Darwin Comes to Town

by Menno Schilthuizen

  You may have asked yourself the same question while reading the previous chapters. Or you may have doubted that the examples I have given can truly be called evolution. After all, with a few exceptions (which I’ll save for later), we are not talking about the evolution of entirely new forms of life. Mostly, urban evolution is more subtle than that—not surprising, because it takes place within such brief time frames. The urban ermine moths of Basel that are less attracted to light are only so by a small degree compared with their rural relatives. The investment in heavyweight seeds by the urban hawksbeard in Montpellier is only a fraction greater than outside the city. Measurable and statistically significant, yes, but still only rather minuscule. It’s not as if, when shown an urban and a rural hawksbeard plant, you are blown away by the difference. To the untrained eye, they would still look precisely the same.

  What’s more, the genetic tweaks that allow urban evolution to take place are often not new. The dark feathers that aid urban pigeons in dealing with heavy metals, for example, are darkened thanks to a mutant plumage color gene that also exists in wild rock pigeons and was already there long before these birds were tamed by man, escaped, and became city birds. And the genes that permit plants to grow on urban soil polluted with heavy metals are exactly the same ones that have already floated around in populations of these plants for thousands of years, maintained because they occasionally save a stand that grows on some talus slope rich in copper or zinc minerals.

  In fact, ever since geneticists began screening chromosomes, they have been surprised by how genetically variable most species in nature are. Pick a gene, any gene, from a wild species—say, a gene that affects leg length in the Anolis lizards in the cities of Puerto Rico. Usually, such a gene will consist of a sequence of several thousands of DNA “letters” of genetic code. This genetic code specifies the exact structure and shape of a protein. In the case of Anolis’s leg-length gene, this protein may, for example, let cells in the embryo divide at the rate and directions required to produce a limb-like outgrowth.

  The thing is, the genetic code for a gene is very rarely exactly the same across all individuals of a species. It could very well be that, if you were to read the code for the lizard-leg gene in a thousand Anolis lizards from a Puerto Rican city, you’d find thirty or forty different versions of that same code. Most of those would differ from one another in minor details only: a changed letter here and there, perhaps a short bit of DNA deleted or duplicated—the products of copying errors made in the loins of some ancestral lizard many generations before. And, in most cases, these variants would all still do the exact same thing, that is, produce a lizard leg in a lizard embryo—hence their unhindered passing down the generations. But, it could be that one variant produces an almost imperceptibly slenderer leg, or a slightly stubbier one; or one that begins growing just a little later in the animal’s development.

  This palette of subtly different gene variants, most of which are so similar that they are inconsequential for a species’ evolution most of the time, is called “standing genetic variation.” And it is this palette that evolution dabs its brushes in to create new works of urban art. For when the environment changes and suddenly offers a new, previously nonexistent benefit for Anolis lizards with slightly longer legs, those gene variants already able to do the job are right there in the population, ready to rise to the occasion and yield to the opportunities of natural selection.

  Hence, standing genetic variation is a species’ evolutionary capital. It encapsulates the ability of a species to dip into its genetic savings and immediately come up with any combination of genes that a changed environment requires. That is why urban evolution can proceed so rapidly: the animals and plants that need to adapt to whatever new feature humans release in their urban environment do not need to wait for the right mutations to come along. Mostly, the necessary gene variants are already there, waiting in the wings of the standing genetic variation. It only takes natural selection to bring them out into the limelight, and give them a chance to shine.

  Evolution employing pre-existing gene variants is what biologists call “soft selection.” But urban evolution could also make use of new mutants that arise there and then (“hard selection”). To distinguish soft and hard selection, geneticists do a close-reading of the genetic code involved in an urban adaptation. In the PCB-tolerant mummichog fish, for example, Andrew Whitehead discovered that different genes are involved in different harbors along the US east coast. And even within the same harbor, the same gene variant that affords protection against PCBs may, in different mummichog fish, be flanked by different genetic codes on either side. These are all tell-tale signs that the PCB-tolerant gene variant already arose long ago and has since become detached from its neighbors due to the frequent chromosome breaking and crossing-over that occur during reproduction. So, the mummichog PCB tolerance clearly evolved via soft selection, using only its pre-existing standing genetic variation.

  But as we saw in a previous chapter, it’s a different story for the peppered moth in England. It adapted to soot-covered trees by virtue of a mutation that took place in the cortex gene right at the onset of the industrial revolution. Throughout all of England, the dark-colored moths carry the same variant of cortex and the gene’s neighboring regions are also identical. This is a clear signal of hard selection: the new cortex gene gave such an advantage that it swept through the population like wildfire, so fast and pervasive that it dragged its neighboring genes with it, before these found the time to be decoupled by chromosome breakage.

  So, yes, rapid urban change may be subtle. It may also employ genes that are already floating around in the species. Nonetheless, it really is evolution, pure and simple.

  One of the readers of my New York Times piece was not convinced. Cornelius Hunter, a blogger for the website Darwin’s God, used my exposition of urban evolution as a peg for a fine piece of creationist writing, in which he stated, “Adaptation and evolution are two very different things. Biological adaptation relies on the preexistence of […] genes, alleles, proteins, […] and so forth. Evolution, on the other hand, is […] the origin of all those things.”

