Predictable unpredictability and 25 stickleback biologists in the field.

Ecology and evolutionary biology – and their intersection (evolutionary ecology, eco-evolutionary dynamics) – strive for inferences that are robust, consistent, and stable. For instance, investigators commonly explore how organisms differ between habitats (different “ecotypes”) and how these ecotypes have different ecological effects. Once the differences are discovered and the patterns established, we would expect them to be at least relatively consistent through time: year after year after year low-predation guppies should look like a low-predation guppies and high-predation guppies should look like high-predation guppies. With such consistency, we can draw robust general conclusions about the way the world works. Without such consistency, what do we have beyond a series of snap-shots with little generality to connect them?

Sampling the Misty Inlet Stream.

I spent last week in the field on Vancouver Island helping to start some new projects on the threespine stickleback that live in lake and stream environments. This is a system where the patterns are well established, robust, consistent, and stable. For instance, lake stickleback are always shallower-bodied than are stream stickleback – and surely 15 years of studying the same stickleback populations should allow a researcher to draw many such generalities.  

Dieta shows how it's done.

One of this year’s projects, led by PhD student Dieta Hanson, seeks to understand how differences in breeding time contribute to reproductive isolation (i.e., low gene flow) between adjacent lake and stream populations. In particular, previous observations suggested that stream populations start to breed earlier than adjacent lake populations, which should mean that the two ecotypes will show reduced interbreeding and thus restricted gene flow. With this prior experience as her motivation, Dieta has been repeatedly sampling a variety of lake and stream stickleback populations so as to assess changes through time in the number of reproductive males and females, which will allow her to calculate overlap in breeding time and thus the potential restriction on gene flow. This past week, a group of us joined Dieta to sample the Beaver, Misty, and Robert’s watersheds.

The Misty crew hard at work

I had asserted that stream fish breed earlier than lake fish not only to Dieta but also to everyone else on the crew, including stickleback savants Katie Peichel and Rowan Barrett. Much to my surprise, our Misty Lake sample turned up a fair number of reproductively mature individuals but the Misty Inlet stream sample turned up none – not one gravid female. After having not-so-subtly pitched myself as the resident expert on stickleback, I had to start back-tracking to somehow limit the damage to my reputation caused by this new observation. I think I failed because the crew started poking fun at me (or rather with me) – not just for incorrect stickleback assertions but for my tendency to misplace the truck keys in grocery stores, for my failure to have brought any soap or shampoo or towel, for my affinity for hot chocolate, and so on. However, the next day we sampled the Misty Inlet stream again and found a number of gravid females – so perhaps I rehabilitated my reputation somewhat (at least the stickleback part), especially after winning the pool for predicting how many stickleback we would catch (I was only off by one). Overall, however, it was becoming clear that the dramatic difference in breeding time that I had come to expect might not be strong and consistent.

Rowan and Katie: are they laughing at me or with me?

After working on the Misty and Beaver lake-stream pairs, both located on northern Vancouver Island near Port McNeill, we drove south for a couple of hours to Robert’s Lake Resort near Campbell River. Here we were to continue our lake-stream work, starting with the Robert’s pair, and here we would be joined by our collaborators from the University of Texas at Austin, including team leader Dan Bolnick. On the night that everyone arrived, all of us (one-quarter of a hundred people!) gathered in a room for some discussion, introductions, and a pep talk from Dan. Dan went over safety and security issues, of course, but – more importantly – imparted to us his considerable wisdom regarding the local stickleback populations, especially that in Robert’s Lake itself where he had been working for 13 years. “I have never seen a stickleback breeding in Robert’s Lake before June 6” was the phrase I most remember – perhaps because the next morning I walked down to the dock at the lake and saw two breeding males. One of them had babies already, which meant that it must have started breeding at least a week (and perhaps two) earlier. This means that breeding must have started in Robert’s Lake more than three weeks before the previous earliest date. Now it was Dan’s turn to try to salvage his reputation as the local stickleback guru, and together we converged on the best way to do so – we started trading stories about how unpredictable things could be.

