Eco-evosystem dynamics

In a recent Review & Synthesis paper in Ecology Letters, entitled "Toward
an Integration of Evolutionary Biology and Ecosystem Science", we set out
to find common ground between evolutionary biology, community ecology, and
ecosystem science ( Paper is here ).

This project started with a PhD summer school in 2009 at the Centre for
Ecology, Evolution and Biogeochemistry, in Kastanienbaum Switwerland
(Eawag CEEB). We recruited an all-star cast of lecturers that had a broad interest in eco-evolutionary dynamics, including: Jim Elser, Nelson Hairston Jr., Eric Triplett, Andrew Hendry, Elena Litchman, and Luc De Meester. For two weeks they regaled us (see
participants) with their stories, and inspired us to put something down on paper.

The proposed goal was simple: integrate ecosystem science with evolutionary biology.

Our starting point was a paper by Jim Elser in The American Naturalist
(Biological Stoichiometry: A Chemical Bridge between Ecosystem Ecology and Evolutionary Biology). This paper called for a unification of evolutionary thinking with ecosystem ecology and labelled this challenge "the most important frontier for biological integration".

Several sub-disciplines have taken up this challenge, including biodiversity and
ecosystem functioning research, ecological speciation, and community
genetics. Moving forward, I think the growing field of eco-evolutionary
dynamics can make a substantial contribution to this effort.

To make progress, we need to identify heritable traits that underlie the
effects organisms have on their ecosystems. If such traits are also a target
of natural selection, then phenotypic evolution might have predictable
consequences for ecosystem processes. This sounds easy enough, but to
do this we need to make 'interdisciplinary research' much less of a buzzword,
and more of a working reality.

Some of the best examples of integration between evolutionary biology and
ecosystem science have come from recent manipulative field and mesocosm
experiments. In this review, we have branded such experiments as "common
gardening experiments", to emphasize that organisms differ in how they
modify (or garden) their environment. So far, one in three reviewers
doesn't like this term, but we think it's useful.

Common gardening experiments bring researchers together from disparate disciplines. If you look at the authors lists of papers like Palkovacs et al. 2009 PTRS-B , Harmon et al. 2009 Nature , Bassar et al. 2010 PNAS , you will see a refreshing mix of researchers with backgrounds in both evolutionary biology and ecosystem science. These papers provide some initial proof-of-concept, but really only scratch the surface of the rich role that evolution can play in our natural ecosystems.

God's Advocate?

In science, it is both boring and annoying when everyone agrees. Once that happens, what is there to talk about? That is why every working group, talk, or paper needs a Devil’s Advocate. Devil’s Advocates make things exciting. They make things move. They break a discussion or project out of lethargy and complacency, and they cause everyone to crystallize their arguments and ideas and explore new ground. Where would we be without them?

But what if there were too many? What if everyone was a Devil’s Advocate? What would happen then? Maybe nothing. Maybe everyone would be too critical and nothing would move forward. Maybe everything would bog down and nothing would get achieved. That is why every working group, talk, and paper also needs a God’s Advocate. A God’s Advocate sticks behind an idea, selling it to sceptics, and fighting the Devils’ Advocates to some middle ground – a place where progress is made in some new area and is backed with the best possible logic and clarity.

Just a few weeks ago at Gault Nature Reserve on Mt. St. Hilaire, we convened the second meeting of the Quebec Centre for Biodiversity Science (QCBS) working group on Eco-evolutionary Dynamics. (For a dispatch from the whisky-soaked first meeting, see http://ecoevoevoeco.blogspot.com/2011/01/whisky-rescue.html) The main goal of this meeting was to figure out how quickly ecological function evolves. It is now well known that traits can evolve quickly, although they don't always do so, and that some such changes can have ecological effects – but how common is this and on what time scales does it play out? To this end, we compiled databases that examined how quickly ecological function evolves. A few such datasets exist but they aren’t common, and so we also sought to determine rates of change in traits likely to have ecological function, such as body size or trophic position. Jonathan brought his carnivores, Bea and Nicholas brought their zooplankton, Chris and Eric P brought their fish, Hans brought his dinosaurs (what else), Nash and Mark brought their plants, Andrew and Mart brought their contemporary evolution, Fanie and Eric V brought their R and found some birds, Matt brought his model, Gregor brought his Matlab, and David even brought a manuscript!

