But a recent study by Fordham scientists has found that plants that adapt to wild swings in precipitation still suffer adverse effects, including a reduction of seed production.

For the study, Elena Hamann, Ph.D., a biological sciences post-doctoral researcher, and Steven Franks, Ph.D., professor of biological sciences, harvested seeds from two collections of Brassica rapa plants in Orange County, California, that had experienced two decades of dramatic precipitation fluctuations, including increasingly severe droughts.

Hamann then grew four generations of plants in September 2016 under both drought and normal conditions in a greenhouse at the Calder Biological Field Station in Armonk, New York, and compared how the two different sets fared.

Franks had confirmed the ability of Brassica rapa to evolve rapidly in earlier studies, but this study took it one step further: The plants that had evolved to cope with drought by doing things like flowering earlier in the growing season, then had evolved to cope with heavy rainfall, then had evolved again to cope with more drought, showed signs that the constant changes were taking a toll.

“In the long term, the droughts are becoming more and more severe, and we’ve also seen that in more recent generations, the plants are not able to maintain fitness as well, so they produce less seeds,” said Hamann, who was the study’s principal investigator.

“So, we think that even though they adapt to drought by advancing flowering time and changing other specific traits, they are starting to suffer from the severity of drought. What they’re doing is basically not enough anymore.”

One of the most significant findings of the study is that paradoxically, rainy seasons actually hurt the plants’ ability to evolve in ways to cope with drought.

“After just two wet years, they flowered much later, but then there was another severe drought, so they then had to sort of evolve into earlier flowering again,” said Franks.

“But there’s a delay and they have less fitness, and produce fewer seeds. So they get fewer seeds into the seed bank for the next generation.”

The ability of a plant like Brassica rapa, which is closely related to turnips and bok choy, to weather droughts and rainy spells is important because wild swings in precipitation are the result of climate change that is likely to continue. In the area of California where Hamann and Franks harvested the plants, for instance, the most severe level of drought in 100 years happened only once between 1977 and 2004. But since then, the area has experienced several droughts that are equally severe or worse.

“The most recent report from the Intergovernmental Panel on Climate Change suggests that climate is changing even more than we thought,” said Franks.

“We’re seeing all these really substantial changes in this California system. Plant populations are responding, but there’s good evidence from this study that they may not be able to keep up with the severity of these changes.”

The results of the study, Two decades of evolutionary changes in Brassica rapa in response to fluctuations in precipitation and severe drought, was published this month in the journal Evolution.

This simple observation, a team of researchers led by Fordham scientists has learned, is applicable in cities as diverse as Vancouver, Canada; New York City; New Orleans; and Salvador, Brazil. And it has implications for both how rats evolve and how we learn to cope with their presence in our midst.

In Urban rat races: spatial population genomics of brown rats (Rattus norvegicus) compared across multiple cities, a paper published last month in the Royal Society’s flagship journal Proceedings B, Fordham doctoral candidate Matthew Combs showed how genetic analysis of rats collected by teams in those four cities reveal the ways in which evolution is repeating itself in cities, thanks in part to the geographical features of urban areas.

Working under the direction of Jason Munshi-South, Ph.D., associate professor of biological sciences, Combs collaborated with researchers working in the three other cities who brought rat tissue samples they’d collected as part of separate projects to Fordham’s Louis Calder Center for analysis.

Same Species, But Subtle Differences

At least 150 rats were sampled from each city, and when researchers analyzed the results, they discovered that just as brown rats in Lower Manhattan have evolved to be distinct from their uptown brethren, (a discovery detailed in a 2017 paper) rats in those three cities differ from each other in discernable ways.

In Manhattan, the culprit is Midtown, with its relative paucity of shelter and food sources; in New Orleans, it’s the Inner Harbor Navigation Canal, which divides the Lower Ninth Ward neighborhood from the rest of the city. In both Vancouver and Salvador, major roadways were found to split disparate populations of brown rats.

Combs said previous studies had compared rats around the world, but none had incorporated such a robust number of specimens.

“In this case, we used hundreds of samples within each city to look at some very fine scale movements, and were able to get quite a bit more detail about these four cities, and ask questions about how the same types of landscape features were creating unrelated groups,” he said.

Munshi-South, whose lab has tracked the movement of rats around the world, said he was surprised that the level of differences among the rats was similar in all four cities, given that two are in temperate climates, one is sub-tropical, and one is tropical. All, however, are coastal cities located in the Americas, and are thus a “biological legacy of colonialism and migration.”

“They have a very similar level of genetic diversity in the rat population, and that may indicate a shared ecological and evolutionary history. These rats were likely introduced to these cities around the same time, and have been there for about the same amount of time,” Munshi-South said.

