Monday, September 15, 2014

The ideal experiment...

[ This blog post is by Sinéad Collins; I am just putting it up.  –B. ]

In a previous blog post, Andrew outlined the “ideal approach” for investigating whether plasticity facilitates evolution, and to my delight, he proposed experimental evolution. Not only that, but he proposed the experiment my group got published this week in Proceedings B. I was pleased to be accused of doing anything ideal, much less an ideal experiment, even if Andrew doesn’t seem to remember me presenting this very data at the American Genetics Association Meeting.

When Elisa Schaum (the PhD student behind all this work) and I planned this experiment 3 years ago, our main concern was that it was, if anything, too obvious: in order to test whether plasticity facilitates evolution, take plastic and non-plastic populations, put them in new environments, and watch them evolve. Not so easy if you study elephants, but completely doable if you study microalgae (like we do).

To conduct our “ideal experiment” (do I like the sound of that too much?), we used plastic and non-plastic isolates of the small but mighty marine picoplankton Ostreococcus. Ostreococcus is exciting for many reasons, among them that it is the smallest known free-living eukaryote and yet manages to house a huge virus. However,  we chose it mostly because it is distributed over most of the world’s oceans, and we supposed that Ostreococcus from different locations would differ in how plastic they were in their response to CO2 enrichment (we were right, and we published this in Nature Climate Change). We used 16 different isolates of Ostreococcus from different locations.  We found that isolates from environments with more variable and less predictable CO2 levels showed the largest plastic response to changes in CO2, meaning that we had plastic and non-plastic (and intermediately plastic) genotypes of Ostreococcus.

Two TEM images of Ostreococcus. Photos: C.E. Schaum.

Then, we set up the evolution experiment. We let all of the genotypes evolve in 4 different environments. First, we used a control environment where CO2 levels were normal and stable. Second, we used a fluctuating environment, where mean CO2 levels were the same as the control, but they fluctuated around this mean every few generations – we hypothesized that this environment would select for plasticity, but not for adaptation to high CO2. Third, we used a stable high CO2 environment, where we could look at how the initial plasticity of the genotypes affected evolution in a new environment even if there was no further need for plasticity. Finally, we used a fluctuating high CO2 environment, where mean CO2 levels were high, but also fluctuated every few generations, to look at how plasticity affected evolution in a new environment when there was also selection for plasticity.  Then, we let everything evolve for a few hundred generations. We are now up to 1000 generations in the lab, but the paper was written before we reached this point of insanity.

Aaaannnnnd… plasticity facilitates evolution. Genotypes that were more plastic evolved more in high CO2 environments. Not only that, but populations in fluctuating high CO2 environments evolved more than populations in stable high CO2 environments. And to make matters even more exciting, populations evolved in fluctuating environments were more plastic than populations evolved in stable environments, no matter what the level of CO2. So, even when plasticity itself is selected for, populations evolving in response to an environmental change still evolve faster than populations dealing with that same environmental change who don’t have to bother with selection for plasticity. I may have done a happy dance when I saw that data.

Dr. Collins expressing her love for Osteococcus, post-results. Photo: Jane Charlesworth. [We tried to obtain a video of the good-data happy dance, but it was not available at press time. – The Management]

Of course, things are never that simple. The evolutionary response of Ostreoccocus to high CO2 can only be described as weird. I think this is because CO2 is food for many photosynthetic organisms, including Ostreococcus. So, when CO2 levels increase, Ostreococcus cells divide faster. This means that working with high CO2 here is at odds with the usual way of doing an evolution experiment with microbes, where researchers generally starve, poison, overheat, or do some other horrible thing to decrease microbial fitness substantially at the beginning of the experiment. However, we discovered that we were (eventually, and inadvertently) also guilty of torturing our microbes, as it turns out that a higher growth rate is all well and fine for a few generations for Ostreococcus, but after a while, dividing so quickly takes a toll, and the cells become less able to survive the slings and arrows of outrageous fortune (heat), have leaky mitochondria, and are bad at competing against other Ostreococcus. So, the evolutionary response to high CO2 in Ostreococcus – the response that results in cells that have normally-functioning mitochondria, can handle a bit of heat, and can overgrow other genotypes – is to grow more slowly. Basically, evolution reverses the plastic response to high CO2. Even though cells grow faster in the short term in high COenvironments, they slow back down again if given enough time to evolve. Most theory for evolutionary biology isn’t tested in enriched environments, so it took us a while (and quite a few cups of hot chocolate) to figure that out.

So yes, I would say that the experiment was ideal. It had everything: tiny protagonists (Ostreococcus), clear results (plasticity facilitates evolution!), weird and surprising twists in the clear data (evolving slower growth than your own ancestor!), and a happy dance (possibly two).

Sinéad Collins and Elisa Schaum
Institute of Evolutionary Biology, University of Edinburgh

Proceedings B paper:
Nature Climate Change paper:

Tuesday, September 9, 2014

MYScience: A newer faster cheaper easier BETTER open access journal

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  • Chuffed to say what you want how you want as long and as often as you want?
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If the answer to any of these questions is yes (or no), then we would like to encourage you to submit your paper to our new open access journal: MYScience.

