The green anole lizard, a spectacularly bright reptile found throughout the American south, has difficulty handling temperatures below around 50 degrees Fahrenheit. This doesn’t usually pose a problem in its subtropical habitats along the Gulf Coast and in southeastern states. But during the extreme winter of 2013-2014 (resulting from a southward shift in the polar vortex), the lizard endured temperatures so low that it faced selection pressures and evolved a greater tolerance to cold, according to a study published this week in Science by Shane Campbell-Staton, Ph.D. ’15, and coauthors Jonathan Losos, professor of organismic and evolutionary biology, and Scott Edwards, Agassiz professor of organismic and evolutionary biology.
Relatively few studies have looked at the natural-selection effects of individual extreme weather events, Campbell-Staton explains, given the difficulty of anticipating those events. The concept for the just-published study emerged by chance in 2013, when he was doing dissertation research on a related topic: the evolution of cold tolerance in green anoles. Several million years ago, ancestors of that species migrated from present-day Cuba to the United States; today, their descendants live in regions as (relatively) cold as Tennessee and Oklahoma. Campbell-Staton was trying to understand “what physiological and genetic processes allowed lizards farther north to survive the harsher winter climates.”
Soon after returning from what he thought would be his last collection trip, he came across a photo in the Boston Globe of a green anole in Alabama, lying dead in the snow during the 2014 cold snap. “I immediately went back to Scott and Jonathan with the idea of trying to measure natural selection in response to the event,” he says. Because he already had data from the previous summer on the anoles, he could compare those findings to a new sample of lizards that had survived the winter.
The study compares data collected, before and after the winter, at four sites in Texas—Brownsville, Victoria, Austin, and Arlington—and a fifth in Hodgen, Oklahoma; taken together, they cover a latitudinal distance of almost 800 miles. Each city experienced substantially lower minimum temperatures that winter than during the previous 15 years. The team (which also included Zachary Cheviron, Nicolas Rochette, and Julian Catchen) focused on these sites, Campbell-Staton explains, because their green anole populations are closely related but also display significant variation in cold tolerance—the farther north their habitat, the more resistant they are to frigid conditions. To measure the lizards’ cold tolerance, the team put each specimen in a chamber and gradually lowered the temperature by one degree Celsius per minute. The lizards were placed on their backs and prodded with forceps, to encourage them to right themselves. The temperature at which they could no longer do so, or the critical thermal minimum, explains Campbell-Staton, is used as a proxy for “the temperature at which an animal would not be able to escape the conditions that would eventually lead to its death.” (“The animals do recovery fully,” Losos notes in an email.)
That winter, lizards from Brownsville, at the southernmost tip of Texas, experienced by far the most days on which the temperature was lower than their critical thermal minimum. When the team returned to collect samples in April and July 2014, those lizards surviving in Brownsville showed the most significant increase in their cold tolerance of anoles in any of the five cities: their critical thermal minimum after the winter was lower by about 1.5 degrees Celsius, or 2.7 degrees Fahrenheit. Green anoles from Victoria, about 260 miles to the north, displayed a cold-tolerance increase of 1 degree Celsius, or 1.8 degrees Fahrenheit. Populations from the remaining cities didn’t show such changes, probably because they were already relatively cold-tolerant. The Brownsville and Victoria populations that survived had converged with the other cities’ anoles in their tolerance for cold.
Changes in the reptiles’ cold tolerance were supported not only by their phenotypes—their outwardly observable behavior—but also at the genomic level. The gene-expression and genomic-sequencing profiles of the surviving southern-dwelling lizards diverged after the winter from those of lizards Campbell-Staton had studied during the summer; they more closely resembled those of the northern groups, and showed greater differentiation within their own genomes. The genes that faced selection pressure during the winter, Campbell-Staton says, “all seem to play a role in nervous-system function. We found that survivors of the storm had a high degree of genetic differentiation in a part of the genome that contains genes associated with the transport and breakdown of neurotransmitters.”
Campbell-Staton’s advisers were initially hesitant about approving the study, because it was an apparent departure from his dissertation research. As it turned out, his instinct was not only perceptive, but prescient. If the extreme cold has made some green anole populations more resilient in low temperatures, it almost certainly has also come at a cost. “Lizards that did not survive this cold event may have had genetic variants that would have made them more resilient to a heat wave or a drought—now those lineages may be lost,” Campbell-Staton says. Extreme weather events are likely to become more frequent and severe, and will threaten the viability of species more fragile than the relatively abundant green anole. “We are only beginning to understand how anticipated changes in climate are going to affect biodiversity,” he adds; the present study offers one promising way in.