How urbanisation shapes evolution

By Rachel Chan

Around half the world’s population lives in an urban area: packed in cities that make up 0.5% of our planet’s surface (Ritchie & Roser, 2018; Schneider, Friedl & Potere, 2009). For the flora and fauna in urban areas, life is dramatically altered compared to that of their wild, non-urban counterparts. After all, a concrete jungle is very different from, well, an actual jungle. For some animals living in an altered environment bustling with human activity, full of noise, artificial light, and pollution, local adaptations unique to these city-dwelling populations can arise. A local adaptation is when selection occurs on standing genetic variation rather than novel mutations (Donihue & Lambert, 2015). Urban environments present unique and novel selection pressures, shaping the urban populations that reside in them. 

One such example of local adaptation is in the white-footed mice (Peromyscus leucopus) of New York City (NYC), where city-dwelling mice seem to be evolving in response to novel food resources. Single nucleotide polymorphisms (SNPs) were compared between transcriptome samples of rural populations and urban populations residing in different NYC parks. The urban population showed signatures of positive selection in genes associated with metabolic processes (Harris et al., 2013). As one can imagine, city-dwelling mice have different lifestyles to their rural counterparts, with different energy budgets, physiological stressors, and diets. Divergent allele frequencies of multiple candidate genes point towards diet-mediated selection in urban populations (Harris et al., 2013).

Fatty acid desaturase 1 (FADS1) is a gene important for the biosynthesis of omega-3 and -6 fatty acids from plant sources (Harris & Munshi-South, 2017). Allele frequencies for genes associated with glycine metabolism also differed between the populations – increased amounts of glycine help to regulate high-fat, high-sugar diets. Other intriguing candidate genes included those associated with non-alcoholic fatty liver disease, which is induced by increased consumption of fatty acids (Harris & Munshi-South, 2017). It seems that urban mice populations consume foods of a higher fat content in comparison to their rural counterparts. The typical rural diet includes arthropods, green vegetation, fruits, and nuts (Wolff, Dueser & Berry, 1985) These may be more available to urban populations through human food waste, different arthropod communities and invasive plant species (Harris & Munshi-South, 2017). Speaking of human food waste, these mice are opportunistic generalists and may also have developed an appetite for fast food. Think of NYC pizza (and its fatty acid content). These local adaptations allow the New Yorker mice to efficiently metabolise different types of lipids and carbohydrates. Here, the novel environment of a city park acts as unique selective pressure on the mice. Perhaps the descendant rats from Ratatouille experienced similar changes. 

Great tits (Parus major) are a particular species that thrive as city-dwellers, with them being one of the most dominant urban bird species in Europe (Brumm, 2004). This is owed to their phenotypic plastic in producing bird song. For males, birdsong is crucial in mate attraction and territory defense (Slagsvold, Sætre & Dale, 1994). In ten city-to-forest comparisons across Europe, it was shown that urban birdsong was shorter, faster, and of a higher pitch (Slabbekoorn & den Boer-Visser, 2006). This was not a one-off local phenomenon, and the song divergence was consistently observed throughout Europe. This can be attributed to the noise differences between the two habitats: anthropogenic noise pollution, especially from traffic which tends to be of a lower pitch. To be heard by other individuals, birdsong then needs to be higher pitched. 

It is this plasticity that has allowed great tits to be such a successful urban species. Vocal interactions are thought to be important; song production can be adjusted based on the neighbours in their breeding territory after dispersal (McGregor & Krebs, 1989). Songs that cannot be heard well may not be copied. As phenotypic plasticity allows great tits to survive in urban areas, it is unlikely that the urban phenotype will evolve into an urban species. However, selection can also operate on aspects of vocal production: perhaps morphological, physiological, or neurological aspects. Therefore, phenotypic plasticity can fuel genotypic divergence, providing an evolutionary pathway for urban speciation (Slabbekoorn & den Boer-Visser, 2006).

