'Urban cold islands' and adaptation in cities

The cover of the recent issue of Proceedings B. (Photo: Marc Johnson.)

I was not very optimistic when my M.Sc. supervisor, Dr. Marc Johnson, proposed that we study whether plants were adapting to urban environments. Looking back, with the study being recently published, it is clear that my pessimism was unwarranted. This study ended up being a very fun ‘whodunit’ with unanticipated discoveries around every corner, and one that will, it seems, keep on surprising us into the future.

During the summer of 2014, I was living at the Koffler Scientific Reserve at Joker’s Hill, the University of Toronto’s picturesque* field research station. There, I was conducting an experiment on the evolution of plant defences using white clover (Trifolium repens L.). This plant has a genetic polymorphism for the production of hydrogen cyanide (cyanogenesis), where within-population genetic variation causes some individuals to produce cyanide, and others to lack it.

A long history of research on the topic has armed us with a solid understanding of the ecological factors that drive the evolution of cyanogenesis in clover populations. In the field, populations at high latitudes and elevations tend to lack cyanogenesis, whereas populations at low latitudes and elevations are highly cyanogenic. The general hypothesis is that cyanogenesis is favoured in warm climates because of high herbivory. In cold habitats, cyanide—which is normally stored in tissues in a benign state and is activated locally only where herbivores disrupt the plant’s cells**—is selected against because freezing ruptures plant cells and causes self-toxicity when cyanide is released involuntarily.

Me and my clover mane.

Because I was already familiar with the clover cyanogenesis system, Marc came to me with an idea that cyanogenesis may evolve along urbanization gradients. Our prediction was straightforward: given that freezing temperatures select against cyanogenesis, we expected urban heat islands would reduce the incidence of freezing and therefore relax selection against cyanogenesis in cities. (Herbivores don’t seem to have a consistent relationship with urbanization.) Because the urban heat island causes gradual increases in temperature toward urban centres, we expected to see more cyanogenesis in natural clover populations with increasing proximity to the city.

On a humid July morning in 2014, Marc picked me up at the Koffler Reserve and we set off to collect plants along an urbanization gradient. We stopped every kilometre to sample, and our sites ranged from idyllic countryside to chaotic downtown Toronto. We sampled two additional transects in Toronto—in August and again in September. I screened each plant for cyanide, and quantified how the proportion of cyanogenic plants in populations changed along the urbanization gradient.

From what I hear it’s pretty uncommon to get a clean result in science, and even less common to get a clean result that is the exact opposite of one’s prediction. Our results followed the latter scenario: cyanogenesis was lowest in the urban centre, and increased toward rural areas—the opposite of what we had predicted. The reason for this, we naïvely thought, was so obvious: lower herbivory in the urban centre is relaxing selection for cyanogenesis there.

Figure 1 from our paper. In three of four cities, the frequency of cyanogenesis increased toward rural areas.

We rationed that we needed to do an experiment to test whether herbivory changed along the urbanization gradient***. This came with the unsettling realization that I would have to procure space on lawns from folks that lived in urban, suburban, and rural areas. I secured my urban and suburban sites mostly by emailing people I knew, but I lacked rural sites. Marc advised that I’d need to go door-to-door and solicit people for lawn-space donations in order to cover the full urban-rural gradient. After many discouraging answers of ‘no’ and some slammed doors, I finally hit a stride. In the end, more than half of my 40 study populations were on the private property of generous citizens. 

While the field experiment was ongoing, I wanted to see if the patterns we observed were unique to Toronto. I, along with Marc and our co-author, Marie Renaudin, loaded up the lab car and sampled clover populations along transects in Montreal, Boston, and New York City. The trip had some ups and downs. The downs included being kept awake until the wee morning during a torrential downpour (in a leaky tent) because our campsite-neighbours were blasting Evanescence. Our car also broke down in downtown Boston and needed a new alternator, putting us a day behind. Despite these hiccups, we managed to get plants from all three cities back to the lab. We found that patterns in both Boston and New York City were consistent with what we observed in Toronto, but there was no pattern in Montreal.

