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Rewilding the Gut

Processed foods and overuse of antibiotics can wreak havoc on the trillions of bacteria and other microbes that inhabit the gut. A new study of the gut microbiomes of lemurs looks at whether reconnecting with nature can help restore this internal ecosystem to a more natural state. Credit: Sally Bornbusch.

Modern life messes with the microbiome -– the trillions of bacteria and other microbes that live inside the body. Could reconnecting with nature bring this internal ecosystem back into balance?

A new study suggests it can, at least in lemurs. Led by Duke Ph.D. alumnus Sally Bornbusch and her graduate advisor Christine Drea, the research team collected fecal samples from more than 170 ring-tailed lemurs living in various conditions in Madagascar: some were living in the wild, some were kept as pets, and some were rescued from the pet and tourism industries and then relocated to a rescue center in southwestern Madagascar where they ate a more natural diet and had less exposure to people.

Collecting fecal samples in Madagascar

Then the researchers sequenced DNA from the fecal samples to identify their microbial makeup. They found that the longer lemurs lived at the rescue center, the more similar their gut microbes were to those of their wild counterparts. Former pet lemurs with more time at the rescue center also showed fewer signs of antibiotic resistance.

By “rewilding” the guts of captive animals, researchers say we may be able to better prime them for success, whether after rescue or before translocation or reintroduction into the wild.

This research was supported by grants from the National Science Foundation (1945776, 1749465), the Triangle Center for Evolutionary Medicine, Duke’s Kenan Institute for Ethics, the Margot Marsh Biodiversity Fund and Lemur Love.

CITATION: “Microbial Rewilding in the Gut Microbiomes of Captive Ring-Tailed Lemurs (Lemur catta) in Madagascar,” Sally L. Bornbusch, Tara A. Clarke, Sylvia Hobilalaina, Honore Soatata Reseva, Marni LaFleur & Christine M. Drea. Scientific Reports, Dec. 27, 2022. DOI: 10.1038/s41598-022-26861-0.

Robin Smith
By Robin Smith

Modeling the COVID-19 Roller Coaster

A Duke team looks at the math behind COVID’s waves as new coronavirus variants continue to emerge. Credit: @ink-drop

DURHAM, N.C. — First it was Alpha. Then Delta. Now Omicron and its alphabet soup of subvariants. In the three years since the coronavirus pandemic started, every few months or so a new strain seems to go around, only to be outdone by the next one.

If the constant rise and fall of new coronavirus variants has left you feeling dizzy, you’re not alone. But where most people see a pandemic roller coaster, one Duke team sees a mathematical pattern.

In a new study, a group of students led by Duke mathematician Rick Durrett studied the calculus behind the pandemic’s waves.

Published Nov. 2022 in the journal Proceedings of the National Academy of Sciences, their study got its start as part of an 8-week summer research program called DOmath, now known as Math+, which brings undergraduates together to collaborate on a faculty-led project.

Their mission: to build and analyze simple mathematical models to understand the spread of COVID-19 as one strain after another popped up and then rose to outcompete the others.

In an interview about their research, project manager and Duke Ph.D. student Hwai-Ray Tung pointed to a squiggly line showing the number of confirmed COVID cases per capita in the U.S. between January 2020 and October 2022.

The COVID-19 pandemic has unfolded in waves. Adapted from The New York Times, July 18, 2022

“You can see very distinct humps,” Tung said.

The COVID pandemic has unfolded in a series of surges and lulls — spikes in infection followed by downturns in case counts.

The ups and downs are partly explained by factors such as behavior, relaxation of public policies, and waning immunity from vaccines. But much of the roller coaster has been driven by changes to the coronavirus itself.

All viruses change over time, evolving mutations in their genetic makeup as they spread and replicate. Most mutations are harmless, but every so often some of them give the virus an edge: Enabling it to break into cells more easily than other strains, better evade immunity from vaccines and past infection, or make more copies of itself in order to spread more effectively.

Take the Delta variant, for example. When it first started going around in the U.S. in May 2021, it was responsible for just 1% of COVID cases. But thanks to mutations that helped the virus evade antibodies and infect cells more easily, it quickly tore across the country. Within two months it had outcompeted all the other variants and rose to the top spot, causing 94% of new infections.

“The natural question to ask is: What’s going on with the transition between these different variants?” Tung said.

For their study the team developed a simple epidemic model called an SIR model, which uses differential equations to compute the spread of disease over time.

SIR models work by categorizing individuals as either susceptible to getting sick, currently infected, or recovered. The team modified this model to have two types of infected individuals and two types of recovered individuals, one for each of two circulating strains.

The model assumes that each infectious person spreads the virus to a certain number of new people per day (while sparing others), and that, each day, a certain fraction of the currently infected group recovers.

