Overview Articles

The Complexity of Urban

Eco-evolutionary Dynamics

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MARINA ALBERTI, ERIC P. PALKOVACS, SIMONE DES ROCHES, LUC DE MEESTER, KRISTIEN I. BRANS,
LYNN GOVAERT, NANCY B. GRIMM, NYEEMA C. HARRIS, ANDREW P. HENDRY, CHRISTOPHER J. SCHELL,
MARTA SZULKIN, JASON MUNSHI-SOUTH, MARK C. URBAN, AND BRIAN C. VERRELLI

Urbanization is changing Earth’s ecosystems by altering the interactions and feedbacks between the fundamental ecological and evolutionary
processes that maintain life. Humans in cities alter the eco-evolutionary play by simultaneously changing both the actors and the stage on which
the eco-evolutionary play takes place. Urbanization modifies land surfaces, microclimates, habitat connectivity, ecological networks, food webs,
species diversity, and species composition. These environmental changes can lead to changes in phenotypic, genetic, and cultural makeup of wild
populations that have important consequences for ecosystem function and the essential services that nature provides to human society, such
as nutrient cycling, pollination, seed dispersal, food production, and water and air purification. Understanding and monitoring urbanization-
induced evolutionary changes is important to inform strategies to achieve sustainability. In the present article, we propose that understanding
these dynamics requires rigorous characterization of urbanizing regions as rapidly evolving, tightly coupled human–natural systems. We explore
how the emergent properties of urbanization affect eco-evolutionary dynamics across space and time. We identify five key urban drivers of
change—habitat modification, connectivity, heterogeneity, novel disturbances, and biotic interactions—and highlight the direct consequences
of urbanization-driven eco-evolutionary change for nature’s contributions to people. Then, we explore five emerging complexities—landscape
complexity, urban discontinuities, socio-ecological heterogeneity, cross-scale interactions, legacies and time lags—that need to be tackled in future
research. We propose that the evolving metacommunity concept provides a powerful framework to study urban eco-evolutionary dynamics.

Keywords: adaptation, urban ecology, eco-evolutionary dynamics, coupled human–natural systems, metacommunities

U rbanization is changing Earth’s ecosystems and 

altering the regional and global distribution and
abundance of species. Humans in cities modify landscapes
et al. 2019). Although humans have been altering ecological
processes for millennia, urbanization represents a major
shift in intensity, speed, and scale (Ellis 2015). However,
and microclimates, restructure connectivity among habitat the eco-evolutionary consequences of human-driven niche
patches, alter food webs, change species composition, ini- construction have only recently been recognized (Palkovacs
tiate novel species interactions, and reshape competition, et al. 2012).
predation, and symbioses (Pickett et al. 2001, Alberti 2008, Urban development modifies landscape structure (e.g.,
Grimm et  al. 2008). These ecological changes can cause loss of forest cover and connectivity) and processes (e.g.,
evolutionary change by altering natural selection, neutral biogeochemical cycling), and significantly alters biotic inter-
genetic change, or gene flow, leading to species trait changes actions (e.g., predation), thereby changing species composi-
that could further alter ecological dynamics (Palkovacs tion and community dynamics. The resulting changes in
et  al. 2012, Alberti 2015). By changing the ecological the- selection pressures can cause shifts in ecologically relevant
atre, cities are simultaneously changing both the actors traits that can influence ecological interactions and ecosys-
and the stage, thereby writing a new eco-evolutionary play tem stability (Alberti et al. 2017a, Dakos et al. 2018). Cities
(Hutchinson 1965). are hotspots for contemporary evolutionary change that
With the emergence of global urbanization, humans—as occurs via alterations in the distribution of genetic diversity,
agents of niche construction—have achieved a new capacity changing allele frequencies that might translate into phe-
to shape the ecological and evolutionary forces that drive notypic trait changes (physiology, morphology, behavior,
biodiversity (Odling-Smee et  al. 2013, Boivin et  al. 2016). and life history). Trait changes can affect demographic rates
By building their own ecological niche, humans have trans- (such as reproduction, survival, or dispersal) and, in turn,
formed both their own environment and those of other shape population dynamics (e.g., numbers of individuals
species, generating complex feedbacks in both ecological and population persistence), community structure (e.g.,
and evolutionary processes (Palkovacs and Post 2009, Start species diversity and composition), and ecosystem function

BioScience 70: 772–793. © The Author(s) 2020. Published by Oxford University Press on behalf of the American Institute of Biological Sciences.
All rights reserved. For Permissions, please e-mail: [Link]@[Link].
doi:10.1093/biosci/biaa079 Advance Access publication 17 August 2020

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 Overview Articles

Urban-eco-evolutionary framework
Eco-evolutionary
dynamics
Socio-ecological Urban eco-evolutionary
patterns and drivers Gene
processes evolutionary
Habitat modification processes
Global drivers
Biophysical Connectivity Phenotype

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Demographic demographic
Socio-economic Heterogeneity processes
Policy
Built and Disturbance Populations
technological species
systems diversity
Biotic interactions
Communities
habitat and
resources

Ecosystems

Evolving urban metacommunties

Landscape Urban Socio-ecological Cross-scale Legacies and

complexity discontinuities heterogeneity interactions time lags

Figure 1. Conceptual framework of urban eco-evolutionary dynamics. Drivers of evolutionary change in urbanizing regions
include habitat modification, connectivity, temporal and spatial heterogeneity, novel disturbances, and biotic interactions.
Urbanization affects the balance between evolution and extinction by altering dispersal and genetic diversity, creating
cascading effects across all levels of biological organization. Changes in allele frequencies might translate into phenotypic
trait changes (physiology, morphology, behavior, and life history) that affect demographic rates (e.g., reproduction, survival,
or dispersal) and ultimately population dynamics (e.g., numbers of individuals and population persistence), community
structure (e.g., species richness or diversity), and ecosystem function (e.g., nutrient cycling, decomposition, and primary
productivity). These changes can cascade among levels of ecological organization and ultimately affect evolution.

(e.g., nutrient cycling, decomposition, and productivity; laboratories to study eco-evolutionary dynamics (see the
figure 1). glossary). However, understanding these dynamics requires
Although evidence of contemporary evolutionary change a rigorous characterization of urbanizing regions as coupled
(Fussmann et  al. 2007, Post and Palkovacs 2009, Schoener human–natural systems and their interactions across spatial
2011, Hendry 2016, Szulkin et  al. 2020) and its implica- and temporal scales (Brunner et al. 2019, Hendry 2019, De
tions for ecosystem function is rapidly increasing (Post and Meester et al. 2019).
Palkovacs 2009, Whitehead et  al. 2010, Hendry 2016), the Observations of trait changes across multiple taxa in urban
predominant views of biodiversity and ecosystem function environments provide important clues about the mecha-
that inform current strategies to achieve sustainability are nisms linking urbanization to evolutionary change. Several
still fundamentally static. In the present article, we show reviews of observed urbanization-driven trait changes have
how the rapid evolutionary changes driven by urbaniza- been published over the last decade (Palkovacs et  al. 2012,
tion have the potential to affect species persistence and Donihue and Lambert 2015, McDonnell and Hahs 2015,
ecosystem functions with important consequences for the Alberti et  al. 2017a, Johnson and Munshi-South 2017,
delivery of nature’s contributions to people (box 1; Díaz Rivkin et  al. 2019). However, the development of a theory
et al. 2018). We argue that understanding the complex eco- of urban eco-evolutionary dynamics requires a unified
evolutionary dynamics of urbanization and its influence on conceptual framework. Such a framework should draw on
stability and biodiversity is central to inform sustainability advancements in eco-evolutionary theories to support the
strategies (Palkovacs and Post 2009). Cities provide natural design of long-term, multicity experiments across a broad

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Overview Articles

Box 1. Implications of urban eco-evolutionary feedback for nature’s contributions to people.