Dan: “It is amazing how some years the stickleback are small and other years they are large.”

Andrew: “Ah, yes indeed Dan, and how in some years they have incredible nuptial color and some years much less so.”

Dan: “Right you are Andrew, and some years they breed early and sometimes late.”

I am sure you can see here how we had cleverly shifted from our earlier statements of confidence in generalities to statements showing our rich knowledge of variation and exceptions, knowledge that could only be achieved through our long and detailed experience in these systems. Next year, and in those that follow, I will start from this new position and thus never be wrong again.

Dan's other project - the search for assortative mating in stickleback.

The entire crew only overlapped at Robert’s Lake for one day but we did have time for a farewell drink of Scotch (we now “own” a one square-foot plot of land at Laphroaig – and it even has a stream flowing through it) over which we could argue on topics from the trivial to the important. And argue we did, well past when we should have been in bed – but it was somehow appropriate as it was under a very similar situation in the same building and over the same beverage that Dan and I first met many years ago. Up to that point, we had both been working on stickleback in the same lakes for a number of years but hadn’t realized it. So we converged on Robert’s Lake in 2006, played a Hendry-lab verus Bolnick-lab Ultimate Game (I can’t remember who won but I do know that we asked for funding for an Ultimate trophy in our NSF grant.), and hatched several collaborations.

Robert's Lake Hendry v Bolnick ultimate tourney, 2006.

Sadly, field work is now over for me and I am writing this post in the Campbell River airport. But I can rest easy knowing that the field work will continue unabated without me, although I am not sure the tarps will be set so elegantly anymore. Matt will still be wading right to the top of his waders – and sometimes fearlessly beyond. Suzanna and Elena will still be tucking their jackets inside their waders and cooking amazing dinners. Katie will still be making hundreds of stickleback babies and organizing data by headlamp while in her sleeping bag. Rowan will still be the red canoe that every photo needs. Dieta will still be two steps ahead of everyone else. And Carol will be there to film it all. And –most importantly – large bags of nuts will still be three for five dollars at Sayward Junction. Have some for me!

Be the red canoe, Rowan.

24 of 25 - with a stand in for Duncan.

The Nature of Natural History: Kelowna CSEE 2013

Every few years a group of ecologists or evolutionary biologists experiences existential angst about the decline of natural history knowledge. This angst is wholly justified when many biologists no longer take the time to experience how the organisms they study actually live in nature. At best (and this is better than most), many biologists run off to the field for a day, stop at a bridge over a stream or along a forest trail, quickly collect their samples, and then run back to the lab to extract the DNA, run PCRs, and genotype their critters. Organism reduced to molecules. And yet we can’t possible hope to understand how organisms have evolved and how they fit into the polity of nature without careful observation and experimentation IN NATURE. After all, genotypes do not directly experience selection, nor do genotypes have ecological effects: instead it is phenotypes that experience selection and that have effects. And these phenotypes evolve and have effects through interactions with the environment that usually cannot be discerned without careful observation and study.

A five minute walk from the conference center.

This year, the Canadian Society for Ecology and Evolution held their annual meeting – organized by Jason Pither – in Kelowna, British Columbia. The overall theme was Range Margins in a Rapidly Changing World and I was in a symposium organized by Root Gorelick and Kevin Judge on – you guessed it – natural history. My own talk was about the role of photography as a way to bring readers and listeners a bit of a feel for the natural history of the systems under study. I told two stories through data and pictures. One story was about the interaction between bears and salmon and how the former drive evolu-tion in the latter.  The second story was about how humans are altering the evolution of Darwin’s finches in Galapagos.  I ended my talk by pointing out that, yes, photography was expensive but that anyone could set themselves up well from scratch for only about $3,000. The talk after me was about the role of illustration (as opposed to photography) toward the same goal. Lyn Baldwin pointed out that – in contrast to cameras – you can set yourself up well for illustration with a pencil costing less than a dollar. I don’t think that is really fair though as some pencils cost considerably more than a dollar.