  In other words, Hunter the creationist made a distinction between soft selection, which he saw as an inevitable physical process, building on already existing materials, and the origin of something entirely new, new genes and new “kinds of organisms.” Only the latter, in Hunter’s opinion, deserves to be called evolution (and, needless to say, to his mind cannot exist).

  It’s amusing to see how creationism, in the face of ever-improving evolutionary knowledge, keeps moving the goalposts about what counts as evolution. Fortunately, this is not a matter of opinion. Biologists have a very clear definition of what evolution is, namely the change, over time, of the frequencies of gene variants. The origin of those gene variants is, contrary to what the Darwin’s God blog would like its readers to believe, not evolution. Instead, it is chemistry—errors made in the stitching together of DNA from molecular building blocks in the cell. But the natural selection that causes these chemically originated gene variants to become common or rare, that is the stuff of evolution. Over longer periods of time such small, short-term evolutionary steps coalesce into bigger evolutionary changes for many different genes, eventually leading to entirely new species.

  But even if you’re not a rabid creationist, and perfectly able to see that the urban hawksbeards, mummichog, anoles, bridge spiders, ermine moths, and all the other creatures that have peppered these pages, did, in fact, evolve, there may be room for doubt. After all, for a trait to actually evolve, it is necessary that it is genetic—encoded in the organism’s DNA. And biologists who see a change in an urban organism’s looks or behavior do not always have firm evidence that this is the case.

  The color and color patterns of animals, for example, are usually genetic. Our own bodies are testimony to that: the color of our hair, skin, and eyes is determined by the genes we inherit from our parents. But we also know that ski
n can be tanned and hair can be bleached by sunlight, and eye color sometimes changes as we age. So, genes are not everything. For most aspects of our appearance, both nature and nurture come into play. This is true for animals, too. For example, when Tetrix ground hoppers (a kind of drab, camouflaged grasshopper) grow up on light-colored sand, their body color is lighter than when the same animals would grow up on dark sand. This is a form of “plasticity”: with the same DNA, you can get different outcomes. So, it’s easy to imagine that when, in a certain species of animal or plant, you find a color difference between the ones living in the city and the ones living outside, you might mistakenly think this is urban evolution, whereas in fact, there is only plasticity.

  Behavior is especially tricky. If some species of bird, for example, behaves more boldly in the city than in the countryside, this does not necessarily mean that the city gene pool is rich in genes for bold behavior. They could simply have learned that boldness pays off in an environment where there is food to be snatched and fear for predators is unwarranted. Or, the reverse, the countryside birds may have learned that out in the wild nature, one had better be circumspect, whereas the city birds have grown more naïve.

  We know that in many animals, behavior can be genetically determined, but we also know that it can be learned and passed on from one individual to the next by instruction and imitation. To figure out what the relative contribution of each is, you’d have to do complicated experiments involving a lot of rearing and crossing and breeding—something that is not always practicable. The reason that Astrid Heiling in the previous chapter took the trouble to hatch bridge spider eggs and hand-rear the spiderlings in the lab was to make sure that the spider’s attraction to light was innate, and not a habit they had picked up while growing up in an artificially lit environment. And even if an urban behavior is entirely down to an animal’s ability to learn, this is not to say that evolution may not eventually kick in. If boldness is beneficial, for example, then learning to be bold may, over many generations, be replaced by genes that cause an animal to be bold from birth—hard-wiring the useful behavior that otherwise would need to be built up slowly during life.

  Then there is epigenetics. I apologize for littering this chapter with new terms, but I promise that epigenetics is the last one. It might be an important one. We don’t really know, because epigenetics is still such a new thing in evolutionary research.

  The meaning of the term “epigenetics” was only cast in scientific stone at a conference in Cold Spring Harbor Laboratory in 2008. It denotes a change in some characteristic of an animal or plant that is the result of “changes in a chromosome without alterations in the DNA sequence.” Now that may sound strange because chromosomes are made of DNA, right? Well, yes and no. Chromosomes contain the DNA, but they are much more: they also contain proteins and other molecules that package the DNA like bubble wrap. And only when the packaging is peeled off to reveal the naked DNA, can a gene do its work. As it turns out, some of this packaging material can be added or removed during an animal or plant’s life to muffle or amplify a gene’s voice, as it were.

  What’s more, the offspring can sometimes inherit certain types of this packaging conformation. So, if the toils of life place high demands on a certain gene, then some of the packaging may be removed, making this gene churn out protein at a higher rate. The offspring may then inherit DNA from their parents with the packaging pre-removed, to give them a better start in life. That way, epigenetics can enhance or suppress a certain gene for several generations on end. You can probably imagine that this could lead an urban evolutionary biologist astray. If some aspect of an organism is beneficial and genetic, then an increase in it in a city environment would be taken as a clear sign that it is evolving. And yet it may be that the DNA is actually unchanged and that the “evolution” is really only epigenetics at play.