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Wednesday, September 3, 2014

The Ghost of Plasticity Past, or Why Plasticity Inferences are too Plastic

Several months ago, I attended a meeting of the American Genetics Association organized by Robin Waples in Seattle, Washington. The theme for the meeting was “Evolution and Plasticity: Adaptive Responses by Species to Human-Mediated Changes to their Ecosystems.” The meeting was a particularly clear example to the current excitement about the role of plasticity (including epigenetics) in the evolutionary process – an enthusiasm that really crystalized around Mary Jane West-Eberhard’s “Developmental Plasticity and Evolution”. Much of the excitement centers around the idea that plasticity (a single genotype has different phenotypes in different environments) can promote evolutionary change. For instance, plasticity can provide the raw material necessary for evolutionary change by revealing otherwise cryptic variation. In addition, plasticity might generate immediate adaptive phenotypic shifts that allow individuals and populations to persist in new environments, thus allowing and promoting subsequent adaptation (without the initial adaptive plastic shift, the population would have gone extinct). This idea is not new, having originated with James Baldwin in 1896, but it has certainly become vastly more popular of late.

These (and other) ideas for how plasticity might promote evolution are certainly interesting, but how does one go about testing them? One of the things I found simultaneously most interesting and frustrating about the Seattle meeting was that seemingly any pattern in the data was being interpreted as evidence that plasticity promotes evolution. Perhaps most commonly, a finding that plastic responses to a particular environmental difference were in the same direction as evolved differences between populations evolving under the same environmental difference was interpreted as evidence that plasticity promoted evolution. For instance, guppies might shoal more in the laboratory when exposed to predator cues and guppy populations evolving with predators might shoal more than those evolving without predators (independent of proximate predator cues in the laboratory). On the exact opposite hand, however, evidence that plastic responses to a particular environmental condition were in the opposite direction as evolved differences was also interpreted (by other presenters) as evidence that plasticity promoted evolution. In this case, the idea is that the plasticity is likely maladaptive and so requires evolutionary compensation.

The current inferential scheme for whether or not plasticity promotes evolution
If either of two opposite patterns is interpreted as evidence for the same thing (i.e., plasticity promotes evolution, albeit in different ways), how do we proceed with rigorous hypothesis testing. Surely we also need a set of results that would be interpreted as evidence that plasticity does NOT promote evolution. That is, the hypothesis must also be clearly falsifiable through some particular outcome in the data. The lack of such a criterion reminds me of the classic criticism by Joseph Connell that competition was invoked when species have similar diets (because they obviously then use the same resources) and also when species have different diets (because past competition had presumably reduced diet overlap – the ghost of competition past).

In the past, when I pointed out to some ecologists that competition seemed of little importance as a mechanism determining a particular species' distribution, they often gave the following answer. The reason, they said, for my inability to find evidence for competition was because it had already been eliminated by past coevolutionary divergence between those species. However, for the reasons discussed in this paper, and until some strong evidence is obtained from field experiments along the lines suggested above, I will no longer be persuaded by such invoking of "the Ghost of Competition Past". (Connell 1980 – Oikos)

Although the Seattle meeting ended several months ago, I was just prompted to write a post about the topic owing to the recent publication in Nature of another study about the role of plasticity in evolution: “Developmental Plasticity and the Origin of Tetrapods.” Em Standen, Trina Du, and Hans Larsson wanted to test whether plasticity would promote major evolutionary transitions, especially the transition from swimming in water to walking on land. To test this possibility, they invoked a classic hypothesis test: if an ancestral species shows adaptive plasticity in response to an environmental shift, and that plasticity mirrors the evolutionary changes that accompanied the environmental shift, then plasticity likely promoted the transition. Specifically, they reasoned that rearing an air-breathing fish out of the water (by misting them regularly) would cause developmental changes in morphology that would lead those fish to be better walkers out of water. If so, the same thing may have taken place in the water-to-land transition. This is a cool idea – although, of course, plasticity in the ancestor is merely consistent with the hypothesis rather than proof of it.

The difficulty in any such study is that the actual ancestor (here the ancestor of land-dwelling tetrapods) is not accessible for study – and so Standen and colleagues needed an analog species. Coecocanths obviously wouldn’t work and lungfish are just too pathetic on land. So the authors chose to use another basal tetrapod – the Polypterus or “bichir.” Performing the experiment, they found that Polypterus raised out of water were indeed better at walking out of water than those raised in the water (see the cool video below) and showed developmental morphological changes that were similar to those in the fossil record associated with the move out of water.

This result is fascinating and I was privileged to see its implementation as the work was done in the lab of my close colleague Hans Larsson. In fact, I was able to talk to him about it multiple times on the train on the way to work. In addition to simply be jealous that I hadn’t thought of it first, I came to crystallize a particular criticism of the work. Specifically, I contend (if only as Devil’s Advocate) that the results could just as easily be interpreted as showing that developmental plasticity does NOT promote evolution. The reason is that Polypertus has never made the transition to land despite millions of years of opportunity to do so. Thus, all this wonderful plasticity did NOT accomplish the task it is inferred to assist.

Given all these flexibility in ad hoc interpretation, it seems to me that the field needs a critique and a careful (a la Connell) outline of the various patterns that might be observed in an experiment and what inferences they would and would not allow. Until such an endeavor is undertaken and adopted, inferences about plasticity are simply too plastic.