Rapid local changes within urban populations show the scope at which urbanisation has altered the lives of our non-human neighbours. These local adaptations are reminiscent of a more well-known example of rapid transformation in response to anthropogenic changes: the peppered moth (Biston betularia) during the Industrial Revolution. In the early nineteenth century, all peppered moths were cream-coloured with blackspots. By the end of the century, this original phenotype had been replaced by completely dark-coloured moths in industrial cities like Manchester, with lighter-coloured moths present in rural areas instead (Cook, 2003). The selection pressure driving this was soot. As coal burned, soot would cover trees where the moths rested. While dark-coloured moths were camouflaged, lighter moths were more likely to be predated upon by birds (Cook, 2003). It has recently been discovered that the mutation event responsible for the dark-coloured form is an insertion of a tandemly repeated transposable element in the first intron of the gene cortex (Van’t Hof et al., 2016). This transposition event occurred around 1819, meaning this mutation spread throughout industrial populations in the span of less than a century. Under human pressure, evolution is accelerated, leading to the rapid transformation of the moth. 

So, what happens to the species that do not evolve local adaptations quickly or lack phenotypic plasticity? Urbanisation tends to have a homogenising effect on species composition (Donihue & Lambert, 2015). Indeed, the same few species that thrive in a city environment are found in every city, such as the great tit, an ‘urban-adaptable’ species. Behavioural plasticity in great tits allow them to thrive, but bird communities lacking this would be severely impacted by noisy areas. For some species, city life is simply not an option. 

Globally, species in cities exhibit differences from their rural counterparts, developing these at often lightning speeds. As urban ecology becomes more prominent, more studies need to link phenotypic changes to genotypic changes and fitness benefits in order to demonstrate adaptation (Donihue & Lambert, 2015). Urban changes that induce these adaptations must also be experimentally identified. As it stands, the changes in urban species offer us insight into one of the many changes we inflict onto the natural world. 

References:

Brumm, H. (2004) The Impact of Environmental Noise on Song Amplitude in a Territorial Bird. The Journal of Animal Ecology. 73 (3), 434-440. Available from: doi:10.1111/j.0021-8790.2004.00814.x. 

Cook, L. M. (2003) The rise and fall of the Carbonaria form of the peppered moth. The Quarterly Review of Biology. 78 (4), 399-417. Available from: doi:10.1086/378925. 

Donihue, C. M. & Lambert, M. R. (2015) Adaptive evolution in urban ecosystems. Ambio. 44 (3), 194-203. Available from: doi:10.1007/s13280-014-0547-2. 

Harris, S. E., Munshi-South, J., Obergfell, C. & O’Neill, R. (2013) Signatures of rapid evolution in urban and rural transcriptomes of white-footed mice (Peromyscus leucopus) in the New York metropolitan area. PLOS One. 8 (8). Available from: doi:10.1371/journal.pone.0074938. 

Harris, S. & Munshi-South, J. (2017) Signatures of positive selection and local adaptation to urbanization in white-footed mice (Peromyscus leucopus). Molecular Ecology. 26 (22), 6336-6350. Available from: doi:10.1101/038141.

McGregor, P. K. & Krebs, J. R. (1989) Song Learning in Adult Great Tits (Parus Major): Effects of Neighbours. Behaviour. 108 (1-2), 139-159. Available from: doi:10.1163/156853989X00105. 

Ritchie, H. & Roser, M. (2018) Urbanization. Available from: https://ourworldindata.org/urbanization [Accessed 16th May 2021].

Schneider, A., Friedl, M. & Potere, D. (2009) A new map of global urban extent from MODIS satellite data. Environmental Research Letters. 4 (4). Available from: doi:10.1088/1748-9326/4/4/044003.

Slabbekoorn, H. & den Boer-Visser, A. (2006) Cities Change the Songs of Birds. Current Biology. 16 (23), 2326-2331. Available from: doi:10.1016/j.cub.2006.10.008. 

Slagsvold, T., Sætre, G. & Dale, S. (1994) Dawn Singing in the Great Tit (Parus Major): Mate Attraction, Mate Guarding, or Territorial Defence? Behaviour. 131 (1-2), 115-138. Available from: doi:10.1163/156853994X00244. 

Van’t Hof, A.,E., Campagne, P., Rigden, D. J., Yung, C. J., Lingley, J., Quail, M. A., Hall, N., Darby, A. C. & Saccheri, I. J. (2016) The industrial melanism mutation in British peppered moths is a transposable element. Nature. 534 (7605), 102-105. Available from: doi:10.1038/nature17951. 

Wolff, J., Dueser, R. & Berry, K. (1985) Food Habits of Sympatric Peromyscus leucopus and Peromyscus maniculatus. Journal of Mammalogy. 66 (4), 795-798. Available from: doi:10.2307/1380812.

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