The rules of nature apply everywhere in the world: they keep the fragile ecosystems of reefs, grasslands and islands in balance; they determine the rhythm of flowering woods, they control the explosive growth of jungles; they create a global web of interactions and relations among all living species and their inorganic environment. From the Arctic to the Antarctic, every natural community unfolds, grows, collapses and develops following the laws of ecology and evolution. But there is one place in the world that doesn’t seem to play according to these rules – even stronger, it seems to be almost completely exempt of nature. It is a place where just one single life form sits on its lonely throne: cities.
Cities have been part of the world’s landscape for thousands of years. The oldest known towns – Jericho and Çatalhöyük – date from the 8th millenium BC and had estimated populations of several thousands. Although they were proto-cities lacking planning and central rule, it didn’t take long for more complex, large and organized metropolises to arise once agriculture spread throughout the Middle East in the Neolithic. In China, India and the Americas too, cities sprung up, flowered and dominated large areas of land in ancient times.
A view of Çatalhöyük, a proto-city in southern Anatolia, Turkey, after the first excavations.
Ten thousand years later, our cities have reached very different dimensions. The largest cities of 2019, such as Tokyo, New York or São Paolo span over areas up to ten thousand square kilometers and host up to 35 million inhabitants. In such places, it is rare to encounter more wildlife than a few mice creeping in the subway and some pigeons scavenging in the streets. Similarly, the city greenery is represented by just a few, often exotic plants that grow in the local park thanks to our extensive attention and care. Yet, even in the greyest and largest cities, nature finds her way. Although rarely considered as such, cities are in truth ecological landscapes, in which unique and rapidly evolving ecosystems have developed. As we will see, natural communities have invaded cities over time and obey the same – if slightly modified - natural rules as their coastal, forestry, desert, grassy, arctic, alpine and marine equivalents do.
Just like any other environment, cities exert pressure on the living beings that inhabit them, which not all can withstand. This automatically sets the process of natural selection in motion, since only those who have what it takes to survive and reproduce in the city will give rise to the next generation. In the long run, urban populations of animals and plants will change and adapt to best fulfil the requirements for survival in the urban jungle, just as their equivalents have done in other habitat types. Although cities haven’t existed for nearly as long as and are far more dynamic than other natural landscapes, several studies have proven that natural selection is continuously at work in our cities and natural communities are slowly establishing themselves in this brand-new, vacant habitat.
The oldest recorded example of urban adaptation dates from Darwin’s time and is widely regarded as one of the best examples of natural selection at work. Even though it wasn’t Darwin himself who discovered it, it convinced many people of his theories when a first report was published 14 years after his death. Even today, all scholars of evolutionary biology will learn about this very special case: the fantastic evolutionary story of the peppered moth. In the early 1800’s, the peppered moth was known as a white, specked bug that was often found resting on lichen-covered, white-coloured tree bark in the English countryside and city surroundings. Interestingly, a previously unknown black specimen of the moth species was discovered in 1811, which appeared to be an extremely rare variant of the moth. Already then, it was thought that the black moths were rare because they were more vulnerable to predators, since their black bodies would jump out against the white tree bark on which they would rest during the day[1].
Left: a white specimen of the peppered moth (Biston betularia) is marvellously camouflaged against the white lichens that cover tree stems in unpolluted forests (by Heath McDonald). Right: the black morph of the peppered moth is very easy to distinguish from the white background (by Ben Sale).
By the end of the 19th century, when England had become heavily industrialized and the coal-burning factories had painted the trees of city forests black[2], entomologists recorded much higher frequencies of the black peppered moth. In some areas, the darker morph dominated entirely: in 1895, 98 % of reported peppered moths in Manchester were black. The shift from being extremely rare to becoming the default variant baffled naturalists and gave rise to the hypothesis that the black morph could survive better in polluted forests near cities due to the darker coloration of the tree bark. Such a case study fitted Darwin’s ideas of natural selection perfectly and rapidly became a text-book example.