I wrote the above on the train a few seats away from Hans and, while then walking to work, we discussed what the optimal experiments would look like. We think that the ideal approach would be experimental evolution: have replicate plastic and non-plastic genotypes/populations, expose them to new conditions, and track their subsequent evolutionary trajectories. If the most plastic genotypes show the fastest and most dramatic evolution, then plasticity promotes evolution. If the least plastic genotypes show the fastest and most dramatic evolution, plasticity constrains evolution. If plastic and non-plastic genotypes don’t differ, plasticity does not influence evolution. Until then, I will no longer be persuaded by such invoking of "the Ghost of Plasticity Past".

Thursday, August 28, 2014

Carnival of Evolution #74

Well, it’s a couple of weeks late, but Carnival of Evolution #74 is now out.  Our contribution was Craig Benkman’s fascinating post about “A small mammal with an outsized impact”.  With more than 500 views already, it’s one of our most popular posts ever, and deservedly so.  So if you haven’t read it, check it out!  There are lots of other goodies in the carnival; I was very interested in the discussion of ring species by Jerry Coyne, for example.  Enjoy!

A ring species.

Saturday, August 16, 2014

The Divide: a survey about interactions between theoretical and empirical researchers

What is the proper role of theoretical versus empirical work in biology?  I self-identify as a theorist, and I do pretty much all of my work sitting at my Mac Pro.  However, I did my Ph.D. in Andrew Hendry’s lab, surrounded by empirical biologists working on stickleback, guppies, salmon, and other slimy real-world critters.  This was somewhat of an accident; initially, I was interested in doing an empirical Ph.D., but my past as a software engineer meant that I soon shifted into modeling.  (An early attempt at doing fieldwork on stickleback in British Columbia also convinced me that perhaps that was not my strongest suit.)  My position as the “token theorist” in the Hendry Lab worked out really well; I got a lot of exposure to empirical concerns and perspectives that informed my modeling work, both in what I chose to study and how I wrote about it.  At the same time, I provided a theoretical perspective that I hope was interesting and useful to the others in the lab.

This situation meant that I was often thinking about the way that theoretical and empirical approaches interact in ecology and evolutionary biology.  Should theoretical ideas drive new empirical work to look for the patterns and outcomes predicted by theoretical models?  Or should pure “natural history” observations of the real world drive new theoretical work to explain the patterns and outcomes observed?  Or is the ideal perhaps for the two perspectives to mutually drive each other, in a sort of ongoing feedback?  Do empiricists and theorists interact too little, too much, or just the right amount, in today’s world?  Which aspects of the interactions between these groups work, and which aspects are perhaps dysfunctional?  How do institutions such as journals, funding agencies, conferences, and universities influence (and perhaps hinder) such interactions?

My interest in such questions was whetted by discussions with Dan Bolnick, Andrew Hendry, Kiyoko Gotanda, Maria Servedio, and others too numerous to name, and the further along I got in my Ph.D., the more important these questions came to seem.  Some fascinating (and disturbing) papers came out on related topics, such as Fawcett & Higginson’s paper on the negative citation impact of equations in a paper, and Scheiner’s paper on the dearth of theoretical grounding in ecological research.  Eventually, I decided to conduct a survey of ecologists and evolutionary biologists to see what others thought about such questions.

And so that’s what I did, and the results of that survey are now published in BioScience.  I think the paper is quite accessible (it doesn’t contain a single equation!), so I won’t go into detail here about what I found.  In short, though, my results underscore three themes.  To quote from my abstract:

One theme is a widespread and mutual lack of trust, understanding, and interaction between empiricists and theorists. Another is a general desire, among almost all of the respondents, for greater understanding, more collaboration, and closer interactions between empirical and theoretical work. The final theme is that institutions, such as journals, funding agencies, and universities, are often seen as hindering such interactions. These results provide a clear mandate for institutional changes to improve interactions between theorists and empiricists in ecology and evolutionary biology.

That mention of a “clear mandate for institutional changes” in the last sentence is intended as a sort of clarion call, and although I didn’t devote much space in the article to my own personal opinions, this here is a blog post, so I will write a bit more frankly.

In the present institutional structure of science, attempts to collaborate and interact strongly across the theoretical–empirical divide generally go unrewarded; indeed, respondents to my survey often felt that such efforts were effectively punished, since such research is both harder to fund and harder to publish.  For this reason, it would be both unfair and unrealistic to ask individual researchers in the present climate to increase their interactions across the divide.  Instead, I think what we need are institutional reforms that provide incentives for greater interaction: funding programs specifically devoted to cross-divide research, editorial policies that encourage cross-divide publications, hiring policies in university biology departments that encourage the hiring of people with cross-divide publication records, and so forth.  Once the institutional incentives are in place, individual researchers will adjust their behavior; until then, individuals will continue to respond to the incentives as they presently exist.

So rather than suggesting that you ask “what can I, as an individual researcher, do to interact more across the divide?”, I suggest that you ask instead “What can I, as a faculty member, a journal editor, a manuscript reviewer, a conference organizer, a grant evaluator, a professor, a member of a professional society – a participant in creating the institutional structure of science – do to encourage everyone to interact more across the divide?”  And then please discuss this with others, and take action!