In the study, the team applied the SIR model to data from a database called GISAID, which contains SARS-CoV-2 virus sequences from the pandemic. By looking at the coronavirus’s genetic code, researchers can tell which variants are causing infection.

Study co-author Jenny Huang ’23 pointed to a series of S-shaped curves showing the fraction of infections due to each strain from one week to the next, from January 2021 to June 2022.

When they plotted the data as points on a graph, they found that it followed a logistic differential equation as each new variant emerged, rose steeply, and — within six to 10 weeks — quickly displaced its predecessors, only to be taken over later by even more aggressive or contagious strains.

Durrett said it’s the mathematical equivalent of something biologists call a selective sweep, when natural selection increases a variant’s frequency from low to high, until nearly everyone getting stick is infected with the same strain.

“I’ve been interested in epidemic modeling since the end of freshman year when COVID started,” said Huang, a senior who plans to pursue a Ph.D. in statistics next year with support from a prestigious Quad Fellowship.

They’re not all typical math majors, Durrett said of his team. Co-author Sofia Hletko, ’25, was a walk-on to the rowing team. Laura Boyle ’24 was a Cameron Crazie.

For some team members it was their first experience with mathematical research: “I came in having no idea what a differential equation was,” Boyle said. “And by the end, I was the person in the group explaining that part of our presentation to everyone.”

Boyle says one question she keeps getting asked is: what about the next COVID surge?

“It’s very hard to say what will happen,” Boyle said.

The teams says their research can’t predict future waves. Part of the reason is the scanty data on the actual number of infections.

Countries have dialed back on their surveillance testing, and fewer places are doing the genomic sequencing necessary to identify different strains.

“We don’t know the nature of future mutations,” Durrett said. “Changes in people’s behavior will have a significant impact too.”

“The point of this paper wasn’t to predict; rather it was to explain why the waves were occurring,” Huang said. “We were trying to explain a complicated phenomenon in a simple way.”

This research was supported by a grant from the National Science Foundation (DMS 1809967) and by Duke’s Department of Mathematics.

CITATION: “Selective Sweeps in SARS-CoV-2 Variant Competition,” Laura Boyle, Sofia Hletko, Jenny Huang, June Lee, Gaurav Pallod, Hwai-Ray Tung, and Richard Durrett. Proceedings of the National Academy of Sciences, Nov. 3, 2022. DOI: 10.1073/pnas.2213879119.

Robin Smith
By Robin Smith

For Weary Scholars, a Moment to Regroup, Reconnect…and Write

DURHAM, N.C. — English professor Charlotte Sussman doesn’t get much time in her role as department chair to work on her latest book project, an edited collection of essays on migration in and out of Europe.

“At least not during daylight hours,” Sussman said.

But a recent workshop brought a welcome change to that. Sussman was one of 22 faculty who gathered Dec. 13 for an end-of-semester writing retreat hosted by the Duke Faculty Write Program.

Duke faculty and staff gather for an end-of-semester writing retreat.

Most of them know all too well the burnout faculty and students face at the end of the semester. But for a few precious hours, they hit pause on the constant onslaught of emails, meetings, grading and other duties to work alongside fellow writers.

The participants sat elbow-to-elbow around small tables in a sunlit room at the Duke Integrative Medicine Center. Some scribbled on pads of paper; others peered over their laptops.

Each person used the time to focus on a specific writing project. Sussman aimed to tackle an introduction for her 34-essay collection. Others spent the day working on a grant application, a book chapter, a course proposal, a conference presentation.

Jennifer Ahern-Dodson, Ph.D.
Jennifer Ahern-Dodson, Ph.D.

“We have so many negative associations with writing because there’s always something more to do,” said associate professor of the practice Jennifer Ahern-Dodson, who directs the program. “I want to change the way people experience writing.”

Ahern-Dodson encouraged the group to break their projects into small, specific tasks as they worked toward their goals. It might be reading a journal article, drafting an outline, organizing some notes, even just creating or finding a file.

After a brief workshop, she kicked off a 60-minute writing session. “Now we write!” she said.

The retreat is the latest installment in a series that Ahern-Dodson has been leading for over 10 years. In a typical week, most of these scholars wouldn’t find themselves in the same room. There were faculty and administrators from fields as diverse as history, African and African American Studies, law, psychology, classics, biostatistics. New hires sitting alongside senior scholars with decades at Duke.

Peggy Nicholson, J.D., Clinical Professor of Law, writing alongside colleagues from across campus

“I really like the diversity of the group,” said Carolyn Lee, Professor of the Practice of Asian and Middle Eastern Studies. “It’s a supportive environment without any judgement. They all have the same goal: they want to get some writing done.”

Sussman said such Faculty Write program get-togethers have been “indispensable” to bringing some of her writing projects over the finish line.