To date, several repeated experiments have confirmed that the black variant of the peppered moth survives better in polluted forests, while white morphs have an advantage in clean forests where white-coloured lichens thrive and cover the tree stems. When releasing and tracking a population of moths in both types of forests, one can witness the frequencies of each variant shifting towards fixation or extinction throughout the generations. What’s even more fascinating about this case, is that scientists have discovered the underlying genetic basis of morph changes: the black morph is caused by the insertion of a transposable element in a regulatory gene. A transposable element is a piece of DNA that can ‘cut-and-paste’ itself in and out of the genome at different positions. For a long time, it has been speculated that transposable elements have played a role in the evolution of many species, and the story of the peppered moth is a fabulous example of how a random mutation like that, by total coincidence, helped the species adapt to its urbanized environment. Additionally, it has been estimated that this mutation occurred as late as the early 19th century, which demonstrates how much faster evolution can occur than we usually think.
Genetic map showing the presence of a transposable element (yellow bar) in a regulatory gene in the black peppered moth. This insertion is absent in the white morph and probably disturbs a pigmentation pathway, causing the moths to be completely black. From Van't Hof et al. 2016 (See Further reading).
The peppered moth is not the only animal that has evolved to survive in urbanized areas. The common blackbird, whose melodic song can be heard from every European rooftop in the early summer morning and late afternoon, thrives in cities like nowhere else. In gardens, blackbird nests occur with densities ten times higher than in their original habitat, woodlands. The urban success of the blackbird has led to numerous changes in its behaviour, for example in its daily rhythm (urban birds start singing earlier in the morning), singing pitch (urban birds sing louder and at a higher pitch), and migration pattern (male urban birds migrate less and tend to adopt a sedentary lifestyle, while woodland birds overwinter in North-Africa and the Mediterranean). For the latter trait, studies have found indications that these changes have a genetic basis: by hand-raising chicks from both urban and woodland populations in a controlled, identical environment[3] and measuring their migratory behaviour, scientists observed that the reduced migration of urban male birds is innate. This means that the trait is at least partially genetically determined (though early processes in the development of the embryo could also have played a part). Urbanized areas offer a more abundant and constant source of food than seasonally fluctuating woods do. This might make migratory behaviour disadvantageous over staying in the city, as those who don’t migrate get a head start in the mating season. A study found that birds who stay tend to develop their testicles earlier, which results in a longer breeding season. This in turn means that they have more chances to produce offspring, resulting in an increased fitness. Once again, the blackbirds show that through natural selection, nature can make a city its home and even benefit from it.
Also in the world of plants, signs of adaptation to urban environments have been picked up by evolutionary biologists. One important effect of cities, especially for plants, is the fragmentation of their habitat. Plants need good soil to germinate and use different strategies to disperse their seeds, but these are costly[4]. In a city where small patches of earth are surrounded by concrete wastelands, it might be disadvantageous to keep up seed dispersal, since there’s a high change of seeds ending up on impenetrable ground.
In Montpellier, France, a group of researchers studied patterns of seed dispersal of the weed Crepis sancta. They studied plants that grew in the crevices of sidewalks or around lone trees within the city and showed that in such circumstances, dispersing seeds had a 50 % lower chance of settling and germinating out of the motherplant’s reach than non-dispersing seeds that settled near the motherplant. The researchers did a common-garden experiment where they grew urban and non-urban plants in the same conditions, and showed that, although the different plants had grown from seed to adult in the exact same, neutral environment, plants of urban origin tended to lack seed-dispersal strategies compared to plants with non-urban roots. This is direct proof that the absence or presence of seed dispersing strategies is genetically determined in this weed and have potentially been directed by natural selection to adapt to a more fragmented habitat. Lastly, the researchers applied theoretical models to the data and predicted that the shift from dispersing to non-dispersing seeds occurred in only a few generations, once again demonstrating what fast rates of evolution can be triggered by urban environments.
Left: A male eurasian black bird (Turdus merula). Right: The weed Crepis sancta, flowering.
