When ecology graduate student Lindsay Miles visited Las Vegas a few years ago, she had a clear objective in mind. “I’m looking for the really gross, dirty alleyways,” she tells The Scientist. Scouring these alleys after dark, Miles—with a colleague accompanying her for safety—located thin, wispy webs tucked away in concrete nooks and crannies. With great care and a bowl-like scoop, she trapped western black widow spiders (Latrodectus hesperus) clinging to the silk, dropped them into a vial of 90 percent ethanol, and put them in the back of her Jeep Compass.
Las Vegas was just one of the cities in the western United States that Miles visited in 2012 and 2013 on spider-collecting missions. Over a few months, she amassed more than 200 of the highly venomous but reclusive arachnids from these urban environments and from surrounding rural areas, and took...
The black widow spider has recently expanded its range from rocky outcrops scattered in desert landscapes to crevices in modern cities. At the time of Miles’s project, ecological theory predicted that populations of animal species living in the city would likely have lower genetic diversity than those living in rural areas, because urban environments contain roads, buildings, and other physical barriers that can fragment species’ habitats and block dispersal, reducing the circulation of new genetic variants.
But Miles’s analysis, published last summer, revealed that city black widows had more within-population genetic diversity than their rural counterparts, and there was more genetic similarity between urban populations than between rural ones—pointing to greater gene flow among urban arachnids.1
Miles suspects that the differences between the genetic diversity levels of urban and rural populations were driven by genetic drift—the random accumulation or loss of genetic variants in a population—and the greater circulation of such variants by humans in cities than in the desert. Black widows are known to build their webs inside cars parked in urban areas, for example, so it’s possible that “when people drive around, they’re bringing these spiders with them,” she says. This would maintain gene flow among urban spiders while rural populations become isolated, and thus more genetically dissimilar from one another as they evolve in parallel.
Miles’s results illustrate one of the many ways cities are having profound effects on their animal and plant residents. Globally, about 0.5 percent of Earth’s land area is urbanized, including 1.2 percent of North America and 2.3 percent of Europe, according to one 2015 analysis of satellite maps of nighttime light. As researchers are realizing that evolution can, and regularly does, happen at a much faster pace than previously thought—on the order of decades and centuries rather than millennia and eras—they are beginning to observe the effects of this global urbanization on species’ genetic makeup. Biologists now know that cities not only influence factors driving nonadaptive change, via such evolutionary processes as genetic drift and gene flow, but present a suite of special selection pressures for species living there, promoting adaptation too.
The world is full of cities, and for many species, each city is an independent theater of evolution.
—Jonathan Losos, Washington University in St. Louis
The study of this so-called urban evolution “is an area that’s rapidly gaining momentum,” says Marc Johnson, an evolutionary ecologist at the University of Toronto who recently accepted Miles as a postdoc. He and a colleague reported in 2017 that the number of published studies on how species are evolving in the city had more than doubled in the preceding five years.2 Urban environments, he says, are seen by many as an exciting new playground for research into evolution in action.
“From an evolutionary biologist’s point of view, this is a massive, unplanned experiment. . . . It became this idea of a very powerful way to study evolution across the globe, replicated thousands of times.”
Urbanization shapes gene flow
Matthew Combs, a graduate student in Jason Munshi-South’s lab at Fordham University, has spent the past five years exploring how urbanization drives nonadaptive genetic changes in New York City’s second most abundant mammal, the brown rat (Rattus norvegicus).
Munshi-South’s group had previously found that urban populations of white-footed mice (Peromyscus leucopus) were geographically restricted to the city parks, and that mouse populations in different parks were genetically isolated from one another and much less genetically diverse than their rural counterparts.3 The researchers concluded that barriers to gene flow in the form of concrete buildings and roads separating parks are helping to shape these animals’ evolutionary futures. But Combs wondered what the picture would be like for a pest species such as R. norvegicus that, rather than being relegated to green areas, seems quite comfortable in the city’s concrete landscape.
To find out, he recruited a team of undergraduate students and set off with a handful of traps to the northern part of Manhattan in mid-2014. Working south in a series of trips over two years, the trio captured and collected tail tissue from 262 rats—a tiny fraction of the 200,000 to 2 million estimated to live in the Big Apple, but enough to paint a picture of the population’s genetic structure. Back in the lab, Combs analyzed more than 60,000 single nucleotide polymorphisms (SNPs) in the samples, reporting last year that New York’s rat population could be separated into two distinct evolutionary clusters: uptown rats and downtown rats.4
“There seems to be a soft migration barrier within the island of Manhattan,” says Combs. “Uptown and downtown areas are more residential and seem to be better habitat for rats,” whereas Midtown has less food waste and higher tourism and traffic, making the area less rat-friendly. Indeed, while Midtown is no stranger to the odd rodents passing through, it has relatively few resident rats. The uptown and downtown subpopulations that Combs identified were so well-defined that only one animal—Rat 126—bucked the trend, he notes. Found in a trap near uptown in Central Park, Rat 126 had downtown DNA; Combs guesses it was released into the park by someone who’d trapped it downtown but didn’t have the heart to kill it.