Participants say the program not only fosters productivity, but also a sense of connection and belonging. Take Cecilia Márquez, assistant professor in the Duke History Department. She joined the Duke faculty in 2019, but within months the world went into COVID-19 lockdown.

“This was my way to meet colleagues,” said Márquez, who has since started a writing group for Latinx scholars as an offshoot.

The writing retreats are free for participants, thanks to funding from the Office of the Dean of Trinity College of Arts and Sciences and the Thompson Writing Program. Participants enjoy lunch, coaching and community in what’s normally a solitary activity.

“I appreciate the culture of collaboration,” said David Landes, who came to Duke this year as Assistant Professor of the Practice in Duke’s Thompson Writing Program. “In the humanities our work is intensely individualized.”

Assistant Professor of Biostatistics & Bioinformatics Hwanhee Hong (left) and Adam Rosenblatt, Associate Professor of the Practice in International Comparative Studies (right)

Retreats are one of many forms of support offered by the Faculty Write program: there are also writing groups and workshops on topics such as balancing teaching and scholarship or managing large research projects.

“One of the distinguishing features of Faculty Write is the community that extends beyond one event,” Ahern-Dodson said. “Many retreats are reunions.”

After two hours of writing, Ahern-Dodson prompted the group to take a break. Some got up to stretch or grab a snack; others stepped outside to chat or stroll through the center’s labyrinth at the edge of Duke Forest.

It’s more than just dedicated writing time, Ahern-Dodson said. It’s also “learning how to work with the time they have.”

The retreats offer tips from behavioral psychology, writing studies, and other disciplines on time management, motivation, working with reader feedback, and other topics.

As they wrap up the last writing session of the day, Ahern-Dodson talks about how to keep momentum.

“Slow-downs and writing block are normal,” Ahern-Dodson said. Maybe how you wrote before isn’t working anymore, or you’re in a rut. Perhaps you’re not sure how to move forward, or maybe writing simply feels like a slog.

“There are some things you could try to get unstuck,” Ahern-Dodson said. Consider changing up your routine: when and where you write, or how long each writing session lasts.

“Protect your writing time as you would any other meeting,” Ahern-Dodson said.

Sharing weekly goals and accomplishments with other people can help too, she added.

“Celebrate each win.”

Ultimately, Ahern-Dodson says, the focus is not on productivity but on meaning, progress and satisfaction over time.

“It’s all about building a sustainable writing practice,” she said.

Ahern-Dodson leads an end-of-semester writing retreat for Duke scholars.

Coming soon: On Friday, Jan. 27 from 12-1 p.m., join Vice Provost for Faculty Advancement Abbas Benmamoun for a conversation about how writing works for him as a scholar and administrator. In person in Rubenstein Library 249 (Carpenter Fletcher Room)

Get Involved: Faculty and staff are invited to sign up for writing groups for spring 2023 here.

Learn more about sustainable writing practices: “The Productivity Trap: Why We Need a New Model of Faculty Writing Support,” Jennifer Ahern-Dodson and Monique Dufour. Change, January/February 2023.

Robin Smith
By Robin Smith

Traveling With Friends Helps Even Mixed-Up Migrators Find Their Way

North American monarch butterflies migrate each winter to just a few mountaintops in central Mexico, with help from an internal compass that guides them home. New computer modeling research offers clues to how migrating animals get to where they need to go, even when their magnetic compass leads them astray. Credit: Jesse Granger, Duke University

DURHAM, N.C. — Some of us live and die by our phone’s GPS. But if we can’t get a signal or lose battery power, we get lost on our way to the grocery store.

Yet animals can find their way across vast distances with amazing accuracy.

Take monarch butterflies, for example. Millions of them fly up to 2,500 miles across the eastern half of North America to the same overwintering grounds each year, using the Earth’s magnetic field to help them reach a small region in central Mexico that’s about the size of Disney World.

Or sockeye salmon: starting out in the open ocean they head home each year to spawn. Using geomagnetic cues they manage to identify their home stream from among thousands of possibilities, often returning to within feet of their birthplace.

Now, new research offers clues to how migrating animals get to where they need to go, even when they lose the signal or their inner compass leads them astray. The key, said Duke Ph.D. student Jesse Granger: “they can get there faster and more efficiently if they travel with a friend.”

When their internal compasses go bad, migrating animals like these sockeye salmon don’t stop to ask directions. But they succeed if they stay with their fellow travelers. Credit: Jonny Armstrong, USGS

Many animals can sense the Earth’s magnetic field and use it as a compass. What has puzzled scientists, Granger said, is the magnetic sense is not fail-safe. These signals coming from the planet’s molten core are subtle at the surface. Phenomena such as solar storms and man-made electromagnetic noise can disrupt them or drown them out.

