Physical Address

304 North Cardinal St.
Dorchester Center, MA 02124

This biologist discovered that lizards and other organisms can influence their own evolution

On a hot day in July, evolutionary biologist Martha Muñoz is leading four undergraduate students on a scouting expedition in the Smoky Mountains of North Carolina. As they hike up a steep trail, Muñoz turns over rocks and pokes leaf litter to assess where they might find salamanders when they return that night. She quizzes the students about how the weather might affect their chances, then demonstrates how the crunch of leaves underfoot is an easy way to assess an area’s dryness. Too much crunch means the salamanders won’t be out that night.

When one student falls behind, Muñoz hangs back to lend a hand if needed. Aha Anderson has a balance disorder and apologizes for their slowness. “No apologies needed,” Muñoz assures them. Later the crew will stop by Walmart to pick up a walking stick for Anderson. When another student, Jesús Buenrostro, proves squeamish about spiders, centipedes, and even grasshoppers, Muñoz reassures him with a few words in Spanish.

After dark, the group will return with headlamps, thermometers, and humidity sensors—and the goal of collecting 10 gray-cheeked salamanders to add to the growing salamander collection in Muñoz’s lab at Yale University. They’ll document the precise environment in which each one is found.

The southern Appalachians are a diversity hot spot for these creatures, but many of the roughly 30 species of lungless salamanders here look similar. Their environment also seems uniform, at least at first glance—creating a puzzle about how so many species could have evolved. Muñoz suspects subtle differences in behavior or habitat may have driven the salamanders to diversify, and she wants to figure out what they could be.

The Smoky Mountains are home to about 30 species of lungless salamanders, including Plethodon montanus.Mike Belleme

At 37, Muñoz has already won recognition for her discoveries about underappreciated influences on evolution, some of which buck classical thinking in the field. Her extensive studies with Caribbean lizards called anoles, for example, have provided some of the best empirical evidence that organisms can shape their evolutionary trajectory through their behavior, either speeding up or slowing down the evolution of physiological and morphological traits. She brings perspectives from multiple disciplines to evolutionary questions, says Robert Pringle, an evolutionary ecologist at Princeton University. “Her research is at the nexus of ecology, evolution, and physiology, and she has been in the vanguard of testing whether behavior acts as a drag on evolution or instead accelerates it,” Pringle says.

Muñoz sees a parallel in her own career path. The daughter of Cuban refugees, she knows firsthand the challenges people from underrepresented groups face as they try to get a toehold in academic science. “There is power in knowing that we can take control of our own circumstances, that we can guide our futures,” she says. “And there is even more power in knowing that this is a process that has unfolded for millions of years. It’s not the exception; it’s the norm.”

With that in mind, not only does Muñoz work hard to influence evolutionary thinking, she also strives to make sure others have a chance to make their own impact, no matter their background. “In my home you could often hear, ‘El éxito de uno de nosotros es el éxito de todos’—the success of any of us is a success for all of us,” she explains. “This is how I run my lab.”

Muñoz credits her grandmothers and parents for her work ethic and success. After fleeing Cuba in the 1970s, her maternal grandmother scrubbed toilets to keep Muñoz’s mother and aunt housed and fed and later took care of Muñoz so her parents could work. The family eventually moved to a semidetached house in Queens near LaGuardia Airport, where despite regular insults from a racist neighbor, Muñoz found the diverse neighborhood exciting and inspiring. “We were all immigrants, all trying to get ahead,” Muñoz recalls. To help out, Muñoz took a job as a cashier at the local Rite Aid, where she endured threats from angry patients being refused expired prescriptions, met customers who had to choose between food and medicine, and put up with condescending doctors. “There isn’t anything about being a PI [principal investigator] that you can’t learn by being in retail,” she says.

Muñoz fell in love with nature at an early age. She and a friend scaled the chain link fence at a local park, pretending they were climbing trees in the wilderness. “I dragged every adult I could find” to the American Museum of Natural History, the Bronx Zoo, and the New York Botanical Garden, where she could connect to the natural world.