The stories I told through data and photos.

The Natural History symposium was fascinating and yielded many curious tidbits about organisms that reminded me of the game I play with my kids at dinner “what did I learn that was new today.” (I did a similar post a few years ago based on a symposium in Leuven.) If I were home today, here is what I would tell my kids:

1. Many cactuses have a large and extravagant cephalium which – according to Root Gorelick – has no function and could well be maladaptive. Of course, I would then tell my impressionable kids that, no, Darwin was not wrong, instead Root must be, but that, yes, biologists still have no clear explanation of what benefit the cephalium brings.
2. Jumping spiders, those charismatic midgets with forward facing eyes that leap on their prey, have crazy mating colors and displays. I will also tell my kids how Wayne Maddison, when he was a kid in Ontario, discovered that two species found on sand dunes have incredibly different strategies for building their “nests.” Wayne told the audience that he feared that he would go to his grave before he published this observation and so I here pledge that, should this be so, my kids (one of whom loves spiders) will take up the study and published it (without mentioning Wayne of course).
3. Feather mites are tiny (often microscopic) mites that cling to the feathers of birds. Heather Proctor explained how these mites show an incredible diversity of forms - even on the same birds – and have a number of crazy features. Males apparently grapple with each other for access to females by trying to throw each other off the feather – just like tiny sumo wrestlers on a tight-rope. And some groups show handed-ness, with the individuals on one wing of the bird showing a different body coiling pattern than individuals on the other wing of the bird.
4. Like a number of other insects, male Mormon crickets give nuptial gifts to females – in this case, little “cheese balls” that the female munches on while the male mates with them. Cheese balls appear to be quite costly for the males to produce and they are an important part of the diet for females. This leads to so-called “sex role reversal,” where males become the limiting sex during mating and females compete intensely for males. When asked during the question period whether he had ever tasted these cheese balls, Darryl Gwynne admitted proudly that he had and that they weren’t actually that bad.
5. Hump-winged grig males, like Mormon crickets, provide a nuptial gift for females but not a yummy cheese ball. Rather, they offer up their wings for the females to munch on while mating. Kevin Judge showed an amazing video of grigs mating, with the female on the back of the male munching vigorously away at the male’s wings (and seemingly trying to get at other male parts too), while the male simultaneously tried to keep her wandering mouth under control with his legs while crimping her abdomen with a structure that looked like a small staple remover (and at least once it removed part of the female’s abdomen).

That is just a small selection of natural history tidbits from the symposium – my apologies for any inaccuracies which I am sure the above hyperlinks can clear up. After sitting through this great symposium, I happened to see Sally Otto, who had some binoculars around her neck. “Have you been bird watching” I cleverly asked, and she proceeded to tell me about a nearby lake with nesting Avocets and many other great birds. How could I not take my own advice, and that of everyone in the symposium? So I ran off to take some photos of the natural history of Kelowna. Amazing stuff. In just a few walks, I saw 45 different bird species, including one – the Pygmy Nuthatch – that I don’t think I have seen before. The conditions were great and I was able to get some good photos, which I show below (many more are here).

So that is it for CSEE 2013 – now I am off to Vancouver Island for field work on stickleback. After that, it is time to get geared up for CSEE 2014, which we are hosting in Montreal. It will be the first ever joint meeting of CSEE, the Canadian Society of Zoologists (CSZ), and the Society of Canadian Limnologists (SCL). The meeting title is “GENOMES TO/AUX BIOMES” and it is supported equally by the three societies and by four Montreal Universities (McGill, UQAM, Condordia, and Universite de Montreal) – we hope to see you there. Montreal has some natural history too!

Breeding Avocets.

The omnipresent chipmunk

A robber fly (thanks for the ID Bob).

Common Flicker - the red-shafted flavor.

The ever-cute California Quail

A Wilson's Phalarope takes flight.

Life after death: When does your phenotype expire?