It’s as if the ‘needle’ of their inner compass sometimes gets thrown off or points in random directions, making it hard to get a reliable reading. How do some animals manage to chart a course with such a noisy sensory system and still get it right?

“This is the question that keeps me up at night,” said Granger, who did the work with her adviser, Duke Biology Professor Sönke Johnsen.

Multiple hypotheses have been put forward to explain how they do it. Perhaps, some scientists say, migrating animals average multiple measurements taken over time to get more accurate information.

Or maybe they switch from consulting their magnetic compass to using other ways of navigating as they near the end of their journey — such as smell, or landmarks — to narrow in on their goal.

In a paper published Nov. 16 in the journal Proceedings of the Royal Society B, the Duke team wanted to pit these ideas against a third possibility: That some animals still manage to find their way, even when their compass readings are unreliable, simply by sticking  together.

To test the idea, they created a computer model to simulate virtual groups of migrating animals, and analyzed how different navigation tactics affected their performance.

The animals in the model begin their journey spread out over a wide area, encountering others along the route. The direction an animal takes at each step along the way is a balance between two competing impulses: to band together and stay with the group, or to head towards a specific destination, but with some degree of error in finding their bearings.

The scientists found that, even when the simulated animals started to make more mistakes in reading their magnetic map, the ones that stuck with their neighbors still reached their destination, whereas those that didn’t care about staying together didn’t make it.

“We showed that animals are better at navigating in a group than they are at navigating alone,” Granger said.

Even when their magnetic compass veered them off course, more than 70% of animals in the model still made it home, simply by joining with others and following their lead. Other ways of compensating didn’t measure up, or would need to guide them perfectly for most of the journey to accomplish the same feat.

But the strategy breaks down when species decline in number, the researchers found. The team showed that animals who need friends to find their way are more likely to get lost when their population shrinks below a certain density.

Prior to the 1950s, tens of thousands of Kemp’s ridley sea turtles could be seen nesting near Rancho Nuevo, Mexico on a single day. By the mid-1980s the number of nesting females had dropped to a few hundred.

“If the population density starts dropping, it takes them longer and longer along their migratory route before they find anyone else,” Granger said.

Previous studies have made similar predictions, but the Duke team’s model could help future researchers quantify the effect for different species. In some runs of the model, for example, they found that if a hypothetical population dropped by 50% — akin to what monarchs have experienced in the last decade, and some salmon in the last century — 37% fewer of the remaining individuals would make it to their destination.

“This may be an underappreciated aspect of concern when studying population loss,” Granger said.

This research was supported in part by the Air Force Office of Scientific Research (FA9550-20-1-0399) and by a National Defense Science & Engineering Graduate Fellowship to Jesse Granger.

CITATION: “Collective Movement as a Solution to Noisy Navigation and its Vulnerability to Population Loss,” Jesse Granger and Sönke Johnsen. Proceedings of the Royal Society B, Nov. 16, 2022. DOI: 10.1098/rspb.2022.1910

Robin Smith
By Robin Smith

Feeling Lonely? What We Want From Our Relationships Can Change With Age

Not feeling the holiday cheer this year? The gap between expectations and reality can leave people feeling lonely. Photo by madartzgraphics.

Not everyone’s holiday plans resemble a Hallmark card.

If the “most wonderful time of the year” isn’t your reality, you’re not alone. You might have an idea of a festive picture-perfect holiday season, but what actually transpires doesn’t always measure up.

And that’s where loneliness comes from, says King’s College London graduate student Samia Akhter-Khan, first author of a new study on the subject.

“Loneliness results from a discrepancy between expected and actual social relationships,” Akhter-Khan said.

Together with Duke psychology and neuroscience Ph.D. Leon Li, Akhter-Khan and colleagues co-authored a paper on why people feel lonely, particularly in later life, and what we can do about it.

“The problem that we identified in current research was that we haven’t really thought about: What do people expect from their relationships?” Akhter-Khan said. “We work with this definition of expectations, but we don’t really identify what those expectations are and how they change across cultures or over the lifespan.”

In every relationship, we expect certain basics. We all want people in our lives who we can ask for help. Friends we can call on when we need them. Someone to talk to. People who “get” us. Someone we can trust. Companions with whom we can share fun experiences.

But the team’s theory, called the Social Relationship Expectations Framework, suggests that older people may have certain relationship expectations that have gone overlooked.

Akhter-Khan’s first clue that the causes of loneliness might be more complex than meets the eye came during a year she spent studying aging in Myanmar from 2018 to 2019. At first, she assumed people generally wouldn’t feel lonely — after all, “people are so connected and live in a very close-knit society. People have big families; they’re often around each other. Why would people feel lonely?”

But her research suggested otherwise. “It actually turns out to be different,” she said. People can still feel lonely, even if they don’t spend much time alone.