Muñoz on one knee in a forest at night, holding a small green instrument at her eye level close to a mostly out-of-frame sapling.
Martha Muñoz measures wind speed and humidity where salamanders are found to investigate what microhabitat each species prefers. Mike Belleme

In freshman biology at Boston University, she learned about the rapid diversification of animal species during the Cambrian explosion more than 500 million years ago. It “moved me to tears,” she recalls, and inspired her to study evolutionary biology. She was accepted into a Ph.D. program at Harvard University, which had rejected her undergraduate and midcollege transfer applications. “I was so proud to be able to tell my parents I got into Harvard because then they relaxed—they knew they had done their part,” she says.

At Harvard, she worked with evolutionary biologist Jonathan Losos, whose research on Caribbean anoles has become a classic example of how evolution can follow a predictable path. For decades Losos and his students have studied lizards introduced to new islands, finding that when faced with similar challenges, these newcomers often adapt by evolving similar characteristics.

Muñoz added a twist to this story with field research on anoles in the Dominican Republic, which boasts some of the region’s highest peaks. Tropical lizards there can thrive at 3000 meters’ elevation, where it can be bitter cold. Most researchers had assumed that when a tropical lizard expands to the top of a mountain, its body would change over generations to tolerate the cold. But after comparing different species, Muñoz found little evidence of physiological differences that would confer cold tolerance. Instead, whereas sea-level anoles seek shelter from Sun in moist vegetation, the high-altitude lizards stayed warm by spending their days perched on boulders. They were “behaviorally nimble, exploiting Sun and shade to their advantage to stay optimally warm,” Muñoz explains.

The mountain lizards’ shift in behavior sped up morphological change, Muñoz found. Compared with their peers at low elevations, they had quickly evolved shorter hindlegs and flatter skulls that enabled them to hide from predators in narrow crevices in the rocks where they bask, she and her colleagues reported in 2017. The work showed a single behavior could slow one aspect of evolution, such as physiological changes in heat tolerance, and speed up another, such as the changes in anatomy she’d observed. “Far from being passive vessels at the mercy of their circumstances, organisms can influence evolution directly,” she says.

That idea wasn’t new, but prior to Muñoz few researchers had gone looking for empirical evidence. The influence of behavior on evolution “is an underemphasized problem that has not received nearly enough attention,” says Harry Greene, an emeritus evolutionary biologist at the University of Texas, Austin. With her data, “Muñoz is causing us older folks to think harder.”

One student holds open a small Ziploc baggie filled with leaf litter, while another student pours water from a plastic bottle into the baggie. It's nighttime and both students are wearing headlamps.
Closeup: a student's right hand holds a handheld Garmin GPS device, and her left holds a smartphone. The smartphone screen displays a spreadsheet with about 15 rows of data, with a cell in the final row selected.
Students add water to a plastic bag containing leaf litter to keep a captured salamander moist and add its GPS coordinates and environmental data to a spreadsheet on a cellphone.Mike Belleme

After finishing her Ph.D., Muñoz did a postdoc at Duke University, where she explored another underappreciated influence on evolution: biomechanics. Duke integrative biologist Sheila Patek had been figuring out how predatory mantis shrimp evolved such fast, powerful forelimbs for crushing the shells of the snails they eat and snagging prey swimming by, and what influenced their evolutionary trajectories. These invertebrates use what’s called a four-bar linkage, in which components of the forelimb act (mechanically speaking) as four “bars” connected end to end via movable joints to form a closed loop that can resemble a parallelogram. This arrangement abounds in nature and in human-engineered devices, such as locking pliers. Many researchers had assumed each bar had a similar influence on the forces produced and would be equally likely to evolve.