Evolution ArenaUrban environments have the potential to influence the evolution of species in numerous ways. Some of these effects are nonadaptive, and are largely driven by changes in gene flow between populations. But others result from selection pressures that are unique to cities, such as greater nighttime illumination and more-extreme temperatures than rural areas. © lUCY CONKLIN
|
Studies that have delved into the population genetics of other city animals have detailed additional ways urbanization can affect gene flow. For example, researchers have linked the prevalence of Barcelona’s parks to increased genetic diversity in urban great tit (Parus major) populations, suggesting that green areas help maintain gene flow between subpopulations in different parks across the city.5 And a study of the common wall lizard (Podarcis muralis) in Trier, Germany, identified multiple urban structures that influenced gene flow, from obstacles such as walls and rivers to facilitators such as urban vineyards.6
Whatever the dynamics of the effect, these results are helping to confirm that the structure of city environments has profound evolutionary implications for its inhabitants. “The specifics will vary from species to species,” says Luc De Meester, an evolutionary ecologist at the Katholieke Universiteit Leuven in Belgium. “But there are generalities.” While most research has focused on species of conservation concern, “even species that tend to be abundant . . . are very strongly impacted by city life,” he adds.
Given this potential for urbanization to influence the genetic structure of populations, some researchers have posited that cities could act as hotspots for the evolution of new species. Especially in small or fragmented populations, the breakdown of gene flow can help promote speciation. “It’s a tantalizing idea,” says Munshi-South. But there’s a long way to go before scientists can point to a specific case with certainty, he says. “Even in the few cases that have been talked about as potential examples of urban speciation, there are a lot of unresolved questions.”
From an evolutionary biologist’s point of view, this is a massive, unplanned experiment.
—Marc Johnson, University of Toronto
In one famous example from 1999, researchers in London published data that seemed to show that mosquitoes living in the city’s subway had genetically differentiated from street-level insects.7 Crossing aboveground and belowground mosquitoes didn’t produce viable progeny in the lab beyond one generation, they observed. But a subsequent analysis found that the subterranean mosquitoes had likely originated not from local northern European mosquitoes, but from a population in southern Europe that has since been found in other subway systems, implying that London’s underground mosquitoes hadn’t diverged from the aboveground locals after all.8
While concrete evidence of urban speciation is lacking, some researchers think that cities may provide an especially interesting setting for the process to occur. Johnson points to some intriguing hints that cities may increase the rate of genetic mutations, potentially accelerating the divergence of separated populations. In 1996, for example, researchers at McMaster University in Canada reported that herring gulls living near polluting steel mills had a higher mutation rate than the general population.9
Subsequent experiments from the same lab showed that pollution—specifically, airborne particulate matter—elevated the mutation rate in lab mice.10 “Amazingly, no one has followed up on that,” says Johnson. “I think this is one of the most important and fundamental gaps in our knowledge about how urbanization is influencing evolution.”
Species adapt to city life
Beyond provoking nonadaptive genetic evolution of the sort studied by Miles and Combs, urbanization presents a set of predictable environmental stressors that potentially act as strong selective pressures on specific parts of genomes—a phenomenon that researchers have only begun exploring in cities relatively recently. Increased light pollution may select for genotypes conferring lower light sensitivity, for example, while abundant food waste could select for particular metabolic traits. (See sidebar below.) And increased temperatures—the urban heat island effect—could select for higher heat tolerances.
See “The Vanishing Night”
Case Western Reserve University evolutionary ecologists Sarah Diamond and Ryan Martin have explored the effects of urban heat on acorn ants (Temnothorax curvispinosus) living in and around Cleveland, Ohio. In 2017, the pair reported that urban ants were more heat tolerant and less cold tolerant than their rural counterparts—an effect that was present even when rural and urban populations were raised at the same temperature.11 The results of this so-called common garden experiment indicate that the differences are heritable, lending support to the idea that the city-dwelling insect populations had adapted to the warmer urban environment.