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Urbanization-driven trait changes have the potential to affect human wellbeing by altering nature’s contributions to people, includ-
ing food production, primary productivity, pollution control, spread of infectious diseases, and cultural values. Pacific salmon
(Oncorhynchus spp.) have evolved smaller body sizes (Carlson et al. 2011). Earthworms (Lumbricus rubellus) are well able to tolerate
contaminants in soil (Kille et al. 2013). The water flea Daphnia has adapted to cyanobacteria (Hairston et al. 2001, Ger et al. 2014),
thermal environments (Brans et al. 2017b 2017a), and road salt (Coldsnow et al. 2016). The white-footed mouse (Peromyscus leucopus),
a common resident of New York City’s forest fragments, carries the bacteria for Lyme disease and exhibits signatures of directional
selection (Munshi-South et  al. 2016). Great tits (Parus major) show significant but contrasting effects of urbanization on genome-
wide genetic diversity and structure (Björklund et al. 2010, Perrier et al. 2018). Photographs: (a) Ernest Keeley, (b) Malcom Storey,
(c) Pul Hebert, (d) Linelle Abueg, (e) Michela Corsini

range of taxa to understand the convergence and divergence 2019); and do not consider eco-evolutionary dynamics over
of genetic and phenotypic responses. Trait shifts in urban deep time scales (Weber et al. 2017).
environments across diverse taxa are likely a result of both A framework for studying urban eco-evolutionary dynam-
adaptive changes in allele frequencies (evolution) and phe- ics should be trait-based (functionally linking individual
notypic plasticity (Palkovacs and Hendry 2010). However, organisms with community structure and dynamics), should
most studies that document observations of urbanization- be spatially explicit (representing spatially dependent popu-
induced phenotypic changes do not establish the genetic lation dynamics), and should include intra- and interspecific
basis of these changes. In addition, observations are often interactions within and across trophic levels (Brans et  al.
limited to individual cities and to single species (Donihue 2020). The evolving metacommunity concept and its appli-
and Lambert 2015, Johnson and Munshi-South 2017). cation through individual-based models have the potential
Theoretical models of eco-evolutionary feedbacks provide to integrate these complexities (Govaert et  al. 2019). A
a useful framework for investigating urban eco-evolutionary metacommunity is a set of local communities linked by the
interactions, but simplifying assumptions and generaliza- dispersal of multiple potentially interacting species. The
tions over many dimensions may bias predictions (Govaert evolving metacommunity framework also assumes that
et  al. 2019). For example, ecological and evolutionary genetically determined trait variation within populations of
responses to climate change show varying results when each species can modify their responses to local environ-
introducing eco-evolutionary feedbacks, multiple species, ments and interspecific interactions such that ecological
and spatial interactions. In particular, most current models and evolutionary processes of selection, dispersal, gene flow,
focus on a single species (Urban et al. 2012); ignore species and diversification operate jointly and sometimes nonad-
interactions, trophic interactions (Mellard et al. 2015), and ditively (Urban and Skelly 2006, Urban et al. 2008, Leibold
food webs (Rossberg et al. 2006, Bolchoun et al. 2017); dis- et  al. 2019). Because ecological and evolutionary processes
regard interactions across space and the regional dynamics jointly affect trait change in populations and communities,
of linked communities (Urban et al. 2012, De Meester et al. it is also important to partition their separate contributions

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urban heterogeneity, variable activities and impacts, and

cross-scale interactions among multiple agents of change
(Szulkin et al. 2020).
The reality of urbanization is more complex (Alberti
2015, Alberti et  al. 2017a). Urbanization represents a
­discontinuity—a system transition between two alternative
states along a continuum of anthropogenic change (figure 2;
Alberti 2008). Urban ecosystems exhibit habitat character-
istics, spatial and temporal heterogeneity, connectivity, dis-

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turbance, and biotic interactions that are distinct from the
original ecosystems (figure 3). These system-level properties
emerge from complex interactions among heterogeneous
human agents and ecosystem processes operating at mul-
tiple scales (figure 4; McDonnell and Hahs 2015, Alberti
2016). Urban ecologists have uncovered cities’ unique pat-
terns of ecological succession, water flow regimes, soil
properties, nutrient cycles, and distinct signatures of biotic
interactions and species diversity (Pickett et al. 2001, Alberti
2008, Grimm et al. 2008, McPhearson et al. 2016), but only
Figure 2. Urban discontinuities. Urbanization represents recently have we begun to understand how these properties
a discontinuity in the dynamic of ecological systems. As a change the dynamics between adaptation and the relative
region urbanizes, ecosystem function declines. The system abundance of different species (cf. species sorting) that
moves along the upper continuous line until a threshold is determine species persistence and extinction and therefore
reached and the system becomes unstable (dashed portion shape emergent patterns of biodiversity. Although growing
of curve). As urbanization increases multiple stressors evidence suggests that ecosystem transitions affect and are
modify ecosystem dynamics and reduce ecosystem function affected by species trait variation and evolutionary change
until reaching a point where the system flips into a new (Dakos et  al. 2018), the causes and feedbacks are particu-
state, governed by new dynamics and feedbacks. The system larly difficult to disentangle in urban settings (Alberti 2015,
shift can cascade across the levels of ecological organization Hendry et  al. 2017, Des Roches et  al. 2018). In urban set-
and affect the eco-evolutionary dynamic. For example, tings, rapid evolution and ecological feedbacks may result
increasing temperature and nutrient loading in urban from multiple selection pressures operating simultaneously,
lakes pose increasing selection pressure on zooplankton increasing both the total strength of selection on a given
behavioral and physiological traits that improve tolerance trait and the selection on a greater number of traits (Alberti
to cyanobacteria (Ger et al. 2014). Variation in a response et al. 2017a).
trait (e.g., tolerance of zooplankton to cyanobacteria) We believe that it is critical to take into account the com-
affects tipping points of urban shallow lakes that can plexity of urban systems and the heterogeneity of emergent
shift their state to a eutrophic state (Dakos et al. 2019). patterns of urbanization for advancing our understanding
Photographs: Mannahatta Project, Eric Sanderson. of eco-evolutionary dynamics and their feedbacks. Despite
their commonalities, cities are highly diverse in physical
structure, human population density, social heterogeneity,
to community structure and ecosystem function using eco- social institutions, and biophysical environments, reflecting
evolutionary partition metrics (Govaert et al. 2016). different levels of development, history, culture, demograph-
An urban eco-evolutionary framework should carefully ics, economic structure, and infrastructure (Szulkin et  al.
account for urban complexity. Despite an increased atten- 2020). This results in variable types and levels of disturbances
tion to anthropogenic drivers, current perspectives in urban and multidimensional gradients. The capacity of different
evolution and eco-evolutionary dynamics make relatively organisms to cope and adapt to urban environments varies
simple assumptions about how the urban human–natural greatly across different disturbance gradients depending on
system is structured in time and space. In most models species-specific dispersal ranges, generation times, standing
(Govaert et  al. 2019) and empirical studies (Johnson and genetic variation, and trophic positions. Factoring in urban
Munshi-South 2017), human activity is considered to be an complexity is key to predicting how biodiversity will respond
external driver operating along a continuous disturbance to rapid environmental change, generating new insights for
gradient, and the ecological and evolutionary responses conservation and urban planning (Kinnison et al. 2015).
to urbanization are assumed to remain constant across
time and space. Urbanization is frequently reduced to a Drivers of urban eco-evolutionary dynamics
few aggregated variables (e.g., impervious surface, human Global urban biodiversity is a product of the interac-
population density), which typically do not capture the full tions among multiple urban and natural agents that affect

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Figure 3. Drivers of eco-evolutionary change in urban environments are emergent properties of interacting socio-ecological
systems. Habitat modification due to land cover change leads to loss and configuration changes of natural habitats.
The building of dams has been a major driver of loss of hydrological connectivity. Dam removal projects are restoring
the hydrological connectivity of rivers and streams. Green infrastructure as constructed habitats and corridors shapes
landscape heterogeneity in cities. Novel disturbances such as artificial light at night can influence circadian rhythms and
migrations of birds. Human mobility mediates species dispersal and increases the chance of species introduction that drive
biotic interactions. Photographs: (a–c) and (f) Welikia Project, Eric Sanderson; (d) NASA; (e) Jill Hubley.

eco-evolutionary dynamics across levels of biological orga- Although ecologists have previously assumed that these
nization (figure 1). The key drivers that shape urban evolu- impacts change predictably with distance from the urban
tionary dynamics include habitat modification, connectivity, core (Alberti et  al. 2001), evidence shows that urbanizing
spatial and temporal heterogeneity, novel disturbances, and regions are a mosaic of ecological gradients (McDonnell and
biotic interactions (figure 3). Although these drivers of evo- Hahs 2008). Urban landscapes are best described by a set of
lutionary change characterize most anthropogenic systems, patterns representing complex interactions between human
their intensity, spatial cooccurrence, and time compression in and natural processes (Alberti 2005, Liu et  al. 2007). Few
urban environments set urbanization-driven eco-evolutionary studies have explored how alternative urban landscape pat-
dynamics apart from those of other anthropogenic contexts. terns and infrastructure control the distribution of energy,
materials, and organisms in urban ecosystems (Sukopp
Driver 1: Habitat modification. Urbanization modifies both 1990, Alberti 2005, 2016, Kaye et  al. 2006). Instead they
the structure and functioning of natural habitats. It simul- typically relate ecological and evolutionary changes with
taneously alters physical and chemical characteristics, as simple aggregated measures of urbanization (e.g., human
well as species composition, and together, these can affect population density, percent of impervious surfaces). To
biogeochemical cycles nonadditively (Alberti 2008). Land understand how urbanization-driven habitat modification
cover conversion results in rapid loss of native habitat drives evolutionary processes it is essential to quantify the
(Grimm et  al. 2008) leading to extinctions, shifts in the multiple axes of environmental variation that characterize
relative abundance of species, and evolution (Alberti urban environmental gradients across multiple spatiotem-
et  al. 2017b). Altering the land surface also modifies poral scales (Szulkin et al. 2020).
microclimates and generates heat islands. Furthermore,
an increase in impervious land area affects both geomor- Driver 2: Connectivity.  Cities change patterns of structural and
phological and hydrological processes, causing changes in functional connectivity by altering terrestrial and aquatic
water quality and dynamics of aquatic habitats. Human landscapes, isolating habitat patches, subpopulations, and
activities also alter the availability of nutrients and water, species, and by transporting organisms (Bullock et al. 2018).
affecting population, community, and ecosystem dynam- Habitat fragmentation, which isolates populations from
ics (Alberti 2008). gene flow, is a major driver of both neutral and adaptive

