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Meet Lizard Man, a reptile-loving biologist tackling some of the biggest questions in evolution - Science Magazine

DAY’S EDGE PRODUCTIONS

The morning of 17 October 1996 started as usual for Jonathan Losos. The evolutionary biologist donned a broad hat and slathered on sunscreen, then headed by boat to several unnamed islets off Great Exuma Island in the Bahamas. Three years earlier, he and ecologist David Spiller had introduced local lizard species there to learn how they would compete in a once lizardless place. The pair spent the day snaring lizards, noting their exact locations, and taking stock of the insects, spiders, and vegetation. They were worried about reports of an impending hurricane, but the locals seemed confident it would veer off and spare the islands, as usual.

Not this time, however. The next day, Losos and Spiller helped their hotel owner board up the windows of their beachfront cottage on Great Exuma as Hurricane Lili bore down on the island. As the wind picked up and the first squalls dumped rain, they scurried to a cinder block building up a hill. That night, the wind blew off parts of the roof and felled palm trees. A 4-meter storm surge flooded the streets, and 2 days later they found their rented motorboat stuck in a tree.

The lizards had it even worse. When Losos and Spiller finally made it back out to their most exposed study sites, the islands were stripped nearly bare of brush and all the lizards were gone. But the setback for Losos’s project was the start of a new chapter in his research on how the animals adapt to the varied, changeable environments on islands in and around the Caribbean.

Since Lili, a half-dozen other hurricanes have inundated islets and swept away animals relocated there by Losos, who is based at Washington University in St. Louis (WashU), and his team. But he and his colleagues have persevered, collecting data on how the animals adapt to predators, storm damage, and other challenges—natural and those contrived by the researchers. A lifelong reptile enthusiast, Losos is driven in part by his passion for a group of lizards called anoles, which thrive in South and Central America and throughout the Caribbean.

He also views them as an opportunity. Almost half of the 400 anole species live on islands, and their diverse lifestyles, habitats, and histories have proved to be a vehicle for exploring some of evolution’s biggest questions. “Jonathan’s islands are like giant test tubes, and he is the ultimate tinkerer,” says Martha Muñoz, an evolutionary biologist at Yale University.

Called the Pinocchio anole (Anolis proboscis), this South American lizard is one of Jonathan Losos’s favorites and was once thought to be extinct.

LUCAS BUSTAMANTE

Losos’s research on anoles has shown that evolution can happen faster than most scientists had assumed, and that—contrary to what some leading thinkers have proposed—it is often predictable. Faced with similar challenges, separate populations often evolve similar solutions. Along the way, Losos has mentored dozens of young scientists, and some are now carrying his work in new directions. “Beyond his many contributions to the field, Jonathan has also changed the course of science simply by being who he is,” Muñoz, a former student, says. “He is proof that success is richer and more rewarding when accompanied by kindness and humility.”

Oddly enough, the 1950s TV show Leave it to Beaver started Losos down this path. When 7-year-old Beaver brought home a pet alligator, young Losos asked his parents whether he, too, could get one. His mom was against it, but his father said he would ask a family friend, the deputy director of the St. Louis Zoo, for advice. A successful businessman, the senior Losos also loved animals, taking his family on nature vacations, joining the zoo’s board, and even financing the zoo’s acquisition of a baby elephant from Thailand, which he named Carolyn in honor of his wife.

To everyone’s surprise, the director heartily approved, saying that having an alligator as a childhood pet was how he got his start in herpetology. So the junior Losos acquired several baby caimans, which lived in a baby pool in the basement in winter and in a horse trough in the yard the rest of the year. Only a few times did the animals escape and terrorize the neighbors. Losos worked summers at the zoo until partway through college, eventually donating his caimans to a zookeeper. “Jonathan started off as a little kid loving nature, endlessly pestering staff at his local zoo, catching lizards on family vacations, and he’s never lost that spark,” says Harry Greene, herpetologist emeritus at Cornell University and Losos’s graduate school adviser.

At 12, Jonathan Losos caught a green anole, one of the species that would become his life’s work.

