In urban areas, the forces of rapid natural selection are leading to striking genetic changes in animals. Dutch biologist Menno Schilthuizen talks to Yale e360 about the transformations seen in creatures ranging from mice in Central Park to anole lizards in Puerto Rico.

The unprecedented influence that humans are exerting on the natural world is a given in this epoch of the Anthropocene. Now, in his latest book, Darwin Comes To Town, evolutionary biologist Menno Schilthuizen explores how that influence is rapidly reaching down into the genes of plants and animals. In an interview with Yale Environment 360, Schilthuizen, a researcher at the Naturalis Biodiversity Center in the Netherlands and a professor at Leiden University, describes how, through fast-paced natural selection, creatures in cities and suburbs are genetically evolving to deal with the omnipresence of humans. Examples abound. Urban populations of some birds, adjusting to traffic noise, are becoming hard-wired to sing at a higher pitch than their country cousins. White-footed mice in Central Park are evolving to better deal with the fatty foods that New Yorkers serendipitously drop their way. Caribbean lizards are undergoing genetically driven physical changes so they can better maneuver along urban surfaces that are far smoother than the rough bark of trees.

Menno Schilthuizen

Schilthuizen also discusses some theories that challenge current conservation orthodoxy, noting, for example, that corridors that enable isolated wildlife populations to connect may not always be advantageous in an urban setting in which “local adaptation to deal with the very specific local conditions is something that’s important for these animals.” Still, says Schilthuizen, the ability of some species to adapt to city life in no way lessens the urgency to preserve the earth’s remaining natural areas. “You can appreciate what’s going on in evolution in very artificial human-constructed environments like cities,” he says. “[But] as someone who is inspired by biodiversity, to me it would be a tragedy to lose those species that need untouched areas to survive.” Yale Environment 360: You write about some fascinating examples of how species have rapidly changed in an urban environment, including American cliff swallows, whose wings have become shorter so they can take off faster vertically in the face of oncoming cars. And then there’s the case of the white-footed mice in New York City, who live in isolated populations in various parks. What’s genetically different about these populations, and what was the pressure to diverge in that way? Menno Schilthuizen: This is work that’s been done by Jason Munshi-South of Fordham University. He found a number of genes that are different in several of the parks that he looked at. And they mostly seem to have to do with diet, but also a bit with pollution and with disease resistance. In Central Park, he found that mice there had two genes that seem to have evolved in a different direction compared to all the other isolated mouse populations in the city, and those genes have to do with resistance against aflatoxin, which is a harmful compound that is formed when nuts get infected with a particular type of fungus that grows on discarded peanuts, for example, and which is toxic to many mammals, including ourselves. And the second gene has to do with [accommodating] very fatty diets. Central Park is by far the most visited park of the ones that he looked at. Twenty five million visitors go there every year and of course they leave junk food, discarded nuts, muesli bars, and what-have-you. And presumably the mice there get a substantial portion of their nutrition from these human-derived foods, which are fattier and may have these aflatoxins in them.

“The idea that it’s always good to connect populations by corridors is maybe not always true when local evolution… [is] important for these animals.”

e360: You give other examples of how some plants and animals have adapted through natural selection to our traffic noise, our use of road salt, heavy metals, city lights. And then there’s the case of the foot pads of the Puerto Rican crested anole lizard. Tell me about this example of urban-induced genetic change. Schilthuizen: Anole lizards are really one of the poster boys for evolution in the first place. They’ve diversified in hundreds of species in the Caribbean, normally under natural conditions. There’s one species that lives in Puerto Rico, both in the forest and in cities. In the forest, this particular species of anole lizard runs on branches and catches insects, but in the city it mostly hangs around on human structures, on walls and windows, on large and often much smoother surfaces than in the forest. And these lizards need to grip onto their substrate quite tightly. They’re heavy enough to break bones when they fall from a great height. So they have toe pads, just like geckos do, with lamellae that help them to grip on the surfaces. But sometimes they fall, and that’s of course where the evolution comes from, from animals that die from falls, or animals that cannot move fast enough on a surface to get out of the way of a predator or to get prey themselves. And we see that in the cities, the legs have become longer and they have obtained more of these lamellae under their feet. And the idea is that the surfaces in the city are smoother so they need a better grip. Also, because the surfaces are usually much larger and flatter than the branches in the forest, the lizards need longer appendages to move faster and to hold on better. There are very nice videos where you can see that these forest lizards, when you put them on a tiled, slippery urban slope, that they really have trouble walking up properly, whereas a city lizard runs up like it’s no problem at all. Kristin Winchell [a post-doctoral research associate at Washington University] is a researcher working on this.