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a
Atmosphere
K
Biotic interactions

Soil B
A Air pollution
Temperature
J B Fragmentation

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Vegetation L C Heat island
D
Water D Artificial light
A and noise
N E Transportation
G F
C I F Landscaping
G Parks and corridors
M
H Stormwater
H I Wastewater
J Soil contamination
K Water and food resources
E L Species introduction
G M Loss of natural habitat
N Hydrological connectivity
b
1000yr Neighborhood City Region Globe
Climate change
Hydrological connectivity
100yr
Loss of natural habitat
10yr Parks and corridors Fragmentation
Heat island
Soil contamination
Time scale

1yr Species
Water and food resources
introduction
1mon Air pollution
Landscaping
1wk Stormwater and wastewater

Artificial light and noise

1d
Transportation
Built networks
1hr

1min
3 4 5
10m 100m 1km 10km 100km 10 km 10 km 10 km
Spatial scale
Figure 4. Agents and scales of urban eco-evolutionary change: Panel (a) shows the urbanization-driven selective pressures
and direct ecological processes involved. Panel (b) identifies the spatiotemporal scales of ecological processes affected by the
urban pressures (Modified from McDonnel and Hahs 2015).

evolutionary change. Isolation can prevent the influx of new reducing the swamping of maladaptive gene flow. Natural
genetic variation and increase inbreeding and neutral drift. habitat patches and their biological communities are often
When enough genetic variation exists in isolated habitats, isolated from each other by the built environment. New bar-
reduced gene flow can also facilitate local adaptation by riers make dispersal difficult and can penalize less-mobile

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organisms or allow them to become more locally adapted highly heterogeneous biophysical conditions as the varied
(Rebele 1994). behaviors of landowners result in fragmented management
Conversely, there is some evidence that urbanization can patterns. Such trends may reverse at a larger scale because
connect, intentionally or not, habitat patches, subpopula- of consistent patterns of urban development and habitat
tions, and species previously isolated from each other (Miles fragmentation, which are likely to be influenced by cultural
et  al. 2019). Green infrastructure (e.g., green corridors)— and historical legacy as well as climate (Szulkin et al. 2020).
designed to provide habitat for wildlife and simultaneously Temporal heterogeneity in urban environments is altered
mitigate storm water flows, reduce surface heat, cool the by the type and timing of urban pressures associated with
atmosphere, absorb atmospheric pollutants, and provide human activities. Physiological and reproductive cycles of

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leisure opportunities for people—can allow for the move- many organisms of plants and animals are often triggered
ment of organisms and strongly influence habitat connectiv- by climatic variation and resource availability (Cleland
ity (Rudd et  al. 2002, Bullock et  al. 2018). Transportation et  al. 2007), which are both, in turn, altered by urbaniza-
infrastructure might, through traffic, act as an unintended tion. Using three decades of high-resolution remote sens-
dispersal vector for many organisms. These networks can ing observations, Li and colleagues (2017) found that that
allow range expansion and increase both dispersal rates and the phenology cycle (changes in vegetation greenness or
distances. Urbanization therefore profoundly rewires con- senescence) in urban areas starts earlier and ends later than
nectivity and differently affects species with alternate dis- in rural areas resulting in a longer growing season. In addi-
persal strategies, sometimes leading to evolutionary change tion to changing environmental conditions such as food and
in dispersal mechanisms (Cheptou et  al. 2008). Through temperature, cities’ artificial lights at night alter organisms’
changes in species composition and altered food webs, natural photoperiod (the daylight period of a 24-hour day),
rewired connectivity networks affect ecosystem function an important proximate cue that organisms use to time bio-
and feedback on trait evolution. logical rhythms (Helm et al. 2013).
At some scales, temporal heterogeneity of urban areas
Driver 3: Spatial and temporal heterogeneity. Urban land- tends to be reduced because of human behavior and built
scapes exhibit unique spatial and temporal heterogeneity infrastructure (Walker et  al. 2009). In warm, dry climates,
(Cadenasso et  al. 2007, 2013). Because the amount, form, irrigation evens out the otherwise widely varying primary
and timing of urban development affect the mosaic of productivity of native grassland or desert ecosystems. Dams
habitat patches and their ecological properties, we expect modify riverine ecosystems, eliminating high-flow events
alternative urban development patterns to differently affect and increasing low flows. Bird lovers provide seeds that can
ecological and evolutionary dynamics (Alberti 2005). This modulate food availability (Faeth et al. 2005). This buffering
heterogeneity would suggest greater niche differentiation of environmental change, however, contrasts with distur-
and a relatively high species diversity in urbanizing regions. bances that can occur over very short time scales. The tem-
However, most studies report that habitat changes associated poral heterogeneity of human activities can result in higher
with urban land uses, along with other urban pressures, act variability of environmental pollution (e.g., night lights,
as a filter for urban species composition (Piano et al. 2017, atmospheric emissions, and noise) and physical structure
Merckx et  al. 2018), with clear winners and losers, poten- (e.g., cleaning of urban ponds). In one example, real-time
tially driving the homogenization of ecological structures monitoring suggests significant effects of temporal hetero-
and functions across cities (Groffman et al. 2014). However, geneity of traffic patterns on the spatial concentrations of
findings are not consistent across cities, and urban biodiver- atmospheric pollutants (Liu et al. 2018).
sity might strongly be shaped by the regional species pool Changes in spatial and temporal heterogeneity together
(Aronson et  al. 2014). Urbanization pressures might dif- with the reduction in habitat quality may therefore gener-
ferently affect the many dimensions of biodiversity (Pearse ate asymmetrical selective pressures and species responses.
et al. 2018). These asymmetries favor certain species and traits over
Urban spatial heterogeneity and its effect on community others, changing biotic interactions and community compo-
dynamics is not well understood partly because studies sition, and could potentially result in ecological homogeni-
have tended to focus primarily on aggregated measures of zation (Groffman et al. 2014).
urbanization (e.g., population density or impervious sur-
face cover) and at biologically irrelevant spatial resolution Driver 4: Novel disturbances. Human activities can increase
(Szulkin et al. 2020; e.g., census blocks), and partly because or decrease the magnitude, frequency, and intensity of
we have insufficient knowledge on how this heterogeneity natural disturbances (Rebele 1994), and can also introduce
varies with scale (Band et al. 2005, Satgé et al. 2019). Recent novel disturbances, defined in the present article as discrete
observations show that urbanization tends to increase spa- events that disrupt system structure, which includes social,
tial heterogeneity on some scales and reduce it on others ecological, physical, and built components (Grimm et  al.
(Pickett et al. 2016). At the scale of meters or below, urban- 2017), and that are unique to urban systems. For example,
ization may reduce the heterogeneity of land cover, but at although building and construction regulations have dra-
the landscape patch scale, urbanization may introduce new, matically reduced the risk of severe fire in cities and water

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flow regulation has decreased flow variability and “con- testable hypotheses about how urbanization affects coloniza-
trolled” floods, changes in impervious cover have increased tion and extinction and therefore determines local diversity.
the intensity of floods. Also, the construction of new build- In urban environments, diversity still emerges as the balance
ings and infrastructure can mean vegetation is permanently between extinction and colonization, but species invasion
removed; surfaces are excavated, filled, and graded; and plays a prominent role.
streams are buried (Elmore and Kaushal 2008)—all of which Human activities in cities also alter food webs and trophic
can disrupt habitat connectivity. Planting and maintaining structure of biological communities (Faeth et  al. 2005). A
ornamental vegetation introduces novel habitat and food study of the urbanizing Sonoran Desert, conducted at the
resources, but also replaces native vegetation, eliminating Central Arizona–Phoenix Long-Term Ecological Research

