Received: 3 July 2020 | Accepted: 31 July 2020

DOI: 10.1111/mec.15589

NEWS AND VIEWS

PERSPECTIVE

Genomic evidence for parallel adaptation to cities

Colin J. Garroway | Chloé Schmidt

Department of Biological Sciences,

University of Manitoba, Winnipeg, MB, Urban evolutionary biology is the study of rapid evolutionary change in response to
Canada humans and our uses of land to support city dwellers. Because cities are relatively

Correspondence
Chloé Schmidt and Colin J. Garroway,
Department of Biological Sciences,
University of Manitoba, Winnipeg, MB,
Canada.
Emails: schmid46@myumanitoba.ca (CS);
colin.garroway@umanitoba.ca (CJG)
Funding information
Natural Sciences and Engineering Research
Council of Canada
modern additions to the natural world, research on urban evolution tends to focus
on microevolutionary change that has happened across a few to many hundreds of
generations. These questions still fall under the broad purview of evolutionary ecol-
ogy. However, the severity, rapidity and replication of environmental changes that
drive evolution in this context make it worthy of specific attention. Urban evolution
provides the opportunity to study the earliest stages of evolution in a context that is
scientifically interesting and societally important. The newness of urban populations
and their proximity to natural populations also creates challenges when trying to de-
tect population genetic change. In a From the Cover article in this issue of Molecular
Ecology, Mueller et al. use whole genome resequencing data to address some of these
challenges while exploring genetic changes associated with urbanization in three rep-
licate urban-rural burrowing owl (Athene cunicularia) populations. Combining multiple
approaches across these sample sites Mueller et al. find evidence for selection on
genes whose function is related to synapses, neuron projections, brain connectiv-
ity and cognitive function in general. That selection was parallel suggests that phe-
notypes related to brain processes were probably particularly important for urban
adaptation.

KEYWORDS

adaptation, birds, contemporary evolution, ecological genetics, natural selection

It wasn't until the early 20th century that ecological geneticists dis-
covered that natural populations harbour considerable amounts of
genetic variation (e.g., Dobzhansky & Queal, 1938; Ford, 1964). Since
then we have built our modern understanding of evolution on the
exploration of how this genetic variation arises and changes through
space and time. The relatively recent emergence and subsequent
expansion of cities has created a natural experiment well suited for
studying how rapid environmental change reshapes populations and
their genetics at the earliest stages of evolutionary divergence and
adaptation. The land covered by cities expanded by 80% between
1985 and 2015, having grown from 362,747 to 653,354 km2 (Liu
et al., 2020). The rate of urban expansion substantially outpaced the
growth rate of the global human population (52%) during the same
period (United Nations, 2019). This suggests urban growth well be-
yond simple housing needs. The proportion of the human population
living in cities is projected to grow from 55% to 69% by 2050 (United
Nations, 2019). It seems clear that cities are the planet's newest
major habitat type and that their growth will continue to disrupt
natural lands for the foreseeable future. The increasing ability for
single research groups to produce resequenced full genome-based
data sets provides the data resolution needed to explore important
aspects of the demography of urban colonization and the genetic
basis of adaptation.
All evolutionary processes shape evolution in cities (reviewed by
Johnson & Munshi-South, 2017). The most comprehensive evidence
for urban evolution comes from work on selection on phenotypes
(e.g., Alberti et al., 2017) and analyses of drift and reduced gene
flow based on neutral genetic markers (e.g., Miles, Rivkin, Johnson,
Munshi-South, & Verrelli, 2019; Schmidt, Domaratzki, Kinnunen,
Bowman, & Garroway, 2020). Work on adaptive urban evolution at

