The City as an Evolutionary Hothouse—The Search for Rapid Evolution in Urban Settings

Abstract

Cities are ubiquitous and, though a novel phenomenon by evolutionary standards, provide a home for many species and exert particularly strong and novel selection pressures on them. They thus offer a unique opportunity to study rapid evolutionary processes. We conducted a scoping review of published studies documenting evolutionary processes in urban environments, focusing primarily on more recent work. Unfortunately, cities have not been attractive environments for biological research and thus remain poorly studied, despite slowly growing interest in recent years. Nonetheless, we found studies documenting the effects of mutation, genetic drift, and selection in cities. However, studies show some geographic bias and were not always as conclusive as might be desired. There is even support for incipient urban speciation. Evidence across the board is less abundant and less conclusive than desirable, suggesting the need for more data collection. The urban setting, with its stronger selection, more common intermixing, and abundance of both human and widespread potential non-human zoonosis hosts and human-associated species offers great opportunities to further document evolution in action and explore its conservation implications.

1. Introduction

Speciation is a gradual process whereby one genetic stock splits, over time, into distinct forms. The rate at which this occurs primarily depends on the strength of selection and the amount of internal and external gene flow (e.g., [1]). In nature, weak or fluctuating selection, large population size, and ongoing gene flow among differentiating forms can make the process slow. For example, the split between polar bears (Ursus maritimus) and brown bears (U. arctos) progressed over roughly 500,000 years, with repeated admixture occurring [2]. Similarly, frog lineages gradually evolved genetic incompatibilities, leading to reproductive isolation over the course of about six million years [3]. Holliday (2006) reported a benchmark of speciation for medium-sized mammals of at least 1.4 million years [4]. Human evolution has also played out over several million years [5,6]. When we think of evolution, this is often the time scale that comes to mind. However, there are also examples of evolution occurring over much shorter periods. For example, Grant and Grant (2006) were able to illustrate the evolutionary response of Darwin’s finches (Geospiza fortis) to natural selection in the Galápagos over only a few years [7]. As Darwin (1868) first pointed out, the process of speciation can be vastly sped up in human-dominated environments [8]. Strong selection, as occurs during both domestication and feralization [9], can result in diversification within a few generations (e.g., [1,8,10]). Limited gene flow among populations or a small population size reducing the potential for genetic mixing can also speed up the process. And, intentionality is not necessary for evolution to occur in human environments. For example, Howe et al. (2024) showed that being raised in a fish hatchery led to what they termed “domestication selection” in Chinook salmon (Oncorhynchus tshawytscha) [11]. All those conditions occur in urban environments, perhaps the most human-dominated non-captive setting experienced by most species. Urbanization is also a relatively recent and geographically uneven phenomenon [12,13], allowing ongoing evolution to be studied directly [14,15]. Yet, despite the extensive theoretical understanding of population genetics and growing prevalence of urban environments (e.g., [16]), relatively little research has looked at evolution in cities [17,18]. Here, we review the existing literature, emphasizing more recent work, and identify both emerging insights and apparent needs for further research.

Traditional approaches to evolution, however, are of limited help in the context of research on urban evolution. Dramatic environmental transformation within a very short period of time, rapid adaptation to novel environments, and the origin of novel phenotypes through transgressive hybridization between native and introduced taxa and other phenomena assume greater importance. The overall goal of this paper is to reflect on the current state of the art of urban evolution research, a field which has had growing but still insufficient attention. We included a wide range of topics, using examples from microbes to humans in a range of geographical regions and environments. We conducted a scoping review, combining a search of the current literature using Google Scholar and Web of Science, searching backwards to examine relevant references cited by the found studies, and forward examinations of studies citing previous work identified as relevant. By providing this wide scope, we hope to bring insight and provide substantial arguments for the need to conduct more studies on evolution in action in urban settings.

2. Urbanization as an Ecological Phenomenon and a Conservation Concern

We often think about human presence in general, and urbanization in particular, as affecting ecological processes and having negative conservation impacts [19]. For example, Roque et al. (2024) showed that even relatively sparse human settlements had strong negative effects on the presence of large herbivores in the Limpopo National Park in Mozambique [20]. In non-urban settings, rapid evolution can stem from limited anthropogenic change [21,22]. In the more human-crowded urban setting, McDonald et al. (2020) reviewed almost 1000 studies of ecological impacts [16]. Many species simply avoid areas where humans are present [23] or modify their behavior to allow coexistence [24,25], but some taxa are actually attracted to anthropogenic influences [20]. For plants, urbanization can decrease the availability of needed pollinators [26]. It can also affect the soil biota [27], important or even essential for plant growth and reproduction [28]. Certain species, described as “winners”, are better able to tolerate human presence than others (“losers”, a roughly similar proportion; [29]). A species becoming an urban dweller may simply be responding to conditions resembling those under which it evolved [30].

Just as impacts vary among species and settings, so do the mechanisms leading to them. For example, predation by domestic cats (Felis sylvestris f. catus) is an important cause of urban bird declines (e.g., [31]). Birds can also be negatively affected by ambient noise, at least partially because it interferes with their vocal communications [32]. Urbanization thus creates a new biological milieu for species, for example by removing predators they coevolved with, adding unfamiliar competitors, or forcing changes to migration patterns [33]. While the urbanization process was previously viewed almost exclusively as a threat scenario for biological diversity, this perception is changing and the ecological value of urban habitats is increasingly coming into focus (e.g., [34]). Overall, however, the effects of urbanization extend beyond the city limit, for example, through agricultural efforts in support of human nutrition in the urbanized areas [16]. Cities and outlying areas are interlinked in important ways. For example, evolutionary change can result from human-caused changes related to urbanization, such as the use of salt to keep roads ice-free or changes in thermal regimes, even outside of cities (reviewed in [35]).