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habitat or food resources for many native species (Narango site, revealed some surprising human-induced modifications
et al. 2018). The application of herbicides and pesticides and of factors controlling trophic dynamics. Species composition
deliberate or inadvertent release of other pollutants into air, was radically altered (e.g., generalist species increased) and
water, and soil cause mortality and persistent contamina- resource subsidies from people increased and stabilized
tion. In many cases, continued management of these novel productivity (i.e., via modified water availability; Faeth et al.
ecosystems (which could be viewed as a press disturbance) 2005). Birds as top predators were able to control abundance
prevents the reestablishment of previously extant communi- of arthropods. This suggests that urbanization may cause
ties and sets the stage for novel biotic interactions (Collins a shift from a system that is resource-based or bottom-up
et al. 2011). These novel environments lead to novel selec- controlled—typical of the Sonoran Desert—to a combined
tion pressures and unexpected eco-evolutionary dynamics. bottom-up and top-down system.
New spatial and temporal heterogeneity emerges from Urbanization-driven changes in habitat quality interact-
discrete disturbance events that modify the natural envi- ing with rewired food webs also change eco-evolutionary
ronment, creating a mosaic of built and highly managed feedbacks. Although research on eco-evolutionary dynamics
natural components that form the urban ecosystem. Once has focused predominantly on individual species and at sin-
established, these components are subject to disturbances gle trophic levels, evidence shows that intraspecific variation
such as fire, wind, pest outbreaks, and flood that may or in multiple species can affect interactions between bottom-
may not transform their structure and identity. The type of up and top-down forces that shape communities (Rudman
disturbance that is most likely to transform them is another et  al. 2015, De Meester et  al. 2019). To fully understand
land conversion, such as the removal of a park to make way urban evolutionary effects on ecosystems will require greater
for a freeway, or the expansion of housing into previously knowledge about how urban effects on genetic variation and
undeveloped patches—with attendant losses or changes in genetic trait shifts can alter the strength of top-down control.
species’ habitats. However, the larger social–ecological– Urbanization also leads to an increase in human–wildlife
technological system is likely to maintain its structure, func- interactions, with negative (e.g., physical attacks, disease
tion, and identity (i.e., to be resilient) except in the face of transmission, property damage) and positive outcomes (e.g.,
potentially catastrophic disturbances, such as hurricanes, ecosystem services, human well-being) that affect species
sea-level rise, or major earthquakes. Once transformed to traits and community composition (Soulsbury and White
a new (urban) system state, eco-evolutionary dynamics will 2016). Humans serve as de facto apex predators in urban
play out under the complex mechanisms of change that systems (Suraci et al. 2019), but at the same time have very
characterize urban social–ecological–technological systems strong effects on large carnivores that produce dampened
(Grimm et al. 2017). top-down effects on urban animals (Oro et  al. 2013). This
results in overall increases in fearlessness and habituation
Driver 5: Biotic interactions.  Urban development modifies spe- directed toward people, which enables exploitation of novel
cies interactions, including competition, predation, para- niches and occasionally leads to increasing opportunities for
sitism, and symbiosis by introducing nonnative species, conflict, both of which may serve as novel selection pres-
altering species behavior, and by changing species com- sures in cities (Cox and Gaston 2018).
position. In cities, frequent introductions of exotic species Anthropogenic food subsidies in cities also augment
provide avenues for their colonization (Marzluff 2008) and species habituation and risk-taking that can shape eco-
establishment (McDonnell and Pickett 1993). This phenom- evolutionary responses of urban populations (Oro et  al.
enon is exacerbated as nonnative species take advantage of 2013, Martínez‐Abraín et al. 2019). At the community level,
poorly integrated communities and patches typical of the food supplementation decouples predator–prey interactions
disturbed sites in urban centers. Studies of genetic patterns that fundamentally alter food web dynamics (Rodewald
and evolutionary consequences of urban colonization on et  al. 2011, Fischer et  al. 2012, Newsome et  al. 2015).
native species include dark‐eyed juncos (Junco hyemalis) Wildlife–pathogen dynamics are also linked to increased
in Southern California (Atwell et al. 2012), red fox (Vulpes resource provisioning by altering host exposure and toler-
vulpes) in Zurich (DeCandia et  al. 2019a), and coyotes ance to pathogens (Becker et al. 2015, Murray et al. 2019).
(Canis latrans) in New York City (DeCandia et  al. 2019b, Accordingly, direct and indirect human–animal interactions
Henger et  al. 2019). Marzluff (2008) developed a series of create ample opportunities for changed eco-evolutionary

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pathways in urban wildlife, as well as feedback to human Urbanization mediates natural selection by influencing
health and well-being via zoonotic disease transmission and the fitness of individuals. Individuals with certain traits have
ecosystem services. higher survival and reproductive success rates than others
and pass on these traits, when heritable, to their offspring.
Urban eco-evolutionary dynamics and feedbacks Phenotypic change exhibits a clear urban signal (Alberti
Evidence of urbanization-driven evolutionary change is et  al. 2017a). However, we do not know how mechanisms
rapidly expanding, but we lack a systematic mechanistic of selection in the urban environment interact and what
understanding of how urbanization affects evolutionary traits are most likely to evolve. Despite evidence of divergent
changes and their ecological feedbacks. Allele frequencies in phenotypic evolution in a wide diversity of traits (including

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a population may change because of mutation, genetic drift, life history, morphology, physiology, and behavior) between
gene flow, and natural selection. Research on eco-evolution- urban and rural environments, only a few studies link
ary dynamics has primarily focused on adaptive evolution, genetic mechanisms with phenotypic evolution. Perhaps the
but neutral evolutionary processes may also influence feed- best known case of human-induced evolution is the increase
backs. Mutation is the original source of genetic variation. in frequency of the darker color of the peppered moth
Mutations arise in response to air pollution; carcinogenic (Biston betularia) in the 1800s, associated with industrial air
hydrocarbons, which cause increased mutation rates in birds pollution (Kettlewell 1958). San Diego populations of the
(Yauk et  al. 2000) and mammals (Somers et  al. 2004); car- dark-eyed junco (Junco hyemalis) have less white in their tail
cinogenic pollutants in water (Atlantic killifish; Whitehead feathers as a result of sexual selection (Yeh and Price 2004).
et  al. 2010); and toxins in soil (earthworms; Kille et  al. The Atlantic killifish (Fundulus heteroclitus) has rapidly
1999). Although there are a few documented examples of adapted to high concentrations of PCB in four urban estuar-
new mutations resulting from urban pollution (Alberti et al. ies (Nacci et al. 2010).
2017a), adaptation typically follows from existing allelic Urbanization might shift the relative contribution of adap-
diversity or standing genetic variation (Barrett and Schluter tive evolution versus species sorting to species persistence
2008, Johnson and Munshi-South 2017). and biodiversity patterns. For example, urbanization might
Urbanization often causes drastic declines in population decrease colonization rates enough to prevent species from
sizes, thereby exacerbating the effects of genetic drift—ran- colonizing isolated urban environments. Free from disrup-
dom changes in allele frequencies across generations. Genetic tive gene flow and frequent colonizations, resident species
drift, which is more prominent in small, isolated popula- might adapt to novel conditions and monopolize resources,
tions, results in reduced genetic diversity within populations and thereby reduce or prevent the colonization success of
and increased differentiation among populations. Examples new species (De Meester et al. 2016). This scenario assumes
include populations of white-footed mice (Peromyscus leu- enough genetic variation to mount an adaptive response,
copus; Munshi‐South et al. 2016) and salamanders (Munshi- but genetic drift might reduce this potential especially in
South et  al. 2013; Desmognathus fuscus) in New York City small populations. When urbanization enhances connectiv-
and foxes (Vulpes vulpes) in Zurich (DeCandia et al. 2019a). ity, species sorting is likely to be dominant over adaptation
Other studies have shown that urbanization may increase and monopolization, promoting the spatial insurance effect
regional genetic diversity by creating new habitats and eco- (Loreau et al. 2003)—whereby species can track their opti-
logical networks, thereby allowing for population growth mal environments by shifting their range. These patterns are
and increased connectivity, which decrease genetic drift. not consistent across taxa and cities. An urban environment
Björklund and colleagues (2010) documented high genetic can reduce or increase colonization rates, genetic drift, and
diversity in populations of the great tit in Barcelona. Miles gene flow, changing the relative importance of species sort-
and colleagues (2018) found high genetic diversity in west- ing and evolutionary dynamics depending on the character-
ern black widow spider populations across eleven US cities, istics of species and built environments.
as well as low genetic differentiation among populations. Eco-evolutionary feedbacks resulting from urbanization-
Contrasting findings are also emerging from studies driven evolutionary change may be amplified or modified
examining the effect of urbanization on dispersal and gene by the divergent responses in ecologically relevant traits
flow (Miles et al. 2018). Urban landscape fragmentation and to complex urban signatures characterized by interactions
the built structures are generally expected to impede gene among multiple environmental gradients (Alberti et  al.
flow, which reduces local genetic diversity and increases 2017a) such as changes in microclimate, species interactions,
genetic divergence between urban and rural populations. and habitat fragmentation. Eco-evolutionary feedbacks are
Urban landscapes affect gene flow by rewiring connectivity insufficiently studied in an urbanization context, but are
networks through introducing artificial barriers that isolate likely very important. Urbanization has been associated with
populations and by establishing new corridors that may the evolution of ecologically relevant traits such as body size
bring together previously isolated populations and species and dispersal ability within and among species (Johnson
(Partecke 2013). Depending on the idiosyncratic effects of and Munshi-South 2017). Evidence of ecological responses
urbanization on dispersal for different species, urban land- to evolutionary trait changes in microbial (Fukami et  al.
scape features can decrease or increase gene flow. 2007, Hiltunen et  al. 2017), aquatic (Matthews et  al. 2011,

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Pantel et  al. 2015, Des Roches et  al. 2018) and terrestrial and heterogeneity) that sets the eco-evolutionary dynamics
(Fitzpatrick et al. 2015, terHorst and Zee 2016) ecosystems of urban ecosystems apart from natural and other anthropo-
show potential feedback on key ecosystem functions that genic systems. Urbanization gradients are multidimensional
provide important contributions to people (e.g., primary and have complex effects on biological assemblages and
productivity, nutrient cycling, pollution control, carbon ecosystem processes across a range of temporal and spatial
sequestration, and community composition). scales (Alberti et al. 2003, Cadenasso et al. 2006).
Future studies will need to treat urban landscapes
Tackling emerging complexities as spatially heterogeneous patch mosaics, characterized
Cities provide a unique opportunity to advance our under- by multidimensional gradients structured hierarchically.