  The salt tolerance of Kayla Coldsnow’s Daphnia water fleas, for example, might be down to epigenetics. It’s known that when these animals are exposed to toxic chemicals, they turn on genes that help detoxify their bodies. And it seems that their offspring are born with the epigenetic switch already in the “on” position. If the same thing is true for salt, then this could explain the very fast adaptation to road salting that Coldsnow discovered. Only finding and sequencing the genetic codes of the genes involved would definitively answer this question.

  As Kevin Gaston says in an overview article, almost no study in urban evolution has distinguished between genetic adaptation and epigenetic effects. “Addressing these limitations will be a major challenge for urban ecology in the future.” At the moment, most experts think rapid urban evolution is still mostly due to actual changes in the DNA, rather than epigenetics, but few people dare to state this with any great confidence, and the next few years may well prove that epigenetics is a force to be reckoned with.

  I hope you’ll forgive me this short exposé on epigenetics, plasticity, soft and hard selection, and all the other intricacies surrounding urban evolution. With a process that is so subtle, and yet so important for the survival of biodiversity in our urbanized future world, it’s crucial to be well versed in modern evolutionary biology. Now you are ready to be taken to the next level of urban evolution. Enter: the Red Queen!

  III.

  CITY ENCOUNTERS

  “Well, in our country,” said Alice, still panting a little, “you’d generally get to somewhere else—if you run very fast for a long time, as we’ve been doing.”

  “A slow sort of country!” said the Queen. “Now, here, you see, it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!”

  LEWIS CARROLL, Through the Looking-Glass (1871)

  14

  CLOSE URBAN ENCOUNTERS

  You probably know those scenes of killer whales launching themselves onto Argentinian beaches to snatch up unsuspecting seals. Dramatic footage of the bulky black-and-white giants emerging from the surf and grabbing seals as if they are cookies on a counter has featured in countless nature documentaries. If you hold on to that image and scale it down, then you have something akin to what French biologists in the city of Albi began witnessing in 2011.

  Albi is a small city in southern France, the capital of the department of Tarn, named after the river that slowly meanders through Albi’s medieval, UNESCO-registered center. In the heart of the city, the Tarn is spanned by the Pont Vieux, a bridge that connects two heavily built-up districts on either side. Like urban areas everywhere, these city quarters are home to the customary flocks of feral pigeons. Here, though, the pigeons have more immediate concerns than the accumulation of lead and zinc in their feathers that we saw earlier in this book. For every day, when groups of pigeons gather on a gravel island underneath the Pont Vieux to bathe and preen, they are the target of what French biologists Julien Cucherousset and Frédéric Santoul call “freshwater killer whales.”

  The killer whales in question, Cucherousset and Santoul explain in an article in the journal PLoS ONE, are European catfish (Silurus glanis). The continent’s largest freshwater fish, they can easily reach a length of five feet, and even individuals of over six and a half feet are occasionally reported. Catfish are native to eastern Europe and western Asia, but they did not occur in western Europe until people began releasing them for sport. The river Tarn was first stocked with catfish in 1983 by local angling societies. The fish did well, expanding fast on a diet of smaller fish, crayfish, worms, and molluscs that live in the river’s muddy bottom. But at some point, the urban catfish of Albi began doing something that no other catfish had ever been seen doing before: launching themselves out of the water, grabbing bathing pigeons by their feet, dragging them under water and swallowing them, metal-laden feathers and all.

  For a whole summer, Cucherousset, Santoul, and their team of students took turns observing this spectacle from the Pont Vieux, capturing a total of 72 hours of fish-pigeon encounters. Their videos, shot st
raight from above, make for nail-biting viewing. We see a flock of pigeons frolicking on the gravel beach, dipping their beaks into the river to drink, and happily flapping their wings to spray themselves with river water—seemingly oblivious to any danger. Meanwhile, a menacing dark shape in the water looms closer and closer. As the catfish approaches the shore where the birds are splashing about (you have to imagine the musical soundtrack), it raises the long whisker-like barbels around its mouth to detect its prey’s vibrations more precisely. It singles out one bird that is standing with its feet just in the water and then, with a few wild tail swings, launches itself onto the beach, grabs the pigeon by a foot and quickly retreats back into its watery habitat, taking the desperately flapping bird with it, and swallowing it in a few large gulps of its gaping mouth. The other pigeons take off in momentary consternation, but then return to their bathing spot as if nothing had happened. Soon, a second catfish attempts the same trick on another pigeon. In all, the researchers filmed fifty-four attacks, of which about a third were successful. A chemical analysis of the catfish, the pigeons, and several other prey animals (smaller fish and crayfish) proved that the pigeons make up around a quarter of the catfish diet, with some catfish individuals getting nearly half their nutrients just from eating birds.

  Eating birds. Beaching themselves to catch them, for crying out loud! Let this sink in for a second. According to the handbooks, catfish are supposed to feed on fish and aquatic invertebrates that they rustle up from the mud. That is their catfish niche. They never evolved to launch their bulky bodies onto shore to pull winged animals down in mid-takeoff. And yet, here we are: humans brought rock pigeons and catfish into their cities, introduced them to each other, and thus created an ecological opportunity that never existed before.