As time and urbanization progress, they result in the loss of some taxa originally found in an area (Figure 1, left). At the same time, non-native species arrive via pet trade, ornamental plant trade, and other economic activities (Figure 1, center; [36]). As the process continues, a new biota emerges, comprising some remnants of the original biodiversity and an increasing number of non-native arrivals (Figure 1, right) that are initially contained in small areas; become more broadly distributed over time; and may eventually be invasive and damaging to the local ecology, economy, or both. All of these are important issues that are receiving increasing attention.

3. Urban Generalists, Specialists, and Invaders: Different Settings for Evolutionary Processes?

Some species have coexisted with and benefited from the proximity of humans for thousands of years. This is expressed in some common names: house martin (Delichon urbicum), house sparrow (Passer domesticus), and house mouse (Mus musculus). We tend to consider anthropogenic environments as the main habitat for these species. But, cities host many species, particularly within and around urban green spaces [34]. While some of these are synanthropes shared in many cities across the globe, cities also offer important refuges for species that are becoming rarer in the rural landscape as a result of the increasing intensification of land use and agricultural practices [37]. In addition to bird species that typically occur in insect-rich, open grasslands or in semi-natural forests with appropriate nesting opportunities (Figure 2), there are numerous other examples of specialized species that are increasingly occurring in urban habitats. The city of Berlin in Germany, for example, features European otter (Lutra lutra) and beaver (Castor fiber) [38]. European hares (Lepus europaeus) are increasingly colonizing urban areas while disappearing from farmland in Denmark [39]. Tawny owls (Strix aluco) manage to utilize the minimal forest structures present in urbanized areas in Spain [40]. The spot-bellied eagle-owl (Ketupa nipalensis) can be found in Bharatpur Metropolitan City, Chitwan, Nepal [41] and forest red-tailed black cockatoos (Calyptorhynchus banksia) occur in urban areas in Australia [42]. Thus, cities host both extreme generalists and more fastidious native species. The adjustment may include learning, habituation, and acclimatization processes on the one hand and evolutionary change based on genetic mechanisms on the other [43].

Generalists, specialists, and invasive species may face different evolutionary scenarios [44]. For example, phenotypic plasticity might allow exploitation of diverse environments regardless of where it evolved and might be more likely to emerge in homogeneous environments [45]. In the urban context, human-tolerant generalists should be more tolerant of environmental homogenization, compared to specialists with their narrower niche breadth. For example, generalist butterfly species are less affected by advancing urbanization [46] and might therefore be under weaker selection pressures. Generalists might therefore be expected to increase in urban settings, as has been reported by Clavel et al. [47]. Alternatively, environmental heterogeneity [48] might encourage and favor the evolution of specialists [49], or the degree of within-generation variation might determine whether generalists are favored [50].

Often, non-native species end up outnumbering urban natives, creating an artificially inflated “biodiversity” (e.g., [51]). Similarly, the biota of cities around the world are becoming increasingly similar, even within groups such as archaea and fungi that are not intentionally trafficked and most urban residents do not notice [52]. The role of evolution in invasion of and dispersal from urban areas has not been thoroughly studied [53], and the process of non-native arrival and spread in urban setting is likewise poorly explored [54,55]. We do know that cities are common entry points for invaders, often through the pet or ornamental plant industries. We also know that cities serve as stepping stones, such that once a species has adapted to an urban setting included in or nearby to its native range, it has “preadaptations” that help it in a non-native city it is secondarily transported to [53]. Such adaptations as tolerance of human settings may also make a non-native species successful in spreading out of the city it initially arrived in or create the setting for additional evolution as it becomes feralized [9]. For example, the cabbage white butterfly (Pieris rapae) evolved larger wings in urban settings [56,57], and these can aid in dispersal not only within a city but also in further dispersal. Importantly, the physical structure of a city and the dense network of roads connecting it to the outside world makes dispersal of non-natives especially likely [58]. Conversely, traffic leads to road mortality or simple avoidance by multiple species, reducing genetic connectivity in even relatively large and mobile ones such as bobcats (Lynx rufus [59]). Species that are common but native generalists, perhaps even pests, in one setting have the potential to become invasive elsewhere. Once they are in a novel environment, their potential for evolution may be especially large [53,60].

Ultimately, a better understanding of how organisms evolve in urban settings is critical for better management of the risks posed by potential or realized urban invaders. However, a global systematic review of the genetic, morphological, physiological, and behavioral changes occurring in sciurid in response to urbanization [61] found no consistent pattern of changes over a rural–urban gradient. Rather, the direction of changes appears to be species-specific, even within this relatively close phylogenetic group. Differences were sometimes even found among individuals of the same species studied in different geographical regions. Thus, different settings might result in even closely related species responding to urbanization in different ways.