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standing of urban eco-evolutionary dynamics. Cities’ shared Drawing on gradient (Whittaker 1967), patch (Levin and
ecological features enable us to test hypotheses about the Paine 1974), network (O’Neill et  al. 1986), and hierarchy
repeatability of evolution (Donihue and Lambert 2015, theories (Wu and Loucks 1995), we can quantify different
Santangelo et al. 2020) and to determine whether traits show aspects of urban habitat and landscape complexity that
convergence across different species or parallel changes we expect to affect evolutionary and ecological processes
across populations of the same species (Campbell-Staton using selected habitat and landscape metrics that have
et  al. 2020). The heterogeneity and connectivity caused by been shown to capture the spatiotemporal signatures of
variable patterns of urbanization within and among cit- urbanization (table 2; Liu et al. 2016b). These metrics offer
ies pose different challenges for different organisms and a concrete approach to link urban landscape complexity
therefore provide opportunities to test both convergent and to ecosystem function (Levin et al. 1998) and explore how
divergent evolution. alternative development patterns across and within cities
Disentangling the diversity of urban mechanisms produce distinct signatures of eco-evolutionary change.
and complex interactions that determine eco-evolution- Using landscape genomics (Manel and Holderegger 2013)
ary dynamics poses significant practical challenges. It and spatially modified partition metrics (Govaert et  al.
may require common garden experiments (Brans et  al. 2016), we can further determine the ecological and evolu-
2020) or reciprocal transplants of coevolved communities tionary contributions and assess what landscape properties
(Alexander et al. 2015), and such approaches may be pos- explain the observed variation.
sible only for certain species. Coupling landscape genom-
ics (Manel and Holderegger 2013) with partition metrics Urban discontinuities. Urbanizing landscapes represent spa-
(Govaert et al. 2016) can help determine the ecological and tial and temporal discontinuities (Holling 1992, Allen and
evolutionary contribution of different urban drivers to eco- Holling 2002) in the relationships between human and
evolutionary change across and within cities (Fenderson natural systems across a continuum of anthropogenic dis-
et al. 2020). turbance (figure 2; Alberti 2008). These discontinuities can
We propose five key aspects of complexity that need to be be either caused by abrupt changes in selection pressures in
considered in future research, propose concrete approaches space and time or by nonlinear responses to a gradient in
to tackle these complexities (table 1) and suggest an inte- anthropogenic disturbances (Scheffer et al. 2001). The cooc-
grated approach using the evolving metacommunity frame- currence of multiple disturbances can lead to synergistic
work. For example, we can begin to ask whether organisms interactions and multiplicative effects. In addition, the eco-
are adapting to specific pressures (e.g., increased tem- logical and evolutionary responses to the stress gradients can
perature) or to the cooccurrence of multiple pressures influence these discontinuities (Dakos et al. 2018). Tipping
(e.g., temperature and pollution), how spatial interactions points represent system transitions between alternate states
affect adaptation, whether there are detectable thresholds, that occur when a controlling variable in a system reaches
and how their adaptation may be affected by cross-scale a threshold. Subtle environmental change then can set the
interactions (e.g., regional climate change and urban heat stage for large, sudden, surprising, and sometimes irrevers-
islands), and whether the cooccurrence of stressors limits ible changes in ecosystems. Regime shifts depend not only
or strengthens adaptation to individual stressors. Ideally, to on the perturbation but also on system resilience (Holling
explore generalities, this complexity should be unraveled 1973, Scheffer et al. 2001). Tipping points can be influenced
for multiple organisms. The water flea Daphnia is perhaps by eco-evolutionary feedbacks—for instance, when reduced
one of the most documented examples of eco-evolutionary genetic diversity in urbanized regions lowers the resilience
dynamics and provides an excellent model system to study of populations to deal with certain environmental fluctua-
urbanizing regions (box 2). tions (Dakos et al. 2019). Even if environmental fluctuations
would remain similar across the urbanization gradient, it
Landscape complexity.  We propose that urban landscapes are might then still be that the population crashes at a given level
emergent phenomena resulting from local interactions of of urbanization.
human agency, built infrastructure, and biophysical factors. Regime shifts have been observed in many ecological and
It is the cooccurrence of multiple and largely novel changes social systems and have been described in coupled socio-
in habitat (habitat modification) and landscape (connectivity ecological systems (Scheffer et  al. 2001). In one example,

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Table 1. Emerging complexities, hypotheses, principles, and approaches.

Complexities Concepts Hypotheses Principles for urban Research approaches/methods
eco-evolutionary
research
Landscape Urban landscapes are Diverse urban Urban landscapes Identify social and ecological processes
complexity emergent phenomena patterns (i.e., urban exhibit emergent necessary to predict urban ecosystem-level
resulting from local form, land-use properties— properties.
interactions of human distribution, and properties that Use landscape metrics to characterize habitat
agency, built infrastructure, connectivity) generate cannot be understood and landscape complexity.
and biophysical factors. differential effects by studying the

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Couple landscape genetics and metrics to
Examples are urban sprawl, on eco-evolutionary properties of their estimate gene flow across landscapes.
habitat connectivity, and dynamics. constituent parts. The
heterogeneity resulting from nature and structure Genome scans combined with genetic
We hypothesize samples across urban landscapes to identify
local-scale interactions that alternative of the relationships
among variables such as between system molecular markers indicating adaptive genetic
urbanization patterns variation (Manel and Holderegger 2013).
topography, land cover, have variable impacts components and
transportation infrastructure, on the sources of selective pressures Use spatial modified partition metrics
real estate markets, and ecological and genetic have to be considered (Govaert et al. 2016) with landscape
social preferences. variance that are explicitly in metrics (Liu et al. 2016b) to determine eco-
expressed at fine designing urban eco- evolutionary contributions of urban landscape
spatial and temporal evolutionary studies. properties to eco-evolutionary change across
scales. and within cities.

Urban Urbanizing landscapes Urban discontinuities Ecological structures Identify feedbacks across different spatial
discontinuity represent spatial and emerge from the and processes and temporal scales.
temporal discontinuities in interaction of multiple occur at specific Explore complex causalities that emerge from
the relationships between drivers (e.g. habitat spatiotemporal multiple interacting factors, starting points
human and natural systems modification and scales, and and pathways (Preiser et al. 2018).
through abrupt changes change in connectivity interactions that
in selection pressures, or and heterogeneity) occur across multiple Detect thresholds and early-warning signals
by non-linear responses to amplified or scales mediate of possible regime shifts (Dakos et al. 2018).
anthropogenic disturbances. dampened by scale-specific (e.g., Anticipate alternative future outcomes by
E.g. reduction in nitrogen feedback loops that individual, community, developing scenarios (Preiser et al. 2018).
retention capacity caused can lead to tipping local, or regional)
Assess ecosystem states across cities (e.g.,
by land cover change points, regime responses to
clear versus turbid ponds) in relationship to
can constrain responses shifts, and feedback disturbance. Urban
variable urban landscapes to explain drivers
to increases in nutrient structures. Urban ecosystems represent
of urban discontinuities (Dakos et al. 2018).
loading, shifting urban discontinuities can a discontinuity in
lakes to an eutrophic state. be detected in eco- eco-evolutionary
Adaptation of zooplankton evolutionary change. dynamics.
to cyanobacteria can affect
at which disturbance level
a shallow lake shifts to a
turbid state.
Socio-ecological Urbanizing landscapes Social heterogeneity Scale is a Integrate socio-economic variables in
heterogeneity exhibit unique heterogeneity might amplify critical factor in sampling design using multiple socio-
due to natural and dynamics of understanding economic and ecological data sources
engineered landscape ecological the interactions combining grid, vector, and network data to
elements, socio-economic heterogeneity in between human develop multi-dimensional transects.
and cultural factors, and the urban systems, and natural sources Extend methods that quantify eco-evolutionary
behaviors of individuals and while evolution might of evolutionary contributions (Govaert et al. 2016) to include
institutions. more often dampen change since spatial socio-cultural dynamics.
it. Environmental and temporal
inequalities such as heterogeneity may
uneven distribution affect the outcome
of parks, tree canopy of changes in driving
cover, and vacant forces only at certain
lots create patterns scales.
of eco-evolutionary
dynamics.
Cross scale Cities affect eco-evolutionary Increasing cross- Creating a Identify hypothesized cross-scale interactions
interactions change well beyond the city scale interactions predictive, integrated and feedbacks among drivers and focal
boundaries and interact between human and understanding responses (Soranno et al. 2014); measure
with other sources of natural systems, of urban eco- eco-evolutionary responses at multiple
evolutionary change (e.g., from preurban evolutionary dynamic scales and test for significant effects
climate change). to more human- requires tackling the of variables’ interactions at each scale
Interactions between drivers dominated systems, complex interactions (Peters et al. 2007); integrate data from
occur across multiple alters the dynamic of human and natural observations, long-term experiments, and
spatiotemporal scales; relationship between processes operating theoretical models to examine ecosystem
including global sea level species sorting at different space and processes at multiple spatiotemporal scale
rise and geologic formation, and adaptation time scales. (Peters et al. 2018); sensitivity analysis of
global trade and regulations, that might shift the scaling relationships to urban structure and
local-scale microclimates, balance between heterogeneity using simulation methods (e.g.
point source pollution the probability of Markov Chain Monte Carlo) (Wei et al. 2017).
or microbial activity, and evolutionary rescue
community practices and versus extinction.
businesses.

