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).