COURTESY OF JONATHAN LOSOS

As an undergraduate at Harvard University, Losos fell under the tutelage of herpetologist Ernest Williams. Sometimes referred to as the father of anole biology, Williams had recognized that anoles on different Caribbean islands evolved independently. Yet on each island he’d found a similar set of body types or “ecomorphs”—one specialized for living in the brush, another for gripping twigs, and still others for life high in the trees. These parallels suggested that where circumstances were similar, evolution would converge on the same set of traits and form communities with similar sets of species.

Williams’s lab had already produced several leading evolutionary biologists, and Losos figured the field of anole research was getting too crowded. But no other species both captured his interest and was easy to study. “I went through a dozen failed Ph.D. projects,” he recalls. At a low point, he seriously considered law school, but his dad convinced him that the world needed herpetologists more than lawyers.

Losos eventually realized that anoles were perfect for applying new tools in evolutionary biology. Researchers were just beginning to build family trees and trace evolution based on protein variations among species. For his Ph.D., Losos compared proteins in Caribbean anoles and verified that Williams’s ecomorphs had indeed evolved independently to form similar communities on different islands. That insight alone—support for an idea called convergent evolution—“was a really important breakthrough,” says Frank Burbrink, a herpetologist at the American Museum of Natural History.

Meanwhile, other researchers were calling for more rigor in evolution studies by requiring evidence that supposedly adaptive traits really give an organism an advantage. So Losos began to study different anole ecomorphs, with legs and toepads of varying sizes (see graphic, below). In the lab, he ran them down miniature racetracks and assessed how well they clung to smooth, vertical surfaces. He found that lizards living near the ground, close to predators, had longer legs that made them fast, whereas those living higher in brush and trees had bigger toepads to stick to leaves and smooth bark. By combining these data with his family tree studies, he got a clearer sense of the lizards’ evolutionary history. He “was really one of the first people to move the field into doing evolution by integrating ecology and morphology and getting the bigger picture,” Burbrink says.

Evolution’s stamp on island-dwelling lizards

On islands in and around the Caribbean, 173 species of anole lizards face an array of different environments, predators, and competitors, along with periodic storms. The result is a laboratory of evolution, where scientists have been able to track the speed and course of adaptation.

Similar solutions As anoles arrived on different islands, their choice of habitat—from the ground to the tree canopy—shaped the course of their evolution. Lizards living in similar habitats on different islands independently evolved similar appearance and behavior, in what scientists call convergent evolution. Limb length Running lizards on racetracks and mesh-covered rods demonstrated that the longer limbs of ground dwellers help them outrun predators. Shorter limbs provide greater stability for traversing tiny twigs and work best for lizards living high in the vegetation. Toepads Toepads are the enlarged ends of the digits on a lizard’s foot. Species living high in the forest or where hurricanes are common have evolved larger toepads to help them hang on. Some anoles can climb vertically and even hang upside down. Dewlap color The dewlap, a flap of skin under the chin of male anoles, unfolds to attract mates and warn rivals. Lizards living in shade have lighter ones for heightened contrast, whereas those that hang out in sunny spots have darker ones. 2 3 4 0 200 km Atlantic Ocean CUBA BAHAMAS JAMAICA HISPANIOLA PUERTO RICO Dewlap brightness Habitat brightness 1 Canopy 2 Twig 3 Grass/bush 4 Ground/trunk 1 Toepad

V. ALTOUNIAN/SCIENCE

Inspired by experiments in which researchers monitored evolutionary changes in guppies in Trinidad after relocating them to different streams, Losos began to wonder whether similar studies could be done in Caribbean anoles. And he realized that Thomas Schoener, one of Williams’s protégés, had already laid the groundwork. In the 1980s, Thomas and Amy Schoener (they were once married) introduced local lizards to tiny lizardless islands in the Bahamas to investigate how different vegetation affected the reptiles’ ability to thrive.