B.C. Haller.  (2014).  Theoretical and Empirical Perspectives in Ecology and Evolution: A survey.  BioScience (advance access).  DOI: 10.1093/biosci/biu131

Wednesday, August 13, 2014

Right beneath our feet: amazing nature in our backyards (Reign of Fire II?).

Our normal environs tend not to excite our scientific interest on a daily basis. They can instead become so familiar as to become boring and mundane – or just effectively invisible. We are instead more likely to be captivated and amazed when we go somewhere new – the Arctic, the Galapagos, the Amazon, the Negev Desert. On these trips, we tend to get excited about all sorts of critters, no matter how small or common. When visiting new countries, I find myself eagerly taking pictures of the most typical birds, birds that locals would never photograph, nor even notice, much as I treat a robin or starling or crow around my home.

Jumping spiders are awesome.
Yet our normal environs can become exciting and fresh again when we achieve a new perspective. Macro photography is a good example. Although I have long been interested in photography, I hadn’t spent much time on macro work until recently. Now, however, I often find myself at equestrian events and I need something to occupy myself and the kids in the hours between my wife’s performances. So the kids are tasked with running around in the bushes to find insects for me to photograph. Numerous times, I have been amazed by a cool new spider, mayfly, leaf hopper, lacewing, or any number of other spineless wonders. They were there all along, of course, right beneath my feet, but I simply hadn’t paid them much attention because I hadn’t previously been magnifying the world with a macro lens.

I only saw the parasites when I blew up this macro image of a lacewing.
A robber fly near my house
New perspectives can also be achieved by getting away from solid ground, such as going underwater or into the air. We recently bought my brother, Mike, a quadcopter on which he mounted his Go Pro to shot aerial footage of places we had seen countless times from the ground. We recently assembled a video aerial tour of the Wagner Natural Area, near Edmonton, Alberta, a site near our home that we had explored many times on foot or snowshoe or ski. Now, however, we were able to see patterns of diversity that were not apparent to us while walking on the ground – the trees no longer obscured the forest.

Mike and his quadcopter.
Or one can take a typical perspective and change its speed. Slow motion is a time shift we are used to from sports replays; but speeding things up, less so. I recently shot a time lapse video a sunset in Haida Gwaii, British Columbia. It shows the cool things a time lapse normally does, such as clouds zooming by – but then came a new insight: you can see very clearly the different layers of clouds going in different directions. I certainly already knew that winds go in different directions and different speeds at different altitudes, but here was the first time I could really SEE it so obviously. And, in my very first attempt to shoot a time lapse, I recorded of a wooly bear caterpillar building its cocoon. For the first time, I appreciated that they rip off their own hairs to form the basis for their cocoon.

New perspectives can also come just by chance through witnessing a rare event, like the time I watched an epic game of cat and mouse between a hawk and a squirrel in my backyard. The hawk would repeatedly swoop around the tree trying to get the squirrel on the opposite side only to fail when the squirrel dashed around again to the other side. The hawk eventually won the battle, but only when the squirrel tried to escape by dashing across a patch of lawn. As another example, barred owls are very conspicuous in many forests – to the point that they have become, if not common-place, at least not surprising. A few years ago, I was able to get very close to one in a tree by the side of a pond. I watched it for some time and eventually moved on, which was unfortunate because I was later told by someone else that it swooped down and caught a frog. (I went back and watched for hours but it didn’t happen again.)

Hawk 1. Squirrel 0.
The barred owl before he went fishing.
My brother, Mike, had a barred owl experience several times better. Seeing some owls low in the trees at a remote fishing camp in BC, he wondered if perhaps he could entice them to come down for proffered prey. The camp had a trap that produced five or so freshly-dead mice every day and so he started the process of training the owls to take them. It started with a rubber band attaching the mouse to the end of a fishing line, with the mouse then reeled in in a presumably tempting manner. After several attempts, the owls started swooping down upon the “fleeing” mice, grabbing them and flying off to feast on their perch. Eventually, they were able to get the owl to take mice right out of their hands. Mike made an awesome VIDEO of the experience.

Finally, a new perspective can result from a happenstance shift in the environment that exposes something previously hidden. Just imagine all of the fossils beneath our feet that we will never see unless a rockslide occurs, we dig a new septic tank, or a stream floods and cuts into the bank. The proof is in those numerous construction projects or mines that have uncovered cool new fossils or amazing archeological sites (or those dragons in the movie Reign of Fire). Closer to home, every time they disc the soil in our family vineyard in California, they turn up a slew of obsidian arrowheads that generates a family competition to find the best pieces.

Just last week, Mike, the kids, and I were visiting my mother in Edmonton, where we were helping her move from her home of 30 years into a condo. On the very last day we were all together (we won’t be back before Mom moves out), we were taking the quadcopter for some aerial shots when we crossed a creek we had crossed thousands of times before. Mike, looking down, noticed a bone and sent the kids after it. Upon retrieval, it was clearly a very old bone that had been buried in the ground and recently exposed by high creek flows. Old bones found in the forest are always fun but hardly novel, and so we set it aside and continued on our way.

The site of the find.
On the way back from filming, Mike hopped down into the creek and almost immediately found a piece of skull that seemed to be from the same animal as the leg bone. A bit further along, he found another skull fragment with the bony base of a horn attached – a bison. Now it was time to get excited: bison hadn’t populated this area for at least 140 years.