It turns out that traits evolve – duh - all types of them and at all sorts of different rates. One pattern in particular emerges in almost every dataset: changes can be rapid over short time frames but don’t continue to accumulate into large changes on longer time frames. Kind of like a ball bouncing around in a closed room – fast in any given direction until it hits a wall and then fast in another direction. This isn’t a new result, of course, and so what should we do then? How can we make an important contribution to eco-evolutionary dynamics and go beyond this already recognized pattern? Here was where the advocates – both Devil’s and God’s – came into play. Ideas were raised and trashed and raised and trashed. Sometimes they rose from the ashes of a previous trashing. Sometimes they were never heard from again. And sometimes they just bounced around in that closed room – never coming to rest, but also never getting anywhere.

To my way of thinking, both types of advocates were critical. We came up with some very original and cool ideas for how to analyze rates of evolution – and we used them to find some perhaps surprising patterns in the data that originally seemed to say the same old thing. The new metrics have their limitations, of course, but which metric doesn’t? And they allow us to think about the problem in new ways. I won’t tip our hand in this blog and I could say this was because that the paper is coming soon to an important journal near you. The truth, however, is that the Devil’s Advocates are still doing their job – and so God’s Advocate must find that ultimate magic that finally lets the ball bounce out of the room and into the wide world. Stay tuned for the third meeting.


Mark was missing from the photo -sorry - but perhaps he was checking out these cool shrooms!

Niches schmitches

Lake Balaton countryside

On the steamy shores of Lake Balaton in central Hungary was recently convened the “Niche theory and speciation” workshop, hosted by Geza Meszena, Liz Pasztor, and colleagues. Three days of talks were interspersed with opportunities for discussion and debate. A favourite, or at least convenient, venue for debate was the hotel lounge, with a beer or wine in hand and entertainment provided by retirees tripping the light fantastic on the dance floor while an aging trubidor on a synthesizer played the “classics” suffused with a distinctive Hungarian flavour. Somehow the normally stale debate about sympatry versus allopatry gains a new vitality against the backdrop of whirling gray (or overly black) hair and a tinny synthesized “Ring of Fire.”

So just what are “niches” anyway, aside from some set of conditions that are (or might be) occupied by a particular species? Are they Hutchinsonian, Grinnellian, Eltonian, or other? Are they alpha or beta, fundamental or realized? Are they properties of the organisms, the environment, or both? Can a niche exist without an organism occupying it? To what extent do organisms create or destroy niches for themselves and other organisms? Despite much discussion, no agreement was reached – because the different concepts are differentially useful in different contexts. In the end, however, the truth is – as someone pointed out – that “we can’t define them but we know them when we see them.” With this in mind, we can ask how niches might influence speciation.

For instance, one might ask how critical distinct niches are for speciation. Is speciation is always ecological (adaptive) or can it also be non-ecological (non-adaptive)? Bob Holt was happy to champion the potential importance of non-ecological speciation, whereas many adaptive dynamicists remained sceptical. Nevertheless, at least three talks were given on non-ecological speciation, including two on the “neutral theory of speciation.” (Just when I thought Hubbell’s theory was finally waning, it again rears its unrealistic head.) But to be more honest, the presenters merely wish to explore this theory as an interesting mathematical problem – or as a null model – rather than to assert it really was an important contributor to the diversity of life. And yet, as Michael Kopp pointed out, the pesky theory does often seem to get the right answer (predicting real patterns of biodiversity) even though it is presumably for the wrong reason. So although that neutral stuff is all very elegant, we might as well get back to considering the important thing in the evolution of diversity: niches.

