If you live in North America, Europe, Asia, or almost any other temperate environment, you’ve probably seen Trifolium repens, an unassuming white clover popular with bees and unpopular with homeowners fixated on a perfect lawn. Native to Europe and Asia, this hardy species has spread all over the globe with an assist from humans who introduced it to new environments for livestock to graze on. But T. repens didn’t stay put in those rural farmlands: as the clover was advancing into any available grassy area, cities were encroaching on surrounding countryside. Today, white clover is everywhere — in bucolic fields, urban parks, and the sidewalk cracks of bustling metropolises. Since this country weed has taken up life in the big city, it has also experienced a pronounced evolutionary change…
Where's the evolution?
New research suggests that as T. repens became a city weed, it also lost a common plant adaptation that offers protection from herbivores. This adaptation takes the form of a noxious cocktail. When an herbivore bites down on a plant with a working defense system, two chemicals are released from different parts of the plants’ cells, mix together, and react to form hydrogen cyanide, a bitter compound that disrupts an animal’s ability to use oxygen and can be fatal. While a single bite of clover won’t kill a cow, some insects are repelled. In fact, this mechanism of defense is so common among plants that herbivores have evolved various strategies for dealing with the toxic chemical, allowing them to chomp away happily.
Many white clover plants ward off herbivores with hydrogen cyanide. However, if either of the genes responsible for producing the two chemicals that form hydrogen cyanide is broken, so is the entire defense system. When researchers sampled almost 10,000 clover plants from 20 cities and their outlying areas, they found that the plants closest to the city center were most likely to have “broken” hydrogen cyanide defense systems, with this trait less and less common (and hydrogen cyanide more and more common) the further out of town the plants grew. The pattern was remarkably consistent from city to city regardless of how large the urban area was. Some aspect of city life must be making life more difficult for plants that produce hydrogen cyanide, selecting for plants that carry broken versions of the genes — but what could it be?
In general, producing defensive chemicals involves a trade-off. It requires extra energy that could otherwise be put towards growth and reproduction. One hypothesis is that city plants experience less herbivory, so the advantage of warding off nibbling insects is outweighed by the energetic cost of that protection. This could potentially explain the pattern in hydrogen cyanide production that the researchers observed. However, a well-established side effect of hydrogen cyanide strongly supports another idea: for physiological reasons, this compound makes plants that contain it more sensitive to cold and vulnerable to freezing.
While cities are generally warmer than surrounding areas, in part because of this, less snow accumulates in cities — and snow is actually an insulator; it keeps the ground that it covers from experiencing as high or as low temperatures as does the air above it. With less snow cover, plants in cities experience colder temperatures than plants in rural areas do (though on average, temperatures are warmer). These colder temperatures seem to have given an advantage to city-dwelling plants carrying broken hydrogen cyanide genes. Those plants were less likely to freeze to death and more likely to pass copies of those broken genes on to the next generation than plants that produced hydrogen cyanide. Over many generations, non-functional hydrogen cyanide genes became common among city plants, while remaining rarer among populations in rural areas.
This classic example of natural selection in action illustrates that evolution is going on around us today and that it’s not restricted to so-called “wild” populations. In fact, environmental change caused by humans and their urbanized landscapes is a prime driver of modern natural selection. We should expect to see more of these examples, particularly as climate change begins to affect species more significantly. Even hardy weeds like T. repens will not weather major environmental change without some impact. Climate change models predict that more extreme seasonal temperatures in many areas as well as less snow cover; will other plant species that have a hydrogen cyanide defense system begin to lose it (and the protection from herbivores it offers), just as urban populations of T. repens are? As the climate continues to warm, will we observe this transition in rural plants as well? Stay tuned to find out!