Common garden experiments with the water flea (Daphnia magna) have uncovered similar signs of adaptation to city temperatures. As part of her PhD work in De Meester’s lab, ecologist Kristien Brans found that water fleas living in Brussels had a higher heat tolerance—by up to 2 °C—than Daphnia living in cooler countryside ponds.12 And an analysis of differences in physiology and life-history traits revealed that city water fleas consistently showed higher resistance to stressors such as pollution than their rural counterparts did—another indication that Daphnia may be adapting to its urban digs.13
To conclusively demonstrate that such traits are outcomes of natural selection, researchers need to understand the genotypes underlying apparently adaptive phenotypes. White clover (Trifolium repens), a small perennial plant, is a good model in this respect, says Johnson. Its ubiquity across most of North America reduces the impact of nonadaptive evolutionary processes such as genetic drift that can drive changes in smaller populations. And it possesses a well-described Mendelian trait that happens to be heat-sensitive: the production of hydrogen cyanide (HCN) in response to herbivory. HCN makes plant tissue particularly vulnerable to cold damage, so Johnson and then University of Toronto master’s candidate Ken Thompson hypothesized that populations adapting to urban heat islands, where temperatures are generally warmer, would have higher frequencies of HCN-producing plants than rural populations.
But clover collected along urban-rural transects in Toronto, Boston, and New York City told a different story. “It was the exact opposite,” says Johnson. “Rural areas had the highest [frequencies] of hydrogen cyanide, and urban areas had the lowest.” Herbivory levels were too similar to explain the difference in HCN production, the team observed. It wasn’t until the researchers directly measured the ground temperatures along the transects that they realized what was going on. All three cities have snowy winters, Johnson says, but snow in the city usually melts or is removed during the day, meaning that when the sun goes down, ground temperatures drop much lower than they do in the countryside. Lacking the snowy “thermal blanket” enjoyed by their country cousins, urban plants at soil level were in fact the ones experiencing frostier conditions.14
The team subsequently showed that populations of clover along urban-rural transects had similar genetic diversity and high gene flow, indicating that the change in allele frequencies is likely the result of natural selection rather than genetic drift. That makes it a true example of urban adaptation—but to cold rather than to heat islands.15 Johnson has now launched the Global Urban Evolution (GLUE) project to study the plant species’ evolutionary responses across more than 180 cities worldwide.
Future research is likely to produce more of these results, notes Diamond. “The field is young, so we’re still at the stage of transitioning from descriptive, ecological work to more mechanistic, evolutionary work,” she says. “It will be important for us in the future to figure out exactly what’s driving what.”
City Eats© ISTOCK, DAHRS Compared to raccoons (Procyon lotor) in rural areas or in the city zoo, Toronto’s street raccoons are bulkier—some being almost a meter long and weighing up to 15 kilograms (33 pounds). Last summer, researchers documented signs of hyperglycemia in city populations of the nocturnal animals, a condition not observed in rural raccoons (Conserv Physiol, 6:coy026, 2018). The likely cause: a diet of high-fat, sugary food from the city’s garbage cans. Researchers have also reported diet changes in other urban mammals, birds, and even some invertebrates. A 2015 study found that Manhattan’s pavement ants (Tetramorium sp.) showed isotope signatures in their tissues consistent with increasing consumption of human fast foods (Proc R Soc B, 282:20142608). Researchers are now beginning to work out how these changes affect species in the long term. A recent study on house sparrows (Passer domesticus) suggests that urban living has led to strong positive selection at AMY2A, a gene that produces amylase and is associated with high-starch diets in humans and dogs (Proc R Soc B, 285:20181246, 2018). And Jason Munshi-South, an evolutionary biologist at Fordham University, and colleagues have identified signs of selection in white-footed mice (Peromyscus leucopus) at loci associated with lipid and carbohydrate metabolism—indicating that dietary adaptation may be occurring in urban populations of this species, too (Mol Ecol, 26:6336–50, 2017). City conditions could favor “self-domestication” of urban animals, Munshi-South notes—much as early man’s trash heaps are thought to have encouraged the domestication of dogs’ wild ancestors. But the ecosystem-wide effects of large-scale dietary adjustments are generally unknown. “What happens when lots of species suddenly shift to a very unique diet that humans have been able to provide?” he says. “That’s a really interesting phenomenon [in cities] that isn’t really happening anywhere else.” |
How general is urban evolution?
As case studies accumulate, researchers are beginning to take advantage of the nature of urban environments to look for patterns that might reveal underlying urban evolutionary principles. “The world is full of cities, and for many species, each city is an independent theater of evolution,” says Jonathan Losos, an evolutionary biologist at Washington University in St. Louis. “That allows us to test, to my mind, one of the great questions of evolution, which is how repeatable or predictable it is. Does evolution, when faced with the same circumstances, follow the same course?”
It’s a tricky question. For starters, it’s challenging to quantify how aptly cities serve as experimental replicates—particularly when researchers don’t fully understand which factors are most important in driving a particular urban species’ evolution. And the urban-rural divide often isn’t clear-cut, notes De Meester. Some cities are more developed than others, and many are making deliberate attempts to increase urban biodiversity via the construction of parks and other green areas. Even “rural” environments vary from pristine wild habitat to managed agricultural land.