4. Urbanization as a Driver of Evolution

Human evolution has been ongoing for millions of years [5,6]. In contrast, urbanization has only existed for a few millennia [13]. Thus, the emergence of cities is a very new phenomenon, though human settlements of various kinds preceded the emergence of cities. Given the usual slow progression of evolutionary processes outlined above, we must assume that the many properties and ecological adaptations of urban species were already developed before human-made structures could serve as a backdrop for evolution. In other words, the existence of houses cannot have played an originating role in the initial evolution of the house sparrow. However, this does not mean that evolutionary processes are not concurrently taking place (e.g., [17,62,63]). However, our understanding of the actual evolutionary pathways experienced by organisms in urban settings is partial. Not surprisingly, perhaps, the term “evolution” does not appear in the index of many urban ecology texts (e.g., [64,65,66]). Others briefly mention that cities create a novel evolutionary landscape [24,67]. In their introduction, Hedblom and Murgi (2017) likewise mentioned that adaptation is one possible explanation for the success of some bird species in urban environments [68]. Later in the same book, Fidino and Magle (2017) stated that “behavioral plasticity alone cannot account for [bird] species persistence” in urban settings but found few concrete examples of studies showing evolutionary mechanisms to point to [69]. Below, we focus on the evolutionary, rather than ecological or behavioral, impacts of urbanization on other species.

Discussions of genetic evolution in the city mostly appeared over the past two decades and especially more recently (Figure 3). Yeh and Price (2004) considered but mostly rejected evolution in studying the settlement of dark-eyed juncos (Junco hyemalis) around San Diego, California, USA [70]. More positively, Shochat et al. (2006) stated that “changes in ecological processes … should alter selective forces in cities, leading to the genetic differentiation of urban and wildlands populations or genetic changes associated with the fragmentation and isolation of wild populations” [71]. Yet, a decade later, Alberti (2015) still complained “we do not know what role human activity plays in the reciprocal interactions between ecological and evolutionary processes” [72], an observation shared by others as well (e.g., [18,73,74,75]). Nonetheless, Alberti (2015) was able to find close to twenty studies and identify a number of evolutionary processes that do occur or might occur in urban plants, invertebrates, and vertebrates [72]. A few years later, Johnson and Munshi-South (2017) were able to document more cases by combining urban evolution of human commensals with that of other taxa [17]. Many of the examples provided by Johnson and Munshi-South [17] came from non-native species, a topic we return to below. Both Johnson and Munshi-South [17] and Thompson et al. [21] discussed the evolutionary mechanisms that might be involved. Below, we provide the background for each of those and then focus on work that has been published in recent years.

4.1. Mutation

Three reasons lead us to expect mutation to be particularly relevant to urban populations. First, because mutation is an uncommon phenomenon (e.g., [76]), a larger population is more likely to see it arise and, if beneficial, spread [77]. In the urban setting, this gives an evolutionary advantage to species that are already common, whether they are native but human-tolerant taxa or, more likely, non-native commensals. Thus, common species already favored by other processes can benefit and become even more widespread if selection (see below) favors newly emerged traits. Second, small populations, which are typical of many urban species, are particularly likely to see deleterious mutations that arise spread because of genetic drift [77]. Finally, exposure to radiation, as occurred following the nuclear accident at Chernobyl, Ukraine, in 1986 and Fukushima, Japan, in 2011, is especially concerning, and there is evidence for increased mutation rates and possibly other evolutionary effects in nearby areas [78,79].

Radiation is not the only mutagen released by human activities [80]. A variety of mutagenic substances are particularly common in cities, especially in their industrial areas [81,82]. Elevated pollution levels in urban areas, for example, can induce DNA damage resulting in increasing mutation rates [83]. Although there is considerable literature on the relevance of urban mutagens to humans (reviewed in [84,85]), studies on impacts in other urban organisms are still relatively uncommon [86]. This is an area that would benefit from additional research.

4.2. Genetic Drift

Small populations are particularly susceptible to the effects of genetic drift (e.g., [87]), and urban populations tend to be small because of increased population subdivisions and higher death rates [88]. They can become effectively smaller as behaviorally reduced mobility sometimes leads to increased sub-population isolation [19]. This kind of bottlenecking can also result in inbreeding and a reduced capacity to genetically respond to novel situations, further reducing population viability (reviewed in [89,90]). This is the case in urban populations of the endangered San Francisco gartersnake (Thamnophis sirtalis tetrataenia [91]) and newly introduced populations of the Asian tiger mosquito (Aedes albopictus) in Russia [92]. Yet, the effects of urbanization on genetic diversity are more diverse than expected, supporting multiple predictions and limiting our ability to generalize [90]. For example, Schmidt and Garroway (2021) found little evidence for it in nineteen amphibian species, and not all studies show evidence of genetic drift in cities [93]. Studying the genetics of urban white clover (Trifolium repens), Johnson et al. (2018) instead found evidence for urban-induced natural selection that “repeatedly drives parallel evolution of an ecologically important trait across many cities” [94]. The effect of urbanization on gene flow, which is closely related to genetic drift, varies greatly among species (e.g., [95]) and urban designs [94].

