A newly published global study of white clover shows its strong evolutionary adaptation in urban environments despite human encroachment, tough conditions and climate change,  according to a Global Urban Evolution (GLUE) Project team led by evolutionary ecologist Marc Johnson, a professor of biology at the University of Toronto, Mississauga.

The 287-member team included urban landscape entomologist Emily Meineke of the UC Davis Department of Entomology and Nematology and marine evolutionary ecologist Joanna Griffiths of the UC Davis Department of Environmental Toxicology. 

The research, “Global Urbanization Drives Adaptation in the Plant White Clover,” published March 17 in the journal Science, reveals that “urbanization leads to similar environmental changes across 160 cities throughout the world, which leads to repeated adaptive evolution in the cosmopolitan invasive plant white clover,” said Johnson, the  principal investigator (PI) of the 160-city, 26-country project and director of the Centre for Urban Environments  at the University of Toronto. 

“It is the largest scale study of parallel evolution and urban adaptation ever performed, involving 287 collaborators across 26 countries,” said Johnson, adding “This project would have been impossible without the hard work and dedication of an amazing network of collaborators around the world, people like Emily Meineke and Joanna Griffiths at UC Davis.” 

White clover, Trifolium repens, is considered an ideal evolutionary organism to study: it is one of the most rapidly evolving species of flora and one of the most widespread.  The plant adapts well in both rural and urban environments throughout the world, from Norway to Mexico to India. Often used as a cover crop, it is a good source of nitrogen and a good nectar source for bees, but it is considered invasive when it pops up in urban lawns or on golf courses. 

Of the main forces behind evolution--natural selection, genetic drift, and gene flow—the white clover's dominant evolutionary force is natural selection, Johnson pointed out.

Team members performed cyanogenesis assays to determine the plant's defense production of a toxin called hydrogen cyanide (HCN).  White clover is less likely to produce HCN in colder environments but more likely in rural areas, the research shows.  Half of the world's population lives in urban environments, but by 2050, that figure is expected to jump to 70 percent. 

“Urbanization transforms environments in ways that alter biological evolution,” the scientists explained in the abstract. “We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.” 

Both Meineke and Griffiths worked on the project when they were doctoral students: Meineke at North Carolina State University (NCSU), Raleigh, and Griffiths at Louisiana State University (LSU), Baton Rouge. 

Meineke, who holds a doctorate in entomology (2016) from NCSU, designed the sampling effort in Raleigh, collected clover from there, and did cyanogenesis assays. 

“Increasingly, it is clear that we are living in a time when humans are the dominant drivers of biotic change globally,” commented Meineke, who joined the UC Davis Department of Entomology in Nematology in 2020 as an assistant professor.  “Somehow, we still don't understand how we are affecting the species we see every day, in part because biologists have only recently become aware of our complex effects on species that live in our own habitats.” 

“This project sparked my interest because it focuses on the evolution of clover, a plant that I've had under my feet my entire life,” Meineke said. “I remember stepping in clover as a kid and watching bumble bees bob across it during PE class in elementary school. It turns out that kids worldwide have had this experience because white clover is a cosmopolitan plant. Being part of this study gave me the opportunity to be part of a large group studying effects of humans on clover all over the world.” 

Griffiths, a postdoctoral researcher in the UC Davis labs of Professors Andrew Whitehead and Nann Fangue, received her  doctorate in ecology and evolution (2020) from LSU. She said her LSU team, including Luis Santiago-Rosario and Katherine Hovanes, "collected clovers from Baton Rouge, and my contribution was performing the lab work, that is, I quantified the amount of hydrogen cyanide present in each clover sample from rural Baton Rouge all the way to the city center. Each sample was digested and incubated for a couple hours. (See image of data sheet.) “The cyanide in the sample chemically reacts with the special paper, turning it blue. Thus, a blue spot on the paper indicates that the clover sample had cyanide present.”  

Urbanization is a global phenomenon, in which thousands of cities cover up to three percent of Earth's land surface, according to the GLUE Project website.  “For an evolutionary biologist, these cities represent an amazing opportunity to study evolution in action.” 

The website describes the GLUE project as “an initiative that will provide the largest scale, best replicated test of parallel evolution ever attempted. To do this, we will study the evolution of the production of hydrogen cyanide (HCN) in white clover (Trifolium repens). We previously showed that white clover evolves parallel clines in HCN (a potent chemical defense) along urban-rural gradients in eastern North America.” 

In addition to lead PI Marc Johnson, the 12-member leadership team included two University of Toronto scientists: co-PI and assistant professor Rob Ness, the second author of the paper; and doctoral student James Santangelo, first author.

The project drew financial support from a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant; Canada Research Chair; and NSERC E.W.R. Steacie Fellowship. 

Many plant species are leafing out and flowering earlier in response to rising temperatures, and those that are not are “declining at alarming rates in some circumstances,” says urban landscape entomologist Emily Meineke of the UC Davis Department of Entomology and Nematology in newly published research in the journal Global Change Biology. 

“However, the plants that are keeping up with climate change might also experience costs to earlier leaf-out,” said Meineke, lead author of the first-of-its-kind study, Phenological Sensitivity to Temperature Mediates Herbivory. 

