Top Urban Evolution Papers of 2021

Humans are increasingly a dominant driver of evolutionary change within populations. Since its inception, the Life in the City Blog has brilliantly shown that some of the most stunning examples of human caused evolution relates to how urbanization affects species’ evolution. This area of research has gained a lot of attention from scientists in recent years, with an increasing number of research articles on the topic each year. Here is my curated list of the top 10 urban evolution papers from 2021, or in some cases a collection of related papers. This list originally appeared as a thread of tweets on January 3, and I’ve taken the liberty to reorganize it to correct some unintended omissions in the original list. Here is the list in no particular order:

 

10. Reviews & Perspective Papers

There were a bunch of great Reviews, Ideas and Perspective papers in 2021 that I think deserve special attention from anyone interested in urban evolutionary biology. I’m cheating a little by putting them all under #10, but they all deserve some attention.

The first is “Urban evolution of invasive species” by Jesse Borden and Luke Flory, published in Frontiers in Ecology and the Environment (and summarized by the author here). In this Concepts and Questions paper, the authors conclude that urban evolution of non-native species can enhance invader establishment, spread, and ecological impact, which can facilitate an invasive species’ success under future climates. I am excited to see tests of these ideas in future years.

Sarah Diamond and Ryan Martin offered the latest comprehensive review of urban evolutionary biology in their Annual Reviews of Ecology, Evolution and Systematics article. In their review they develop a framework to help guide future research in evolutionary biology.

Justa Heinen-Kay, Adam Kay and Marlene Zuk focused their review on how urban environmental changes affect sexual communication. The authors argue that multiple forms of pollution (noise, light, chemical), as well as changes to the physical and biotic environment, may alter sexual communication, with potential consequences for sexual selection and adaptive evolution.

Finally, Chloe Schmidt and Colin Garroway had a new quantitative analysis/review of published  microsatellite data, examining whether amphibians exhibit a consistent loss of genetic diversity or differentiation among populations if urbanization elevates the effects of genetic drift while disrupting gene flow, predictions that Jason Munshi-South and I boldly made in our 2017 review in Science. In analyzing microsat data from 19 amphibian species, they find no consistent change in genetic diversity in urban populations, or differences in genetic differentiation among populations. I’ve got to admit, I was pretty shocked by this finding (or lack of effect) given the strong effects found on Ne and gene flow for some salamander and frog populations from previous publications. Chloe and Colin’s results shows that we still don’t really understand how urbanization affects populations size (and thus genetic drift) or the movement of organisms (and their genes – aka gene flow), and maybe that our earlier prediction was a little (a lot) naïve.

 

9. Pikus et al 2021 Peer J. 

Pikus et al’s study represents one of the latest attempts to understand the adaptive genetic consequences of how urbanization affects wildlife. They show that urbanization drives divergence in Eurasian coots at the major histocompatibility complex, consistent with adaptation to city and rural pathogens that is dependent on the age of urban populations.

8. Harpak et al 2021 Genome Biology and Evolution. 

Rats are one of the most characteristic urban species found in cities throughout the world. Despite recent work led by Jason Munshi-South’s lab showing the consequences of urbanization on rat population genetic structure and demography, understanding the effects of urbanization for adaptation of rats to cities has been less studied. Arbel Harpak, Munshi-South and colleagues examined genomic adaptation of New York City rats and find evidence of adaptation in multiple genes associated with metabolism, diet, the nervous system, and locomotory behavior.

 

7. Brans, Tuzun et al 2021 J Animal Ecology.

Understanding how evolution affects ecological dynamics and patterns is hard to study and to the best of my knowledge has never been studied in an urban context, although many have mused about such eco-evolutionary feedbacks. This is why Kristien Brans and Nedim Tuzun’s (and company) paper is so impressive. In studying the predator-prey dynamics of damselflies (predators) and waterfleas (prey), they show that the ecological effects of evolution in of these species on one another are hidden when evolution of one of the species dampens the ecological effects of evolution in the 2^nd species that it interacts with. So there are eco-evolutionary feedbacks but they are cryptic, hence the term they introduce of “cryptic evo-evo feedbacks”. Does it sound complicated? Well it is, but that’s nature in the city for you.

6. Rivkin et al 2021 Ecology and Evolution.

A large gap within urban evolutionary biology is understanding whether and how urbanization alters natural selection of natural populations. This is true in general, but it is especially true in tropical regions and islands, where we know very little about how urban development affects evolution, let alone selection. This is why Ruth Rivkin et al’s study in Ecology and Evolution is so important. In this paper she studies the interactions between Darwin’s finches and their food plant Tribulus on the Galapagos Islands. She provides some of the first evidence that urban development alters natural selection on species’ traits, sometimes completely reversing the direction of selection on defence traits.