What efforts to reduce loneliness have neglected, she said, is how our relationship expectations change as we get older. What we want from social connections in, say, our 30s isn’t what we want in our 70s.

The researchers identified two age-specific expectations that haven’t been taken into account. For one, older adults want to feel respected. They want people to listen to them, to take an interest in their experiences and learn from their mistakes. To appreciate what they’ve been through and the obstacles they have overcome.

They also want to contribute: to give back to others and their community and pass along traditions or skills through teaching and mentoring, volunteering, caregiving, or other meaningful activities.

Finding ways to fulfill these expectations as we get older can go a long way towards combating loneliness in later life, but research has largely left them out.

“They’re not part of the regular scales for loneliness,” Li said.

Part of the reason for the oversight may be that often the labor and contributions of older people are unaccounted for in typical economic indices, said Akhter-Khan, who worked in 2019-20 as a graduate research assistant for a Bass Connections project at Duke on how society values care in the global economy.

“Ageism and negative aging stereotypes don’t help,” she added. A 2016 World Health Organization survey spanning 57 countries found that 60% of respondents said that older adults aren’t well respected.

Loneliness isn’t unique to older people. “It is a young people’s problem as well,” Akhter-Khan said. “If you look at the distribution of loneliness across the lifespan, there are two peaks, and one is in younger adulthood, and one is an old age.”

Even before the COVID-19 pandemic, world leaders began sounding the alarm on loneliness as a public health issue. Britain became the first country to name a minister for loneliness, in 2018. Japan followed suit in 2021.

That’s because loneliness is more than a feeling – it can have real impacts on health. Persistent loneliness has been associated with higher risks of dementia and Alzheimer’s disease, heart disease and stroke, and other health problems. Some researchers suggest it’s comparable or riskier than smoking and obesity.

The researchers hope that if we can better understand the factors driving loneliness, we might be better able to address it.

CITATION: “Understanding and Addressing Older Adults’ Loneliness: The Social-Relationship Expectations Framework,” Samia C. Akhter-Khan, Matthew Prina, Gloria Hoi-Yan Wong, Rosie Mayston, and Leon Li. Perspectives on Psychological Science, Nov. 2, 2022. DOI: 10.1177/17456916221127218

Robin Smith
By Robin Smith

How to Encourage Preschoolers to Be More Fair, According to Science

Exposing young kids to different opinions or asking them to explain their thinking can have surprising benefits, Duke University researchers find.

DURHAM, N.C. — “But that’s not fair!” If you’re a parent or a teacher, you’ve probably heard this countless times.

To most young children, “fair” simply means treating everyone equally. Kids are quick to say they shouldn’t have to go to bed earlier than a sibling, or put up with more chores or homework than a classmate.

But as children get older, they begin to grasp that sometimes, things can be unequal and still be fair — especially when people have different needs, circumstances, or abilities. Up until 8 to 10 years of age, most children aren’t yet capable of such moral subtlety, but a new study shows they can get closer, with help from a surprising source: disagreement.

For preschoolers, a 20-minute conversation with someone who disagrees with them or who asks them to justify their ideas can foster more nuanced moral calculations about what it means to be “fair.”

That’s the key finding from a new Duke University study that examines how children develop their sense of morality.

Many theorists have proposed that a child’s interactions with other people can shape their growing sense of right and wrong. But experiments to pinpoint exactly what kinds of interactions are most helpful have been lacking, said first author Leon Li, who did the research with developmental psychologist Michael Tomasello as part of his PhD in psychology and neuroscience at Duke.

In a study that appeared this summer in the Journal of Experimental Child Psychology, the researchers asked 129 children aged 4 to 5 years to discuss simple moral dilemmas with a puppet and try to make the most fair decision.

In one experiment for example, they asked the children to imagine two boys, one of whom missed breakfast, and decide how to split cookies between them at snack time. In another, the question was whether two girls should get in the same amount of trouble for throwing away someone’s lunch, when one of them mistook it for trash.

No matter what the child decided, afterward the puppet responded by either agreeing or disagreeing, and by either asking the child to explain their reasoning or not. Then the researchers observed how the puppet’s responses affected the child’s thinking in future trials.

They found that children who had previously encountered different points of view, or had to justify their decisions, were more likely to favor the more deserving recipient, rather than fall into “fair must mean equal” thinking.

Li cautions that disagreeing with a child or asking them to justify themselves won’t necessarily make them more honest, or hardworking, or generous.

“Those are other domains of morality, but we only found this in fairness,” Li said. “It’s possible it wouldn’t have an effect with, say, social exclusion” or some other aspect of moral behavior that the team didn’t examine.

But when people ask him, ‘is this how I teach my child to be more virtuous?’ — at least when it comes to fairness — “the answer is yes,” Li said.