“Rats are really a reflection of human history. They don’t obviously have a recorded history that’s very good, but the genetics reveal a lot about how we move them around.”

Potential for Understanding Disease

Combs said the collaboration with the teams in the other three cities—some of whom were working on projects disease-related projects—was also noteworthy, because the technique the Fordham team uses to track genetic variations in species can be shared and used for other objectives as well.

“We can tell them about some of these genetic patterns, and they can tell us about disease dynamics and distribution, and hopefully we can put those two pieces of information together and start to understand how the movement of rats and the genetic patterns relate to the movement of disease, which is really what everyone’s worried about,” he said.

“I think there’s a lot of potential there.”

Munshi-South agreed, saying this study is a model for future ones in cities across the globe. The days of studying a single species in a single city are over, he said.

“One of the big hypotheses that’s out there is that urbanization drives the same ecological and evolutionary results over and over again,” he said.

“We’re trying to confirm that with these kinds of studies.”

At the Louis Calder Center, scientists explore ecological mysteries and study society’s impact on the natural world.

To the casual observer, Fordham’s Louis Calder Center might seem to be just another quiet tract of Hudson River Valley forest. But for natural scientists, it abounds with opportunity. Explore the 113-acre biological field station in Armonk, New York, and you’ll find a bounty of ecosystems and animals, from the four-legged to the microscopic. At the heart of the preserve is a 10-acre temperate lake teeming with a diversity of aquatic life. Go high enough and, way off in the distance, you can see another big player in the preserve’s ecology: New York City, which begins only 16 miles away.

Its proximity has never been more relevant. “Humans and our cities are the most dominant forces of contemporary evolution now,” says Jason Munshi-South, Ph.D., a Calder-based biology professor who recently co-authored a paper in the journal Science on how species are evolving within cities. Other scientists at Calder study invasive species that arrive via big-city commerce. And they tackle many other mysteries: why some animals survive new threats while others don’t, how nutrients flow beneath the soil, or how insects transmit disease.

The center was born 50 years ago when the land was given to Fordham by the Louis Calder Foundation, named for the paper and pulp magnate who maintained a summer home on the property. Today, that home is Calder Hall, one of several buildings in which students and professors analyze DNA samples, inspect plant and animal specimens, hold classes, and generate knowledge.

Among many other public services, the Calder Center supports the nation’s longest-running study of ticks and Lyme disease, and its scientists work to illuminate society’s impact on nature at a time of growing concern about biodiversity and climate change.

It is also a crucial training ground: “The most important thing we do here is make scientists,” says Thomas Daniels, Ph.D., an expert in tick- and mosquito-borne diseases who has served as the center’s director since 2014.

On a sparkling autumn day late last October, FORDHAM magazine tagged along as undergraduates, graduate students, professors, and visiting scientists went about their work—gently probing, collecting samples, and explaining the science behind their work and its potential impact.

Evolution in the Big City

In recent years, Fordham biologist Jason Munshi-South, Ph.D., and his team of graduate and undergraduate students have become known for their studies of urban wildlife and pest species, most notably rats.

“The initial idea was to understand what a New York City rat is, from all ecological and evolutionary angles,” he says of one project, which grew to a global scale and has public health implications. “We’re using DNA to understand how they move around the city and how they’re related to other rat populations.”

In a first-floor lab in Calder Hall, doctoral student Carol Henger uses similar methods to study coyotes, animals that only recently moved into the city for the first time, Munshi-South says. She’s looking at DNA markers from coyote scat collected in Pelham Bay Park and elsewhere to infer how individual coyotes are related, what they’re eating, and how they’re dispersing.

Meanwhile, Nicole Fusco, another doctoral student in Munshi-South’s lab, sequences DNA to study gene flow among populations of salamanders.

Biodiversity and Climate Change

In the Calder Center’s Lord & Burnham greenhouse, constructed on the property nearly a century ago, doctoral student Stephen Kutos has been growing pairs of potted trees and studying how they pass water and nutrients back and forth via subsoil networks of fungus.

“Tree stumps have been found that are still alive hundreds of years after the tree was cut down, quite possibly because surrounding trees send them nutrients,” he says. With further study, he adds, it may be possible to restore the wild population of one type of tree he’s growing, the American chestnut, which was eradicated from the wild 100 years ago by blight.

Restoring the tree could help combat climate change, scientists believe, because the American chestnut can absorb and store carbon quickly.