4.3. Gene Flow

It is common to think of urbanization as a process that reduces gene flow, but other processes, sometimes with conflicting outcomes, are also supported by the data [90]. Not surprisingly, some species that survive in cities find their dispersal limited by various features such as roads, which increase mortality, and avoidance of humans. That is the case in the white-footed mice (Peromyscus leucopus [95,96]). Yet, other species, such as the big brown bat (Eptesicus fuscus) studied by Richardson et al. (2021) in the same location where they studied P. leucopus, do not show such reductions in dispersal [95]. Similarly, Schmidt et al. (2020) found evidence for reduced gene flow in urban mammals but not the more volant birds [97]. Thus, dissimilar taxa residing in the city are differentially affected by urban structure, with varying impacts on their genetics. Urban structures can also enhance gene flow, a phenomenon termed “urban facilitation” [98]. Thaweepworadej and Evans (2023), for example, reported that a newly constructed bridge in Bangkok, Thailand, appears to have increased the hybridization rates of two previously separated squirrel species: Callosciurus finlaysonii and C. erythraeus [99].

The examples above primarily relate to within-city dispersal of species. However, the movement of individuals, and therefore genetic material, into and away from urban areas can have important impacts in several ways. One that might be particularly crucial in non-native species is differential success of lineages in the transportation phase of invasion, which can favor (intentionally or not) particular genotypes prior to arrival and establishment in an urban setting or in the dispersal of species into or out of the city from neighboring areas [53,73]. The high density of roads inside a city and connecting it to outlying communities makes such dispersal particularly likely [58]. But, dispersal into and out of the city also occurs in native species such as the great tit (Parus major), which experienced no genetic bottlenecks in repeatedly moving into cities from adjacent rural area [100].

Another important concern is the flow of “urban” genes out to outlying areas. Most concern about such connectivity issues have involved non-native species dispersing from cities to outlying areas, where they can have negative impacts (e.g., [36]). However, Perry et al. (2006) pointed out that the movement of conspecific island populations among islands, where they have been isolated and slowly diverging, would normally go unnoticed because they are considered to be the same species yet could have negative genetic effects that offset unique and possibly adaptive local characteristics [101]. Whether it is urban-adapted genetics negatively affecting less anthropogenically dominated environments or rural genes slowing adaptations that allow species to survive and thrive in urban settings, such impacts are undesirable. Perry et al. (2006) called for such transfers to be prevented [101], and we think the same concern holds here. Additional research to document the extent of conspecific gene flow between urban and exurban populations is badly needed.

A final issue here is the human-aided dispersal of new species into an urban area and their subsequent actions within it. By bringing together a wide array of native and non-native species, often in close proximity when they are used as ornamentals or occur as pests, urbanization also creates an unparalleled opportunity for evolution through interbreeding, creating novel genetic combinations or new polyploid forms. One of the best-known examples is the cattail Typha × glauca, a hybrid of the North American Typha latifolia and the European Typha angustifolia, introduced to North America [102]. Typha × glauca now dominates in many areas and is especially common in some urban environments, most likely as the result of multiple hybridization events [103,104]. Similarly, two polyploid forms of the genus Senecio were described from urbanized region of England after the native groundsel (S. vulgaris) crossbred with the introduced S. squalidus to form two novel genetic species: S. cambrensis and S. eboracensis [105].

4.4. Selection and Adaptation

Concerns about the evolutionary impacts of pesticides in the United States go back some sixty years. In a report prepared for the White House, its Environmental Pollution Panel (1965) expressed concerns about the evolutionary impacts of pesticide use, which they compared to those of excessive use of antibiotics [106]. They explicitly saw this as an urban, as well as agricultural issue, because of “the encroachment of urban development on agricultural areas” [106] (p. 67). They also expressed concerns about air pollution resulting from inefficient burning of gasoline in urban vehicles [106], now considered an important driver of global climate change [107]. Finally, selection explains the adaptive divergence of acorn ant (Temnothorax curvispinosus) thermal tolerance across an urban–rural temperature cline [108]. Despite these studies, more research was needed “to determine whether severe urban atmospheric pollution might have adverse effects on health” [106] (p. 92). More recently, Janas et al. (2024) found that urban environmental factors, including pollution, affected the coloration of birds [109], a trait under strong sexual selection and by no means the only way or taxon that sexual selection has been detected in the city [110].

Whereas some urban species are relatively long-lived, other taxa have rapid generation times and are more likely to show measurable changes to such toxicants in a relatively short time. For example, water fleas (Daphnia magna) show genetic, physiological, and morphological responses to urban environments, at least some of them in response to environmental chemicals and heat-island effects [111,112,113]. Both novel anthropogenic stressors such as chemical, noise, or light pollution [114,115,116], and the absence of traditional ecological competitors or predators in the biologically modified urban ecosystem can create ecological opportunity for adaptive radiation [117].

Substantial support is claimed for (un)natural selection leading to evolution in urban environments (e.g., [17]). Yet, recent analyses suggest that some of it may be less compelling than we would like. For example, evidence for selection resulting from the radiation released by urban nuclear disasters is not all conclusive [78,79]. Similarly, despite the growth in interest and claims, some observations attributed to selection in urban settings, though suggestive, lack sufficient evidence of selection pressure, genetic response, or improved fitness [118]. For example, we know that urbanization reduces the availability of many pollinators, and we also know that some plants, such as the field bindweed (Convolvulus arvensis), show reduced reproductive success and changes in reproductive activities consistent with an adaptive response [119]. Yet, the underlying genetic mechanism(s) remain unknown [119], leaving cases such as this suggestive but inconclusive. The study of Badyaev et al. (2008) goes a step further [120]. They showed that urban house finches (Carpodacus mexicanus) forage on seeds offered at bird feeders that are different from those available outside the city, providing for strong selection for observed bill traits that allow such seeds to be eaten. Further, urban birds had different songs, presumably because of different bill morphologies, and there was a genetic difference between urban and non-urban populations [120]. While highly suggestive of selection leading to evolution of a distinct urban phenotype, Badyaev et al. (2008) did not show the genetic basis of the morphological differences they documented [120]. Though such studies do not meet the strictest guidelines for identifying urban adaptation, they do provide substantial support, especially in aggregate [48].