Molecular Ecology. 2020;29:3397–3399. wileyonlinelibrary.com/journal/mec© 2020 John Wiley & Sons Ltd | 3397
3398 | GARROWAY and SCHMIDT
the molecular level is still relatively rare (DeCandia et al., 2019; Harris
& Munshi-South, 2017; Perrier et al., 2018; Theodorou et al., 2018)
with whole genome-based analyses rarer still. Mueller et al.'s (2020)
work in this issue of Molecular Ecology, which is supported by pre-
vious full genome-based analyses of the demography of the same
study populations (Mueller et al., 2018), exemplifies the new direc-
tions made possible with access to whole genomes.
Mueller et al.'s (2018, 2020) study system is three urban–rural
population pairs of Argentinian burrowing owls (Athene cunicularia;
Figure 1). Burrowing owls typically use the burrows of fossorial
mammals associated with open grasslands for nesting. Intriguingly,
it seems to have been the emergence and spread of a behavioural
innovation, the ability to excavate their own burrows, that allowed
these owls to colonize cities (Martínez, Baladrón, Cavalli, Bó, &
Isacch, 2017). After sequencing and assembling a burrowing owl ref-
erence genome, Mueller et al. (2018) resequenced individuals from
the three population pairs to explore the demography of urban colo-
nization. This is important because the degree to which populations
can diverge and become adapted to local environments depends in
part upon the strength of selection and the homogenizing effects of
gene flow into cities. It is also important to explore demography be-
cause we expect bottlenecks in urban populations, and rapid reduc-
tions in genetic diversity can create false signals of selection. Cities
tended to have fewer rare variants than rural sites. The high-res-
olution genomic data from resequencing meant that they could
detect relatively weak signals of genetic structure that suggested
that the colonizations of cities were independent. These analyses
also suggest consistent but low levels of gene flow. This means that
the cities could be considered replicates in analyses of adaptive
divergence. Approximate Bayesian analyses could reconstruct the
colonization history of the cities well (Boitard, Rodríguez, Jay, Mona,
& Austerlitz, 2016). Effective population sizes in each city over the
past 500 generations (~1,250 years) declined from ~ 100,000 to 100
while rural populations remained relatively constant. Before this pe-
riod urban and rural populations shared the same history. Low effec-
tive population sizes suggest that selection may be less efficient in
cities than in natural populations.
These demographic analyses set the stage for this issue's paper
exploring genomic signals of urban adaptation. Genomic signals
of selection will be tough to detect in most urban situations for
the reasons noted above and due to small sample sizes coupled
with the high likelihood of polygenic adaptation and reduced ge-
netic variation. However, the experimental set-up added con-
fidence to analyses by allowing the authors to assess consensus
across four analytical approaches for identifying loci under selec-
tion replicated across three populations. No genomic site reached
genome-wide significance for any association. Given that effect
sizes would need to be quite large, this is perhaps unsurprising.
However, a gene-set analysis on the strongest signals suggested
significant enrichment of genes related to synaptic function, neu-
ron projections, and genes associated with brain connectivity and
cognitive function. Replication allowed for the probably meaning-
ful but weak genomic associations with urban environments to be
distinguished from false signals.
Although the replication in this study was treated as necessary
for robust analyses of local adaptation, these results also give insight
into the reuse of genomic variants by selection. This reuse seems to
be rare. A synthetic analysis suggested that the probability of gene
F I G U R E 1 Burrowing owls (Athene
cunicularia) typically use the burrows of
fossorial mammals associated with open
grasslands for nesting. Relatively recently
these owls have learned to excavate their
own burrows. This behaviour spread,
allowing some populations to colonize
cities where burrows were otherwise
unavailable. Whole genome resequencing
of owls from three cities suggests that
colonizations were independent, and
that urban populations tend to have
lower effective population sizes and
less diversity than rural populations.
Consensus across multiple analytical
approaches applied to samples from these
three replicate populations suggests
that there has been selection on genes
whose function is related to synapses,
neuron projections, brain connectivity and
cognitive function in general
GARROWAY and SCHMIDT
reuse across species was between 0.32 and 0.55 (Conte, Arnegard,
Peichel, & Schluter, 2012). Ecological experiments with stick insect
ecotypes suggested that just ~ 20% of genomic divergence in similar
environments was parallel (Soria-Carrasco et al., 2014). Laboratory-
based parallel evolution experiments on microbes have confirmed
that natural selection can indeed act in parallel across replicate pop-
ulations; but they also highlight the importance of chance and con-
tingency during adaptive genomic divergence (Meyer et al., 2012).
That selection acted on genomic regions with consistent functional
enrichment in parallel across similar environments in the burrowing
owls is interesting and suggests that urban selection pressures on
cognitive function are particularly strong. Hinting at a general trend
in birds, a recent preprint exploring genomic signals of selection
across multiple cities in great tits (Parus major) also found evidence
for repeated selective sweeps in regions linked to neural function
(Salmón et al., 2020). Additionally, species with larger brains tend to
be more urban-tolerant than those with smaller brains—this is per-
haps due to those species having greater behavioural flexibility (e.g.,
Callaghan et al., 2019; Sayol, Sol, & Pigot, 2020). The replication of
results across multiple sample sites means that we can be confident
in the study's findings. However, most instances of genomic diver-
gence seem not to be parallel. Thus, the challenge of identifying in-
teresting idiosyncrasies acting within individual cities remains.
ORCID
Colin J. Garroway https://orcid.org/0000-0002-0955-0688
Chloé Schmidt https://orcid.org/0000-0003-2572-4200
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How to cite this article: Garroway CJ, Schmidt C. Genomic
evidence for parallel adaptation to cities. Mol Ecol.
2020;29:3397–3399. https://doi.org/10.1111/mec.15589