In an adjacent greenhouse, several researchers work on an evolutionary study initiated by Fordham biologist Steven Franks, Ph.D., and focused on Brassica rapa (field mustard). As Franks demonstrated in an earlier study, the annual plant evolved earlier flowering within just five years to cope with drought conditions in California.

The Mystery of the Red-Backed Salamander’s Survival

Late in the morning, undergrads Dan Khieninson and Erin Carter and doctoral student Elle Barnes enter Calder forest in search of red-backed salamanders.

“You can find them anywhere in the forest as long as the soil’s moist,” Barnes says before the group navigates a steep decline to the forest floor.

She indicates several flat, weathered pieces of wood she’s left behind. “You’re more likely to find them under here.” The three researchers crouch down and soon locate several specimens.

They’re trying to discover why red-backed salamanders are not affected by the chytrid fungus that is devastating other amphibian populations.

“It’s not enough to just study the ones that are going extinct,” Barnes says. “There are solutions in the ones that will survive. What do they have that other amphibians are lacking?”

The answer lies in their microbiome, Barnes says. She, Carter, and Khieninson use cotton swabs on the salamanders’ bodies to collect samples of microorganisms that they can test against chytrid fungus in the lab. The impact of their research could extend beyond conservation biology, Barnes says: “The discoveries we make about disease and microbiomes can be applied to multiple systems, including humans’.”

A Closer Look at a Ubiquitious, Ecologically Valuable Species

Michael Kausch, a doctoral student in aquatic ecology, rows a boat out on Calder Lake to take some water samples he can later test for cyanobacteria at the lakefront McCarthy Laboratories. Meanwhile, inside the lab, his fellow doctoral student Stephen Gottschalk is working with their Fordham supervisor, John Wehr, Ph.D. Gottschalk is studying green algae in the Characeae family.

“They’re an important food source for birds, a habitat for insects, and they support fisheries,” he says.

So far Gottschalk has collected samples in nine U.S. states, and he’s been working at the New York Botanical Garden under the supervision of Kenneth Karol, Ph.D., to examine his samples on a molecular level.

He’s finding that what scientists once thought were just subtle differences among green algae are in fact ecologically important distinctions. “They’re designated as one species,” Gottschalk says, “but what it looks like to me so far is these are very regionally distinct.”

Mosquitoes, Ticks, and the Pathogens They Carry

Insect-borne diseases are a big part of the research focus at Routh House, the vector ecology lab at the Calder Center that’s jointly run by Fordham and the New York state health department. Inside the lab, scientists study samples of various species, such as the aggressive and potentially disease-carrying Asian tiger mosquito. Outside, they collect specimens and conduct surveillance projects.

“We set up mosquito traps all around the lower Hudson Valley,” says Marly Katz, a state employee and Fordham doctoral student. “All the mosquitoes end up here, where I identify them, and then we send a bunch [to the state health department]for disease testing.” She and her colleagues are also collaborating with Columbia University scientists to “map the Asian tiger mosquito,” she says, and determine if changes in climate are affecting its migration patterns.

While Katz checks a mosquito trap, research technician Richard Rizzitello collects ticks by dragging a white cloth across the ground and then pulling them off with forceps (he uses a lint roller to collect any larvae).

One Calder scientist, Nicholas Piedmonte, displays egg-to-adult samples of the blacklegged tick, which can carry the bacterium that causes Lyme disease.

“These are great for education and outreach,” he says, particularly in central New York, “where ticks are kind of a new problem.”

View a timeline of the Calder Center’s history. And watch a July 2017 video celebrating the center’s recent golden anniversary.

“Traditionally, we’ve thought about evolution as a long-term process that happens in relation to natural environmental features and the interactions between species. But now there is one phenomenon that is rapidly changing many other species, which is how they interact with humans and our built environment,” said Jason Munshi-South, Ph.D.

“Humans and our cities are one of the most dominant forces of contemporary evolution now.”

In “Evolution of Life in Urban Environments,” a paper by Munshi-South and co-author Marc T.J. Johnson, Ph.D., published today in the journal Science, the researchers cite direct evidence of evolutionary change among more than 100 species living in cities around the world.

Munshi-South, an associate professor of biological sciences based at Fordham’s Louis Calder Center, and Johnson, an associate professor of biology at the University of Toronto, came to this conclusion after examining the findings of 192 studies that documented evolutionary change due to urbanization.

While it has been observed since ancient times that certain animals—rats, pigeons, bedbugs, roaches, and mosquitoes, for example—adapt to the presence of humans, the number of recent studies confirm this phenomenon is widespread among species. A majority of the studies that Munshi-South and Johnson examined have been published in just the last five years.

