“Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens)”

CITATION:
Marc T. J. Johnson, Cindy M. Prashad, Mélanie Lavoignat, Hargurdeep S. Saini. 2018.  Proceedings of the Royal Society B: Biological Sciences, vol. 285, no. 1883, published on-line July 25, 2018: pp. 8-33.
ON-LINE AVAILABILITY:
ABSTRACT:
Urbanization is a global phenomenon with profound effects on the ecology and evolution of organisms. We examined the relative roles of natural selection, genetic drift and gene flow in influencing the evolution of white clover (Trifolium repens), which thrives in urban and rural areas. Trifolium repens exhibits a Mendelian polymorphism for the production of hydrogen cyanide (HCN), a potent antiherbivore defence. We quantified the relative frequency of HCN in 490 populations sampled along urban–rural transects in 20 cities. We also characterized genetic variation within 120 populations in eight cities using 16 microsatellite loci. HCN frequency increased by 0.6% for every kilometre from an urban centre, and the strength of this relationship did not significantly vary between cities. Populations did not exhibit changes in genetic diversity with increasing urbanization, indicating that genetic drift is unlikely to explain urban–rural clines in HCN frequency. Populations frequently exhibited isolation-by-distance and extensive gene flow along most urban–rural transects, with the exception of a single city that exhibited genetic differentiation between urban and rural populations. Our results show that urbanization repeatedly drives parallel evolution of an ecologically important trait across many cities that vary in size, and this evolution is best explained by urban–rural gradients in natural selection.

The author and collaborators investigating white clover and other turf monoculture resistors at the National Mall in Washington DC, as part of the exhibition EPA meets EPA: Department of Weedy Affairs (image courtesy of the Environmental Performance Agency and Dan Phiffer)

When the phrases “annoying weed” and “urban evolution” ran in a headline in The New York Times last month, I knew about it right away. Yes, I have a Google alert set up in an attempt to catch these sorts of things, but in this case, it was actually my human network who notified me, beating out Google by at least twenty hours. The article in question, a Trilobites column bearing the headline “White Clover Can Be an Annoying Weed. It May Also Hold Secrets to Urban Evolution” was variously emailed, tweeted and texted to me in the days following its publication.

The New York Times column was written in response to the journal article by Johnson et al., which appeared in the Proceedings of Royal Academy of Sciences in July. The article does not contain the phrase “annoying weed”, and in fact fails to use the term “weed” at all. It identifies white clover as “a perennial herbaceous plant, native to Eurasia and introduced globally to temperate environments”. While this could be interpreted as merely a schism in the kinds of language (colloquial versus technical) used in journalistic versus scientific circles, I think there is more at stake. In this post and the one that follows next week, I will attempt to unpack some of the weight borne by the term “weed” (and its omission), while also asking how traits described as “weedy” relate to urban evolution and human complicity in the Sixth Extinction.

White clover (Trifolium repens) sprouted from seeds collected in Bushwick, Brooklyn, growing on the author’s windowsill. (Photo courtesy Dan Phiffer)As an interdisciplinary artist who spends a lot of time observing and interacting with spontaneous urban plants (aka weeds) as part of my practice, I am quite familiar with white clover. It’s a dependable presence and co-conspirator that my collaborators and I work with regularly. We find it thriving everywhere from manicured lawns to street tree pits to crumbling sidewalks. I’ve even discovered it adapts well to indoor living, growing complacently on my kitchen windowsill in a yogurt container after months of display in a gallery space.

Given the species’ ubiquity, I wasn’t surprised to learn it had become the focus of a study on urban plant evolution. The discipline of urban ecology has coalesced relatively recently, as a solid subset of ecologists have shifted focus from biological stations in the so-called wilderness to the streets and sidewalks of rapidly growing cities. Many have asked questions about if and how the pressures of urban life are changing the nonhuman species who manage to stick it out, even citing cities as a kind of petri dish for studying the effects of global warming, given that they tend to have relatively higher annual temperatures. To date, there is a growing body of research that answers an emphatic yes to the question of whether rapid evolution is taking place in cities. Plants, rodents, insects, microbes: are all evolving differently, and more rapidly, in cities than elsewhere.

The study in question sought to answer a more specific subquestion about urban evolution, one that white clover is particularly well-suited to answer. Taking advantage of the fact that white clover thrives in cities large and small and in lawns and pastures in non-urban areas, the authors were able to make a useful comparison. They showed that evolution in clover is taking place across different cities, of different sizes, in similar ways. White clover plants are not just randomly evolving due to chance (genetic drift or the founder effect), but rather are responding in predictable ways in cities large and small in comparison to their rural-dwelling counterparts. This means they are evolving in parallel, proving they are undergoing adaptive evolution: traits are being selected for repeatedly in response to the way humans organize and interact with land.

White clover has a long relationship with humans and our attendant landscape alterations. It exists in cultivated, wild, and what we might call intermediate “feral” forms, all of which are considered subspecies of Trifolium repens. While its ancestors most likely evolved in the Mediterranean region more than 16 million years ago, the species spread throughout Europe and Central Asia before recorded history, and is thus considered native in these regions. White clover has been evolving alongside humans as long as agriculture has existed, and perhaps even before. It provided protein-rich forage for the herbivores that were the ancestors of our domesticated grazers, who probably helped with its spread through Europe and Asia. By the early 1600s it was being cultivated in Holland as “Dutch White Clover” and was subsequently exported around the world during the centuries of colonization and globalization that followed. Even today it is purposefully added to turf and pasture seed mix along with grass, because it’s tough and resistant to trampling, supplements forage for livestock, and enriches soil by fixing nitrogen.  So while it is fascinating to see how quickly clover is adapting to urban life, it is also worth considering how its long co-evolution with human activity may have prepared it for the city. Clover is well adapted to sheering and trampling, whether it comes from elk and cattle, or lawnmowers and human feet.

So what does the term “weed” have to offer in this context? Next week I’ll continue this inquiry with a post on some historical and contemporary uses of the term in relation to Trifolium repens and urban evolution.


References:

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