A decade later, Losos teamed up with Thomas Schoener, by then a renowned ecologist at the University of California (UC), Davis, to revisit those sites. Consistent with Williams’s and Losos’s earlier findings, lizards living in scrubby vegetation had shorter legs and larger toepads than their ancestors, which had lived in tall, broad trees. These adaptations enabled them to cling to tiny twigs as they chased down insects to eat, and the changes had taken just a few generations. “Evolution can happen very quickly when natural selection is very strong,” Losos says.

The idea is now well-accepted, but at the time it went against the entrenched belief that evolution was a slow process. “This is one of the few things that [Charles] Darwin got wrong,” Losos says. He decided to make anoles his life’s work.

He soon had to reckon with hurricanes. Losos and Spiller, now retired from UC Davis, had chosen the islets off Great Exuma to study the effects of competition. On some, they introduced two local species, the green and brown anoles, and on others, just a single species. In the first 3 years, they noticed that on islands with both kinds, the brown lizards were driving the green anoles higher into the bushes, where they were struggling. That’s when Lili hit, ruining the experiment before they could see whether the green anoles would go extinct.

“It would have been so easy, I’m sure, to pack it all in and give up,” says Luke Harmon, one of Losos’s former students and now an evolutionary biologist at the University of Idaho. Instead, Losos and Spiller used the disaster to their advantage. They documented Lili’s great, but also patchy, impact. Islands southwest of Great Exuma felt the brunt of the storm surge and were devoid of lizards and vegetation. Life there would have to start over. On islands to the north, the wind and rain snapped twigs and ripped off leaves but a few lizards remained, they reported in the first of several papers about hurricanes.

The work challenged a widespread assumption that extreme events such as hurricanes do not drive evolution because they are rare and have random, unpredictable impacts on plants and animals. The Losos group discovered instead that storms can be agents of natural selection.

Jonathan Losos (front right), with a Harvard University herpetology class in Costa Rica, has made a name as a mentor as well as a researcher.

COURTESY OF JONATHAN LOSOS

For example, in 2017 Losos’s postdoc Colin Donihue; functional morphologist Anthony Herrel, now with the French national research agency CNRS at the National Museum of Natural History; and colleagues visited two cays in the Turks and Caicos to measure the body proportions of the anoles living there. Four days after they left, two almost back-to-back hurricanes hit the area with winds of more than 200 kilometers per hour. When the team returned a few weeks later and remeasured the lizards, they found that the survivors tended to have bigger toepads, longer forelimbs, and shorter hindlimbs.

Back in the lab, the researchers tested how these traits affect the lizards’ ability to hold onto a perch. In a strong wind, anoles hang on with their forelimbs, but they lose their grip with the hind legs. Cranking up an air-blower, the researchers found that those with longer hind legs (and more surface area for the wind to catch) got blown off their perches onto a padded surface more readily. Conversely, animals with shorter hind limbs and bigger toepads hung on. The hurricanes had apparently selected for those traits, the team reported in 2018. The following year, they found that offspring of the survivors also had big toepads, suggesting the adaptation was genetic and not just a reaction to holding on tight.

The team has since measured toepad size in 188 lizard species across the Caribbean. The more hurricanes an island has experienced, the bigger the toepads of the lizards living there, they reported on 27 April in the Proceedings of the National Academy of Sciences. Hurricanes seem to have had a long-term evolutionary effect.

Losos had been a professor at WashU for 13 years when Harvard came calling in 2005, seeking to recruit him to its evolutionary biology department. A St. Louis native and a hardcore St. Louis Cardinals baseball fan, he hesitated. He even did a yearlong sabbatical at Harvard before finally accepting, in large part because the position included a curatorship at the Harvard Museum of Comparative Zoology. “That was the one thing St. Louis didn’t have,” he recalls.

There, he continued to build on a reputation for being a kind, enthusiastic mentor. “I have seen him give high school students the same attention and respect that he gives his closest colleagues,” says Melissa Kemp, a former postdoc now at the University of Texas, Austin. “He seems to always be focused on his work, but he also has a whimsical sense of fun at the same time,” says Michele Johnson, a former student and an evolutionary biologist at Trinity University. Losos sports a watch with an anole he photographed as its face and is not above lecturing undergraduates while dressed as a platypus—one of his favorite animals since childhood.