From Isolation to Divergence

Their research reveals that a significant number of species have become isolated in cities, in either pockets of habitat that have survived or in other spaces they’ve adapted to. Urban species have diverged from other populations through multiple evolutionary processes such as genetic drift and natural selection. They have also become different not only from populations in the more rural surrounding environments, but from other urban populations of the same species.

Munshi-South said the studies raise more questions than answers, but they also hint at some intriguing possibilities.

“In some of the more recent studies on selection that have looked at the same organism in multiple cities, there seems to be this tantalizing pattern of correlated changes across cities,” he said.

“We see cities as these amazing evolutionary experiments. Some species occur in many cities all over the world, and all of those populations may be evolving in the same direction. It implies that there is some directionality and repeatability to the evolution process. There haven’t been good ways to study that outside of the laboratory or [some]small islands in the Caribbean.”

Munshi-South’s own research on rats in New York City has shown that rats living in lower Manhattan are genetically different from their relatives further uptown—likely because traveling through the habitat of midtown skyscrapers is more difficult for the colonies. Urban white-footed mice found in places like the New York Botanical Garden or Central Park also exhibit genetic changes for digesting fats and carbohydrates, compared to their rural counterparts.

White Clover and Evolution

Johnson studied the white clover plant, which produces cyanide as a defense against feeding animals, but which is poisoned by its own cyanide if the plant freezes. Survival depends on a cover of insulating snowfall in the winter. In North American cities where there is less snow cover to insulate the plants, however, Johnson found that white clover has evolved to produce less cyanide than its rural counterpart.

The researchers suggest in their paper that urban planners embrace management and design practices in cities, such as “green belts,” to help native species thrive and to mitigate disease-carrying pests.

Munshi-South said the large number of urban evolutionary biology studies that have come out recently proves that the field has become a coherent discipline in its own right.

“It started out with people, like Mark and me, studying organisms that were living near our urban universities. We started noticing changes—some small, some significant—right in the back yards of our labs,” he said.

“And they seem to be driven by changes happening in the city.”

“We used to think that evolution was such a slow process, but we really realize at this point that evolution really can be studied over experimental timescales, even less than ten generations,” he said.

To celebrate the 50th anniversary of the Calder Center, we sat down with Sekor to learn more about his research there.

The changes came in just seven years, according to the study published this week in the journal Molecular Ecology and led by Fordham biology professor Steven Franks, PhD. It’s just the latest example of how organisms can evolve more quickly than was generally thought possible, he said.

“Previously, people generally thought that evolution was always a really slow process, but more and more lately over the past decade or so, there’s been a lot of examples of evolution happening really rapidly,” he said. “[It] can happen while we study it.”

The study builds on Franks’ earlier study that he said was the first documented example of a natural plant population rapidly evolving in response to a natural change in the climate. The study found that field mustard plants in Southern California evolved to flower earlier in response to a drought that lasted from 1997 to 2004.

For the latest study, the researchers sequenced the genomes of pre-drought and post-drought plants from the first study to see how the post-drought generation was genetically different. They found hundreds of genes had rapidly evolved in response to the drought, many of them involved in traits like flowering time and stress response. The plants that flowered earlier were either more likely to survive the drought or to have a greater number of offspring, Franks said.

The study shows the value of comparing generations of species over a shorter time to study changes that are genetically based, he said.

“If you just watch the populations over time, then the traits might be changing, but maybe the organisms are just changing the traits themselves in response to the environment; [maybe]it’s not an evolutionary change that’s passed on from ancestors to descendants,” he said.

“This study allowed us to show that there really were genetic changes and we could see what they were,” he said. “By putting those ancestors and descendants in common conditions we could have more direct evidence that it was an evolutionary change.”

They also carried out a “heritability” calculation to see the degree to which traits were passed on.

He noted other studies showing rapid evolution, like one from decades ago that focused on Galapagos finches. There has always been rapid evolution of species, he said, but it could be happening more often because of a changing climate. “Conditions are changing so fast there’s a mismatch between organisms and their environment,” he said.

The study also shows how climate change can either quickly drive genetic changes in species or imperil other species that can’t evolve as quickly, he said. He added that fragmentation of plant habitats resulting from greater urbanization could impair evolution, since smaller plant populations have less of the genetic variation that allows hardier members of the species to emerge.

“Even though we can see some evolution, even rapid evolution, we need to aim for greater sustainability and lower environmental impact to protect species from extinction,” he said.

Gordon Plague, an evolutionary biologist at the Louis Calder Center, studies the evolution of bacteria in insects, among other things. Ideas are his stock in trade and he, like Ellison, can rarely point to their genesis. Except for the weevils.