These three examples, together with a long list of other similar cases, illustrate how nature manages to cope with the new, quite extreme pressures involved in settling in the city. Although it’s sometimes hard to believe when you walk down a concrete street with not a single tree on it, nature is adapting to this man-made environment and slowly conquering it by means of natural selection. Yet, as we saw in a previous article, there are three other forces that drive the evolution of species: mutation, drift and migration. How do these play out in the urban environment? Do cities drive such processes differently from other habitats?
Mutations oil the evolutionary machine: they generate new variations that feed into other processes such as selection and drift. Mutations occur randomly as mistakes are made when DNA is copied in an organism’s cells. Yet, the rate at which mutations occur varies across species and can be influenced by external sources. Could urban environments increase mutation rates, for example because of higher concentrations of mutagens due to pollution? Possibly, but there is at the time not enough proof for that. The story of the peppered moth seems to hint in that direction, since the mutation that gave rise to the black morph occurred very recently, after the onset of pollution. It has been shown that air pollution can increase mutation rates in animals, but whether these increases are evolutionarily significant and inherently bound to cities is unknown. In many other cases of urban adaptation, for example in the blackbird, it has been shown that the selected mutations were already present in the species long before it settled and adapted to cities[5].
We also have to consider the random aspect of evolution: genetic drift. After all, the evolutionary course of a species or population is not only determined by the adaptive force of natural selection, but also by arbitrary events or changes in the environment, such as the rise of a sudden barrier which splits a population in two, or the occurrence of a natural catastrophe which eliminates most of the population. Urbanization often leads to similar dramatic changes and – at least from nature’s point of view – quite arbitrary divisions in the landscape. The outcome is a perturbed and randomly fragmented habitat, with plants and animals becoming limited to a few disconnected green spaces such as parks, cemeteries and gardens. In other words, urban populations of plants and animals are being strongly reduced in numbers and isolated.
Apart from fragmentation and isolation, city landscapes also deal with a different form of population dynamic: colonisation. As soon as a new, empty habitat arises, innovative and opportunistic species will settle in small colonies. This is the case, for example, with red foxes and blackbirds invading European cities. Both the new colonies and old fragmented populations will suffer from the effects of isolation and reduction: since these populations start out with only a small subset of the genetic variation of their original populations, they will have a reduced genetic diversity. Because mutations occur at a low rate, it takes very long for these new, small populations to recover the genetic diversity of their original population. Migration, an evolutionary force which could increase genetic diversity by bringing in individuals from other populations, is probably also inhibited due to physical barriers in the city. The resulting reduced genetic diversity makes populations more vulnerable to dramatic changes in their environment - which tend to happen frequently in the city - as natural selection will only have a limited repertoire of genetic variations to choose from. The chance of an adaptive variation existing purely by chance in a small population is very tiny, which reduces the species’ ability to adapt. So, it looks like settling in an urban environment is a bit of a gamble: some species will be successful and adapt rapidly to their new habitat, but for others the bar is set too high. Yet, it is quite clear from previous examples that many, rather innovative species can overcome these difficulties and settle in cities.
On the other hand, the decrease of migration and increase in drift can considerably accelerate the process of evolution and even lead to speciation, as populations differentiate more quickly. A good example of this is the rise of the London Underground mosquito. Mosquitoes invaded the London tube before the Second World War and became completely isolated from their above-ground relatives. Over the decades, they have diverged so much that they can no longer reproduce with above-ground individuals and are even being considered as a different species or subspecies by some scientists. It thus seems that the combination of strong genetic drift, isolation and natural selection can, at least in genetically robust species, lead to the introduction of plants and animals to the city and possibly even to the creation of new, urban species.
The predicted effect of urbanization on wild populations along an urbanization gradient: due to stronger isolation and a more dynamic environment, populations become smaller and more disconnected from each other, which leads to a reduction in genetic diversity. This, in turn, accelerates genetic differentiation between populations. This image is slightly modified from Johnson et al. (2017) (See Further Reading).
