Challenge 2: Trait-environment relationships and the natural
history of organisms
General Application — Understanding the natural history of an
organism, including how it interacts with the environment, provides the
foundation for conducting hypothesis-driven adaptation research (Greene
1986, Tewksbury et al. 2014). Conducting research on trait-environment
relationships and natural history is challenging because it requires
time-consuming and detailed studies of how organisms utilize
environmental spaces, which may differ on spatial and temporal scales
and may be difficult to accomplish for cryptic or elusive taxa (Morris
1987). Adaptation research can benefit from museum collections to
understand historical and contemporary selective landscapes (Wandeler et
al. 2007), although geographic, taxonomic, and temporal bias in specimen
collection limit our ability to universally rely on this resource (Vawda
2019). Although there are challenges to obtaining high-quality DNA from
museum specimens, new methods applied to ancient DNA (e.g.,
Castañeda-Rico et al. 2020) are promising and open up new opportunities
for exploring temporal trends. In addition, plasticity can modify
trait-environment relationships on local scales (Lajoie and Vellend
2015, 2018), and thus, can make it difficult to make generalizations
about trait-environment relationships across populations and taxa.
Human Element — Urban organisms are relatively understudied, in
part because of a historical perspective that urban populations provided
little value in understanding “natural” selection due to their
proximity to humans, or because their perceived lack of potential for
novel research (Sukopp 1998, McPhearson et al. 2016). Evolutionary
ecology has only experienced a recent, but growing, appreciation of
urban ecosystems (Rivkin et al. 2019, Szulkin et al. 2020b), relying on
decades of natural history research in non-urban systems to develop
hypotheses of urban adaptation. Importantly, the human biases in
organism focus, specimen collection, and deposition into museum
collections have resulted in a paucity of historical resources for many
urban organisms, making urban retrospective analyses more difficult,
particularly for commensal species (Shultz et al. 2021, but see Major
and Parsons 2010, Meineke and Davies 2019). Although many environments
and taxa have been historically understudied, urban environments and
their associated organisms have been systemically understudied until
recently. Consequently, relatively little urban historical data exists
across taxonomic and geographic extents compared to other globally
distributed habitats (e.g., tropical rainforests) or global non-urban
taxa (e.g., stickleback fish). Framing contemporary adaptations in a
historical context is important because species may evolve through novel
adaptations in the contemporary selective landscape or through
filtering, or adaptive modification of existing traits (i.e.,
exaptations; Gould and Vrba 1982, McDonnell and Hahs 2015, Rivkin et al.
2019, Winchell et al. in review ). In addition, observational
studies can be time intensive in human-dominated spaces, in some cases
potentially generating suspicion and conflict with the community, and
private property boundaries limit access when conducting research on
urban organisms.
Misconceptions — A misconception perpetuated by knowledge gaps
in the natural history of urban organisms is that non-urban or historic
populations are always appropriate baselines in a comparative framework.
Although such comparisons are often informative, if we do not know how
trait-environment relationships differ within and between urban
environments then we may be misled about the nature of adaptation by
employing an inappropriate baseline. Inaccurate inference of present
interactions between traits and urbanization hinders our ability to make
informed predictions about urban adaptation. These gaps in natural
history knowledge are particularly consequential for species that are
more common in urban areas than in non-urban areas, such as rats and
pigeons. For example, urban rats (Rattus norvegicus and R.
rattus ) have been placed in historical contexts mainly from
archeological collections because museum collections lack specimens of
the species that commonly cohabitate with humans (Guiry and Buckley
2018), and so we might not know the true ancestral state to urban
adaptive responses. In extreme circumstances where we have no contrast
at all with non-urban populations, such as with the common bedbug
(Cimex lectularius ), we might reach incorrect conclusions about
how they have adapted specifically to urban environments based solely on
their present adapted state (Gould and Lewontin 1979).
Moving forward — To address gaps in knowledge regarding the
natural history and trait-environment relationships in urban organisms,
integrated research that combines observational studies (e.g., natural
history and behavioral research) with experimental data of species
living in cities is important. One approach to building a foundation of
natural history information for urban organisms that has been successful
in non-urban environments (Sforzi et al. 2018, Fontaine et al. 2021) is
to incorporate community-sourced data collection into research. For
example, Puckett et al. (2020) used museum specimens to study changes in
brown rat cranial shape over time, and Cosentino and Gibbs (2022) used
community-sourced data to demonstrate parallel evolution of clines in
melanic Eastern gray squirrels (Sciurus carolinensis ).
However, community-sourced data is often limited due to socioeconomic
biases of regions sampled or due to a limited sampling of overlooked,
camouflaged, or microscopic species that are less charismatic (Shirey et
al. 2021). Community partnerships in overlooked geographic regions can
provide a more comprehensive sampling of the urban landscape (Shirey et
al. 2021), while also augmenting museum collections with urban organisms
and building stronger relationships with local communities. Moreover,
equitable community partnerships provide benefits to both visiting
scientists and local communities, facilitate access to research
products, reduce potential for conflict, and provide valuable outreach
opportunities (Sforzi et al. 2018, Haelewaters et al. 2021, Shirey et
al. 2021, Shultz et al. 2021).