Bison and moose bones
Then the mad hunt began. Mike and the kids found another 15 or so bones right away – of all shapes and sizes and types. Then, the next day after Mike left, the kids went off to find more. They took a walkie talkie and had great fun reporting their finds back to me as I was working on the house. At one point they had so many bones that they had filled their pail and so called me to come and replace the bucket so they would have room for more bones. And, then, of course, I had to take my own turn through the creek, finding a few more bones in places kids wouldn’t normally look. By the end, we had quite a pile of bones, which were certainly from a number of bison (and a few moose).

Grandma and the kids show off their find.
Now we need to solve the puzzle. The previous day we visited a friend to look at mammoth bones that had been collected in the Arctic. Now we immediately began hoping we were looking Pleistocene bison, which were larger than modern bison. However, comparison to various skull images online suggested the latter; but why so many in this one place? Our neighbour, a taxidermist who had worked for the Royal Alberta Museum, came over to look and told us that he too had found bison bones when digging a new pond. He suggested they might be 300 to 600 years old and were from a boggy area in which plains bison not used to soggy conditions had become mired. It is a good hypothesis and now we aim to test it, starting by dating some teeth we brought back to Montreal. These discoveries and questions and projects have brought a completely new perspective on our childhood home that was revealed to us out of the blue on the very last day we were all there together.

Big bison bones
Many amazing things are just beneath our feet right in our own backyards, awaiting only a new perspective. Sometimes we need to actively engage that perspective with an underwater camera or a quadcopter or a microscope or a fishing rod and a mouse. Sometimes we merely need to wait for the right moment when new conditions expose previously invisible phenomena (those bones were there the whole time!). Other times (indeed, all times), we have to keep our eyes open for when rare events finally happen (when that owl dives for that frog). Natural history, ecology, evolution, and biodiversity are just as fascinating at home as they are in the Antarctic or the tropics, sometimes we just have to shift our perspective to see it.

Quite literally beneath our feet - under the flagging stones near the fire pit.

Wednesday, August 6, 2014

Standing and flowing

Our paper on "The genomic signature of parallel adaptation from shared genetic variation" is finally out in print. Check out the funky cover they used.

The paper is also subject of a News and Views by John Welch and Chris Jiggins:

Here is the paper:

Here is the original blog post:

Tuesday, July 29, 2014

It’s all about the variance: science and life at N > 2

Variation is the grist for, and the flour from, the evolutionary mill. Without variation, no evolution occurs. With variation, evolution can generate even more variation by causing organisms in different environments to evolve different traits. We all know this, and we proceed accordingly in our research; but perhaps we too often take it for granted. Only sometimes are we smacked in the face by variation in such a way that it makes us pause and re-evaluate the way we view the world. Well, variation smacked me upside the head a few weeks ago during a trip into the field. In so doing, it made me reflect on how we estimate and interpret variance – and how this flavors the way we view our research and our daily experiences.

Threespine stickleback (Gasterosteus aculeatus)
Threespine stickleback could be the world’s most variable vertebrate. In some populations, average size at maturity is less than 30 mm – in others it is greater than 85 mm. In some populations, the pelvis is a huge structure – in others it is completely lacking. In some populations, the side of the fish is almost completely covered with bony plates – in others plates are entirely absent.  In some populations, mature males are almost entirely black – in others they have massive amounts of red – and in others black and red can be minimal. In some populations, the head is huge and the mouth massive – in others they are very small. In some populations, mean egg size (dry mass) is less than 0.047 mg – in others it is greater than 0.089 mg. This is just a small set of examples: stickleback, even just in freshwater, vary dramatically both within and among populations in almost any trait one cares to measure. This is why they are such a spectacular model system for studying adaptation.

A representation of stickleback diversity. The marine ancestor is surrounded by various freshwater forms.
Tom Reimchen, a professor at the University of Victoria, has long maintained that variation in stickleback on Haida Gwaii, a modest-sized archipelago off the coast of northern British Columbia, Canada, are as variable as are stickleback across the rest of their massive range in the northern hemisphere. Ever the skeptic, I have – when reviewing or editing Tom’s papers – pointed out that this assertion isn’t strictly true as (slightly) smaller stickleback are found in North Uist, Scotland. I am sure my nit was annoying to Tom as it was just a technicality and it required him inserting some rather pointless qualifiers into a few of his papers.

Several weeks ago, I had the opportunity to visit Tom in the field to see Haida Gwaii stickleback for myself. The first lake we visited was Drizzle, where Tom lived for 15 years and worked for 40. Drizzle is a modest-sized (112 ha) and heavily-stained (tannic, the color of very strong tea) lake with large and dark stickleback. A highlight here (besides camping and having a breakfast of bannock beside the lake) was walking the shoreline on Tom’s annual survey of loon-induced stickleback mortality. Several species of loon, particularly common and red-throated loons, congregate on Haida Gwaii lakes like Drizzle in numbers I had not thought possible, despite visiting countless lakes in my life. On Drizzle, dozens of loons would cruise nearby checking us out during our survey. And they would capture stickleback as if on cue – probably dozens were dispatched as we watched. Not surprisingly, many of the stickleback we found on the shore had been captured and killed, but not eaten, by loons. (Of course, many others are eaten - but we obviously can't find those on the shore.) Tom has an effective strategy for motivating search efforts. The person in front gets one point for every dead stickleback found. The following person gets two points. The third person gets three points. Tom was first, then Hannah, then me. Although it was like following two vacuum cleaners – I named one Hoover and the other Roomba – I held my own as tail-end Charlie (on points anyway).