Other studies appear more compelling, however. For example, anoles (Anolis cristatellus) subjected to urban heat island effects show greater tolerance to high temperatures than do non-urban congeners. This response arose independently in multiple populations, has a genetic component, and appears adaptive [121,122], thus addressing the concerns raised by Lambert and Donihue [118]. A similar genetic response to urbanization was noted in great tits in multiple European cities [100]. Nonetheless, such detailed examinations remain less common than might be expected [17].

5. Urbanization and Pathogen Evolution

Human residents of early European cities had markedly lower life spans than those of rural areas [123]. Although increases in urban standard of living, sanitation, and medical accessibility have since reversed this trend [124], the underlying mechanisms—greater connectivity and human density in cities—have not changed, and most likely became more extreme in intervening years. As a result, built environment conditions can favor the undesirable emergence and spread of antibiotic resistance [125]; for example. Urban karst groundwater can become an important reservoir for antibiotic resistance [126] and urban runoffs are places of rapid evolution of microbial communities and antibiotic resistant bacteria [127]. Where cities abut animal facilities administering large amounts of antibiotics which are then spread by wind, as is the case in Lubbock, Texas, USA [128], the potential for both zoonotic spillover and emergence of resistance in other species seems high. Once resistant forms arrive, cities, especially megacities, can become incubators for infectious diseases that can rapidly spread to other locations [129,130]. For example, the severity of the COVID-19 pandemic was greatest in countries with large urban populations and the evolution of the pandemic was partially dependent on human population size, since urbanization and high population mobility can enable pandemics [131]. Yu et al. (2021), however, reported that while increasing the density of buildings following urbanization increases the risk of the spread of infectious diseases, this does not necessarily apply to the population increase brought by urbanization [132]. Rather, basic public services such as sanitation that typically co-occur with urbanization can help to lower the risk of the spread of infectious diseases. Much of the work on urban zoonoses has come from the tropics, where more such problems are prevalent [130]. Here, again, however, most of the discussion to date has centered on landscape, ecological, economic, and social predictors, with little attention to evolutionary components.

Of course, not all urban pathogens affect only people, with many unique to other species or using wildlife as reservoirs for viruses that can cause human pandemics [133]. Some diseases are not shared between humans and other species, whereas others, zoonoses, can cross over with some frequency. Of particular concern are “mixing vessel” hosts, such as pigs (Sus scrofa f. domestica), that can simultaneously be infected by two or more viruses capable of genetic reassortment, leading to novel viral genotypes and capabilities [133]. Indeed, urban-adapted mammals are known to carry more zoonoses than non-urban taxa [134]. Thus, urbanization can be a key driver of disease emergence through human exposure to novel, animal-borne pathogens under conditions of high human and commensal densities and close, frequent contact with a variety of potential hosts [133,135]. However, the transmission of parasites from wild animals to humans and domestic animals in urban and peri-urban environments is not well understood [136]. Even less is known about human viruses jumping to non-human hosts [137]. Kürschner et al. (2024) reported that resource asynchrony and landscape homogenization, both common in urban systems, are important drivers of pathogen virulence evolution that results in an increasing frequency of zoonotic disease outbreaks [138]. The biotic homogenization caused by urbanization [139] can help the transmission of pathogens and enhanced evolution of virulence in urban-adapted common hosts [140]. Climate change in general, and the urban heat island effect [141] in particular, may further exacerbate matters. For example, Gusa et al. (2023) examined the effects of heat stress on a pathogenic fungus and found that higher temperatures favor the evolution of the pathogen Cryptococcus deneoformans [142], and Heidecke et al. (2023) speculated that climate change could lead to “[m]ore frequent and intense outbreaks … potentially accelerating the adaptation of the pathogen to novel conditions as well as benefiting the emergence of high-fitness strains” [143]. Moreover, the spread of zoonotic pathogens can also be promoted by changing the gut microbiomes of host species, which might influence pathogen susceptibility [144].

A final note in this context is that the arrival of novel pathogens in the city is not just an opportunity for the disease-causing organism to evolve but also for rapid evolution in the species it affects in its novel habitat (e.g., [35]). This appears to even be true for humans, where genetic resistance to tuberculosis and leprosy is more common in long-urbanized populations [145].