Does increasing competition for one niche favour shifts to new niches – as theory predicts or assumes? Of course it does – right? Well, Christine Parent showed that flour beetles stubbornly refuse to obey the laws of niche theory – no matter how often you explain it to them. Other topics of discussion ranged from the classic and general to the new and specific. On the classic end of things, no meeting on speciation would be complete without an impassioned debate on allopatry versus sympatry versus parapatry. Nearly everyone recognized that sympatric contributions to speciation would be most effective following an initial period of allopatry, which led to Ole Seehausen’s pithy observation that perhaps “allopatry is necessary for sympatric speciation.” And, of course, one always needs a vigorous discussion as to whether or not the terms themselves are even useful. In response to a disparaging comment on this point Jon Bridle, Jim Mallet was clear to assert that what he really meant in his earlier statements was “APPROXIMATELY sympatric” and “APPROXIMATELY allopatric.” A new addition to the lexicon of evolutionary biology?

As for the more specific, I was intrigued to learn that a persistent problem in the theoretical world is whether or not continuous coexistence (essentially a very large number of species that partition themselves very finely along a continuous resource gradient) is possible. And the answer proved to be ... YES ... or NO ... or maybe - depending on who was speaking. But, of course, this is a theoretical question since it never happens in nature, which then contributed to a long discussion on the frequent disconnect between theory and empirical data.

And then there were the two hours a small group of us spent debating Joel Brown’s unified theory of human evolution – this one decidedly not based on a neutral theory. Weaving a beautiful adaptive tale with liberal anecdotes from squirrels, culture, politics, and G functions, Joel constructed a convincing simultaneous explanation for those three traits that among the mammals are unique to humans: high maternal mortality at birth, menopause, and concealed ovulation. At least I think he did.

Fisher is dead - long live Fisher.

I recently spent four days at the meeting of the European Society for Evolutionary Biology (ESEB) in Tubingen, Germany. A pleasant surprise was that the meetings were very eco-evolutionary, at least from the perspective of how ecology drives evolution. Lots of talks were given on ecological speciation, interactions between natural and sexual selection, phenotypic plasticity, and the genetics of adaptation. So I had no shortage of talks that I wanted to attend. At one point, five people I wanted to see were talking simultaneously. As the storm clouds gather over Tubingen, however, what I really want to do in this post is rail against a communication problem between the practitioners of a particular field of study and the rest of the evolutionary community.

A contemporary debate in evolutionary biology, and indeed in biology in general, surrounds the genetic basis for adaptation and speciation. Is adaptation the result of many genes of small effect, as Fisher famously declared, or is it instead the result of relatively few genes of large effect? The many-small view held sway for much of the last fifty years – notwithstanding a number of examples of genes that had large phenotypic effects. More recently, however, increasingly powerful molecular methods have led to a seeming sea-change toward the few-large view. In particular, the discovery and characterization of specific genes with large effects on adaptive phenotypes has led a fair number of biologists to now assert that Fisher is dead in both senses, and that we now finally see the world of adaptation in its true – oligogenic – form. This is nonsense – but I can see where it comes from.

Every time I attend a scientific conference – and this year’s ESEB meeting was no exception – most talks on the genetics of adaptation report a search for THE GENES that determine adaptation: sometimes they find such genes and, if not, become apologists for failing to do so. (And published papers are the same way.) This gives the audience the impression that studying the genetics of adaptation must involve a search for THE gene that underlies divergence in the trait. What is often lost on the audience is that investigators normally screen large number of traits for large effect genes and then specifically choose – for practical reasons – to focus only on those of largest effect. In addition, it is often forgotten that Fisher’s assertions were about ADAPTATION per se, not adaptive TRAITS. In general, adaptation to different environments in nature will involve many traits (life history, morphology, physiology, behaviour) and, even if one or two traits within these classes are indeed mainly oligogenic, those same genes will almost certainly contribute to only a small proportion of the variation in overall ADAPTATION.

As just one example, Rowan Barrett gave an outstanding talk about natural selection on EDA, a gene that strongly influences variation in lateral plate number of stickleback fishes, which differ dramatically in this trait between freshwater and marine populations. This work on EDA, along with Hopi Hoekstra’s work on MC1R in field mice, represent some of the best-characterized effects of a single gene on selection and adaptation in natural animal populations. However, EDA gives a misleading picture of overall adaptation to freshwater. For example, genome scans for evidence of divergent selection across the whole genome (work from the lab of Bill Cresko and others), and studies of gene expression (such as by the groups of Louis Bernatchez and Juha Merila), show that adaptation to freshwater in stickleback clearly involves many – probably hundreds – of genes. Thus, while EDA may explain a substantial fraction of the variation in lateral plates, it will not do so for overall ADAPTATION. And similar data on the polygenic nature of adaptation is accumulating from similar studies of other organisms, such as whitefish, mosquitoes, walkingsticks, and so on.