CITATION: “Disagreement, Justification, and Equitable Moral Judgments: A Brief Training Study,” Leon Li and Michael Tomasello. Journal of Experimental Child Psychology, July 14, 2022. DOI: 10.1016/j.jecp.2022.105494

Robin Smith
by Robin Smith

Lemur Gut Isn’t One Ecosystem, It’s Many

Lemurs like Ferdinand are leaf-eating machines, says Duke microbiome researcher Lydia Greene. Credit: Lydia Greene

DURHAM, N.C. — A jungle. A rainforest. A wetland. A wilderness. Researchers have used various metaphors to describe the complex, interconnected community of microbes (most of them bacteria) living inside your body, and all over it too.

If you were to count up all the trillions of cells inside and out, we are more bacteria than human. Fortunately, perhaps, the microbes that make a cozy home inside your nose, or clinging to your teeth, aren’t the same ones that are living behind your ear or busily multiplying in your belly button.

The same is true for our distant primate cousins the lemurs, particularly in their guts, say researchers Lydia Greene and Erin McKenney in a new study.

Lemurs rely on gut microbes to digest their leafy diets, explains Greene, a research scientist at the Duke Lemur Center. Microbes in lemurs’ GI tracts help ferment plant fiber, detoxify plant chemical defenses, and synthesize vitamins and nutrients that lemurs can’t make for themselves. Our own gut bugs do many of the same things for us.

Greene and McKenney study how lemur gut bacteria are shaped by what lemurs eat, how they evolved and the complexity of the route microbes travel through the body. They hope to better understand how these microorganisms keep lemurs healthy, or — when they’re out of balance — make them sick.

Researchers who do this kind of work spend a lot of time collecting poop. For good reasons, says McKenney, an assistant professor at North Carolina State University. Scientists can learn about lemurs by what they leave behind, and poop can be collected repeatedly without harming the animals. But for this study the team tried something different, made possible by a one-of-a-kind biobank:

When an animal dies at the Duke Lemur Center, veterinary staff determine the cause of death, and blood and tissue samples that might be important for research or education are collected and preserved.

Today, the collection holds thousands of samples, collected over decades from more than two dozen species of rare and endangered primates, which the center stores in super cold freezers in their headquarters in North Carolina. It’s a frozen ark maintained at up to minus 80 degrees Celsius, with redundant backup power.

In the event that any one of these species goes extinct, and the last living parts of them are gone, future generations will still be able to study the genetic and other information they left behind.

Using this bank, the team sampled several sites in the bowels of 52 deceased lemurs, including dwarf lemurs, aye-ayes, ruffed lemurs, bamboo lemurs, brown lemurs, ring-tailed lemurs and sifakas.

A trip through a lemur’s GI tract is a journey through a varied landscape. The long, twisting route from the stomach through the small intestine to the colon serves numerous functions, filtering, digesting, absorbing, detoxifying, fermenting.

Not all lemur guts work the same: Fruit-eaters, like ruffed lemurs, generally have short, simple guts. If you stretched them out, they’d be five times their body length — not much shorter than ours, relative to body size. Leaf-eaters like sifakas have more complex GI tracts with relatively longer colons and a leaf-fermentation pouch called a cecum. Their guts are the lemur champions — up to 16 times body length.

Having whole lemurs to study instead of just poo enabled the researchers to sample different regions of the gut to figure out what kinds of microbes were present in each spot. They used genetic sequencing technology to identify microbes and compare their relative abundance in different sites.

Sampling along the digestive tract, they found that different spots along this long, twisting pathway have their own communities of bacteria doing different kinds of jobs. The complex ecosystem lurking in a lemur’s small intestine, for example, isn’t the same as the microbial menagerie setting up camp in their colon.

Levels of biodiversity varied too. The stomach supports less microbial life because fewer species can tolerate its acidic digestive juices. But if the upper regions of the gut are a garden, the lower regions are more like a tropical rainforest. About two dozen types of bacteria were more abundant in the cecum and colon than elsewhere. Lemurs with relatively longer lower guts host the richest microbiomes, to better ferment high-fiber foods.

“We probably couldn’t have detected these relationships without such an extensive comparative dataset,” McKenney said.

“This kind of lemur research can really only be done at the Duke Lemur Center,” Greene said.

Rodelinda, a Coquerel’s sifaka lemur, munches on leaves at the Duke Lemur Center. Credit: Lydia Greene.

This research was supported by the National Science Foundation (DBI PRFB 1906416) and by a Duke Lemur Center Director’s fund.