An assistant professor of biological sciences, Plague raises maize weevils (Sitophilus zeamais) and rice weevils (Sitophilus oryzae) in the lab at Calder to study their symbiotic bacteria. “They’re easy to raise,” Plague says. “You can just grow them in jars with some corn or rice in an incubator in the lab.” (The incubator is used to control humidity and optimize growth, according to Plague.)

Weevils, in case you’re wondering, are insects that primarily feed on plant material. Maize weevils and rice weevils spend their larval and pupal stages within a kernel of stored grain, living off the endosperm—the starchy portion from which the seed draws nutrition (analogous to the “white” of a chicken’s egg). The weevils need the bacteria to break down the starches into nutrients the weevils can use, and the bacteria can only live inside the weevils’ specialized host cells, called bacteriomes.

Periodically, Plague and his students need to remove some weevil larvae (the sub-adult stage of the insect) from a jar to harvest bacteria from them. When they did so, Plague says, they noticed that the adult rice weevils seem to climb the walls of the jar much more vigorously than adult maize weevils after the larvae had been removed.

“A lot of times you can’t pinpoint exactly what sparked a particular question or line of research,” Plague says. “I do a lot of my best thinking when I’m walking my dog, and I can let my mind wander. But in this case, we saw that the rice weevils were climbing like crazy after the jar had been disturbed, much more so than the maize weevils. We wondered why that was.”

Enter Gaelle Voltaire, an undergraduate student in biological sciences who needed a research project. (Before we get on with the science portion of our program, let us give thanks for an article that includes the surnames “Plague” and “Voltaire.”) Plague turned Voltaire loose on the climbing weevils. Job one was to confirm that they were seeing what they thought they were seeing: that the rice weevils were indeed more vigorous climbers. Or in the language of their paper, “Our objective was to quantify this climbing behavior in both species under a variety of environmental conditions to assess whether our anecdotal observations were correct.”

Read the paper by Plague, Voltaire and lab members Bridget E. Walsh and Kevin M. Dougherty: “Rice Weevils and Maize Weevils (Coleoptera: Curculionidae) Respond Differently to Disturbance of Stored Grain,” published in the Annals of the Entomological Society of America, Vol. 103, No. 4, 2010.

It turns out that careful observation confirmed what Plague and his students had noticed in the Calder lab: the two species exhibited markedly different climbing behaviors after the jars were disturbed, with the rice weevils climbing significantly more than maize weevils under a variety of environmental conditions..

We know what you’re thinking: “Some bugs in a jar on a countertop in Westchester climbed more than some other bugs in other jars? Really? This is why I majored in English!”

But measuring the climbing rates of two species of insects isn’t an end unto itself. As a biologist, Plague sees this behavior shedding light on the deep evolutionary history not just of weevils, but of human beings. (There are also the practical considerations that his findings may have for pest control.)

It turns out a lot of insects that live and feed on stored grain exhibit this climbing behavior (“negative geotaxis” in the jargon) when the store is disturbed, and probably evolved many times in different species. Because both the rice and maize weevils exhibit the behavior, it is likely that it existed in their last common ancestor, 20 million years ago (at least 15 million years before the split between the chimpanzee and human lines). So weevils very likely infested the stored seeds and nuts of rodents and birds before humans started growing and storing surplus grain.

What would be adaptive (in other words, what would confer an advantage in leaving behind offspring) about this climbing behavior?

“These weevils have a 30-day lifecycle from egg to adult,” Plague says. “When the caches of rodents and birds were disturbed, it was probably a signal that the owner was coming home. That poses a risk that the weevil might be eaten, or at least that the cache was going away. The weevils would have to get away so they could lay eggs in another cache.”

In the simplest terms, weevils that climbed away from disturbed grain, whether in an animal cache or a silo, were more likely to leave behind offspring. Over time the offspring of the climbing weevils outnumbered less vigorous climbers until the climbing behavior was the norm. And the fact that weevils which don’t escape disturbed stores leave behind fewer offspring continues to exert selection pressure for the climbing behavior.

“The difference in climbing behavior between the rice weevils and the corn weevils may be because corn weevils are better flyers than rice weevils,” Plague says. “The rice weevils may climb more vigorously because they need more time to get away.”

“Complex behaviors are primarily maintained because they provide a survival or reproductive benefit to the animal,” Plague says. “Therefore, taking an evolutionary approach to studying animal behavior can shed insight into an animal’s biology, both past and present. This project not only did that, but the results also potentially have implications for controlling these worldwide stored grain pests. And also significantly, it was a pretty simple experiment that gave students experience with the complete scientific process, from the generation of a question to the publication of the paper.”