep your eye on.

Ben Haller
McGill University


References cited

Allen, G.E., & Dytham, C. (2009). An efficient method for stochastic simulation of biological populations in continuous time. BioSystems 98, 37-42.

Doebeli, M., & Dieckmann, U. (2003). Speciation along environmental gradients. Nature 421, 259-264.

Enberg, K., Jørgensen, C., Dunlop, E.S., Heino, M., & Dieckmann, U. (2009). Implications of fisheries-induced evolution for stock rebuilding and recovery. Evolutionary Applications 2, 394-414.

Peischl, S., & Schneider, K.A. (2009). Evolution of dominance under frequency-dependent intraspecific competition in an assortatively mating population. Evolution 64, 561-582.

Sasaki, A. (1997). Clumped distribution by neighborhood competition. Journal of Theoretical Biology 186, 415-430.

Seehausen, O., Terai, Y., Magalhaes, I.S., Carleton, K.L., Mrosso, H.D.J., Miyagi, R., van der Sluijs, I., Schneider, M.V., Maan, M.E., Tachida, H., Imai, H., & Okada, N. (2008). Speciation through sensory drive in cichlid fish. Nature 455, 620-626.

Science from the edge – part 2: chew and spit, scratch and sniff.

In the previous instalment of this series, which basically amounts to papers I would like to have written, I discussed the groundbreaking experiments by Carl Puke and Richard Taylor on the effects of explosions of various sorts on fish of various types. Although it was beyond the purview of the typical eco-evo research, it was at least eco-evo-explo. In this second instalment, I would like to move from auditory and visual extravagance to olfactory and gustatory revelation. Eco-evo-gusto?

The first classic paper I want to discuss is by Richard Wassersug, now of Dalhousie University and, at the time, of UC Berkeley. Perhaps the paper I will describe, published in The American Midland Naturalist in 1971, facilitated the upgrade in institution. Much science is motivated by simple observation, in this case the fact that tadpoles of many species seem common and conspicuous in tropical rainforests. Why aren’t they eaten by the numerous predators? Perhaps it is because they taste bad – but this wasn’t known for these tadpoles. Clearly this conundrum calls for a predation experiment where the predators are forced to eat the tadpoles and their judgement then passed on the experience. I will let the author take up the story of “On the comparative palatability of some dry-season tadpoles from Costa Rica.”

“The mock predator in this experiment was a sample of 11 students and faculty... The volunteers were two females and nine males aged 22 to 36 ...” One wonders how many students were in the course but did not volunteer for this particular experiment! And in the true spirit of good scientific practice, enough information is provided should one wish to replicate the study. “The standardized tasting procedure included several steps. A tadpole was rinsed in fresh water. The taster placed the tadpole into his or her mouth and held it for 10-20 sec without biting into it. Then the taster bit into the tail, breaking the skin and chewed lightly for 10-20 sec. For the last 10-20 sec the taster bit firmly and fully into the body of the tadpole. The participants were directed not to swallow the tadpoles but to spit them out and to rinse their mouths out at least twice with fresh water before proceeding to the next tadpole.”

Yum?

The first interesting result was that two of the nine volunteers in the experiment had to be eliminated as outliers because they either couldn’t taste anything or were outliers in finding the tadpoles less distasteful. Turns out they were smokers: why haven’t the smoking companies pick up on this benefit of their product? I can see the new label now: “Warning. This project may reduce your ability to find bad food distasteful.” A second important result was that the tadpoles differed in their palatability, with Bufo marinus (cane toad) being the worst and several other species sometimes being ranked reasonably high. However, it is hard to say more given that “No attempt has been made to put these data to any more rigorous statistical tests.”

If something like this can be done so effectively with taste – why not smell? Again, an observation sets the stage. Ever had to change the diaper of your sister’s or brother’s baby - nasty right? Indeed, much fouler than that of your own baby’s diaper, should you have one. If not, take my word for it. Or don’t, because we have a definitive objective controlled and replicated experiment. Writing in Evolution and Human Behavior in 2006, Case and coauthors asked mothers to smell the diapers of their own babies and other mother’s babies, with and without labels – with the labels sometimes correct and sometimes switched between babies. Turns out that other baby’s diapers are indeed more disgusting than your own baby’s – regardless of the label. The title says it all “My baby doesn’t smell as bad as yours: The plasticity of disgust.”