Throughout an organisms’ life, the expression of genes, regulated by the biotic and abiotic environment, gives rise to traits that determine how fast it can run or how tall it can grow. Many traits also affect species interactions; for example, are you fast enough to outrun predators? Do you look tasty to herbivores? Most traits (e.g., running speed) cease to be important once an organism dies, but some traits linger and have “afterlife” effects on the environment. A prominent example of afterlife effects can be found in decomposing plant material, which is a crucial part of nutrient cycling. Microbes and fungi are critical to many stages of nutrient cycling, such as the mineralization of organic matter and the nitrification of NH4+, which plants cannot use, to NO3-, which is usable by plants. However, microbes and fungi can be “picky eaters” in a sense, as they prefer substrates with labile simple sugars instead of defensive molecules such as lignin. Simple sugars have carbon and nitrogen supplies that are easily accessible, while larger, more complex molecules require degradation by energetically-costly enzymes. Therefore, genetic and environmental influences on the chemical composition of plant material can persist after a plant sheds its leaves and affect how quickly its nutrients are cycled.

Afterlife effects aren't a new concept; exposure to herbivores and ozone has been shown to indirectly affect decomposition by altering leaf chemistry. However, we recently documented a new type of afterlife effect by showing that genotypic variation in a focal plant’s neighbors could affect the chemical composition of the focal plants litter. Although we don’t have the mechanism completely nailed down, it appears that focal-plant biomass allocation (putting carbon into roots vs. rhizomes vs. stems, and so on) is affected by neighbor-plant genotypic variation, and that shifts in focal-plant biomass allocation are correlated with focal-plant litter quality (specifically, lignin:N). This type of afterlife effect can also be considered an indirect genetic effect (technically, an interspecific indirect genetic effect because the neighboring plants belonged to different species), through which the expression of genes in one individual affects the phenotype of a different, heterospecific individual.

Solidago altissima, one of the study's focal species, along the TN-NC border.

We (Jen Schweitzer, Joe Bailey, and me) were curious whether genetically­-based afterlife effects were unique. Do they have consequences that, for example, ozone-driven afterlife effects would not? Ultimately, we started to think about ecosystem processes (productivity, nutrient cycling, among many others) and the basic drivers of these processes. We argue that ecosystem processes are the “gene-less products of genetic interactions”, meaning that the plant, animal, and microbial traits that interact to create ecosystem processes all have a genetic basis, although the expression of that genetic basis may change depending on how an organism’s genes interact with the biotic and abiotic environment. So, you may ask – “What does this mean?” We’d argue that the “ecosystem processes are gene-less products” perspective allows us to put ecosystems in an evolutionary framework. We can then ask questions like: How might nitrogen cycling or plant productivity change as natural selection acts on the genes that are the most basic drivers of these processes?

If you’re interested in the research behind this post, head to http://www.plosone.org/article/related/info%3Adoi%2F10.1371%2Fjournal.pone.0053718.

More Galapágos Adventures

This year I joined Team Pinzon for the first (and hopefully not the last) time – and so it is time to do my first Galápagos post on this blog. Previous expeditions (sadly, without me) have done a number of posts about our work, including Suskewiet as a new statistical method for comparing beak size and shape, a five day re-cap of a field season that included posts on blood sucking maggots, people sleeping on the job, and adventures in 3-D. It's hard to beat that, though I suppose I should mention parasites to skew Joost's statistics about them. Actually, this year we worked closely with another team from the University of Utah who are studying the ecological effects of the blood sucking maggot, Philornis downsi. Thus, I'm allowed to mention parasites in this post.  Cha-ching!

The Galápagos islands have much to offer in terms of data, but the first thing that one notices in the Galápagos are the unique animals and environment. These experiences figured heavily in my own blog on the adventures of field work in Galápagos – and I would like to recap just a few of them here.

I'll start off with a time series going from nest building to fledging. One of the best parts of being in the field for an extended period is that you get to follow ‘mother nature’ doing her thing. In this case, I got to watch the entire process of finches raising their babies, over the span of one month. It starts with nest building...