So every time I hear one of those “THE GENE FOR” talks, I can’t wait to corner the author later at the pub – plenty of those in Tubingen – to ply them with fine ales and regale them with polygenic tales. Recently, I have been able to debate the many and the small with Rowan, Hopi, Katie Peichel, David Kingsley, and Dolph Schluter. It turns out that all of the above points are recognized and embraced by these investigators. That is, people actually studying the genetics of adaptation to divergent environments in nature believe that it involves many genes of small to modest effect. It is just that they are specifically studying only those few of largest effect – and it is much easier to study the genetics of a few traits than of overall adaptation to a given environment.

It really is a many-small world after all.

Broken barriers

[ This entry was written by Erika Crispo; I am just posting it.  I added the images and captions, so if they are screwed up somehow, that's not Erika's fault.  BCH ]

Humans are directly affecting wildlife through various activities, leading to declines in the numbers of individuals, populations, and species. It is less clear, however, how these activities are indirectly affecting wildlife through impacts on the genetic constitution of populations and species. In a recent review paper, we identify two general ways in which human activities can influence genetic exchange.

Humans may be reducing post-zygotic reproductive isolation in the Medium Ground Finch of the Galápagos Islands by augmenting the food supply.  Photo by Putney Mark.

First, lineages that were previously isolated by geographic barriers can be put into contact, thus allowing genetic exchange should these lineages be able to interbreed. This might occur if (1) humans alter landscapes such that increased dispersal is possible, (2) anthropogenic climate change allows increased dispersal into areas that were previously uninhabitable, or (3) humans introduce individuals directly (intentionally or unintentionally) by physically moving them.

A second way in which humans can influence genetic exchange is by disrupting reproductive barriers, such that lineages that were previously reproductively isolated in sympatry can now interbreed. This might occur if (1) the sensory (e.g. visual, chemical, auditory) environment is altered so that individuals are no longer able to recognize and chose suitable mates, or (2) the adaptive landscape is altered so that selection against hybrid individuals no longer occurs.

Habitat degradation due to human activity in Lake Victoria (East Africa) has led to biodiversity loss through hybridization between the endemic haplochromine cichlids there, a process called reverse speciation.  Photo by Haplochromis.

Whether genetic exchange has positive or negative effects on fitness and population viability is context-specific. For example, negative effects of genetic exchange should occur if populations are locally adapted and gene flow results in the incorporation of maladaptive alleles into the populations. On the other hand, positive effects of genetic exchange would occur for small, isolated populations by increasing genetic variability and thus evolutionary potential. An additional consideration is that increased gene flow and decreased reproductive isolation could lead to genomic extinction, i.e. extinction of the unique combinations of genetic material that are characteristic of a particular species or lineage. For conservation and management purposes, we argue that it is important to take a gene-centric approach, by appraising not only the direction and amount of genetic exchange, but which genes are being exchanged and their relevance to the sustainability and uniqueness of the populations in question.

For further information and empirical examples, please see our manuscript:

Crispo, E.*, Moore, J.-S.*, Lee-Yaw, J.A., Gray, S.M., and Haller, B.C. (2011) Broken barriers: human-induced changes to gene flow and introgression in animals. BioEssays, 33, 508-518.
*Both are first authors

Selection, mutation, gene flow, and drift: the Canadian Institute of Ecology and Evolution

I spent the last two days at the meeting of the Management Board of the Canadian Institute of Ecology and Evolution (CIEE). The meeting was hosted by CIEE Director Art Weis at the University of Toronto’s Koffler Scientific Reserve. Additional conspirators in attendance were Mark Forbes (Carleton University), Steve Heard (University of New Brunswick), and Locke Rowe (University of Toronto). Sally Otto (University of British Columbia) joined us by Skype. Our task was to plan and implement the continuing development of the CIEE and its programs.

