To swim, or not to swim?
That was the question
Whether ’twas Nobler for the Fish to suffer
The Slings and Arrows of outrageous Current
Or to take Flight against a Stream of Turbulence,
And by opposing end them: to rest, to swim
No more: and by drifting, I say we end
The energetic expenditure and the thousand Natural selections
That Fish are heir to? ’Tis a consummation
Desired by some fish.
– with apologies to William Shakespeare
It was summer 2007 and my graduate student Will Stutz and I had been setting up a large experiment in Blackwater Lake on northern Vancouver Island. For two weeks we (and multiple assistants) had been building large (10 m2) cages – 30 of them, installing them in the littoral zone, and stocking them with stickleback, trout, and sculpin. The goal was to test whether interspecific interactions altered patterns of individual and between-individual niche breadth in stickleback (answer: yes; Bolnick et al 2010). We had wrapped up the construction, and found ourselves with a rare opportunity: a few hours of uncommitted time. Living in Austin, but having a field site on Vancouver Island, I tend to push my crew pretty hard to exploit our limited field time to the fullest, which means little recreation.
Do we head back to the cabin, or go start sampling elsewhere for our secondary project? Or, go exploring? To paddle, or not to paddle? On the spur of the moment we pushed off in my lab’s bulky red canoe, and set a course for the far end of the lake, where I had never been. Blackwater Lake is long and thin, and we had been doing experiments in its north end for a couple of years. The north end is easily accessed from a logging road, and the littoral zone is mercifully free from big underwater tree trunks, the bane of cage-builders like myself. The paddle was pleasant – the weather was perfect, cool and sunny. We passed a pair of loons, but no people; I’ve only once spotted a stranger on this lake (more on him, later).
Will and I pulled up at the far end of the lake, maybe half an hour later. The south end of Blackwater is beautiful and undisturbed, so we climbed out onto a marshy spit of land (a floating mat of vegetation, really) to look around. We found ourselves next to a fast-flowing stream that drained directly into the lake at a fairly high velocity. It was about waist-deep, cold, with a firm sandy substrate and a stiff current that carved a 2-meter-wide channel into the marshy banks covered with muskeg (Fig. 1). We explored upstream a little; it was a nice uniform channel until we hit a beaver dam at 70 meters upstream, above which the ground became still wetter and the stream was slow but still visibly flowing. There were stickleback everywhere in the stream, in both the fast channel and above the beaver dam (See videos of stickleback swimming in a moderate-current stream here: https://youtu.be/2wttxQGhuv4 and here https://youtu.be/nHZh1V7xCSc).
Figure 1. Blackwater inlet stream. Note the pale sandy substrate.
We stood around, enjoying the sunlight, and speculated about this remarkably abrupt lake-stream interface. Until then, I had focused exclusively on lake stickleback, partly out of habit and partly to avoid stepping on the toes of Andrew Hendry, who I knew was studying lake–stream stickleback in this area. Andrew and I had talked about lake–stream stickleback a bit the year before when his crew crashed on my cabin’s floor for a week, providing a bottle of excellent Scotch in payment. I recalled expressing some skeptical curiosity about one of his results, in which he described a very abrupt transition (across tens of meters) in fish morphology when moving from an inlet stream into a lake. I thought that the spatial scale in question was bizarrely small – surely migration from the lake into the stream, and vice versa, should erode divergence at that scale. Unless… unless the fish themselves avoided switching habitats. Andrew and I had talked about the possibility of divergent habitat preferences accentuating the lake–stream divergence, but he seemed relatively uninterested. So perhaps that was an opening for me to foray into lake–stream stickleback without stepping on toes.
Recalling that conversation, with the Blackwater inlet at my feet, I took stock of the scene: I could see stickleback swimming in the still shallows of the lake, on my right, a few meters away. A few meters to my left, I could see stickleback swimming in a rapid current (Fig. 2). Did these fish care about that difference in water flow, and if so would they sort themselves into their preferred habitat? If there was habitat preference, perhaps we could see phenotypic, maybe even genetic, divergence arise not by mortality or differences in fecundity, but by non-random spatial sorting of individuals. Could adaptation proceed by choice, rather than by force?
Figure 2. Blackwater inlet stream (foreground) and the lake (on the far side of the muddy flat peninsula. Fish caught in the foreground are significantly different, morphologically, from the fish on the far side just 5 meters away. At the top left end of the stream, just before it enters the lake, you can see ripples due to a strong current, and you can see eddies in the stream in the mid-ground if you look closely.
Soon after, I paddled back to the inlet with Will Stutz, On Lee Lau, Travis Ingram, and Lisa Snowberg. We trapped in the lake and stream, marked fish with elastomer dye, and released them right where the stream entered the lake (Fig. 3). More exactly, we released them just inside the stream channel so that they had an equal arc of up- and down-stream options. We had fun sitting in the sun marking fish and talking, until we had our first and only visitor on the lake: a guy in his 70’s paddling an open top kayak, with a huge white beard but otherwise buck naked. He pulled up to the shore where we were marking fish, got out of his boat and asked, with genuine curiosity, about what we were up to. He was very chatty, and stayed talking with us for quite some time. He offered to help, while some of my students squirmed.