Although cities seem exempt of and unattainable for nature at first sight, all of these examples clearly show the very opposite: cities are fantastically dynamic hotspots of evolution and offer risky but attractive opportunities to the animal and plant species which have what it takes to colonize them. The evolutionary dynamics steered by such a young and rapidly changing environment offer one of the most exciting opportunities to study fast and extreme evolution and show once again how versatile and resilient nature can be. One can choose to see a city as a barren, sterile world made of concrete, but it is in fact a place where life thrives in a most unique and diverse way.
Even more exciting than the fact that one can witness and study amazing cases of evolution in the city, is the fact that we can use the knowledge scientists are gathering on how species evolve and adapt to it, to make cities a more natural, self-sustainable and green place. Initiatives are being taken in many places by scientific institutions, citizens, or governments to make the city a more welcome place for native animal and plant species that are maybe not as strong colonizers as blackbirds and foxes. Natural history museums and botanical gardens around the globe try to educate citizens on native plants and encourage them to grow them in their gardens, citizens build insect hotels in parks and in their streets to stimulate pollinator densities and some governments take greenery more and more into account in city planning. Just the examples of the metamorphosizing peppered moth, the sedentary blackbird, the London Underground Mosquito and the non-dispersing Crepis sancta weed give us a lot of insight on how we can plan and organize our cities so that even more species can settle in it and co-exist with us in a delicate, but healthy equilibrium. Of course, there’s still a lot to do to make our cities a greener place. Yet, to know that that so many exciting opportunities to improve our cities will arise from studying the natural course of evolution in urban environments, is undoubtedly a thought full of hope.
[1] This hypothesis is already built on the theory of natural selection, with the “un-fit” black moths naturally contributing less to the next generation due to higher rates of predation, which leads to their extremely low frequency in the population.
[2] The reason why pollution leads to dark-coloured trees is because light-coloured lichens, which feed on particles in the air and cover the trees in pure forests, die from certain gas emissions such as sulphur dioxide.
[3] This is a classical way of testing whether a trait is determined genetically and is a standard experiment in evolutionary genetics. It is commonly known as a “common-garden experiment”.
[4] They are costly in the sense that the plant has to invest resources and energy into producing the necessary organs or structures for such strategies to work, such as tasty fruits or sticky seeds that animals carry with them.
[5] Such “background” genetic variation which is accumulated over the ages in organisms without having a direct adaptive role is called “standing variation” and seems to often play a much more important role in adaptation than new mutations.
For further reading:
A scientific review summarizing previous studies on urban evolution, with a discussion on the role of every evolutionary force in the city and the possible applications of urban evolution :
Johnson, M. T., & Munshi-South, J. (2017). Evolution of life in urban environments. Science, 358(6363), eaam8327.
Scientific paper reporting a transposable element as the genetic cause for the black morph of the peppered moth:
van’t Hof et. al. (2016). The industrial melanism mutation in British peppered moths is a transposable element. Nature, 534(7605), 102.
Scientific paper reporting potentially adaptive changes of migratory behaviour in blackbirds:
Partecke, J., & Gwinner, E. (2007). Increased sedentariness in European blackbirds following urbanization: a consequence of local adaptation?. Ecology, 88(4), 882-890.
Scientific paper on the rapid evolution of seed dispersal in urban populations of the Crepis sancta weed.
Cheptou, P. O., Carrue, O., Rouifed, S., & Cantarel, A. (2008). Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proceedings of the National Academy of Sciences, 105(10), 3796-3799.
Scientific paper on the London Underground mosquito and its reproductive isolation from above-ground mosquitoes:
Byrne, K., & Nichols, R. A. (1999). Culex pipiens in London Underground tunnels: differentiation between surface and subterranean populations. Heredity, 82(1), 7-15.
A recently published popular science book on urban evolution:
Schilthuizen, Menno (2018). Darwin Comes to Town: How the Urban Jungle Drives Evolution. Picador USA.