But that’s not what Patek and Muñoz found. By comparing bar lengths in 36 species with known relationships on the mantis shrimp family tree, they showed the shortest bar often changed as a new species evolved. That bias most likely arose because the shortest bar has the most dramatic effect on mechanical output, amplifying force more than any of the other three when it got shorter.

Patek and Muñoz made a similar discovery in certain fish with four-bar linkages in their jaws. This arrangement enables wrasses, cichlids, and sunfish to snap open their mouths extra wide and suck in prey, and the proportions of the bars in these fish vary depending on whether their prey is fast moving or stationary. Fish that chase faster prey have shorter short bars that generate more force and enable them to snap prey faster, the researchers reported in 2018. Much like behavior, biomechanical principles can sculpt the rate, pattern, and direction of evolution, Muñoz says.

In 2020, Muñoz won the Society of Integrative and Comparative Biology’s award for achievements in biomechanics. The following year she won the society’s comparative physiology award, becoming the first researcher to win both. “She is able to integrate diverse concepts in novel and interesting ways, says Raymond Huey, an emeritus ecologist at the University of Washington, Seattle. “Most people focus on ‘A’ or ‘B,’ a few can add A plus B, but Martha can multiply them.”

In 2019, Muñoz landed her current job at Yale, where ecology and evolutionary biology department chair Thomas Near has been working to recruit faculty from underrepresented groups and provide a welcoming environment. In his interview with Muñoz, Near acknowledged the challenges she’d face if she took the job. “He understood that I would have to battle the diversity dimension as well as the academic dimension,” she says.

These were challenges she knew well, having previously experienced the “imposter syndrome” common among scientists from underrepresented groups, who feel (however unjustly) that they don’t deserve to be where they are. She’d endured slights and insults as well, such as being told she’d have to work hard even though she was a diversity hire. The reality, Muñoz says, is that scientists from underrepresented groups feel tremendous pressure to work even harder than their peers. “We know that we have undue visibility due to our sparse numbers and correspondingly, we have a responsibility to be the best role models possible.”

At Yale, Muñoz signed up to be a resident fellow in one of the colleges, where undergraduates are housed, so she and Vigo, her German shepherd, would be embedded in the community. Seven months after arriving in New Haven, Connecticut, COVID-19 grounded her—and gave her time to write a proposal for the grant that now supports the salamander work.

At right, a student holds up a Ziploc baggie filled with leaf litter, while another caps a plastic bottle, both looking closely at the baggie. At left, a third student holds a smartphone in one hand and a handheld GPS in the other. It's nighttime and all three students wear headlamps.
Emmy James (center) and Jesús Buenrostro assemble a specimen bag for a snagged salamander as Jessica Coutee (left) records measurements on her phone.Mike Belleme

The dozens of woodland-dwelling Plethodon species in the southern Appalachians posed irresistible evolutionary questions. These salamanders look so much alike, and the environment they live in seems so uniform, that researchers have considered them an example of “nonadaptive” radiation, in which organisms split into multiple species through the accumulation of random mutations and the slow march of geographic isolation, not because they have evolved different traits. Based on her work on lizards, Muñoz suspected there might be more to that story. Perhaps these salamanders have evolved behavioral or physiological differences that make each species distinctive, or perhaps their environment isn’t as uniform as it appears, creating subtle selective pressure to diversify.

Like about two-thirds of the 700 or so species of salamanders, Plethodon species lack lungs, breathing instead through their skin. Lungless salamanders have limited oxygen to fuel their activities and must make sure their skin stays moist enough to absorb as much oxygen from the air as possible. They’ve adapted by hiding and resting during the day, and by having a simplified nervous system to reduce their energy needs. As the evening cools down, they emerge from burrows, leaf litter, or rock crevices to sit, wait, and nab any insects or other prey that wander by. Most salamanders spend their lives within just a few square meters.

In the past few years Muñoz and her colleagues have collected thousands of observations of these animals, carefully recording the temperature and humidity at the exact spot where each salamander was spotted and at many other spots nearby. Already, they have documented diverse “microhabitats” in their study area—at the base of trees, under rhododendron leaves, on rocky ledges, and elsewhere—each with a specific range of temperature and humidity.