 

5. Merckx, Nielsen et al 2021 PNAS.

Some of the clearest examples of adaptation to urban environments comes from adaptation to urban heat islands. One of the latest examples of this comes from the work of Thomas Merckx, Matt Nielsen and company. They used long-term monitoring and citizen science data to show that the flight season of two Lepidoptera spp. (one moth and one butterfly) are longer and end later in multiple northern European cities. They then conducted common garden experiments and found genetic shifts in diapause induction that were consistent with adaptation to urban heat islands but not adaptation to artificial light at night.

 

4. Campbell-Staton et al 2021 Nature Communications.

We know very little about how urbanization affects phenotypic plasticity, especially adaptive phenotypic plasticity (but see the series of great papers from Sarah Diamond and Kristien Brans of the years!). Given this gap, the paper by Shane Campbell-Staton, Jonathan Velotta and Kristin Winchell in Nature Communications came as sweet relief to the dearth of data on this topic. Building on Kristin’s series of papers showing adaptive morphological evolution of Anolis lizards to urban environments in Puerto Rico, they show that urban and forest Anolis lizards show divergent expression in multiple genes related to heat tolerance. More specifically, forest lizards tend to show heat-induced gene expression changes that generally relate to reduced thermal tolerance, whereas urban lizards show reduced gene expression changes to similar changes in thermal environment. These differences suggest urban Anolis lizards are exhibiting adaptively diverged difference in gene expression that allow them to tolerate warmer urban environments.

3. Martin et al 2021 Evolution.

While several studies have shown data consistent with adaptation to urban environments in recent years, there are few experimental demonstrations of local adaptation to urban areas. By this I mean experiments that show urban populations have higher fitness than nonurban populations when they are both put in urban environments, and vice verse in nonurban environments. Ryan Martin and colleagues provided one of the first experimental demonstrations of local adaptation to urban environments in their recent paper in Evolution. To make a long story short, tiny urban ants that live in acorns fair better in the city than rural areas, and the opposite for rural acorn ants.

 

2. Salmón et al 2021 Nature Communications.

This next paper was an embarrassing omission from my initial tweet thread. The groundbreaking paper of Pablo Salmón, Caroline Isaksson & co published in Nature Communications shows stunning evidence for repeated adaptive evolution using genomic data in a single bird species (Great Tits) across 9 cities (see the author’s summary here). Whether cities lead to adaptive evolution is an important question, as mentioned above, but whether city living leads to similar adaptations in the same species that occurs across multiple cities has only be touched upon in a small number of organisms, and rarely using genomic data. This study shows that cities frequently lead to shifts in allele frequencies and selective sweeps, but it is rarely the same genetic changes that occur across multiple cities. Look for many more studies of parallel evolution at the genomic level in the coming years – it is a hot and important topic as we seek to understand the importance of cities for the evolution of life.

 

1. Miles et al Special Feature 2021 Evolutionary Applications.

The last but certainly not least is the whole collection of 16 articles edited by Lindsay Miles, Elizabeth Carlen, Kristin Winchell and myself, which were published in a special issue in Evolutionary Applications (see our previous post introducing this set of papers). OK, I realize I’m cheating here when it comes to the unofficial rules of Top 10 lists, but this really was an outstanding collection of 12 empirical papers, 3 reviews and 1 capstone article. This is the 2^nd ever special issue on urban evolutionary biology, the first being in Proceedings B in 2018 (see here). While I don’t have the space to riff about each paper, I want to briefly highlight a few that make exceptional advances.

The paper by Hannah Watson et al provides one of the first demonstrations that urbanization alters methylation across the genome of an organism, in this case great tits. The other example of urbanization affecting epigenetics comes from the recent work of Aude Caizergues et al in the same journal and year, although the latter was not part of the special issue.

The study by Xu Wei et al provided rare insight into how urban expansion over hundreds of years has influenced the demographic history of a native amphibian (the golden frog) in Shanghai, China.

Elizabeth Carlen and Jason Munshi-South provided the first population genomic investigation of how urbanization affects the population structure and gene flow of rock pigeons, another classic urban species. Elizabeth shows that there is widespread connectivity of pigeon populations across the northeast of the USA. Learn more here (and the author summary here on the blog).

A final gem from the Special Issue, and there really are 16 gems in to be read, is the Capstone article by Simone Des Roches and colleagues. This paper originated from the Urban Eco-Evo Network and proposed a new framework to merge the questions, techniques and data from urban ecology and urban evolutionary biology with human social patterns and processes in the social sciences. The proposed urban socio-eco-evolutionary dynamic framework has the potential to create an entire new field of transdisciplinary study.