Nevertheless, several groups have started multicity projects. Combs and colleagues recently expanded their rat research beyond New York, for example, and encountered similar effects of resource-sparse areas like Midtown on populations in New Orleans; Vancouver, Canada; and Salvador, Brazil.16 Miles, meanwhile, found that populations of black widow spiders in Las Vegas and Phoenix showed much higher genetic diversity than those in Albuquerque. What’s more, the two more-diverse populations were more genetically similar to each other than either was to the Albuquerque spiders.17 Those differences are likely driven by human transport networks across the western United States that also end up ferrying spiders, says Verrelli, and highlight the importance of thinking about cities as nodes of a larger network. “It’s really going to become about how you’re connected,” he says, “not about whether you’re in a city or noncity.”
Diamond’s group also uncovered regional differences when it expanded its study of adaptive evolution in acorn ants. As in Cleveland, ants from Knoxville, Tennessee, had higher heat tolerances and lower cold tolerances than their rural counterparts. “But Cincinnati really threw us for a loop,” Diamond says. There, the ants “didn’t show any differentiation in heat tolerance, and they actually showed the reverse trend for cold tolerance.” The results could mean that selection pressures for thermal tolerances differ across cities, or that something other than natural selection is helping to drive the evolution of the trait.18
It will likely be several years before this research is expanded beyond single-species case studies, says Munshi-South, and longer before researchers can answer the question of whether urban evolution follows general principles. But the importance of understanding the mechanisms behind evolution in urban species already extends beyond evolutionary biology. Organisms living in cities are usually the most likely to come into contact with humans, so ways in which urbanization affects their evolution may indirectly influence human health.
“We’re starting to see a lot more species coexist with humans,” says Munshi-South. With that, “there’s the potential for the mixing of diseases.” The white-footed mouse populations that he studies, for example, are important hosts for black-legged ticks, which carry the bacterium Borrelia burgdorferi—the cause of Lyme disease. “Urban public health and zoonotic disease is going to be a huge field moving forward.”
References
- L.S. Miles et al., “Urbanization as a facilitator of gene flow in a human health pest,” Mol Ecol, 27:3219–30, 2018.
- M.T.J. Johnson, J. Munshi-South, “Evolution of life in urban environments,” Science, 358:eaam8327, 2017.
- S.E. Harris et al., “Urbanization shapes the demographic history of a native rodent (the white-footed mouse, Peromyscus leucopus) in New York City,” Biol Lett, 12:20150983, 2016.
- M. Combs et al., “Spatial population genomics of the brown rat (Rattus norvegicus) in New York City,” Mol Ecol, 27:83–98, 2018.
- M. Björklund et al., “Genetic differentiation in the urban habitat: the great tits (Parus major) of the parks of Barcelona city,” Biol J Linn Soc, 99:9–19, 2010.
- J. Beninde et al., “Cityscape genetics: structural vs. functional connectivity of an urban lizard population,” Mol Ecol, 25:4984–5000, 2016.
- K. Byrne, R.A. Nichols, “Culex pipiens in London Underground tunnels: differentiation between surface and subterranean populations,” Heredity, 82:7–15, 1999.
- D.M. Fonseca et al., “Emerging vectors in the Culex pipiens complex,” Science, 303:1535–38, 2004.
- C.L. Yauk, J.S. Quinn, “Multilocus DNA fingerprinting reveals high rate of heritable genetic mutation in herring gulls nesting in an industrialized urban site,” PNAS, 93:12137–41, 1996.
- C.M. Somers et al., “Reduction of particulate air pollution lowers the risk of heritable mutations in mice,” Science, 304:1008–10, 2004.
- S.E. Diamond et al., “Rapid evolution of ant thermal tolerance across an urban-rural temperature cline,” Biol J Linn Soc, 121:248–57, 2017.
- K.I. Brans et al., “The heat is on: Genetic adaptation to urbanization mediated by thermal tolerance and body size,” Glob Change Biol, 23:5218–27, 2017.
- K.I. Brans et al., “Urbanization drives genetic differentiation in physiology and structures the evolution of pace-of-life syndromes in the water flea Daphnia magna,” Proc R Soc B, 285:20180169, 2018.
- K.A. Thompson et al., “Urbanization drives the evolution of parallel clines in plant populations,” Proc R Soc B, 283:20162180, 2016.
- M.T.J. Johnson et al., “Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens),” Proc R Soc B, 285:20181019, 2018.
- M. Combs et al., “Urban rat races: spatial population genomics of brown rats (Rattus norvegicus) compared across multiple cities,” Proc R Soc B, 285:20180245, 2018.
- L.S. Miles et al., “Urban hubs of connectivity: contrasting patterns of gene flow within and among cities in the western black widow spider,” Proc R Soc B, 285:20181224, 2018.
- S.E. Diamond et al., “Evolution of thermal tolerance and its fitness consequences: parallel and non-parallel responses to urban heat islands across three cities,” Proc R Soc B, 285:20180036, 2018.