6. Emergence of New Forms under Urbanization

Thompson et al. (2018) defined urban speciation as “the incidental and contemporary evolution of reproductive isolating barriers caused by the environmental conditions associated with urban environments” [21], and we will maintain the same definition here. Many of the processes described above lead to reduced genetic diversity, most often because they constrain the number of individuals in a reproductive constituent. This, the strong selection pressure and presence of known mutagens in the urban environment can lead to rapid evolution and eventual reproductive isolation, as when mating calls and other communications change (e.g., [146]) to the point of incomprehensibility across urban borders. Required, of course, is that such changes, sometimes termed plasticity-mediated speciation [21], have a genetic basis. Ultimately, this could lead to the emergence of novel species that only exist in urban settings, though we are not aware of any such instances being documented to date. There is, however, valid evidence for evolutionary processes occurring under urbanization. Some authors term this phenomenon “microevolution” [147]. Songbirds are a well-studied group of organisms in this regard. A pioneering study by Partecke and others (2006) showed that stressed urban blackbird chicks (Turdus merula) had lower corticosterone levels than stressed blackbird chicks living in rural areas [148]. Numerous other studies have shown a whole range of other physiological, morphological, and behavioral differences between urban and rural bird subpopulations and communities and demonstrated that these differences are partially genetically manifested [100,149]. Accordingly, Winchell et al. (2023) state that urban environments offer opportunities to observe rapid evolutionary change in wild, geographically separated populations adaptively responding to similar selection pressures over rapid evolutionary timescales—they reported genomic parallelism associated with an adaptive morphological divergence in populations of Anolis cristatellus [122]. These authors highlight the “value of urban environments to address fundamental evolutionary questions”. Before reproductive isolation is reached, however, the process can have several important impacts, including magnification of invasiveness [53].

Perhaps the best-known case of postulated urban speciation is the common house mosquito, Culex pipiens. In London, where the world’s first underground system opened in 1863 [150], below-ground populations had since become both mostly reproductively isolated and genetically distinct [151]. However, the two forms do interbreed in places, and the urban origin of the London underground form was made less certain by more recent work [152]. Another well-known novel form is the cattail Typha × glauca, first seen in the Cayuga Lake region of eastern North America [153], where Europeans began arriving in the 1600 hundreds and settled more aggressively in the 1700. Although it has been common to discuss the spread of the form in terms of subsequent dispersal, recent genetic studies suggest multiple local origins instead, as the progenitor species meet often in urban settings [103] and often quite recently.

7. Epigenetics and Urbanization

Combined, studies like the ones listed above make the likelihood of adaptive evolution occurring because of selection in urban environments seem quite intuitive. But, not all change falls under either behavioral or strictly genetic origins [154]. In recent years, there has been growing recognition of the importance of epigenetic changes, which facilitate rapid adaptation by affecting gene regulation and phenotypic plasticity and potentially contributing to evolutionary processes [155,156]. Some epigenetic states are heritable, affecting offspring phenotypes, and could in turn be subject to natural selection. This relatively new perspective is essential for understanding evolution in dynamic environments such as cities.

Empirical studies have suggested or documented significant epigenetic differences between urban and rural populations. As with other issues, the literature on humans is richer than in other species. In an early study, Galea et al. (2011) suggested that epigenetics might explain why mental illness is more common in human urban populations [157]. In Darwin’s finches, Geospiza fortis and G. fuliginosa, on Santa Cruz Island in the Galápagos islands, epigenetic mechanisms likely play a crucial role in rapid adaptation to urban environments [158]. Similarly, the changes seen in great tits (Parus major) across European urban and forest populations showed both genetic and epigenetic modifications [156,159] and a study of the asexual snail Potamopyrgus antipodarum showed differences in methylation levels, indicating epigenetic response, between urban and rural populations in the Pacific northwest of North America [160].

These studies serve as compelling examples of epigenetic variation in populations living under different environmental conditions, including urbanization. They show the ability for rapid genetic-based phenotypic response and for transgenerational plasticity that can help organisms better adapt to rapid, human-induced environmental change [154]. Whereas transgenerational plasticity can be beneficial, however, it may also produce negative outcomes under the rapidly changing conditions typical of urban areas [161].

8. Research Prospects

Cities, because they are relatively new, are highly artificial, and exert particularly strong selection pressures on the species residing in them, are an especially good system for studying evolution in action [14,21,162]. As Thompson et al. (2018) acknowledged, “given the short timespans involved, it is unlikely that cases of urban speciation will be complete” [21] at this time, particularly at relatively young conurbations, but there is now a growing number of convincing or strongly suggestive examples of urban evolution in action. Nonetheless, the easy access to cities leads us to expect more studies. Verrelli et al. (2022) used a questionnaire-based “horizon scan” approach to identify thirty questions for future research [75]. Here, we focus on a subset of those, aggregating some and adding others.

8.1. Where Should We Look?

Perhaps the best chance of documenting more advanced cases of urban evolution should be sought in some of the oldest continuously settled cities [21], especially some of the larger ones. Unfortunately, most have historically only had a modest human population [13] and therefore presumably exerted a relatively small selection pressure until recently. In addition, most studies of urban evolution occurred in the Global North and most often assessed mammals or arthropods in temperate zones [90]. Since locations, species assemblages, and urbanization patterns are likely to affect outcomes, we need more studies that focus on other locations and taxa. New cities in China, many of them now holding many million humans [163] despite being historically much smaller [13], and relatively novel urbanization in countries such as Papua New Guinea [14], seem to be particularly good candidates for such work. Finally, the timing of human arrival in different parts of the world, and the substantial fauna extinctions that often followed fairly quickly, varies by thousands of years [164]. Although urbanization as we define it now did not start immediately, the presence and growth of human population concentrations did. Faunal extinctions and increasing human presence doubtlessly had an ecological impact, but it would be reasonable to expect they would also have increasingly modified the evolutionary landscape that remaining taxa faced. If so, it might be fruitful to search for evidence of such differences, perhaps especially in comparison with Africa, where such extinctions do not appear in the historical record [164,165,166] and where urbanization in its current form is relatively new [167].

