Watching Fish Climb Darwin’s Mountain

When biologists think about the evolution of life, they think about climbing mountains.

To understand their alpine frame of mind, imagine a biologist studying the fish in a lake. Each fish may be born big or small. Fish born at certain sizes may be more likely to survive and reproduce than others. Each fish may be aggressive or shy. Again, their aggressiveness may determine their odds of having babies.

To picture all of this, it’s very helpful to imagine a landscape. Each point on that landscape is a different combination of aggression and body size. They’re like the longitude and latitude on a map. Each combination leads to a particular level of reproductive success. Picture that success as the elevation of that point on the landscape. The more success, the higher the altitude.

The biology of those fish can give the landscape a topography. Perhaps it produces a single mountain. The peak is the combination of weight and aggression that produces the most possible babies. The landscape drops off in all directions, to combinations that make it more likely the fish will die, or fail to reproduce.

The actual fish in the actual lake might turn out to be clustered on one of the mountain’s flanks. The fish closer to the peak have more babies than the others further downhill. As a result, they’ll pass down more copies of their genes to the next generation. And that means that the population will climb up towards the peak. If a new mutation arises, natural selection will favor it if it helps the fish climb further. Eventually, the fish may reach the mountaintop. Once they plant their flag on the peak, they’ll be stuck. Natural selection won’t be able to nudge them off.

Now imagine that there are two peaks, not one. The fish sit on one mountaintop, while the second peak towers over them in the distance. They can’t get to that second peak, though, because natural selection can only nudge them uphill. They are stuck with a mediocre body.

This evolutionary landscape has floated in the minds of biologists for at least eighty years. A series of scientists, starting with Sewell Wright and George G. Simpson, developed the concept as a way to think about how evolution transforms populations. (For more information, check out the new book, The Adaptive Landscape in Evolutionary Biology.) For many biologists, it’s been a powerfully useful image. It’s even more useful if scientists can map landscapes with real biological data, setting the altitude at each point based on how well organisms really do reproduce.

Chris Martin and Peter Wainwright of the University of California at Davis have done just that, with real fish in real lakes. And their research is helping scientists to understand how evolution has allowed life to plant its flag not just on one mountain peak, but along entire mountain ranges.

The fish in question are three species of pupfish (Cyprinodon) that live in lakes on the island of San Salvador the Bahamas. The lakes are less than 10,000 years old, but they contain three species that feed in fundamentally different ways. One species eats algae and decomposing animal matter–a common lifestyle for pupfish found in other parts of the New World. But a second species is bizarre: it has powerful jaws that it uses to crush snails. And a third is even weirder: it chews off scales from other fish.

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From Martin et al 2011

Just from an anatomical point of view, the emergence of these new forms was spectacular. This diagram shows the parts of the pupfish body that have changed on San Salvador (yellow shows strong changes, and orange is stronger). The changes are among the fastest ever recorded in animals.

To understand how the pupfish managed to evolve so quickly into three such distinct forms, Martin and Wainwright took advantage of the fact that the species are so young. They can still interbreed and produce hybrids. So Martin scooped up fish from the lakes and took them back to Davis, where he bred them for two generations to produce 3,000 hybrids, each with a different combination of the traits.

Martin studied some of the hybrids in his lab, and he found that they all survived about equally well there. Their success told Martin that combining their genes together didn’t create any disorders that cut their lives short. To see how they fared in the wild, he flew back to San Salvador with nearly 2,000 hybrid pupfish.

Martin dumped the fish into enclosures he built in the lakes. He let them fend for themselves for three months. Then he came back to see which ones were still alive, and how much the survivors had grown.

From this data, Martin could draw an accurate landscape of pupfish evolution. And here’s the landscape he drew. The latitude and the longitude represent two different sets of measurements, taking into account features such as the length of their jaw and the depth of their bodies.

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The Adaptive Landscape of Pupfish. Courtesy of Chris Martin

The green peak is the shape found in the algae-detritus feeding species. The red peak represents the snail-crushing form. The intervening landscape is made up of valleys, reflecting the fact that the further away hybrids were from the original species, the worse they did. And down in the blue valley are the hybrids that resemble the scale scrapers.

Most of the San Salvador pupfish are algae-detritus feeders. But Martin’s research shows that if they could switch to feeding on snails, they’d be much better off. To do so, however, they would have to cross a deep evolutionary valley. As a result, they are stuck on their own peak, looking up at a better one.

So how did the snail-crushers evolve in the first place? One clue comes from another experiment Martin ran. He put the pupfish in another set of enclosures, but at much lower density than before. The lack of competition was good for all the fish, hybrids included; they were all much more likely to be alive when he came back to the enclosures. There was just more food to go around, and so being a clumsy hybrid didn’t impose much of a cost on a pupfish.

This result suggests that things were different in the lakes when they first formed thousands of years ago. There were no competitors when the pupfish arrived. In other words, the evolutionary landscape looked different.  Instead of the Himalayas, think gently rolling hills. Some fish were able to start adapting to crushing snails. They were mediocre at first, but they were still the best snail-crushers on San Salvador. Their descendants evolved to become so good at it that they’ll outcompete any pupfish that might wander towards their own evolutionary mountain.

What’s happening in these lakes on one little island could shed light on how other species have evolved over hundreds of millions of years. Again and again, scientists find evidence that lineages explode into diversity quickly, and then their diversification tapers off. It seems that the adaptive landscape allows them to move fast to occupy empty niches. The landscape changes shape, making it much harder to move around it. Scientists who have documented these patterns of diversity in the fossil record have envisioned an evolutionary landscape with several peaks. Now, for the first time, Martin has marked those peaks in a real evolutionary landscape.

This experiment doesn’t answer all the questions scientists have about how diversity evolves, of course, and it even raises some questions of its own. What’s up with those scale scrapers, for example? Why are they down in the depths of the valleys? When Martin put hybrids with scraper-like anatomy in the lakes, they pretty much all died. What’s interesting is that Martin found few scales in their stomachs. It’s as if they didn’t even try to feed this way. It may be that scale eating demands such an extreme anatomy that Martin’s hybrids just didn’t have a chance of surviving in that manner. But they were also outcompeted by the other hybrids for the other food in the lakes, and so they died out.

In other words, even in these little lakes, there is an evolutionary terra incognita Martin has left to map.