Tom's cabin at Drizzle Lake (the lab is the wing at left).
A common loon with a Drizzle Lake stickleback.
The next lake we visited was Mayer, where Ric Moodie had – before I was born – discovered and described what is probably the world’s largest freshwater stickleback. This lake is larger (627 ha) than Drizzle, also quite stained, and even more overrun by loons. I had the good fortune, the day before meeting Tom, to happen by Mayer Lake just as it had stopped raining, in perfect time to cook my breakfast while watching 33 loons swim back and forth in front of me. Our next planned stop was Boulton Lake, in which more than half of the stickleback completely lack a pelvis, but this plan was derailed by happenstance. It seems that some delinquent and potentially dangerous kids had run off into the woods around Boulton Lake, and police parked along the highway nearby strongly discouraged us from going in.

So we instead hiked into Rouge Lake. This lake is a very shallow and small (1.5 ha) lake in the middle of a bog near the northern end of Graham Island (Drizzle and Mayer are on this same island). Rouge Lake stickleback are exceptional in several respects, especially their frequent lack of one of their dorsal spines, their (until recently) extreme red colour, their occasional possession of two dorsal fins, and the complete fixation of an otherwise locally-rare genetic variant (the Japanese clade of mitochondrial DNA). It was on the way back from this lake, tramping my way through bog behind Tom and three students, that variance smacked me upside the head. Just walking to these few lakes and hearing about (and seeing some of) their stickleback had finally brought home Tom’s assertions about the exceptional variation on Haida Gwaii and, more generally, the exceptional variation that organisms can achieve on very small spatial scales.

The Abbey Road of stickleback biology – the Rouge Lake trip. (Note: the picture is inverted for a reason that should be obvious.)
Along with this abrupt realization came a more fundamental epiphany: why had I been really impressed by the variance only after the third lake (not counting our aborted attempt to visit Boulton)? All of a sudden, I was struck by the parallel that, in statistics, we require a minimum sample size of three to get our first proper (albeit still weak) estimate of variance. The reason is that we need at least N = 2 to estimate a mean, and estimating a variance requires first estimating the mean and then needing at least one more data point. This makes sense statistically, of course, but – walking back from Rouge Lake – I began to wonder if our brains work the same way. That is, we really have to experience three things before we begin to get some mental perspective on how much they vary – because we need to consider the possibility of outliers. That is, with N = 3, we can see if any of the points stick out particularly far with respect to the mean – something that is impossible with N = 2 because in that case each point is equally distant from the mean. Stated another way, a sense of how variable things are first requires us to get a sense of the “average” or “typical” value and then a distribution of values around this average, which requires at least N = 3. Perhaps statistical principles match our mental processing machinery.

Now I can hear you saying: “Sheesh, N = 3 is way too low for a proper variance estimate.” You are, of course, correct. My point is simply that an assessment of variation, both statistically and mentally, can only begin at N = 3. Getting this third data point (visiting that third site) is the first moment when one has the potential to be impressed by that variation. Following that, much more data needs to be collected (many more sites experienced) to get a real estimate/understanding of the variance, but N = 3 is the first time you might be inspired by experience to try further. Hmmm, in writing this, I am reminded that I have only two kids. “Sweetheart, I’ve been thinking …”


Some other cool Haida Gwaii experiences:

More Haida Gwaii photos:

Eagles were everywhere.
Bleeding tooth fungus - how cool is that?
Sandhill crane in the rain.
Drizzle Lake
Native tree frog.
Masset, Haida Gwaii.
River otters in a tiny rainforest stream.
Sandpiper squadron.

Thursday, July 24, 2014

Evolutionary costs, ecological currency, and baby fish

[ This post is by Darren Johnson; I am just putting it up. –B. ]

I’m just going to say it – I like cute, baby fish. As a longtime SCUBA diver, I’ve spent countless hours on reefs throughout the world, and one of my true delights is noting the arrival of baby fish. Yes, they are often adorable, but one of the most fascinating things is that sometimes there are giant schools of baby fish, and other times there are few, if any, to be seen.  The future population of adults depends on these babies, yet the replenishment of populations by new babies (a process referred to as recruitment) is notoriously variable.  In fact, it is so variable that this phenomenon has a name.

For decades, fisheries scientists used the term “recruitment problem” to describe both the challenges of understanding why recruitment varies, and the difficulty of predicting adult numbers from the abundance of earlier stages such as eggs or larvae. Relationships between the numbers of young fish and the numbers of adults that those young fish eventually become have been studied for many, many species. Of course, abundance of young matters, but a common conclusion reached by such studies is that we need to know more than just numbers to understand recruitment variability with any degree of accuracy.

You’re prettier when you’re younger… Dascyllus albisella on small patches of coral in Hawai’i. Photo credit: D. Johnson.