Figure 3. (Figure 1 from Bolnick et al 2009 Evolution) showing the mark-displace-recapture experiment layout.
Returning four days later, we retrapped. Now, I expected to find that lake-native fish went downstream to the lake, and stream-native fish went back up into the stream. But I didn’t expect this: 90% of the fish had returned ‘home’ in only 4 days (Fig. 4). As an aside: would all of them go home eventually? How long does this take? Is this a breeding-season phenomenon, or year-round? This habitat fidelity was observed for both the lake fish, who drifted downstream 1 meter into the lake, and also for the stream fish who disproportionately worked their way up-river (as far as 150 meters, many crossing up past the decrepit beaver dam). We were thrilled, and had the stats and figures and half the paper planned out before the end of the day (Bolnick et al 2009). But the coolest bit had to wait months, until an undergraduate (Claire Patenia) measured morphology of our recaptures. We realized that the 10% who switched habitats were morphologically predisposed to do so: lake-like stream natives, and stream-like lake natives. And, the transition from lake- to stream-phenotypes is so abrupt that one can move a mere 5 meters from the lake upstream and get significantly different phenotypes and microsatellite allele frequencies (Fig. 5). This is 1/8th the median distance that our released fish swam in just four days.
Figure 4. (Figure 2 from Bolnick et al 2009) showing the relative frequencies with which lake and stream natives were recaptured in lake or stream habitats, four days after release.
Since that initial study, I’ve become a bit obsessed with the notion of genotype- and phenotype-dependent dispersal, and the potential for biased gene flow to actually aid rather than inhibit adaptive divergence on small spatial scales (Edelaar and Bolnick 2012, Bolnick and Otto 2013, Richardson et al 2014). The vast majority of population genetic theory presumes that gene flow picks a random sample of alleles from one population, and drops them into a recipient population. Sure, there may be stochastic drift during that sampling process, but in this model gene flow is a homogenizing force, not an adaptive one. That changes when certain alleles are more or less likely to move. Depending on the nature of this bias, non-random dispersal can accelerate and exaggerate adaptation, or it can drive maladaptation (Bolnick and Otto, 2013).
Figure 5. (Figure 1 from Bolnick & Otto 2012) showing phenotypic divergence between Blackwater Lake and inlet stream stickleback over a small spatial scale.
There’s been something nagging me for a while, however. Although it was satisfying to find evidence for non-random movement of lake and stream stickleback, I still didn’t know why that happened. Something to do with body shape, it seemed, but what? Over a few months, my graduate student Yuexin (‘Kelsey’) Jiang and I developed a hypothesis that stream fish might exhibit ‘positive rheotaxis’ – a tendency to swim up a current, whereas lake fish might exhibit ‘negative rheotaxis’ – swimming down-current. Where a stream flowed into a lake, this divergent rheotactic response would tend to sort stream fish into the stream, and lake fish into the lake.
To test this idea, Kelsey designed a very nice circular flow tank that allowed stickleback unlimited opportunities to move up- or down-current. She then tested for rheotactic response of lake and stream stickleback (from our original Blackwater Lake study site). For a great video of lake and stream fish side-by-side, see https://youtu.be/7Uwq_sLu4Jk (challenge: guess which is the lake and which is the stream fish group). This video also shows the layout of the circular flow tank. In a paper that just came out recently (Jiang, Peichel, and Bolnick 2015 Evolution), Kelsey’s results provided a nice mix of expected and surprising insights.
Figure 6. Net displacement was the net movement of individual fish up (+) or down (-) current in the flow tank (see https://youtu.be/7Uwq_sLu4Jk for a video example). This was measured for wild-caught lake and stream fish from both the inlet and outlet of Blackwater lake. Lab-reared fish are not shown here, but are discussed in the paper.
First, the expected: inlet stream fish did a better job of staying put in current. They were displaced an average of 5 m downstream in the experiment, compared to 12–17 meters for lake fish and outlet stream fish (Fig. 6). Strictly speaking, the inlet stream fish showed less negative rheotaxis than the others. But, this should help them remain stationary despite flowing water, keeping them in their stream habitat. Note that in the absence of a current, there were no differences between ecotypes and no net displacement.
We also expected that not all stream fish are equivalent: inlet stream fish need positive rheotaxis to remain in their home habitat; outlet stream fish need to stay in place or go down-current to remain in their stream. So, the ‘positive rheotaxis’ of stream fish is only true for inlet streams. Which makes sense: in an outlet stream, positive rheotaxis brings you into the lake.
Figure 7 Cumulative displacement was measured as the total upstream path length that fish swam. Although lake (and outlet stream) fish were displaced downstream more than inlet stream fish, these groups actually tried the hardest to swim up-stream. However, they alternately swam up, then were blown down-stream, then swam up again, leading to a much larger cumulative effort, even though they had less to show for it at the end of the experiment. The stream fish, on the other hand, stayed in place (Fig. 6) with less effort.