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Table 1. Continued.
Complexities Concepts Hypotheses Principles for urban Research approaches/methods
eco-evolutionary
research
Legacies and Urban landscape patterns Urban eco- Integrating socio- Integrate alternative eco-evolutionary
time lags are often the legacy of evolutionary dynamics ecological legacy outcomes across cities with (dis)similar
multiple natural and human are mediated by and time-lags in the biophysical background and natural history
induced disturbance events persistent legacies study of urban eco- could provide an effective strategy to detect
and the effect of social and of socio-ecological evolutionary dynamic signatures of legacy effects (Cavender-Bares
ecological time lags. interactions across is critical to predict et al. 2016).

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time and space. eco-evolutionary Quantify eco-evolutionary contributions to
Interactions among outcomes because assess relative importance of ecology and
societal, ecological of lingering effects evolution within multiple cities (Govaert et al.
and evolutionary on both species and 2016).
responses may affect genetic composition.
eco-evolutionary
outcomes.

reduction in nitrogen retention capacity caused by long- Socio-ecological heterogeneity. Urbanizing landscapes exhibit
term land-cover change associated with urbanization can unique heterogeneity because of a combination of natural
constrain the responses to rapid increases in nutrient load- and engineered landscape elements and because of the
ing, generating a shift in a lake ecosystem from a clear to a socio-cultural characteristics and behaviors of individuals
turbid, algae-dominated state (Wagener 2003). This regime and institutions (Machlis et al. 1997). Heterogeneity in urban
shift can affect evolutionary dynamics (Alexander et  al. ecosystems is therefore driven simultaneously by natural and
2017) and drive eco-evolutionary feedbacks. human agents operating across the landscape (Alberti 2008).
Dakos and colleagues (2019) show how trait change and Diverse human agents (e.g., income groups, household sizes,
trait variation can influence the probability and timing business sectors) have different opportunities, preferences,
(delaying or anticipating) of a tipping point between two and behaviors that affect the use of land, spatial distribution
ecological states (figure 2). For example, adaptation of zoo- of activities, and the demand for and supply of resources.
plankton to cyanobacteria or evolution of nutrient uptake Development decisions (e.g., housing and infrastructure),
in phytoplankton (Faassen et al. 2015) can affect the distur- management choices (e.g., yard management), and indi-
bance level at which a shallow lake shifts from a clear state vidual preferences (e.g., residential location choices) alter
to a turbid state. High trait variation can provide resilience landforms and drainage networks, and enhance the het-
to populations in the face of environmental change, whereas erogeneity of nutrients, material, and water cycling (Pickett
low trait variation can enhance the risk of regime shift. et al. 1997). Although empirical studies of the effect of urban
Urbanization-driven trait change can also affect the pathway heterogeneity are still limited, initial findings highlight the
to recovery to the previous state and its hysteresis—the time complex interactions and divergent outcomes resulting from
lag of the threshold in the environmental variable for the multiple sources of urban heterogeneity.
system to recover (Dakos et al. 2019). One of the best examples of an emergent urban landscape
Overall, we predict that the likelihood of nonlinear pattern caused by socio-ecological heterogeneity is urban
responses is high in urban systems, because the disconti- tree canopy cover. Trees are unevenly distributed through-
nuities may involve responses to environmental and social out the city because of both natural (e.g., microclimate, soil
changes and their interactions. Multiple stressors in the nutrients) and anthropogenic forces (e.g., income, unequal
urban environment can drastically change the offset point stewardship) that establish an urban habitat mosaic with
of a system shift. For example, in urban ponds the ability of salient fitness consequences for other organisms at higher
zooplankton to adapt to cyanobacteria can be influenced by trophic levels (Zipperer et al. 2011). For instance, urban trees
the ability of zooplankton to simultaneously adapt to higher are concentrated at greater densities in older, high-income
temperature (e.g., heat islands) and the presence of other neighborhoods relative to others (Clarke et al. 2013, Schwarz
contaminants (e.g., pesticides), determining the disturbance et al. 2015, Fan et al. 2019), which subsequently affects the
level at which a pond will shift from a clear state to a turbid distribution and intensity of urban heat islands and water
state. Several strategies can be applied to test this hypoth- quality throughout a city (Jenerette et al. 2011, Huang and
esis, including assessing how a stressor changes a threshold Cadenasso 2016, Wang et al. 2019).
level of a controlling variable, identifying feedbacks across The hypothesis that species diversity tends to increase
different spatial and temporal scales, detecting thresholds with neighborhood income suggests that socio-economic
and early-warning signals of possible regime shifts, explor- inequalities influence the suitability of specific habitats
ing complex causalities with different starting points and as corridors or stepping stones, shaping animal move-
pathways, and anticipating alternative future outcomes by ment, genetic connectivity, and biodiversity (Leong et  al.
developing scenarios (Preiser et al. 2018, Dakos et al. 2019). 2018) and can therefore affect eco-evolutionary dynamics.

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Box 2. Daphnia: A model system for studying urban eco-evolutionary dynamics.

One of the best documented examples of a human-driven eco-evolutionary change is from the
water flea Daphnia, a common zooplankton genus that plays an important role in the functioning
of pelagic freshwater food webs (Miner et  al. 2012). The different species of Daphnia, which are
found in urban lakes and ponds, are excellent study systems for studying urban eco-evolutionary
dynamics, as is illustrated in the following examples. Photograph: Paul Hebert.

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Alewife are anadromous fish that became landlocked in lakes following the construction of Colonial
Dams Era dams. Differences in the population growth rates of Daphnia ambigua that evolved to coexist
with anadromous versus landlocked alewife populations alter consumer-resource dynamics and
Alewife
ecosystem function (Palkovacs et al. 2008, Walsh et al. 2012).
Eutrophi-
cation

Daphnia

Urban eutrophication causes cyanobacteria blooms (made worse by warming), which drive rapid
evolution of Daphnia pulex. Adapted D. pulex can tolerate cyanotoxins produced by cyanobacte-
ria and therefore provide an ecological function (top-down control of phytoplankton) that is not
Eutrophi- provided by the maladapted D. pulex. Therefore, there exists an eco-evolutionary feedback from
urbanization (eutrophication) to D. pulex evolution to ecological function (improvement of water
cation

Daphnia quality for human use; Hairston et al. 2001).

Water
quality

Warming Daphnia magna in urbanized and warmer habitats rapidly evolve heat tolerance, and other changes
in life history traits, and physiological responses (Brans et  al. 2017b). Adaptation to urban heat
islands might interact with population’s response to higher temperature because of climate change
(Brans et al. 2017a). Although for Daphnia magna, the largest cladoceran and most efficient grazer,
urban populations evolve smaller body sizes in response to warming, their persistence in the system
via thermal adaptation (reduced body size, increased heat tolerance) could still mitigate top-down
Daphnia control and ecological functioning rather than be replaced by a smaller species.