One reason it’s so difficult to predict recruitment is that most fish species produce huge numbers of offspring (egg numbers in the millions are not uncommon), and only a few survive to adulthood. So despite the big-eyed optimism of those cute baby fish, the average outlook is grim. As if that weren’t enough, life for baby fish is exceedingly unfair. It is well known that individual fish with certain phenotypes fare better than others. For example, large babies seem to survive much better than their smaller counterparts. Similarly, faster-growing fish often survive better too. Even when such advantages are small, they are important. For populations that typically start out in the millions, even slight variations in survival rates can result in order-of-magnitude differences in the population of adults.

Times of plenty: a school of blackfin chromis (Chromis vanderbilti) hover above a Hawaiian reef.  There’s also a yellow tang (Zebrasoma flavescens) in there. Photo credit: D. Johnson.

Although unfair for baby fish, these links between phenotypes and relative survival might offer some insight into recruitment variability. With this in mind, our recent study examined recruitment from an eco-evolutionary perspective. We wanted to know the extent to which phenotype-mediated differences in individual survival probabilities added up to affect the dynamics of whole populations. In other words, there appears to be an evolutionary cost associated with individuals having an inferior phenotype. We wanted to take these evolutionary costs (measures of selection) and convert them to ecological currency (estimates of average survival within populations). To address this question, we gathered all the studies that we could find that repeatedly measured relationships between phenotypes and relative survival of fish. We then analyzed these selection measurements in combination with observed variation in the distributions of phenotypes.

We found that most of the mortality experienced by populations of larval and juvenile fishes is selective mortality. That is, most mortality is related to variation in phenotypes such as body size, growth, etc.  In addition, the amount of selective mortality varied widely among different cohorts of the same species (e.g., different groups of fish that arrived to the reef at different times). Together, these results suggest that variation in selective mortality, rather than non-selective mortality, is the biggest source of recruitment variability.  Taking these results a step forward, it suggests that if the relationship between phenotype and survival is relatively consistent, then understanding how phenotypic variation interacts with selection might hold the key to understanding recruitment variability.

Tagging fish to measure how phenotype affects relative survival.  A juvenile bicolor damselfish (Stegastes partitus) in the Bahamas gets a tattoo.  Photo credit: Nikita Schiel-Rolle.

Toward this goal, we provide a conceptual and mathematical framework for analyzing fitness surfaces – functions that relate phenotypic value to relative survival across a broad range of phenotypes. The framework can accommodate cases in which fitness depends on multiple traits, and cases in which fitness depends on population density. We illustrate that fitness surfaces can be relatively constant, and that interactions between phenotypic variability and fitness surfaces can vastly increase our ability to explain recruitment variability.

The relationship between selection gradients and mean phenotypes can be used to reconstruct the fitness surface (solid curve in lower panel). Groups of fish whose phenotype distributions show little overlap with the fitness surface (e.g., group 1) have low rates of overall survival (and more intense selection), whereas groups with greater overlap (group 8) have greater survival (and less intense selection).

Beyond fish and recruitment, our study suggests that in many ecological scenarios (though certainly not all of them), fitness surfaces might be reasonably constant. Our study also suggests that fitness surfaces are often nonlinear, which might result in complex relationships among phenotype distributions, selection, and average fitness. For example, in some cases variation in phenotypes has a larger effect on average survival than mean phenotype does.  Understanding (and properly estimating) fitness surfaces will be critical to understanding how variation in phenotypes ultimately drives variation in the dynamics of populations.


Johnson, D.W., Grorud-Colvert, K., Sponaugle, S. and Semmens, B.X. (2014). Phenotypic variation and selective mortality as major drivers of recruitment variability in fishes. Ecology Letters 17(6), 743–755. DOI: 10.1111/ele.12273

Friday, July 18, 2014

Passport required to reproduce: Local adaptation persists despite frequent dispersal

[ This post is by Daniel Peterson; I am just putting it up.  –B. ]

Alaska contains roughly half of the wilderness in the United States. That’s over 230,000 square kilometers of pristine habitat – a place where ecosystem processes disrupted almost everywhere else can be observed in a natural state. Of course, that also means a large proportion of the state isn’t accessible by road, a fact I could barely comprehend as a brand-new grad student stepping off a plane from the East Coast. I soon found myself getting used to travelling exclusively by boat, keeping an eye peeled for bears and moose, and tying a decent bowline (that last trick learned only after the shameful loss of a Secchi disk to the deep). What I’ll never get used to is the thing that brought me there in the first place: gravelly streams full of bright red, desperately spawning salmon.

Little Togiak Lake, Wood-Tikchik State Park, Alaska.

The Alaska Salmon Program at the University of Washington has been doing research in the Bristol Bay region since 1946, well before Alaska became a state. One major focus of our work has been understanding the ecological effects of habitat diversity on Alaskan salmon stocks, now one of the world’s best examples of a productive and sustainable fishery. Hilborn et al. 2003 showed that the Bristol Bay sockeye salmon (Oncorhynchus nerka) are relatively stable in abundance and resilient to shifts in climate conditions because they are not one gigantic, panmictic population, but instead a metapopulation of independent breeding aggregations adapted to unique spawning habitat types (streams, rivers, and lake beaches). But how do these populations that are adapted to different habitats interact with each other on an evolutionary time scale? Are they on the road to speciation or does gene flow limit their divergence and possibly their adaptation to local conditions?