Many of the birds on the island make their nests in cacti, acacia trees, and other prickly plants. The finches make a spherical nest, and you can often find them gathering materials for their nests. I wonder how much beak shape and size affects nest building. We know it affects everything from foraging abilities to singing... perhaps it affects nests?

It's kind of like buying a home. Once you've got a home (and a partner), you can raise a family, starting with the juveniles...

Part of the project is to look at assortative mating – the extent to which finches mate with other finches that have beaks that are similar in shape to their own. There are two ways to do this. One is to band as many birds as possible, and then do focal observations on nests you find and figure out which finches are paired. The other way is to find a nest, and then try to sample the birds you find at the nest. Due to lack of time, we’re going with the second method for now. The coolest thing about this is finding nestlings in the bird nests!

Finch nestlings

Mockingbird nestlings and parent(s)

Finally, the juveniles are ready to leave the nest! Once the nestlings have developed their feathers to be able to fly, they become fledglings and can fly and leave the nest, but they are still dependent on their parents for food. Finches build their nests at all heights, and this particular fledgling was quite curious before it took off from the nest.

Finch fledgling

Some juvenile anis were grooming each other and generally behaving as siblings often do:

Our work is done on the island of Santa Cruz, where the Charles Darwin Research Station is located. There are several other volcanic islands in the Galápagos, a few of which I had the opportunity to visit. One spot I visited is Sierra Negra, on the island of Isabela. Sierra Negra is a caldera where the volcano collapsed onto itself after an eruption, similar to the famous Ngorongoro crater in Tanzania.

 On the rim of Sierra Negra

Bartolome Island is one of the younger islands in the archipelago, and offers a beautiful view. We spotted a juvenile Galapagos hawk there:

Two other famous islands are Wolf and Darwin. These islands rise up straight out of the sea, and you are not allowed to land and go onto the islands. However, as beautiful as the islands are above water, even more treasures lie beneath the water.... (psst, scroll down for photos of underwater critters)

To give you an idea of field work, here’s a post from my blog, talking about how we do field work on the islands:

It seemed the hobbitses did well enough yesterday morning to venture to Rohan, which is complete with an entrance gate and a statue to guard over the mist nets. 

Processing birds under the tarp

Father and son take a break from the intense morning heat

Joost checks out the GPS

The bird banding kit, which we couldn't find in Montreal (where it is normally stored). Banding an individual bird includes a unique silver band with an id number, and a unique colour band combination to identify individual birds from a distance

The statue is a Pegasus, but who says Tolkien and Greek Mythology can’t have a mash-up?

 Team Pinzon with the Pegasus

If Jacques Cousteau had lived before Charles Darwin... hmmmm. Some interesting late night discussions could have been had....

And lastly, if you made it down here, congratulations! Thank you for sharing my adventures with Team Pinzon this year, and I’ve got my fingers and toes crossed that I get to go again next year. Actually, my fingers are not crossed as I need to write some manuscripts. Hopefully, in the near future, one of those manuscripts will be on assortative mating in the medium ground finch. We know that there is a bimodal distribution of beak shape in a population of medium ground finch, and we hypothesize that assortative mating is one of the ways this bimodal distribution is maintained. However, we know there is temporal variation in their assortative mating, but we don’t know the extent or the potential sources of this temporal variation. Stay tuned for future work on this tantilizing project.

OK. My toes are cramping now. Uncrossing toes as well. Still hoping that I'm joining the team in future years...

Carnival of Evolution #59

Carnival of Evolution #59 is up!  Our contribution is Thomas Cameron's recent piece Of Mites and Men, about some fascinating experiments into harvest-induced selection.  Lots of other good stuff in there, check it out!

The theme this month is, somewhat bizarrely, Doctor Who.  It has nothing to do with evolution, but I'll leave you with a picture of Sarah Jane Smith, a companion of the 3rd and 4th Doctors, played by Elisabeth Sladen.  I watched Doctor Who more or less nonstop as a kid, and I had a terrible crush on Sarah Jane.