It would obviously be valuable to replicate these experiments. What about the taste of wet-season tadpoles? What about the aroma of your dog’s poop versus someone else’s dog’s poop? The opportunities seem limitless if not effortless. The truth is out there.

Dinosaurs to scientists: “Think fast!”

(A dispatch from Scott Carroll.)

I suppose few people grow up thinking much about evolution, though for decades kids have had dinosaurs, pterosaurs, wooly mammoths and saber-toothed cats actively released into the refuges of their imaginations. And imagine the thrill of early naturalists like Darwin, raised on different tales, who stumbled upon fossil skeletons of ancient titans and knew at once that the world has at times been a very different place from what the present otherwise suggests.

Fossil discoveries highlight ancient denizens of the evolutionary tree, but there is more immediate information at hand among the living: evolution-in-action. For a century, the blind spot of gradualism has led us to segregate evolution too neatly. Yes, air pollution can influence moth color frequencies, but we assume that’s a freak observation, and things quickly get back to normal. Sure, pathogens evolve to survive antimicrobial assault, but we assume they are a shifty peripheral class of small invisible things with their own rules.

But now we know, to the contrary, that the history of life is still being written, and that an evolutionary perspective is as relevant to our future as it is to our past.

Like a meteor gaining self-awareness at the moment of its impact, it is dawning within the collective consciousness of contemporary naturalists that industrial melanism was but the smoking gun of industrial selection, that microbes indeed ‘are us’, and that even the mighty trees may be light on their evolutionary feet. Anthropogenic evolution has left the farm (and the station), and accepted permanent positions in bathrooms, bus seats and hospitals around the world, near you, and on you (e.g., MRSA).

From equator to pole, metropolis to wilderness, 'refugee taxa' that are not disappearing altogether are persisting by adapting, and much of that adaptation is genetic. Other organisms too are evolving quickly to take advantage of new opportunities created by habitat disturbance, mass agriculture, increased human density, climate change, and other forces. Agricultural, medical and environmental systems thus consist of many 'moving targets' that are evolving their own 'solutions’, sometimes to the detriment of what we value, and sometimes quite the opposite. Meanwhile, what of species that are increasingly mismatched to their changing environments– what can evolutionary analyses tell us about the well-being and future of these adaptive laggards, including ourselves?

Just how widespread and important rapid anthropogenic evolution and maladaptation are in practice was unmistakable at a recent international summit of leading Darwinian ecologists, agriculturists and medicos at Heron Island on Australia’s Great Barrier Reef. Entitled ‘Interdisciplinary Solutions to Evolutionary Challenges in Food, Health and the Environment’, the goal was to both overcome and take advantage of the largely independent histories of evolutionary perspectives in these fields, and to build a common dialog of applied evolution. Interspersed, of course, with inspirational diving and snorkeling in Shark Bay, which lived up to its name.

For example, what are the underlying evolutionary commonalities and differences, for example, of

· immigration and invasions of pests and pathogens?
· emergence of genotype-environment mismatch and its influence on individual and population health?
· evolution of virulence and of antibiotic and pesticide resistance?
· sustainability of exploited populations and biological diversity?

How might these evolutionary challenges themselves interact in the context of broader global change? What strategies and lessons can be co-opted across fields?

The answers, or at least steps toward them, are available in video and print. Summit presentations are at http://www.icevolution.org/. From there, you can link to the papers, which form a special March 2011 issue of Evolutionary Applications, are available for download without charge (thanks Wiley-Blackwell!) through April 2011.