Despite the famous ability of pacific salmon to home to their natal spawning grounds after years in the ocean, dispersal rates among nearby populations have been measured to be 2–10%, potentially high enough to swamp the effects of ecologically divergent selection. However, even in the presence of considerable dispersal, gene flow may be limited if dispersers have low reproductive success in already-occupied habitats. Where local adaptation has arisen, dispersers between populations occupying distinct habitat types might be maladapted to their new habitat compared to philopatric (non-dispersing) individuals and dispersers between similar habitats, reducing gene flow and reinforcing local adaptation.

We set out to empirically assess the effect of local adaptation on the reproductive success of dispersers between beach- and stream-adapted populations. Beach-spawning fish, especially males, tend to be large and deep-bodied, while stream-spawning fish are more slender. Differences between these ecotypes have also been observed in other ecologically important traits such as egg size and migration timing. In order to isolate the fitness effects of local adaptation from those of dispersal itself, we compared the reproductive success of dispersers between populations that shared the same spawning habitat type with dispersers between ecologically distinct spawning habitat types.

Male and female sockeye salmon from the stream-spawning ecotype (above) and the beach-spawning ecotype (below). Photos: Tom Quinn.

To get direct measurements of individual dispersal and reproduction, we conducted exhaustive sampling of adults in two stream-spawning populations (A and C Creeks) every year from 2004 through 2010. We walked the full length of both streams every day during the spawning season (late July through late August), tagging any newly observed fish with unique IDs and noting the location of each previously tagged fish. We observed and fin-clipped a total of 4473 individuals in A Creek and C Creek in 2004 and 2005 (the parent years) and 2008, 2009, and 2010 (the years their offspring returned), plus 166 individuals that settled on the beach habitat in 2004 and 2005 (as a genetic baseline with which to identify dispersers from the beach to the streams). In the two parent years, 12% of sampled fish were immigrants (fish genetically assigned to a population other than the one in which they were sampled). C Creek had more immigrants from the other stream as well as from the beach than A Creek, but there was no clear sex bias in dispersing individuals. The number of individuals immigrating to the streams from the beach-spawning populations (N=108) was greater than the number of dispersers between stream-spawning populations (N=85).

Surveying C Creek. Photo: Jocelyn Lin.

Using pedigree reconstruction to calculate the number of returning adult offspring produced by each individual in the parental generation, we compared the lifetime reproductive success of all philopatric fish, dispersers between streams, and dispersers from adjacent lake beaches to the streams. We found that the reproductive success of dispersers between the two stream-adapted populations did not differ significantly from that of philopatric individuals, but immigrants from the beach population had significantly lower mean reproductive success than both philopatric fish and immigrants from the other stream. On average, beach-to-stream dispersers produced about one fewer offspring than between-stream dispersers, a reduction in fitness equivalent to almost half of the average reproductive success.

We don’t know the mechanistic reasons why dispersers from the beach produced fewer offspring. Morphological maladaptation to the stream environment could have limited the reproductive success of beach-adapted immigrants by reducing adult lifespan during the spawning period through selective bear predation or stranding in shallow water. Previous studies have shown that the abundant brown and black bears preferentially kill larger salmon (thereby selecting against them), but we found that dispersers from the beach were less likely to be found dead after being killed by bears and more likely to disappear without a trace. Recent PIT tagging work by Bentley et al. has shown that stream-spawning sockeye salmon show a wide variety of movement strategies, with many fish moving between stream and lake on a daily basis. It may be that the mere presence of bears indirectly affects the reproductive success of large-bodied dispersers by eliciting predator avoidance behavior and thereby limiting reproductive opportunity. Alternatively, reduced physical access to shallower areas of the stream could limit access to mates and spawning sites, encouraging the departure of larger individuals. Either way, adaptive behavioral differences between ecotypes may influence the conversion of dispersal into gene flow.

Spawning in the stream. Photo: Allan Hicks.

We usually expect that genetic differentiation, adaptive or otherwise, will only develop when diverging populations are insulated from gene flow by barriers to dispersal (either intrinsic or extrinsic). In our study, beach-to-stream dispersers were more prevalent than between-stream dispersers, suggesting that barriers to dispersal between habitat types are not strong in this system. The high fitness cost to dispersers that move between habitats might therefore be crucial to the maintenance of these morphologically and genetically recognizable stream- and beach-spawning ecotypes.

In the long term, we might expect that when dispersers have low reproductive success, selection will drive the evolution of intrinsic barriers to dispersal. However, additional factors might select against such barriers. For example, in dynamic metapopulations, rare subpopulation recolonization events might substantially bolster the long-term fitness of dispersal alleles even if dispersers have limited reproductive success in occupied subpopulations. Moreover, flexible behavior patterns in systems that allow for reversal of dispersal decisions could minimize the fitness cost of dispersal in unfavorable conditions. Thus, in many metapopulations, reduced immigrant reproductive success might be more important than barriers to dispersal for the maintenance of intraspecific biodiversity.


Peterson DA, Hilborn R, & Hauser L (2014). Local adaptation limits lifetime reproductive success of dispersers in a wild salmon metapopulation. Nature Communications, 5.  DOI:10.1038/ncomms4696