CITATION: “Gut Site and Gut Morphology Predict Microbiome Structure and Function in Ecologically Diverse Lemurs,” Lydia K. Greene, Erin A. McKenney, William Gasper, Claudia Wrampelmeier, Shivdeep Hayer, Erin E. Ehmke, & Jonathan B. Clayton. Microbial Ecology, May 14, 2022. DOI: 10.1007/s00248-022-02034-4

Behold: the Cell’s Skeleton in Motion

To many of us, cells are the building blocks of life, akin to bricks or Legos. But to biologist Regan Moore, a former Ph.D. student in Dan Kiehart’s lab at Duke, cells are so much more: they’re busy construction sites, machinery and materials moving about to build and shape the body. And now, new live imaging techniques make it possible to watch some of the nano-scale construction in action.

In time-lapse videos published this month, Moore, Kiehart and colleagues were able to peer inside cells as they filled a hole in the back of a developing fruit fly, a crucial step in the fly’s development into a larva. The process is coordinated with help from a thin mesh of protein fibers just under the cell surface, each one 10,000 times finer than a human hair. The fibers help the cells hold their shape, “kind of like rebar in concrete,” Moore said.

But unlike rebar, she added, “they’re constantly moving and changing.” Normally, features like these are too small and quick to see with conventional microscopes, which can only take a few images a second or are too out-of-focus. So Kiehart’s team used a technique called super-resolution fluorescence microscopy to track individual fibers with nanoscale resolution.

By watching the “rebar of the cell” at work during this hole-closing process in fruit flies, the researchers hope to better understand wound healing in humans, and what goes awry for children with birth defects such as cleft lip and spina bifida.

LEARN MORE: “Super-resolution microscopy reveals actomyosin dynamics in medioapical arrays,” Regan P. Moore, Stephanie M. Fogerson, U. Serdar Tulu, Jason W. Yu, Amanda H. Cox, Melissa A. Sican, Dong Li, Wesley R. Legant, Aubrey V. Weigel, Janice M. Crawford, Eric Betzig, and Daniel P. Kiehart. Molecular Biology of the Cell, July 15, 2022. DOI: 10.1091/mbc.E21-11-0537

Finding the Tipping Point for Coastal Wetlands

Cypress swamp, eastern North Carolina. Photo by Steve Anderson, Duke

DURHAM, N.C. — The Albemarle-Pamlico Peninsula covers more than 2,000 square miles on the North Carolina coastal plain, a vast expanse of forested swamps and tea-colored creeks. Many people would probably avoid this place, whose dense thickets of cane and shrubs and waterlogged soils can slow a hike to a crawl.

“It’s hard fieldwork,” says Duke researcher Steve Anderson. “It gets really dense and scratchy. That, plus the heat and humidity mixed with the smell of sulfur and the ticks and the poison ivy; it just kind of adds up.”

But to Anderson and colleagues from Duke and North Carolina State University, these bottomlands are more than impenetrable marsh and muck and mosquitoes. They’re also a barometer of change.

Researchers surveying plants in Alligator River National Wildlife Refuge in 2016. Photo by Mathew Stillwagon, North Carolina State University

Most of the area they study lies a mere two to three feet above sea level, which exposes it to surges of ocean water — 400 times saltier than freshwater — driven inland by storms and rising seas. The salt deposits left behind when these waters recede build up year after year, until eventually they become too much for some plants to cope with.

Trudging in hip waders through stunted shrubs and rotting tree stumps, Anderson snaps a picture with his phone of a carpet of partridge berry trailing along the forest floor. In some parts of the peninsula, he says, the soils are becoming so salty that plants like these can no longer reproduce or are dying off entirely.

Along the North Carolina coast, understory plants such as this partridge berry (left) are quickly ceding ground to species such as this bigleaf marsh-elder (right) as the soils become too salty for them to thrive. Credit: Steve Anderson

In a recent study the team, led by professors Justin Wright and Emily Bernhardt of Duke, and Marcelo Ardón of NC State, surveyed some 112 understory plants in the region, making note of where they were found and how abundant they were in relation to salt levels in the soil.

The researchers identified a ‘tipping point,’ around 265 parts per million sodium, where even tiny changes in salinity can set off disproportionately large changes in the plants that live there.

Above this critical threshold, the makeup of the marsh floor suddenly shifts, as plants such as wax myrtle, swamp bay and pennywort are taken over by rushes, reeds and other plants that can better tolerate salty soils.

Certain dwindling plants could be an early warning sign that salt is poisoning inland waters, researchers say. Credit: Steve Anderson

The hope is that monitoring indicator species like these could help researchers spot the early warning signs of salt stress, Anderson says.

This research was supported by grants from the National Science Foundation (DEB1713435, DEB 1713502, and Coastal SEES Collaborative Research Award Grant No. 1426802).

CITATION: “Salinity Thresholds for Understory Plants in Coastal Wetlands,” Anderson, S. M., E. A. Ury, P. J. Taillie, E. A. Ungberg, C. E. Moorman, B. Poulter, M. Ardón, E. S. Bernhardt, and J. P. Wright. Plant Ecology, Nov. 24, 2021. DOI: 10.1007/s11258-021-01209-2.