A comparison of how a Puerto Rican anole lizard from the forest (left) and one adapted to live in an urban environment (right) navigate a painted concrete surface, tilted at a 60-degree angle. Videos courtesy of Kristin Winchell

e360: And she did the study in which these urban and forest lizards were raised in the same way and saw a true genetic change. Schilthuizen: That’s a very crucial type of experiment that many of researchers working on this do — these so-called common garden experiments, where you get the eggs or the young animals from the two different habitats, from the city and from the forest, you bring them to the lab under the same conditions, and if you still see the differences then clearly it’s evolution and genetic.

e360: Counter to the notion that fragmentation threatens wildlife, there’s now a theory that urban fragmentation may actually help certain urban populations. I’m thinking in particular of the bobcats in Southern California that you wrote about. Schilthuizen: The bobcat population is a partly urban population in Los Angeles, and they are actually in the process of really invading human-dominated areas. They can cross gardens and streets quite easily, but the one thing they cannot cross are really big highways. In that area, two major highways bisect the region into basically four sections in which bobcats live, but they cannot easily cross from one section to the other. Research by wildlife zoologist Laurel Serieys found that you can see that pattern of those four sections in the genes of the bobcats. These genetic markers are different for each section, suggesting that they mix a lot within every section, but they rarely cross the highway, so these four sections basically evolve independently. In one particular section there was a mange epidemic, which is a disease that is caused and spread by mites that burrow under the skin of these big cats, and which is often exacerbated by the use of pesticides that the bobcats accidentally ingest and which makes their immune systems weaker. And it seems that because so many bobcats died from that disease over the past one-and-a-half decades, the surviving ones were the ones that had genes that are particularly good at affording resistance against this particular disease. And it’s not certain whether the same thing would have happened if those four sections of bobcats would have been in touch with each other, because then the one population that needed the resistance may have been swamped by genes coming in from the other ones, similar to what could have prevented the white-footed mice in New York adapting to their local conditions. So the idea that it’s always good to connect populations by corridors is maybe not always true when local adaptation, local evolution to deal with the very specific local conditions is something that’s important for these animals.

“If we want to make cities greener, then the best candidates for that would be species that have already adapted to urban conditions.”

e360: Urban environments are even having an effect on mating. In the 1980s, a few dark-eyed juncos, which up until then had bred in mountain forests, began to stay year-round in San Diego, California. It was discovered that the female urban birds preferred males with very few white feathers in their tails, while their forest counterparts looked for guys with lots of white feathers. What’s going on there? Schilthuizen: So in competing over a territory in those mountain forests where they normally live, it’s very important to have very bright, white colors in your tail and very dark feathers on your head, and the most striking ones are also the ones that are most aggressive and the most successful in defending a territory. And territories in the mountains are extremely important because the season during which there are insects is very short. And you need to defend a territory against other males so that your female can raise at least one clutch of eggs on the few insects that there are. But in San Diego, which is at sea level, it’s an urban environment so there’s plenty of food and they can start breeding very early in the year. They can easily have three or four nests throughout the year, and the importance of maintaining a territory is not so great anymore. And for the females, it’s actually much more important that the male helps in raising the young rather than fighting other males. So you see that those colors of the males are changing, and also the preference of the females is changing. So in the city, the white in the tail is disappearing and also the darkness of the head is becoming less striking, presumably because those things are important in defending forest territories, which in the city are not so crucial any more. e360: So you need kinder, gentler males in the city? Schilthuizen: Exactly, sort of like metrosexual juncos.

A bobcat photographed by a camera trap in Los Angeles' Griffith Park. National Park Service

e360: You have some interesting thoughts regarding non-native species in urban environments. You say that green urban architecture must accept that many of the plant species that have successfully evolved and adapted to an urban environment are not native, so those are the plants that green urban planners should be using. Schilthuizen: To begin with, urban environments are melting pots anyway. In most cities, the main players in the ecosystem are species that have been brought in by people, and those are not necessarily native species, so for the smooth running of the urban ecosystem the best species may not be native species. And more importantly, I think, if we want to make cities greener, then the best candidates for that would be species that have already adapted to urban conditions rather than species that you pick out of a catalog of a garden center. It’s best to get species that have already experienced a long period of adapting to urban conditions, and those are the species that you find growing in vacant lots in the city. And you’ll find that many of those are in fact exotic and therefore also probably are the species that are best suited to growing on green roofs or green walls or any green you want to design in the city. e360: You’re quite adamant, though, that the take-home message of the book should not be misconstrued to be, “Hey, everything is okay because nature is adapting to our increasingly urban world.”

Schilthuizen: I think it’s a fascinating process to study this adaptation of wild species to human-created conditions, and you see fascinating examples of very rapid evolutionary adaptation there. But it’s important to realize that the flip side of very fast evolution is a lot of death. To be able to evolve very fast you have to have a great difference between the individuals that make it and the individuals that don’t. So the ones that we see evolving are just a few species that were lucky enough to have some variants that were able to live under these artificial conditions that we threw at them. Behind that is probably a much larger group of species that were not able to adapt to the change to the environment that we create. So it’s certainly not true that all species can adapt, because we don’t see the species that didn’t adapt. They simply disappeared. They are extinct. And they can only survive in areas that probably are pristine. As a biologist and somebody who’s inspired by diversity, to me it would be a tragedy to lose those species that need untouched areas to survive. So for preserving the bulk of the earth’s biodiversity we still need to protect those untouched areas. Meanwhile, you can also appreciate what’s going on in evolution in those very artificial human-constructed environments like cities.

“My vision is to have a monitoring system of urban evolution by which we use citizen science to constantly watch this process taking place.”