Daphnia galatea have shown rapid adaptation to road salt. The evolved tolerance of D. galatea to
road salt could mitigate trophic cascades due to the impact of lake salinization that would otherwise
lead to elevated phytoplankton levels (Coldsnow et al. 2016).
Road salt

Daphnia

However, economic inequality and unequal distribution of achieved by integrating socio-economic and socio-cultural
biodiversity do not always converge (Kuras et al. 2020). The variables in sampling design using multiple socio-economic
exact mechanism that links socio-economic variables to dif- and ecological data sources to develop multidimensional
ferences in biodiversity is not known. The legacy effect of transects to compare eco-evolutionary change within and
historical societal processes observed in cities (Grove et al. across cities.
2018, Roman et al. 2018) highlights the need to uncover the
social determinants of urban eco-evolutionary processes Cross-scale interactions. Creating a predictive, integrated
(Des Roches et  al. 2020), and studies focusing on these understanding of urban eco-evolutionary dynamic requires
associations need to take into account the high temporal tackling the complex interactions of human and natural
and spatial heterogeneity of urban centers. This can be processes operating at different spatial and temporal scales.

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Table 2. Urban complexity metrics.

I. Habitat complexity II. Landscape complexity Example
Ia. Composition 1. Mean patch size IIa. Composition 1. Mean patch size
2. Total core area 2. Patch density
3. Normalized total core 3. Percentage of
area (TCA) landscape
4. Shannon diversity
index

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Ib. Configuration 4. Aggregation IIb. Connectivity 5. M ean Euclidean
5. Edge density –– terrestrial nearest neighbor
–– hydrological distance
6. Dendritic connectivity
Index

Ic. Complexity 6. A rea-weighted IIc. Complexity 7. L andscape shape

mean patch fractal index
dimension 8. Perimeter area
7. Perimeter area Fractal Fractal dimension
dimension

Although we have been aware of the existence of spatial and human–nature interactions are more prevalent and occur
temporal asymmetries between nature and society for quite at higher speeds (Liu et al. 2016a). Such complex interac-
some time, we do not yet have a theoretical framework for tions in telecoupled systems make it particularly chal-
studying the dynamics they create. lenging to disentangle urban versus rural anthropogenic
Complex interactions resulting from changes in habitat and natural drivers and to understand the potential eco-
and biotic interactions might produce new trophic dynam- evolutionary implications of cross-scale interactions and
ics across the urban landscape (Faeth et  al. 2005). These the associated feedbacks.
would result in profound changes in the structure and Strategies to tackle cross-scale interaction may include
functioning of communities and ecosystems that need more identifying hypothesized cross-scale interactions and feed-
targeted research. This also needs to be considered at the backs among regional and local drivers and between them
appropriate spatial scale, because urbanization-induced eco- and focal responses (Soranno et  al. 2014); measuring eco-
logical, evolutionary, and eco-evolutionary changes might evolutionary responses at multiple scales and testing for sig-
be scale dependent. There is a need for systematic studies nificant effects of variables’ interactions at each scale (Peters
on how urbanization-mediated ecological and evolution- et al. 2007); integrating data from multiple lines of evidence
ary responses interact differently among areas within cities, including observations, long-term experiments, and theo-
among cities, and beyond cities. Cities differ strongly in their retical models to examine ecosystem processes at multiple
urbanization dynamics. Comparative studies can link these spatiotemporal scales (Peters et al. 2018); and conducting sen-
dynamics to eco-evolutionary feedbacks. In addition, there sitivity analysis of scaling relationships to urban structure and
is an important need for studies that quantify how urbaniza- heterogeneity using simulation methods (e.g., Markov Chain
tion affects community and ecosystem structure and func- Monte Carlo) for a set of socio-ecological indicators for which
tioning in their surroundings and globally. we have disaggregated data (Wei et al. 2017).
Cities affect eco-evolutionary change well beyond the
city boundaries and interact with other sources of evolu- Legacies and time lags.  Theoretical models in biology predict
tionary change. Scale is a critical factor in understanding that species and genotypes are distributed across heteroge-
the interactions between human and natural sources of neous environments according to their local optima, which
evolutionary change. City functions depend on highly vary over fitness landscapes (Norberg et al. 2012). However,
interconnected infrastructures and on flows of material, historical contingency can also play an important role in
energy, and information from both adjacent regions (e.g., community assembly (Fukami 2015, De Meester et al. 2016).
via hydroelectric dams) and distant ones (e.g., via trade and Both ecologists and evolutionary biologists recognize that
telecommunication; Alberti et  al. 2018). Distant coupled the order and timing of species arrival during community

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Glossary

Contemporary evolution. Evolution of species’ traits observed in contemporary time (i.e., less than a few hundred generations).
Eco-evolutionary dynamics. Reciprocal interactions between ecological and evolutionary dynamics.
Ecosystem. An ecological unit that includes all of the organisms in a given area interacting with the physical environment. The flow
of energy and material leads to trophic structure and material cycles.

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Ecosystem function. Processes that control the flux of energy, organic matter, or nutrients in an ecosystem, including the flux of bio-
mass associated with trophic interactions.
Evolutionary change. Changes in allele frequencies within a single population due to natural selection, genetic drift, mutations and
gene flow.
Evolutionary rescue. Demographic recovery preventing extinction due to genetic adaptation within a population facing environmen-
tal stress.
Green infrastructure. A planned network of natural and seminatural areas with other environmental features, designed to protect
biodiversity and deliver a wide range of ecosystem functions.
Habitat. An ecological or environmental area characterized by both physical and biological features, which is inhabited by a particular
species or community of organisms.
Metacommunity. A set of interacting communities that are linked by the dispersal of multiple, potentially interacting species.
Monopolization. An evolution-mediated priority effect whereby the arrival order of species and their evolution influences community
dynamics and structure.
Niche construction. The process whereby organisms actively modify their own and each other’s habitat so that they influence their
evolution.
Press disturbance. Environmental disturbance that may arise sharply and then reach a constant level that is maintained.
Priority effect. The arrival order of species influences community dynamics and structure.
Regime shift. Large, abrupt change in the structure and function of a system causing a shift between two alternate stable states fol-
lowing discontinuous nonlinear dynamics.
Spatial insurance. Biodiversity provides spatial insurance for ecosystem functioning by spatial exchanges among local systems in
heterogeneous landscapes.
Species sorting. Community assembly mechanism in which species composition in a given locality or patch is determined by their
responses to the local environment (i.e., their niche), including the presence of other species in the locality or patch. The resulting
match between species occurrences and abundances with the environment is also fueled by dispersal allowing species to colonize
patches with their preferred habitat.
Urban ecosystems. Coupled human–natural systems in which people are the dominant agents and characterized by high human
population densities.
Urban. Areas where people live at high densities and in high numbers, or where the built infrastructure covers a large portion of the
land surface. The US Census defines urban agglomerations as having 2500 or more inhabitants, generally with population densities
of 1000 or more persons per square mile.

assembly can affect species abundance and the structure an urbanizing landscape are expected to be important, but
and function of the resulting communities. The arrival virtually no studies have tackled this in a systematic way.
order of species or genotypes in a specific habitat patch may We can gain some insights on such dynamics from work
influence the community and genetic structure and their examining climate change. Norberg and colleagues (2012)
dynamics (Fukami 2015). This priority effect influences show how under climate change the outcome depends on
community assembly and diversity through both ecological rates of evolution, dispersal, and environmental change, as
and evolutionary mechanisms and mediates the emergence well as the adaptive and dispersal abilities of different species
of ecological patterns under environmental change (Urban and genotypes.
and De Meester 2009, De Meester et  al. 2019). Time and Understanding the legacy effects arising from evolution-
the fate of local versus immigrant species and genotypes in ary priority effects and biogeographic history on community

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 Overview Articles

assembly and diversity is important for predicting the The evolving metacommunity concept provides a pow-
responses of species to urbanization (Cavender-Bares et  al. erful framework to address the potential for eco-evolution-
2016). Differences in eco-evolutionary responses among ary dynamics in urbanizing landscapes (Brans et al. 2020),
urban regions may reflect legacies from preurban land uses because it explicitly addresses multiple species (De Meester
and associated agricultural and forest practices (Ziter et  al. et  al. 2019) and spatial scales, and aims at integrating
2017). Patterns of biodiversity in urbanizing regions may also community and metacommunity dynamics (Leibold et al.
reflect the legacy of past human settlements and relatively 2004) with intraspecific trait variation and evolutionary
recent infrastructure constructed more than 100 years ago change in spatially explicit landscapes (Urban et al. 2008).
(Hahs et al. 2009). The time lag—the period of time between Urbanizing landscapes are ideally suited for this frame-