One of the costs is that “early” species get eaten more in warmer years. “This seems to be because when they leaf out earlier,” she said, “they also lengthen the amount of time herbivores have in a given year to eat their leaves.” 

Two plant species that showed higher insect damage due to rising temperatures were two native blueberries: Vaccinium angustifolium, a wild lowbush blueberry native to eastern and central Canada and the northeastern United States, and Vaccinium corymbosum, the northern highbush blueberry, a native North American species and a significant commercial food crop. 

The publication is the result of a massive five-year research project involving herbarium specimens collected from the northeastern United States and France from 1900 to 2015.  These two areas have warmed more than the global average, Meineke said, and the plants studied are distributed widely across them.

Meineke, an assistant professor who joined the UC Davis faculty in March 2020, launched her research while a National Science Foundation postdoctoral fellow at the Harvard University Herbaria, where she studied how worldwide urbanization and climate change have affected plant-insect relationships over the past century.

Co-authors are Charles Davis of the Harvard University Herbaria and Jonathan Davies of the Departments of  Botany, Forest and Conservation Sciences, University of British Columbia, Vancouver and the African Centre for DNA Barcoding, University of Johannesburg. 

“This was a true collaboration,” Meineke said. “Each of us was interested in different pieces of the research. Davies and Davis brought the phenology hypotheses and expertise, and I brought an interest in/knowledge of herbivory and how it may change as the climate warms.” 

The authors wrote that “both insect and plant development are sensitive to temperature, though the specific cues plants and associated insects use to time life history events may differ and include photoperiod, chilling, ‘forcing' and precipitation. For the vast majority of insect and plant species, the combined and relative contributions of these cues have not been well characterized.” 

The specimens studied were selected first on the basis of the availability of previously published phenological sensitivity metrics: flowering sensitivity and leaf-out sensitivity. “We use the general term ‘phenological sensitivity' to refer to the extent to which a particular life event (e.g., for plants, budbreak, leaf-out, flowering, fruiting) responds to temperature from year to year (e.g. days change in phenology per ‘C' warming),” they explained. 

The next step? “We are now beginning to look into whether and how herbivory might have shifted over time in California native plants,” Meineke said. “Our focal species so far is the valley oak, Quercus lobata, but we hope to eventually expand these observations to more taxa. We're also looking into other mechanisms that might drive herbivory shifts here in the west, where phenology is driven more by moisture than by temperature.” 

A native of Greenville, N.C., Meineke holds a bachelor's degree from the University of North Carolina in environmental science, with a minor in biology, and a doctorate in entomology from North Carolina State University where she completed her dissertation,  "Understanding the Consequences of Urban Warming for Street Trees and Their Insect Pests.” 

The project was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada. The material is based upon work supported by the National Science Foundation Postdoctoral Research Fellowship in Biology in a grant awarded to Meineke. 

The abstract:

Species interactions drive ecosystem processes and are a major focus of global change research. Among the most consequential interactions expected to shift with climate change are those between insect herbivores and plants, both of which are highly sensitive to temperature. Insect herbivores and their host plants display varying levels of synchrony that could be disrupted or enhanced by climate change, yet empirical data on changes in synchrony are lacking. Using evidence of herbivory on herbarium specimens collected from the northeastern United States and France from 1900 to 2015, we provide evidence that plant species with temperature‐sensitive phenologies experience higher levels of insect damage in warmer years, while less temperature‐sensitive, co‐occurring species do not. While herbivory might be mediated by interactions between warming and phenology through multiple pathways, we suggest that warming might lengthen growing seasons for phenologically sensitive plant species, exposing their leaves to herbivores for longer periods of time in warm years. We propose that elevated herbivory in warm years may represent a previously under appreciated cost to phenological tracking of climate change over longer timescales.  

Global change ecologist Amanda Koltz, a senior scientist with the Department of Biology, Washington University, St. Louis, will speak on "Species Interactions and Ecosystems in a Changing World" at the UC Davis Department of Entomology and Nematology's virtual seminar at 4:10 p.m., Wednesday, Oct. 14. 

"Biological communities and species interactions are changing rapidly as a result of global change," she says in her abstract. "These changes are likely to have cascading effects on ecosystems, but we still have limited understanding of the extent to which organismal responses to global change may also drive ecosystem responses to it. In this talk, I will present some of my work on the potential feedbacks between global change, communities, and ecosystem functioning from two different study systems. First, I will discuss how warming can alter the cascading effects of spiders in the Arctic tundra, and then I will discuss my recent efforts at characterizing the potential consequences of shifting interactions among ruminant hosts and their parasites. The common theme throughout the talk will be the importance of considering species interactions in efforts to understand ecosystem responses to global change."

Koltz describes herself as a "global change ecologist interested in how species interactions influence community composition and ecosystem function in the context of environmental change. I use common, widespread organisms that are sensitive to change-- like wolf spiders, mosquitoes and gut worms--to better understand how the animals in our everyday lives impact the ecosystems we live in. My recent work focuses on two fundamental questions: (1) How do biological communities respond to changes in the environment? and (2) What are the consequences of changes in species interactions for the cycling of energy and nutrients within ecosystems?"