Those traits and a firm belief that “there is no one-size-fits-all in terms of how to interact with and mentor students” have helped Losos launch the careers of 59 graduate students and postdocs. They include at least eight Black, Latino, and Native American scholars, in a field that lacks diversity. (Although 3% of U.S. biologists are African American or Black, for example, only 0.3% of evolutionary biologists are.)

Ambika Kamath, now a postdoctoral researcher at UC Berkeley, says Losos backed her completely when her studies challenged the long-held idea that male lizards hold territories to corral their mates. She argued instead that females move around and play a role in mate choice. “It would have been much harder for me to do that work without his excitement,” she recalls. Losos worked hard with her to get the paper just right and was eager to be a co-author. “Otherwise it would have just been the work of this young brown woman who could have easily been dismissed as an angry feminist.”

Kamath and other students praise Losos for pushing them intellectually without undermining their confidence. Harmon jokes that Losos would never dismiss an idea from his students, no matter how wacky. Instead, he would just pause and say “interesting.” “Eventually I figured out that maybe I should think things through a bit more, if Jonathan thought they were ‘interesting,’” Harmon says.

Losos and his team keep testing their ideas about ecology and evolution on Caribbean islands. In one recent project, Robert Pringle, now at Princeton University, and Losos tested a key principle in ecology—that introducing a top predator tends to increase biodiversity. The researchers added a predatory ground-dwelling lizard to islands with brown and green anoles. To escape this new threat, the brown anoles began to hang out higher in the foliage, displacing the green anoles that normally lived there and driving them toward extinction. Contrary to conventional wisdom, the predator appeared to be pushing the islands toward lower biodiversity, they reported on 5 June in Nature.

In video frames from a lab simulation of a hurricane, the wind first dislodges a lizard’s hind legs, then blows them outward, until the animal loses its grip completely.

Colin Donihue

Another recent study, led by one of Losos’s former postdocs, examined the impacts of an invasive anole species on Dominica. Until 20 years ago, the island was home to a single anole species. Then a lumber shipment introduced a second species that is gradually spreading. To study how the native and invader species interact, behavioral ecologist Claire Dufour, now at the University of Montpellier, used robotic lizards as stand-ins for the invader. The robots did pushups and extended a flap of fake skin under the chin, mimicking the aggressive displays of real lizards. In response, native lizards familiar with the invaders postured more aggressively, suggesting the invaders are forcing the natives to expend more energy defending their territory, the group reported on 27 March in the Journal of Animal Ecology. “Our biggest conclusion is that the species do compete and have negative consequences on each other,” Losos says.

Even as his group continues to churn out papers, Losos is assessing what he has learned so far. In his book Improbable Destinies: Fate, Chance, and the Future of Evolution, published in 2017, he challenged a major contention of one of the field’s great thinkers, Stephen Jay Gould, the Harvard paleontologist who argued that chance plays such a big role in determining nature’s course that evolution would never take the same path twice. Anoles offer evidence to the contrary, Losos wrote: In similar habitats, they have repeatedly evolved similar body shapes, sizes, and behavior. The book was written for the general public, but it made an impression even on his peers. “I’ve been studying evolution for 30-plus years, and this book made me rethink some things I thought I knew about biology and evolution,” says Christopher Austin, an evolutionary biologist and herpetology curator at the Louisiana State University Museum of Natural Science.

Losos left Harvard in 2018, lured by a new job at WashU and the prospect of returning to his hometown, his cats, and his wife, who has a successful real estate career and did not follow him to Massachusetts. He now heads the Living Earth Collaborative, a biodiversity research initiative that unites experts at the Missouri Botanical Garden, the St. Louis Zoo, and WashU. He is working on a book about evolution in the house cat, another of his favorite species.

And he is still dodging hurricanes. Losos and colleagues have been trying to assess the long-term evolutionary impacts of predatory lizards they’ve introduced to some islands in the Bahamas. “I don’t know if we will ever get there,” he says. Every few years a hurricane comes through and blows the evolving lizards away.

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