News update, June 2022
When we last reported on white clover’s evolutionary response to city life, the scientists leading the research had data from eight cities in one Canadian province. This year, they updated their results to include 160 cities in 26 countries around the world, revealing how a common plant is evolving at a global scale. The new data show consistent patterns in which plant populations are most likely to lose or retain the ability to produce hydrogen cyanide, highlighting the likely causes of this evolution. As with the previous research, having lots of herbivores around nibbling at the plants favors individuals that produce hydrogen cyanide, and this effect is stronger in rural than in urban areas. Drought conditions (which often change as one moves from cities to the countryside) also favored plants that produce hydrogen cyanide – a finding further backed up by experiments. However, the additional data from around the world didn’t reveal any important effect of temperature or snowpack on whether hydrogen cyanide production is advantageous. Stay tuned to find out whether pollution or gene flow from clover planted on farms plays a role in this case of evolution in action; the research team plans to investigate these factors in future studies.
- Johnson, M. T. J., Prashad, C. M., Lavoignat, M., and Saini, H. S. (2018). Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens). Proceedings of the Royal Society B. 285. DOI: 10.1098/rspb.2018.1019. Read it »
- Santangelo, J. S., Ness, R. W., Cohan, B., Fitzpatrick, C. R., Innes, S. G., Koch, S., … and Johnson, M. T. J. (2022). Global urban environmental change drives adaptation in white clover. Science. 375: 1275-1281. Read it »
Understanding Evolution resources:
- The basics of how natural selection works to produce adaptations
- A tutorial on common misconceptions about natural selection and adaptations
Background information from Understanding Global Change:
- In your own words, describe the primary difference in urban and rural environments that is driving the evolution of white clover described above.
- What trait is being selected against in clover living in urban areas?
- Having a defense system against herbivores seems like an advantageous trait for a plant. Describe the trade-off associated with this trait and how that trade-off is affecting plants living in cities.
- Review the process of natural selection. Use the four steps described on that page to explain how broken hydrogen cyanide genes might increase in frequency over generations in response to very low temperatures.
- This article from the New York Times states, “It [white clover] is one of the most rapidly evolving species of flora, learning quickly how to survive in the toughest of urban environments.” Is it accurate to say that the clover “learned” how to survive? Describe why or why not.
- Teach about how environmental changes impact organisms: In this classroom activity for grades 3-5, students observe and conduct an experiment to see whether differences in salinity (the environment) have an effect on the hatching rate and survival of brine shrimp.
- Teach about natural selection: In this classroom activity for grades 9-12, students experience one mechanism of evolution through a simulation that models the principles of natural selection and helps answer the question: How might biological change have occurred and been reinforced over time?
- Johnson, M. T. J., Prashad, C. M., Lavoignat, M., and Saini, H. S. (2018). Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens). Proceedings of the Royal Society B. 285. DOI: 10.1098/rspb.2018.1019.
- Kooyers, N. J., Gage, L. R., Al-Lozi, A., and Olsen, K. M. (2014). Aridity shapes cyanogenesis cline evolution in white clover (Trifolium repens L.). Molecular Ecology. 23: 1053-1070.
- Santangelo, J. S., Ness, R. W., Cohan, B., Fitzpatrick, C. R., Innes, S. G., Koch, S., … and Johnson, M. T. J. (2022). Global urban environmental change drives adaptation in white clover. Science. 375: 1275-1281.
- Thompson, K. A., Renaudin, M., and Johnson, M. T. J. (2016). Urbanization drives the evolution of parallel clines in plant populations. Proceedings of the Royal Society B. 283. DOI: 10.1098/rspb.2016.2180
- Weintraub, K. (2018). White clover can be an annoying weed. It may also hold secrets to urban evolution. New York Times. Retrieved September 2, 2018 from: https://www.nytimes.com/2018/07/20/science/white-clover-evolution.html
- Zagrobelny, M., Bak, S., Rasmussen, A. V., Jørgensen, B., Naumann, C, M., and Møller, B. L. (2004). Cyanogenic glucosides and plant-insect interactions. Phytochemistry. 65: 293-306.