Probing the perilous future of the human-biosphere can often grant little more than an ever-grimmer view of how difficult the big issues will be to predict and manage, and for many, to survive. And now we toss evolutionary considerations– yet more variables– into the splashing mix! But I think we should instead take heart: evolution is the predictive core of all the biological sciences. Paleontology was merely a starting point. As we finally integrate evolutionary theory into widespread practice, we will surprise ourselves by designing better means of producing, protecting and preserving the things that we value most.

Photo: the Heron Island crew.

Science from the edge – part 1: explosive impact.

Ever read a paper and think “I wish I had written that”? I do all the time, but perhaps not in the sense you might think. Sure I would have liked to have written that book in 1859, or even those other ones in 1986 or 2000, but I am talking here about something a little less obvious. The ones I would really like to have written seem to be lost gems of science – the ones that have only been cited once or twice – or not at all. Of course, this means that the papers I would like to have written aren’t those that are influential but rather, as you will see, those that are fun and different and obscure for a good reason. I thought it might be a good use of this blog to bring some of these lost classics to the fore so that they can be appreciated or reviled by all as desired. And there are so many that it will take a few posts.

While doing graduate work in the School of Fisheries at the University of Washington, I happened to come across the intriguingly-titled “Use of dynamite to recover tagged salmon” written by Richard Tyler and published in 1960 as the US Fish and Wildlife Service Special Scientific Report 353. Now there is a title that immediately calls for further reading. It seems that the idea here was to put an array of dynamite charges in a stream and sit at the edge of the stream drinking beer and presumably smoking something while keeping an eye on the salmon swimming by. “Holy s**t Bob, there’s one with a tag, quick push the plunger.” BOOM. Then quickly, but probably not too quickly, they would run down to the stream to fish out the bits of fish, hopefully still attached to the tag. Perhaps they sometimes had to collect fish bits from up on the shore too – maybe they even sat under umbrellas to shield them from falling parts. Anyway, it turns out that “The experiments showed that dynamite is an effective means of killing salmon ...” No kidding. In fact, “they proved effective in the recovery of four tags.” Wow – now that seems like a business with a future.



And, in what appears to be a recurring theme from that era of fish biology, I later came across “Experiments in Lake Vaner on the influence on fish of bomb-dropping” published in 1949 in the Report from the Institute of Freshwater Research Drottningholm. And if that doesn’t make you want to read more, consider that the author’s name was Carl Puke. Truth in advertising. So this time, the concern was that the Swedish Air Force used this lake for bombing practice and the local fishermen were upset because the quality of fishing was somehow not the same – not to mention the discomfiture that ensued at the sound of an airplane while out fishing on some lazy Sunday afternoon. To address the hypothesis that bomb dropping was the cause of fish declines, “various quantities of fish were placed into rather large (how’s that for precise!) steelwire cages ... at different distances ... from the spot selected for the explosion.” Then, “the bombs were dropped from an aeroplane or placed by hand ... and blown up electrically.” I am not sure whether this more considered approach would induce more or less adrenaline than the “quick push the plunger” approach of the previous study. However, in contrast to that previous work, “After dropping a large number of bombs from a plane, no unconscious or dead fish could be observed in the area concerned.” But perhaps this reflects more on the quality of the Swedish armory than the quality of the Swedish fish. Maybe everything really is bigger in America – although the size of the explosions in these pictures might suggest otherwise – maybe the Swedes were using trick photography, as one might expect from fishermen.

Writing this post has got me to thinking that maybe I can write this paper after all. Here we have two opposing outcomes vying for academic supremacy. Moreover, perhaps there was some animosity between the groups – given that Tyler did not in 1960 cite Puke from 1949. How could a funding agency not see the logic of solving an outstanding scientific problem once and for all: do explosions commonly kill fish or not and under what conditions? The only problem is figuring out what category of “invasiveness” I need to select on my pending Animal Use Protocol.

Ps. Those in the know argue that the recovery of four tags in the salmon study really was valuable – because these tags were placed on fish in the middle of the Pacific Ocean to determine where salmon from different rivers went when they were at sea – and whose fish were being caught in what parts of the ocean. The problem was that people sitting at counting stations along streams would see a tagged fish swim by with no way to recover it. Until they got the plunger, that is.