Salt is poisoning the soils past a point of no return for some marsh plants; one team is trying to pinpoint the early warning signs. By Steve Anderson.

When the gut’s internal ecosystem goes awry, could an ancient if gross-sounding treatment make it right?

Lemur researchers make a case for fecal transplants to reduce the side effects of antibiotics. Photo by David Haring, Duke Lemur Center.

Dr. Cathy Williams knew something wasn’t right. The veterinarian had felt off for weeks after her 2014 trip to Madagascar.

At first she just felt bloated and uncomfortable and wasn’t interested in eating much. But eventually she developed a fever and chills that sent her to the emergency room.

When tested, doctors found that what she had wasn’t just a stomach bug. She was suffering from an infection of Clostridium difficile, a germ that causes severe diarrhea and abdominal pain and can quickly become life-threatening if not treated promptly.

“It was horrible,” Williams said.

The condition is often triggered when antibiotics disrupt the normal balance of bacteria that inhabit the gut, allowing “bad” bacteria such as C. difficile to multiply unchecked and wreak havoc on the intestines.

To get her infection under control, Williams asked her doctors if they could try an approach she and other veterinarians had used for decades to treat lemurs with digestive problems at the Duke Lemur Center. The procedure, known as a fecal microbiota transplant, involves taking stool from a healthy donor and administering it to the patient to add back “good” microbes and reset the gut.

At the time it was considered too experimental for clinical use in human cases like Williams’. She was prescribed the standard treatment and was sent home from the hospital, though she wouldn’t feel well enough to go back to work for another month. But now new research in lemurs is confirming what Williams and others long suspected: that this ancient if gross-sounding treatment can help an off-kilter gut microbiome get back to normal.

In a recent study in the journal Animal Microbiome, a research team led by Duke professor Christine Drea, former PhD student Sally Bornbusch and colleagues looked at the gut microbiomes of 11 healthy ring-tailed lemurs over a four-month period after receiving a seven-day course of the broad-spectrum antibiotic amoxicillin.

The lemurs were split into two experimental groups. One was a wait-and-see group, with continued follow-up but no further treatment after the antibiotics. The other group was given a slurry of their own feces, collected prior to antibiotic treatment and then mixed with saline and fed back to the same animal after their course of antibiotics was over.

“It sounds crazy,” Williams said. But she has used a similar procedure since the 1990s to treat illnesses in Coquerel’s sifaka lemurs, whose infants are known to eat their mother’s poop during weaning — presumably to get the microbes they’ll need to transition to solid food.

A baby Coquerel’s sifaka tries some of her first solid foods. Photo by David Haring.

Drea, Bornbusch and team used genetic sequencing techniques to track changes in the lemurs’ gut microbiome before, during and after treatment.

As expected, even a single course of antibiotics caused the numbers of microbes in their guts to plunge compared with controls, briefly wiping out species diversity in both experimental groups before returning to baseline.

“Antibiotics had dramatic effects, even in healthy animals,” Drea said.

But in terms of which types of bacteria bounced back and when, the patterns of recovery in the two groups were different. Lemurs that received the “poop soup” treatment started to stabilize and return to their pre-antibiotic microbiome within about two weeks. In contrast, the bacterial composition in the wait-and-see group continued to fluctuate, and still hadn’t quite returned to normal even after four months of observation.

This kind of therapy isn’t new. Reports of using fecal transplants to treat people suffering from food poisoning or diarrhea date back as far as fourth century China. The evidence for its effectiveness in captive settings has Bornbusch advocating for freezing stool at Smithsonian’s National Zoo, where she is now a postdoctoral fellow.

“If we can bank feces from animals when they’re healthy, that can be a huge benefit down the road,” Bornbusch said. “It can help the animals get better, faster.”

And now if any of her lemur patients were to get sick with C. difficile like she did, Williams said, “I would absolutely go with a fecal microbiota transplant.”

“People are put off by it,” Drea said, “But the disgust for this approach might actually have been holding up a fairly cheap and useful cure.”

Ring-tailed lemurs at the Duke Lemur Center in North Carolina. Photo by David Haring, Duke Lemur Center

This research was supported by the National Science Foundation (BCS 1749465), the Duke Lemur Center Director’s Fund, and the Duke Microbiome Center.

CITATION: “Antibiotics and Fecal Transfaunation Differentially Affect Microbiota Recovery, Associations, and Antibiotic Resistance in Lemur Guts,” Sally L. Bornbusch, Rachel L. Harris, Nicholas M. Grebe, Kimberly Roche, Kristin Dimac-Stohl, Christine M. Drea. Animal Microbiome, Oct. 1, 2021. DOI: 10.1186/s42523-021-00126-z.

By Robin Ann Smith

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