The setting was unique – the former country ranch (800+ acres) of Murray Koffler, founder of Shopper’s Drug Mart and the Four Seasons Hotels. The house was once decadent and, although now in some disrepair, was still memorable - and not just because we could visit the bedroom where Pierre and Margaret Trudeau reportedly conceived Justin. My favorite part of the house was (no surprise here) the bar – an oval room paneled with wood from an old barn and stocked by Art, and his wife Donna, with an extensive collection of spirits – including a 21 year old Balvenie, now sadly much diminished. The evenings passed pleasantly in such surroundings and, with the ample liquid encouragement, Art’s sister gave us all tattoos befitting our inspirations and aspirations. No word yet on whether Locke and Sally will follow suit.

The grounds themselves were an interesting mix of forest and old fields, with the fields swimming in flowers and swarming in their pollinators. Several large ponds had been built along the course of a creek and these were home to squadrons of fighting and mating dragonflies – the photographing of which made me late on several occasions. I was also distracted by a group of sparrows foraging for caterpillars on the driveway under the large trees that lined it. It seems that green caterpillars were literally raining down on the pavement and were much more conspicuous there than they would have been on the ground. As far as I could tell, the sparrows would unendingly walk up and down the driveway getting a caterpillar every meter or so – all day long. One wonders if the result will be selection on the adult insects to not lay eggs on trees with pavement below them – but perhaps no genetic variation (and therefore evolutionary potential) exists in such behavior.

And, yes, we did actually do work. We crafted a statement of the vision and mission of the CIEE (a DRAFT is reproduced below); we finalized a plan for funding, membership and governance; we worked on a prospectus and progress report; and we brainstormed candidates for the next Director and the Scientific Advisory Group. On departure, we all promised to get together for another round of drinks and tattoos in the future.

Vision and Mission (DRAFT)

The CIEE provides a national platform for breakthroughs that integrate ecological and evolutionary sciences to address fundamental challenges and practical concerns of importance to Canadians. This integration will be critical to the generation, translation, and mobilization of important knowledge about the world around us. This knowledge then enlightens society as to how best to identify and protect critical components and services of the biosphere now and in the future.

The CIEE will accomplish its vision by

· Identifying existing and emerging challenges that require expertise in ecological and evolutionary analyses;

· Assembling the best teams of scientists to tackle those problems with synthetic and integrative approaches;

· Mobilizing those teams by providing support for them to focus on solutions to those challenges; and,

· Involving students and young researchers, thereby shaping and empowering the next generation of experts who will use synthetic and integrative approaches to solve future challenges.

Quantitative genetics in stickleback: implications for reproductive isolation

We now have a study online in JEB that examines how differences between lake and stream stickleback ecotypes in foraging-related traits (gill raker number and aspects of body shape) are inherited quantitative genetically. The study is a line cross analysis of different lab-reared pure and hybrid lines derived from the well-known ecotype pair residing in Misty Lake and its inlet stream on Vancouver Island. We find that gill raker number is inherited additively (e.g., F1 hybrids are intermediate between the pure ecotypes), whereas there is strong dominance in body depth. That is, F1s and other hybrids between the lake and stream types display the body depth typical of the lake ecotype. We argue that this difference in inheritance has implications for the speciation process between the ecotypes: given divergent selection on gill raker number, hybrids should be at a disadvantage relative to pure types in both the lake and the stream. By contrast, asymmetric introgression from the stream to the lake (but not vice versa) should be easier for body depth because hybrids resemble the lake resident and should therefore not be selected against. It would now be great to have direct information on the strength of selection acting on these phenotypes, and to look into the molecular basis of their divergence.

In addition to these biological findings, the paper has some methodological relevance because we found that a geometric morphometric (relative warp) approach to shape analysis yielded results qualitatively different from an approach based on traditional distance traits. Given that relative warps are principal components extracted from shape variables and that principal component analysis creates artifacts (see Berner 2011, Oecologia), we hypothesize in the paper that the patterns identified through relative warp analysis are artificial to some extent. We have now confirmed this with simulated data; a formal analysis should come soon.

...And who does not agree relative warps indeed look artiFISHal:
If interested, check out "Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation".

Daniel and Joost