There is one another point needing to be made in this context. While it is the metropolises, the capital cities, and economic hubs that each house more than a million residents, particularly in the developed world, that capture the attention of the public, international development efforts, and researchers alike, most people live in secondary cities, typically under 500,000 in size, and often in developing countries [124,168,169,170]. Our understanding of urban biology is thus biased, perhaps in important ways. For example, secondary cities are much more intimately connected with their immediate surroundings than are metropolises or “world cities” [171]. Thus, more attention needs to be paid to processes and species found in secondary cities, particularly in developing countries.

8.2. Which Species Should We Study?

Another possibly underutilized opportunity lies with species that either are not studied in the current context or that are mostly ignored by biologists. For example, there has been much work conducted on the evolution of the COVID-19 virus in recent years, but primarily in the context of human health. We know that much of the early spread of the virus occurred among major global cities, from which it then dispersed into smaller urban areas and then the countryside [172]. But, did the virus mutate more rapidly in cities than would be expected either because of greater transmission among denser host populations or because of greater presence of mutagens? Similar questions can be asked about other novel and otherwise well-studied diseases.

Similarly, urban species perceived as pests—mosquitoes such as the genus Culex and rats (genus Rattus), for example, or sidewalk “weeds”—are mostly studied in the context of pest control, yet some of them have been linked with humanity, and especially cities, for thousands of years (e.g., [173]). Other species, such as many lizards in the genus Hemidactylus and the globally distributed house sparrow, have become so associated with us that their common name and sometimes their scientific name includes the word “house” or “domestic”. In some cases, this association is so tight that knowledge of an organism’s native habitat has been lost. Many are widely distributed around the globe because we serve as vectors for them. For example, house sparrows appear to have emerged and spread in conjunction with the development of agriculture and then spread into human settlements as those emerged and grew [22]. Johnson and Munshi-South [17] (Figure 1) noted that many human commensals—mostly pests—have emerged near urban centers. Some of these species, such as pubic lice (Phthirus pubis), have become so dependent on humans that change in human grooming habits “may lead to atypical patterns of pubic lice infestations or its complete eradication as the natural habitat of this parasite is destroyed” [174]. Some of these species have very short life spans and therefore greater capacity to show evolution in human-measured timelines. Has the city, the main current habitat for such species, provided unique evolutionary opportunities and pressures?

Species associated with humanity offer a particularly promising target for studies of urban evolution. Invasive species offer an especially likely model for rapid evolution [53,175] (p. 5). For example, parrots (Psittaciformes) have been associated with humans for millennia, with introductions documented from over one hundred countries and over fifty reported naturalized populations [176]. Many of the introduced populations occur in urban settings, where their large size, loud vocalizations, and colorful plumage often make them highly visible. Although there is a common core of synanthropic, synurbic species found in many cities around the world [177], each city has its own, unique complement of species created as a consequence of local biodiversity, historical contingency of new arrivals, and ecological interactions among the local biotic and abiotic components over time. Thus, urbanization allows many species interactions to occur that could not happen under natural conditions, and this creates multiple opportunities for species introgression through hybridization (e.g., [104], for Typha × glauca). Thus, repeated urban evolution leading to similar outcomes via hybridization over relatively short time periods—centuries or less—now appears likely.

Finally in this context, organisms found in urban waters seem particularly likely to show the impact of a diverse range of pollution agents [178]. We would expect to find particularly noticeable responses in organisms that live in standing water bodies, such as permanent and playa lakes, where physical pollution buildup is an ongoing process and no flushing downstream is possible.

8.3. Convergent or Parallel Evolution?

Convergent or parallel evolution has long been of interest to biologists. For example, Pianka and Pianka (1970) noted the similarity between the Australian Moloch horridus and the North American Phrynosoma platyrhinos, both dryland lizards with a specialized ant diet and horned skin but members of different families [179]. This instance has often been cited as demonstrating repeated similar solutions arising independently in response to similar selection pressures. Such similarities can arise from the emergence of similar genetic architecture, although they do not have to [180]. In most cases, however, we are left with observing a current similarity as the basis for concluding that disparate taxa responded predictably to similar ecological challenges. Showing genetic similarity underlying the presumed convergence strengthens such inference [180], but laboratory studies of artificial selection show that multiple adaptations can arise in response to similar conditions [181]. Urban environments, hosting an often-similar complement of common species exposed to broadly similar human-created conditions, provide an ideal opportunity to explore this outside the petri dish [18,182]. Indeed, studies reviewed by Santangelo et al. (2020) show that phenotypic and/or genetic parallel evolution was commonly found in studies explicitly seeking it, though relatively few studies encompassed both and some studies found support for neither [182].

8.4. Impact of Biotic Environment

Evolution occurs against a backdrop of biotic and abiotic elements. We therefore expect that the extinction of one species or the addition of an invasive species, especially a strongly interacting one such as a predator will affect the evolutionary trajectory of another [35,183]. Since urban environments are notoriously patchy [184], replicated differences can be found even within a single city. Long-term evolutionary impacts are one of many reasons conservation biologists worry about species extinctions [35]. The altered diversity of the city—sometimes termed xenodiversity to indicate its mostly non-local origin [185]—provides a unique, if somewhat variable, laboratory for examining how the presence or absence of particular taxa and ecological roles can alter the evolution of species. A metacommunity perspective may be needed in such studies [184].

