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This blog post was originally published by the Ecology and Evolution Blog in February 2019.  Credit: Alexandra DeCandia, Princeton University By Alexandra L. DeCandia True to its name, the Anthropocene is characterized by human-mediated environmental change on a global scale. Currently, over 7.7 billion humans reside on our planet, 55% of whom live in cities. As a result, an estimated 3% of earth’s land surface is considered urbanized, with all of these values expected to increase in the next century [1]. As natural lands are coopted for human habitation and resource production, wildlife are left with three options [2]:
In each case, urbanization can raise conservation concerns or increase the potential for human-wildlife conflict. Thus, understanding the ecology and evolution of urban wildlife systems becomes critical for peaceful and long-term coexistence between humans and our neighboring wildlife. Red foxes (Vulpes vulpes) are an ideal study system for examining the effects of urban wildlife colonization. These flexible, mid-sized carnivores are capable of thriving in diverse habitats from natural landscapes through dense city centers [3]. Found across the northern hemisphere, urban fox colonization is especially pronounced in Europe, where foxes have successfully colonized cities since the 1930s. Aspects of their ecology, such as dietary preferences, disease transmission, and movement patterns, have been studied for decades. Yet there are still open questions about the consequences of urban fox colonization, both in terms of ecology and evolution. To better understand the evolutionary side of things, my collaborators and I set out to characterize the genetic effects of a relatively recent urban colonization event [4]. In the mid-1980s, red fox sightings in Switzerland increased dramatically after rabies was successfully eradicated. As rural populations expanded, more and more foxes moved into the Zurich metropolitan area [5]. Interestingly, movement studies showed that foxes settled in rural and urban areas tended to stay within one habitat type – even if they lived right on the border. That meant that rural foxes typically stayed in rural areas, and urban foxes typically stayed in urban ones. Since genetics are the raw material of evolution, understanding patterns of genetic diversity in these rural and urban foxes can provide insights into fox demography, colonization history, and chances of long-term survival. Thus in 2003, researchers used eleven neutral markers – or non-coding DNA with no known function – to describe the genetics of this so-called “city fox phenomenon” [6]. They reported decreased genetic diversity in urban foxes, and hypothesized that Zurich was colonized through two independent founder events: one east and one west of Lake Zurich, the Limmat River, and the city center. Though this study was among the first to examine the genetics of urban colonization, it was unable to consider potential adaptive differences between rural and urban foxes due to its use of neutral genetic markers. This may gloss over functional changes that occur to better suit unique aspects of each environment. For example, city foxes may experience different pressures than rural foxes, such as greater human presence, light and noise pollution, anthropogenic food availability, and disease exposure. Especially if foxes remain localized to one habitat type, these pressures may lead to selection on different behavioral, metabolic, or immune pathways in urban versus rural foxes. In our study, we revisited the Zurich city fox phenomenon with expanded datasets to consider the neutral and potentially adaptive consequences of urban colonization. We used nine genetic markers linked to functional immune genes and another 10,149 markers found throughout the genome. Our samples included resident foxes living in two urban and three rural locations in the Zurich metropolitan area. Consistent with previous movement and neutral genetic data, we found evidence of population structure between rural and urban foxes. In essence, foxes sampled in each area were more similar to one another than they were to foxes sampled elsewhere. We also observed that foxes east of the center-city landmarks (i.e., Lake Zurich, the Limmat River, and urban infrastructure) were distinct from foxes sampled to the west. This suggested that foxes don’t often cross those barriers to mate with individuals on the other side. In addition to population structure, we found decreased diversity in urban foxes when compared to rural foxes. Patterns of diversity at the genome-wide loci suggested a recent genetic bottleneck, whereby a large population quickly reduces in size (as is typical of founder events) and consequently loses variation. (Think of marbles in a bucket: if you have 150 marbles of different colors but only pull out 20 for a small jar, you can’t possibly capture all of the variation of the larger bucket. Genetic bottlenecks work similarly.) Despite these diversity losses, we observed evidence for balancing selection (which maintains variation) at markers linked to immune genes. This may be due to the selective advantage that comes from diversity, which can enable better recognition and response to different diseases [7]. We also found a number of genome-wide markers that were associated with urbanization. Interestingly, these markers were found in genes with functions related to metabolism, drug tolerance, immune processes, and colonization relevant behaviors (such as exploration, movement, circadian rhythms, and fear). These results may suggest local adaptation during urban colonization. As such, they provide a launching point for future studies looking for genes or gene functions that commonly recur across urban colonization events. By examining larger datasets (e.g., full genome sequences) in diverse species (from insects to reptiles to mammals etc.) around the world, we can discover the common ecological and evolutionary processes that characterize urban colonization. We can also identify unique challenges that urban environments pose to wildlife along the urbanophobe to urban exploiter spectrum. This will enable better monitoring and management of urban wildlife populations in the Anthropocene, and facilitate peaceful coexistence with our local wildlife in perpetuity. Works Cited
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