A few surprising insights showed up as well. First of all, we realized that rheotaxis is not a simple trait to interpret. Stream fish actually did a very good job holding their position in current, but they did so with relatively little effort (Fig. 7) and by seeking out low-flow ‘boundary’ areas near the inner part of the circular tank. So they actually avoided current, to stay in place. Lake fish, on the other hand, weren’t very strategic and used the middle of the current. They were tumbled ‘down-stream’, only to swim most of the way back up again. Over the duration of a given trial, lake fish lost a lot of ground down-stream (so did the stream fish, actually, Fig. 6). But the lake fish expended vastly more energy to not-quite hold their place. And they did end up farther down-stream.
Although the rheotactic response of stream stickleback was very striking, we couldn’t recreate it in two subsequent studies. In lab-reared common garden stickleback, everyone showed fairly positive rheotaxis no matter where their parents came from. So either the lake-stream difference in rheotaxis isn’t heritable, or it is heritable but requires prior experience to fully develop. In wild-caught non-breeding stickleback, the rheotactic difference was also absent.
Our conclusion then is quite intriguing: non-breeding fish, and inlet stream fish, show positive rheotaxis. Breeding lake fish do not. So is the lake condition the derived/induced trait? Perhaps: stickleback are ancestrally anadromous after all, swimming from the ocean upstream into estuaries and rivers and lakes to breed. Perhaps that same instinct persists, but must be actively suppressed in lake fish to prevent their dispersal into the stream?
To really answer this speculative question, we will need to replicate this result more extensively with both marine and multiple lake and stream stickleback, and begin genetic mapping of rheotactic response to understand the mechanisms and polarity of either gain or loss of this swimming behavior. We will be aided in that endeavor by the fact that we have recently found some of the phenotypic traits that contribute to rheotactic response and are heritable. But I can’t tell you more about that yet, as it isn’t published. In fact, I should probably go back to working on finalizing that manuscript right now. But before I sign off, I want to reiterate a few key lessons.
First and foremost: gene flow is an evolutionary effect of individuals’ movement across a landscape (and their ability to survive that movement), and both behavior and morphology can influence that movement. As a result, different phenotypes (or genotypes) may move non-randomly through space. Local adaptation can therefore result from individuals’ movement behavior, rather than differential survival or reproduction (Bolnick and Otto 2013). This poses all sorts of curious puzzles: what are the traits and loci driving non-random movement? What does this directed movement do to eco-evolutionary feedbacks, for instance as predators and prey interact not just through attack rate but also movement? What is the genetic signature of adaptation-via-dispersal? Does this generate peaks of high FST that we might interpret as an effect of natural selection?
Second: read theory, understand theory, and don’t be intimidated by theory, but at the end of the day don’t let theory box in your thinking. Population genetics from the new synthesis onward would have me believe that adaptive divergence isn’t possible within a dispersal neighborhood. But it is (Richardson et al 2014).
Lastly: paddle. When in the field, it is important to take some time to let your mind drift, and to explore your surroundings. As a discipline, we are inspired by biological diversity, but too often we enter the field intensely focused on our own planned project, our hypothesis testing. Many of my own areas of research emerged not from a priori planning, but from these all-too-infrequent mental breaks in which I happen to notice something that catches my interest. So, if you find yourself wondering, “to swim, or not to swim”, or some variant thereon, you’d best put on your mask and snorkel. That’s where the biology is. In particular, that’s where you’ll find something that you didn’t expect, that theory hasn’t trained you to see.
Bolnick, D.I., T. Ingram, L.K. Snowberg, W.E. Stutz, O.L. Lau, and J.S. Paull. 2010 Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proceedings of the Royal Society of London, Ser. B. 277: 1789–1797. doi: 10.1098/rspb.2010.0018. PMCID: 20164100
Bolnick, D.I. and S. Otto. 2013. The magnitude of local adaptation under genotype-dependent dispersal. Ecology and Evolution 3:4733-4735. doi: 10.1002/ece3.850. PMID: 24363900
Bolnick,D.I. L. Snowberg, C. Patenia, O. L. Lau, W. E. Stutz, and T. Ingram. 2009. Phenotype-dependent native habitat preference facilitates divergence between parapatric lake and stream stickleback. Evolution 63:2004-2016 doi: 10.1111/j.1558-5646.2009.00699.x. PMID: 19473386.
Edelaar, P. and D.I. Bolnick. 2012. Non-random gene flow: an underappreciated force in evolution and ecology. Trends in Evolution and Ecology 27: 659-665. doi: 10.1016/j.tree.2012.07.009. PMID: 22884295
Jiang, Y., L. Torrance, C.L. Peichel, and D.I. Bolnick. 2015. Differences in rheotactic responses contribute to divergent habitat use between parapatric lake and stream threespine stickleback. Evolution 69: 2517-2524. doi: 10.1111/evo.12740.
Richardson, J.L., M.C. Urban, D.I. Bolnick, and D.K. Skelly. 2014. Microgeographic adaptation and the spatial scale of evolution. Trends in Ecology and Evolution 29: 165-176. doi: 10.1016/j.tree.2014.01.002. PMID: 24560373
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