Challenge 1: Methodological approaches
General Application — Studies of adaptation have historically
relied on a mix of observational and experimental methods. Adaptation
research often focuses on divergent habitats, although clines across
environmental transitions have also been instrumental in studying local
adaptation (Endler 1986, Kawecki and Ebert 2004, Hereford 2009). Yet it
can be difficult to define the boundaries of habitats and populations in
heterogeneous landscapes (see Challenge 4) and environmental variation
may present as mosaics rather than gradients. Certain organisms may be
more tractable for the quantification of natural selection because of
their reproductive cycle, demography, generation time, and geography,
which may bias the organisms we choose to study. In particular,
approaches requiring movement of organisms between habitats, such as
reciprocal transplantation, are not feasible for all organisms, can be
prohibitively expensive and time consuming, may require unattainably
large numbers of replicates to obtain sufficient statistical power, can
facilitate the spread of diseases and parasites, and may be impossible
for ethical or legal reasons (Cunningham 1996, Kawecki and Ebert 2004,
Blanquart et al. 2013, Johnson et al. 2021). Common approaches for
adaptation research, such as mark recapture and long-term monitoring,
which have been crucial in disentangling the temporal dynamics of
adaptive evolution (e.g., Grant and Grant 2014), may be compromised by
external factors such as natural disasters and logistics of carrying out
such projects (e.g., funding and researcher continuity). Genomic
approaches to identifying local adaptation are becoming increasingly
common and may be valuable complements to field research methods, yet
genomic approaches come with their own methodological limitations as
well (Hoban et al. 2016, Perrier et al. 2020). Lastly, interpersonal
interactions between researchers and local community members in any
environment can be friendly and educational — offering opportunities
for broader impacts of research activities — but can also pose safety
risks for researchers (Demery and Pipkin 2021).
Human Element — Some methods that may be relatively easy to
employ in non-urban settings may be untenable in urban environments (or
vice versa). Urban adaptation can be influenced by factors related to
greater human activity that are difficult to control using traditional
manipulative experiments or may be difficult to predict. Direct and
indirect human interactions with wildlife can shape behavioral responses
and adaptations (e.g., pedestrian behavior, Bateman and Fleming 2014)
and human activities can drastically transform urban environments even
on short timescales (see Challenge 3). Rapid or unanticipated
anthropogenic modifications in cities limit the establishment and
success of studies that involve repeated sampling and long-term
monitoring (McPhearson et al. 2016). The mosaic of private and public
lands in urban environments intersecting with human and wildlife
activity adds additional complexity to the methods that can be employed
to conduct urban adaptation research. For example, mark-recapture
methods to estimate selection gradients can be challenging because
marked individuals can move into inaccessible anthropogenic spaces that
dominate urban landscapes, such as restricted-access private property
(e.g., backyards or inside homes). Similarly, a random sample of the
environment for population genomic analyses could be hampered by private
property access in non-random ways across the urban landscape. Some
methods may unintentionally facilitate human-wildlife conflict (Treves
et al. 2006, Kansky et al. 2016, Schell et al. 2020), disease
transmission between urban wildlife and domesticated animals and humans
(Bradley and Altizer 2007, Brearley et al. 2013), and biological
invasion (Hufbauer et al. 2012, Borden and Flory 2021). Community
members tend to be more concerned and vocal about these potential
threats when they occur near their homes (Dickman et al. 2014, Drake et
al. 2020). Additionally, urban areas are characterized by a higher
density of human presence, which increases interactions between
researchers and the public and law enforcement, both positive and
negative, and can be problematic when urban sites are repeatedly
accessed (Dyson et al. 2019, Des Roches et al. 2021).
Misconceptions — A misconception perpetuated by methodological
challenges to urban adaptation research is that only specific
approaches, such as reciprocal transplants, provide strong support for
local adaptation (e.g., Donihue and Lambert 2015, Lambert et al. 2021,
Diamond et al. 2022). Although common garden and reciprocal transplant
studies are informative for evaluating evidence of local adaptation in
some taxa, such as invertebrates or plants (Yakub & Tiffin 2017, Gorton
et al. 2018, Chick et al. 2020, Tüzün and Stoks 2020, Yilmaz et al.
2020, Diamond et al. 2022), they are not informative or feasible for all
taxa. Advocating broadly for “gold standard” methods might lead to an
overrepresentation in urban adaptation research of organisms,
microhabitats, or geographic regions most amenable to these approaches.
Extrapolating findings based on a restricted set of methods or taxa
could lead to incorrect conclusions regarding the generalizability and
prevalence of urban adaptive responses.
Moving Forward — To address the methodological challenges
associated with human presence and activity in urban landscapes,
research efforts that employ complementary and innovative methods will
provide different pieces of the adaptation puzzle (Figure 1). As in
non-urban environments, multifaceted approaches will be most robust for
detecting and characterizing local adaptation (Kawecki and Ebert 2004,
Barrett and Hoekstra 2011). As a result of increased human interactions
in urban areas, collaborations among diverse disciplines can become more
commonplace and bring new technology and methodology into urban
adaptation research (McPhearson et al. 2016). Interdisciplinary
approaches may be particularly valuable in urban ecosystems, where both
empirical and applied science involve human activities and have the
potential to promote human well-being (McPhearson et al. 2016).
Inclusion of local communities in urban and non-urban systems alike can
improve the success of methodological approaches via the incorporation
of local knowledge (Uprety et al. 2012, Camacho et al. 2021) and will
help improve researcher outcomes in terms of safety, access, and study
continuity (e.g., continued or repeated access, reduced vandalism).
There are several examples where integrated approaches have been used to
build a more comprehensive picture of urban adaptation: research onAnolis lizards has incorporated behavioral, phenotypic,
experimental, and genomic analyses to understand adaptation to thermal
and structural habitats (Winchell et al. 2016, Aviles-Rodriguez et al.
2019, Campbell-Staton et al. 2020); work on white clover
(Trifolium repens ) has involved the global community in sampling
efforts complemented with experimental, phenotypic, and whole genome
sequencing analyses to test for parallelism (Thompson et al. 2016,
Santangelo et al. 2020b, 2022); research on Galapagos finches
(Geospiza spp.) has employed morphometrics and behavioral
approaches to understand how access to human foods alter historical
patterns of diet-based selection on beak shape (De León et al. 2011,
2018); and a combination of reciprocal transplants, phenotypic
variation, and mate choice experiments in Tungara frogs
(Engystomops pustulosus ) has revealed adaptive sexual selection
(Halfwerk et al. 2019).