In a 2020 study of 26 species led by her postdoc Vincent Farallo, now at the University of Scranton, Muñoz and colleagues found that each prefers a slightly different combination of temperature and humidity. By choosing certain spots, each species is hydro- and thermoregulating, Muñoz says. Overall, the species mostly fall into two groups. One chooses warm, wet surroundings, where the moisture helps their skin absorb oxygen. “If their environment is wet, then they can capitalize on warmer temperatures,” which allows them to be more active, Muñoz explains. A second group can tolerate drier environments—but must opt for shade or other cooler places to keep from dying out.

A gray-cheeked salamander. It is small, only a few inches long, with a gray underside and black back.

Comfort zone

Habitat details for each animal could hint at how lungless salamanders have evolved.

Air temp. (°C) 23.1
Wind speed (km) 0
Dew point (°C) 17.7
Humidity (%) 72.2
Surface temp. (°C) 16.2
Soil temp. (°C) 18
Behavior Sit
Substrate Dirt
Mike Belleme

Muñoz hosts hundreds of salamanders from dozens of species in her lab, where she and colleagues are measuring metabolic rates, water loss rates, preferred temperatures, heat tolerance, cold tolerance, and other traits. They hope to learn whether the animals’ preferences for specific spots, combined with physiological adaptations, may be contributing to the formation of new species.

So far they’ve found that resistance to water loss varies considerably among species, suggesting this physiological trait is evolving rapidly. Species that are less tolerant of water loss prefer wetter environments in the wild, whereas species that are more resistant to desiccation can use drier environments. If salamanders have chosen different microhabitats to suit their different moisture requirements, some populations could be becoming isolated from others, potentially setting the stage for them to become a new species.

After working in the lab all summer, Muñoz’s students are eager to see the salamanders in their native habitat. The first night out is challenging, as the species they’re seeking proves elusive. But by the second night the students know the routine better, and they’ve set their sights on a different species that proves to be more plentiful. Anderson, with the aid of the new walking stick, catches a few to help the group meet its goal. And Buenrostro, who as a youth worked alongside his mom packing fruit, shows no fear as he digs into the dirt. They finish up before midnight, far earlier than expected. “You guys are awesome,” Muñoz says. “In one day, you figured it all out.”

Such encouragement is quintessential Muñoz, says Jessica Coutee, one of the students on the trip. Coutee, an Army veteran, admits she wasn’t sure what to make of Muñoz when they first met. Muñoz was wearing an elegant red dress as she led a group of veterans on a tour of Yale’s natural history museum. But she didn’t hesitate to don a pair of long yellow gloves and plunge her hands into a tub of chemicals to pull out a preserved giant iguana to show the group. “When you look at her, you might think she’s a girly girl, but she’s not,” Coutee says. Coutee, who calls herself Louisiana Creole as she’s a mix of Black, French, and Native American, is part of the first generation in her family to go to college. She, too, has wrestled with imposter syndrome, but not in Muñoz’s lab. “I feel I belong,” she says. “It’s an unbelievable feeling that I just don’t want to let go of.”

Providing a nurturing community for students of all backgrounds is Muñoz’s goal. “The first step into science is the hardest, so I try to make it as easy as possible,” she explains. Meanwhile, she’s still trying to figure some things out for herself. She is thinking about starting a family, but she has yet to receive tenure and still feels pressure to be perfect. “It feels as if I’m barely above water.”

Those closest to Muñoz say she works too hard, and she doesn’t deny it. But she says her work keeps her optimistic. “What nature is teaching us is that—like the lizards and salamanders I study—we are not passive vessels at the whim and mercy of our environments,” she says. “While we cannot extract ourselves from existing in a certain environmental context, I see hope and possibility in our future.”

Source link

Leave a Reply

Your email address will not be published.