Cooperative Extension specialist and agricultural entomologist Ian Grettenberger,  assistant professor, UC Davis Department of Entomology and Nematology, coordinates the fall series of virtual seminars. They are held on Wednesdays at 4:10 p.m.

Host for the Koltz seminar is Emily Meineke, assistant professor of urban landscape entomology, who researches insect-plant interactions.

Grettenberger announced that this is the form to obtain the zoom link:

https://docs.google.com/forms/d/1JHRitzyKtU2MzBTywYq6AyzuX6sIjVL-NDk_s8Ilnp4/edit

Koltz's research has appeared in a number of recent publications: 

• Small but Mighty: Measuring Parasites' Footprints
• Wolf Spiders May Turn to Cannibalism in a Warming Arctic
• Warming Alters Predator-Prey Interactions in the Arctic
• Bugged Out by Climate Change
• Higher Education Channel: Arctic Wolf Spider's Changing Diet May Help Keep Arctic Cool & Lessen Some Impact of Global Warming

Meet new faculty member Emily Meineke, who joined the UC Davis Department of Entomology and Nematology as an assistant professor of urban landscape entomology on March 1. She studies how climate change and urban development affect insects, plants, and how they interact with one another.

Before accepting her UC Davis appointment, Meineke served as a National Science Foundation postdoctoral fellow at the Harvard University Herbaria, where she studied how urbanization and climate change have affected plant-insect relationships worldwide over the past 100-plus years.

A native of Greenville, N.C., Emily received her bachelor of science degree in environmental science, with a minor in biology, in 2008 from the University of North Carolina, Chapel Hill, and then went on to obtain her doctorate in entomology in 2016 from North Carolina State University. Advised by Steven Frank and co-advisor Robert Dunn, she completed her dissertation on  "Understanding the Consequences of Urban Warming for Street Trees and Their Insect Pests."

Some questions:

1. Please expand on the kind of research you do.

"Insects have eaten plants for around 400 million years. These interactions have given rise to most of terrestrial biodiversity. Over the past 12,000 years, humans have disrupted plant-herbivore relationships by building cities, domesticating crops, and changing the global climate."

"I investigate these disruptions, focusing on species that are of cultural importance, such as street trees, crops, crop wild relatives, and plants that support rare insect species. My work combines experiments, observations, citizen science, and biological collections to address key hypotheses in ecology."

2. What do you like best about your work?

"I love discovery, the moment when you as a scientist know something that no one else knows. I love passing that experience on to students. I also love that my work reflects my personal values. Biodiversity is critically important, and the fact that I get to study it for a living is a real privilege."

3. How did you get interested in entomology? Can you recall an occasion that sparked your interest? 

"I have no idea, honestly. I never had an insect collection as a kid, and I was equally interested in all living things, from my family's pets to the toads that lived in my backyard. At some point after my undergraduate education, I realized that insects are both invisible to us most of the time and are incredibly present in our lives and imaginations. Ecologically, because they are small in size, they can seem unimportant because we are biased to think creatures our size or larger are important, but insects are really the little things that run the world."

4. How would you describe yourself?

"I'm a pretty serious person who is always working to be more light-hearted. I am both easily discouraged and tenacious. I would describe myself as creative and am drawn to diversity in all forms."

5. What drew you to UC Davis?

"When I visited, I got the feeling that UC Davis encourages creativity while valuing research that produces real solutions. When I interviewed here, I felt I would be able to be myself as a researcher and that my fellow faculty would support that. On top of that, UC Davis is such an established institution with great resources in a beautiful part of the world. I can't think of a better place to be."

6. What do you like to do in your leisure time?

"All I really ever want to do is eat and spend time with people I love. 'People' includes my two dogs, who rule the house."

9. What would people be surprised to know about you?

"I have a hidden talent. I can make very realistic cat meows. I can fool anyone's cat and most humans."

Other
In addition to her NSF Postdoctoral Research Fellowship, she received a number of other honors, including Student Appreciation for the Biology of Insect Pests Award; Garden Club of America Urban Forestry Fellowship; and the EPA Science to Achieve Results (STAR) Fellowship.

A member of the Entomological Society of America (ESA), Ecological Society of America and the Botanical Society of America, she has presented talks across the continent, as well as in Finland, Spain, Canada, France and Denmark. She delivered a presentation at the 2016 International Congress of Entomology in Orland, Fla., and at ESA's national and regional meetings.

Meineke has published her work in Ecological Monographs, Ecology and Evolution, Journal of Applied Ecology, and the Journal of Urban Ecology, among others.

The Boston Globe featured her research in a news story published Oct 11, 2018: "Rising Temperatures May Cause Insects to Eat More Plants, Harvard Study Says"

Nature journal featured her in a research highlights piece, "Warmer Forests Store Less Carbon," published Oct. 12, 2016

Los Angeles Times spotlighted her in its Oct. 6, 2016 piece, "As Cities Get Warmer, These Trees Lose Some of their Ability to Take Carbon Out of the Atmosphere."

Contact:
ekmeineke@ucdavis.edu.