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a disturbance and its effect—might play an important role work because of the importance of spatial structure within
in urbanizing landscapes. For example, wetland biodiversity cities, the patch-like nature of urban centers in the land-
response is better explained by historical than current den- scape, the striking difference in size and spatial structure
sities of road construction (Findlay and Bourdages 2000). of environmental gradients among cities, and the explicit
Lagged eco-evolutionary responses to urban environments spatial context of urban sprawl. The evolving metacom-
interact with the cumulative nature of legacy effects of the his- munity context allows us to capture interactions between
torical development of cities to shape biodiversity responses ecological and evolutionary dynamics in the context of
to urbanization. In addition, both the speed of change in urbanization, and to also consider cross-scale interac-
urban environments and the variability across time, are criti- tions—for instance, when the metacommunity dynamics
cal to understanding whether species will evolve, disperse, or in urbanizing centers influence community assembly in the
go extinct. In many ways, urbanization might be one of the rural matrix by changing the pool of dispersing species or
fastest environmental changes and therefore might swamp genotypes. So far, very few studies have tried to tackle both
the adaptive responses of some species, replacing them with community and evolutionary dynamics along urbanization
generalist, short generation, or invasive ones. gradients (Brans et  al. 2017a). This is in part because of
How can we disentangle the impact of regional bio- the challenging nature of integrating space, ecological and
geographic processes and historical contingencies from evolutionary dynamics, and in part because most stud-
contemporary urbanization-driven evolutionary change on ies documenting evolutionary responses to urbanization
community assembly and diversity? Developing cross-com- are rather recent (Johnson and Munshi-South 2017). The
parative studies of cities where alternative eco-evolutionary approaches that can help move the field forward are very
outcomes have been observed against similar biophysical diverse and include the analysis of inter- and intraspecific
background and integrating evolutionary history could pro- trait variation along urbanization gradients and among
vide effective strategies to detect signature of legacy effects cities (Brans et  al. 2017a), the application of eco-evolu-
and explain urbanization-driven eco-evolutionary dynamic tionary partitioning tools, transplant experiments (Merilä
(Cavender-Bares et al. 2016). and Hendry 2014), manipulating community identity or
genetic identity along urbanization gradients, comparative
Evolving urban metacommunities surveys on evolving metacommunity structure across cities
Despite an increased understanding that the variation that differ in history or size, and monitoring both commu-
among and within species, including evolutionary dynam- nity and evolutionary dynamics in areas of urban sprawl
ics, can profoundly affect community dynamics and shape (Brans et al. 2020).
biodiversity (Bolnick et al. 2011), these processes have been The evolving metacommunity framework can also pro-
primarily studied in isolation. The multivariate and dynamic vide insights on how urbanization might influence responses
gradients typical of urbanizing landscapes can lead to both to other aspects of global change, such as climate warming or
species sorting and evolutionary trait change. This com- exotic species, because the spatial dimension of the spread of
plexity offers plenty of opportunities for eco-evolutionary exotic species and the fact that their evolution can affect the
interactions in a spatially explicit context. Recent research, success of invaders are characteristics captured by the evolv-
primarily in the context of climate change, has explored how ing metacommunity framework (Faillace and Morin 2016).
genetic variance and dispersal together affect eco-evolution-
ary dynamics and biodiversity along a dynamically changing Rethinking urban sustainability with an eco-
gradient (Norberg et al. 2012). Dispersal can prevent extinc- evolutionary perspective
tion by allowing species to move to areas with suitable envi- Evidence of accelerated evolutionary change associated
ronmental conditions (spatial insurance; Loreau et al. 2003), with urbanization highlights the importance of rethinking
whereas genetic adaptation can allow populations to persist urban sustainability strategies. However, our current limited
in a changing environment (evolutionary rescue; Loreau understanding of eco-evolutionary feedbacks and the lack
et  al. 2003, Bell 2017). Both processes interact, leading to of agreement on the overall ecological and evolutionary
dynamics that are profoundly different than one would prevalence and magnitude of these changes pose significant
expect in the absence of evolution or in the absence of other challenges to attempts to translate an eco-evolutionary per-
species (Urban et al. 2012, De Meester et al. 2016). spective into sustainability strategies.

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Overview Articles

A novel understanding of urban eco-evolutionary dynam- (De Meester et  al. 2016). However, lower genetic diversity
ics that fully accounts for cities’ complexity and hetero- may reduce the capacity of local populations to evolve and
geneity will constitute a key step toward bridging the gap therefore may limit the degree to which monopolization
between the science of urban eco-evolutionary dynamics occurs. Current findings show that urbanization can both
and sustainability practices. For example, different designs reduce and increase genetic drift and gene flow, differently
of urban infrastructure (e.g., stormwater or flood control) influencing genetic diversity and changing the dynamics set
have different impacts on pollution loading and hydrologi- in place by global environmental change (Miles et al. 2019).
cal connectivity, and different management strategies have Identifying the outcome of these dynamics across cities and
different effects on evolutionary mechanisms and ecosys- organisms’ groups is an important research question. Can

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tem feedback (Post et  al. 2008, Walsh et  al. 2012). Green alternative patterns of urbanization explain these alternative
infrastructure (e.g., street trees, bioswale, green roofs, and trajectories? What general properties of urban ecosystems
detention ponds) can facilitate adaptation and help main- can facilitate adaptation and maintain evolutionary poten-
tain genetic diversity (Lundholm 2015, Beninde et al. 2018, tial? Answering these questions requires characterizing the
Ksiazek-Mikenas et al. 2019). Alternative conservation and complexity of urban eco-evolutionary dynamics to generate
restoration strategies can reverse or buffer eco-evolutionary the knowledge that can inform the development of new
feedbacks (Kinnison and Hairston 2007, Carroll 2011). An principles for urban design and planning and a new urban
accurate representation of the variability of urban mecha- sustainability paradigm.
nisms associated with varied configurations of the urban
habitat is crucial to determining the importance and sensi- Conclusions
tivity of different factors to policy scenarios. Urbanization is altering biodiversity by directly and indi-
The uncertainty of future eco-evolutionary feedbacks rectly changing eco-evolutionary dynamics. Changes asso-
highlights the importance of maintaining both ecological ciated with urbanization alter interactions and feedbacks
and evolutionary diversity in a rapidly changing world. between ecological and evolutionary processes that can shift
Identifying early warning indicators might be critical to the balance between the probability of evolutionary rescue
anticipate potential consequences and implement miti- and extinction, affecting long-term evolutionary processes
gation strategies to promote ecosystem health in urban and ecosystem dynamics. But so far, little is known about
environments. Furthermore, uncertainty in species’ adapt- how patterns of urbanization shape eco-evolutionary out-
ability highlights the importance of conserving evolutionary comes at the scale of single cities, across urban centers in an
potential—the capacity of a population to evolve in response urbanizing landscape matrix, and even on a planetary scale.
to environmental change. Genetic diversity, together with We propose that emergent patterns of urbanization
dispersal, may shape the eco-evolutionary effects of environ- alter eco-evolutionary dynamics in ways that can generate
mental change. For example, although recent models of evo- complex feedbacks and unexpected outcomes. Cities affect
lutionary response to climate change disagree on whether ecological and evolutionary dynamics and their interac-
or not dispersal rates in evolving species assemblages can tions through habitat modification, changes in connectiv-
preserve biodiversity under environmental change, most ity and heterogeneity, novel disturbances, and altered biotic
models find that high genetic diversity minimizes extinction interactions. Different patterns of urbanization can pro-
risk (Thompson and Fronhofer 2019). duce different landscape signatures influencing ecological
Diverse strategies have been proposed to facilitate adapta- and evolutionary processes. These landscape signatures
tion and maintain or enhance genetic variation with respect can result in variable interactions between dispersal, local
to fitness and historic gene flow, including assisted migration genetic adaptation and species sorting that might reduce
and translocation of individuals likely to be more adapted to or reinforce the links between environments and species
new environments (Smith et  al. 2014). Maintaining eco- composition. We contend that accurately characterizing
logical diversity, particularly in the form of antagonistic the complexity of emergent patterns of urbanization is an
interactions (e.g., predation, herbivory, and parasitism), essential element to advance our understanding of eco-
also promotes resilience within species networks (Toju et al. evolutionary dynamics and feedbacks in an urbanizing
2017). For example, high levels of predation, parasitism, world and suggest that adopting an evolving urban meta-
and competition are characteristics of healthy ecosystems. community perspective can inform a new urban sustain-
Therefore, the persistence of antagonisms can help sustain ability paradigm.
eco-evolutionary feedbacks under perturbations in urban
habitats. To succeed, urban biodiversity conservation strate- Acknowledgments
gies must account for evolutionary processes in defining This overview article has benefited from collaborations of
management targets (Lambert and Donihue 2020). the National Science Foundation Research Coordination
Urbanization alters the distribution of genetic diversity Network (RCN): Eco-Evolutionary Dynamics in an Urban
through strong selection, changes in population size, and by Planet: Underlying Mechanisms and Ecosystem Feedbacks
altering gene flow. By reducing species diversity, urbaniza- (grant no. DEB 1840663) and from discussions among and
tion can increase the potential for monopolization effects input from the participants of the first RCN Workshop

788 BioScience September 2020 / Vol. 70 No. 9 [Link]

 Overview Articles

(Seattle 2019). We thank the editor and two anonymous global species distributions. Proceedings of the National Academy of
reviewers for their valuable comments that improved the Sciences 113: 6388–6396.
Bolchoun L, Drossel B, Allhoff KT. 2017. Spatial topologies affect local
manuscript. food web structure and diversity in evolutionary metacommunities.
Scientific Reports 7: 1818.
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