8.5. Importance of Epigenetic

The study of epigenetics is relatively new but shows the potential for rapid phenotypic response that is not based on traditional genetic mechanisms. This can be especially important in the context of rapid, human-induced environmental change such as urbanization or global climate change [154], yet the number of studies of non-human urban responses remains small. The urban–rural divide provides a unique setting to explore epigenetic variations linked to environmental exposures and their impact on diseases. Such research can leverage demographic differences in developing countries to further understand epigenetics in urbanization [186].

8.6. Urban Human Evolution

Cities are built by and for humans. Arguably, though, cities are not optimally designed for their residents, nor are humans perfectly adapted to the habitat we created. For example, depression is more common in some urban than surrounding areas, though that pattern is not universal and access to green space appears to reduce it [187,188]. Moreover, urbanites tend to have fewer children than their rural relatives [189,190]. On the other hand, access to services such as education and health care is often enhanced in urban settings [124]. The literature dealing with human biology (including evolution) and wellbeing is normally quite separate from that dealing with the biology and survival of other species. Yet, the urban setting is habitat for both groups, and some of the literature reviewed above shows that human evolution, just like that of other taxa, may be showing rapid response to this novel environment. Milot and Stearns (2020) found the existing evidence suggestive but insufficient, but studies on this topic are particularly lacking [189]. Research on the human dimensions of urban evolutionary issues, whether related to this or to less personal matters such as identifying the priorities of urbanites in addressing the evolution of other organisms in city environments, also remains deficient [48]. Although we have generally avoided the human literature in this review, we see many opportunities for expanding on it because of the unique features of cities.

A final thought in this context relates to the similarity in the biological architecture of humans and other organisms. By identifying the mechanisms driving evolution in non-human urban organisms, we also help characterize candidate drivers of human evolution, and vice versa. If light pollution disrupts the physiology of urban amphibians [114], should we be surprised that it also negatively affects human health [191]? And, if we identify mechanisms that are of non-human concern, can we perhaps incentivize efforts to address them by pointing out that similar impacts may be accrued to the human population?

8.7. Relevance for Urban Conservation

Evolutionary insights have a lot to offer in making decisions about managing urban biodiversity, both in terms of encouraging the persistence of desired species and control of undesired ones [53,118]. Determining whether a particular trait shown by an urban inhabitant resulted from genetic evolution or not would be a crucial early step in tailoring a management approach to a particular population and setting. If cities and the species they hold do indeed have conservation value [34], then the question arises of how we can maximize the evolutionary benefits of rapid adaptation and minimize the negative effects related to small population size via other evolutionary processes. At the same time, we also need to understand urban evolution so we can reduce the negative impacts of introduced pests and diseases [18]. Moreover, given that the United Nations identified as one of its Sustainability Development Goals a high global priority for “sustainable cities and communities”, such an understanding is particularly important. Moreover, the evolutionary impacts of human–wildlife conflict in urban settings could also benefit from additional attention [192].

Further reflection identifies a need for greater attention to the implications of alien species invasion, which can lead to introgressive hybridization with native (and sometimes declining) species. This genetic admixture is often viewed as a threat to the native populations, though several recent studies suggest that it may at times offer a potential benefit because of increased adaptive potential in some highly endangered taxa [35,193,194,195]. Although this has been an explicit and successful approach in the restoration of peregrine falcons (Falco peregrinus (e.g., [196])), it is rarely considered elsewhere and conflicts with some common perceptions of the role of conservation science.

Finally, a better understanding of urban evolution might provide useful lessons for predicting adaptation outside of the city. For example, much has been made of the heat island effect which keeps cities warmer than their surroundings. In that, urban organisms act, to some extent at least, as antecedents to the effects of climate change elsewhere. Other differences notwithstanding, if urban organisms can adapt to the warming environment, that should give us some comfort about the ability of other organisms to adapt. Conversely, if urban taxa cannot evolutionarily respond to a warmer environment, that is a strong warning about the lack of potential for such response elsewhere.

9. Conclusions

Like previous reviews, and despite the ongoing growth in relevant studies (Figure 3) and the time that has elapsed since previous reviews (e.g., [17,18]), we also found that the number of convincing demonstrations of urban evolution remains small. Also, like other assessments in a variety of context (e.g., [34], for conservation), we believe that this primarily represents a lack of city-based research effort rather than a lack of opportunity for research or a lack of urban evolutionary events. There is an apparent bias in the biological fields against urban studies [48,197,198,199], though bird species found in multiple cities are more frequently studied [200]. To make matters worse, where such studies do occur, specimens are seldom deposited in scientific collections where they can serve for future research [201]. The literature on mutations and epigenetic effects in urban settings remains particularly sparse. Unfortunately, the city as a habitat for biological studies remains a mostly squandered opportunity, especially in smaller cities [202].

A combination of methodological approaches will be needed to address the relative paucity of studies on urban evolutionary biology [48]. Recent developments in high-throughput genetic sequencing offer promising tools for asking questions about gene flows and genetic changes at scales we have not been able to attain in the past and at much cheaper costs. Increased success in extracting and sequencing ancient DNA derived from archeological digs suggests the ability to obtain high-resolution data from much older specimens than have previously been used to analyze genetic differentiation in urban settings may also be close.