The three authors about to depart on a ferry crossing the Ottawa River to Oka, QC.

When the field experiment ended, we were surprised to find that there was no change in herbivory along the urbanization gradient in Toronto. This was initially disappointing because I was left with no ideas about the causal factor, but this feeling didn’t last. At my committee meeting, the ever-insightful ecologist, Peter Kotanen, posed an alternative explanation for our findings. Peter suggested that reduced urban snow cover caused by the heat island effect could ultimately leave plants exposed to cold air temperatures, while rural plants would be kept warm by a relatively thick layer of insulating snow cover.

After Peter’s ecological revelation, I was especially glad that Marc had asked me to put out some ground-level temperature probes during the previous winter. Sure enough, when I looked closely at the data from these probes, it was perfectly in line with Peter’s hypothesis. The data show that urban ground temperatures were much colder than rural ground temperatures during the winter, and that this pattern reverses following snowmelt. We’ve taken to calling this pattern the ‘urban cold island’ effect****. In the paper, we use remote sensing and weather station data to suggest that this urban cold island effect doesn’t happen in Montreal because of exceptionally high snow cover along the entire rural-urban gradient.

Figure 3A from our paper. The 'relative urban coldness' index shows the cold island (values above 0) appearing during the winter, and then changing back into a heat island (values below 0) following snowmelt at the end of winter.  Curve is 95% CI. More details in paper.

The next steps of this work, on which other lab members are taking the lead, are very exciting. We’re testing whether snow cover actually changes selection on cyanogenesis. We’re also quantifying gene flow along urbanization gradients, and sampling transects in cities of different sizes and with different climates. From what I've seen of the preliminary results, it seems that many more surprises await. 

Sampling clover at the Washington Monument.

Growing up in a big city is a fantastic way to be exposed to a wide range of diverse cultures, perspectives, and ideas. Just as exposure to diversity of human ideology/sexuality/culture (etc.) is important for generating an appreciation of the human world, exposure to biological diversity is important for us to attain a grounded perspective of our place in the world. Unfortunately, when human diversity and abundance increases, biodiversity tends to decline. Today, urban areas are expanding rapidly and an increasing proportion of humans are living in cities. With this, more young people than ever are growing up disconnected from nature. (A poetic example of this is how city lights erase the stars, making it even easier to forget our origins.) While some people are able to regularly leave the city, many—especially those from disadvantaged groups—are stuck in the city and thus can only experience nature there.

While urban evolution studies may be well-suited for testing fundamental questions in evolution, they have a unique ability to motivate ecologically-minded urban design & policy. There have been many ecological studies conducted in urban environments, but it’s not always clear that the variables measured are important for the biology of organisms. The unique promise of urban evolutionary studies is to identify the ecological variables that affect biological fitness (i.e., 'reverse ecology') in cities, and in doing so can motivate urban design that mitigates such stressors. My ultimate hope for the field of urban evolutionary biology is that its discoveries are used to generate in city-dwellers a curiosity for the natural world. And who knows, maybe some theoretical advances will be made along the way.

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Ken A. Thompson is a Ph.D. student studying adaptation and speciation at the University of British Columbia. To learn more, visit his website.

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*This isn’t just my opinion—a recent film adaptation of Anne of Green Gables, staring Martin Sheen, chose to film there because of its rural scenery. 

**Over 3000 plant species from 110 different families (from ferns to flowering plants) are cyanogenic. The release mechanism invariably is akin to a ‘bomb’, where the two cyanide compounds—a cyanogenic glycoside molecule and an enzyme that cleaves the HCN molecule from the glycoside—are stored in different parts of the cell and only brought together following tissue disruption.

***Studying patterns of herbivory on wild plants wouldn’t work because we knew that defense was strongly associated with the gradient.

****To our knowledge we are the first to document this phenomenon.