October 16, 2017 at 8:52 am

Study Provides First Evidence of Natural Selection on Thermal Preference, Climate Change

Anthony Gilbert at the Chiricahua mountains in Arizona.

Anthony Gilbert at the Chiricahua mountains in Arizona.

Biological Sciences graduate student Anthony L. Gilbert and Dr. Donald Miles published an article that provides a critical study for those interested in climate change and the effects of climate change on species and ecosystems across the globe.

They authored “Natural selection on thermal preference, critical thermal maxima and locomotor performance” in the Proceedings of the Royal Society B. Miles is Professor of Biological Sciences at Ohio University.

“Our study details the first ever published evidence of natural selection on thermal preference, where lizards that preferred warmer body temperatures had a survival advantage after the reproductive season,” says Gilbert.

“The body temperature that a lizard prefers is used more often than any other trait in predicting how they will respond to climate change. This is because you can predict if they will be active in their environment defending their territory, or foraging, or trying to find a mate based on the temperature in the environment and the temperature the lizard prefers to be at. If temperatures get too hot due to climate change, then lizards cannot be active doing all of the activities that contribute to their survival or reproduction. However, a lot of paramount studies that have shown how vulnerable lizards are to extinction have not considered that preferred body temperatures could affect survival, and thus be a target of natural selection.”

Natural selection is a mechanism of evolution by which traits that which can be measured on adult or juvenile animals, like how fast they can run, how fast they can grow, or how large they are, influence how well these animals survive and reproduce. If these traits can be passed from parent to offspring, then natural selection becomes a mechanism of evolutionary change.

“Climate change is changing the way animals interact with their environment, and this can change the way traits like their speed, size or behavior are related to survival and reproduction,” Gilbert says. “Traits that used to be very good at helping individuals survive might be maladaptive as the climate warms, so understanding how changing temperatures change the relationship between organismal traits and their survival and reproduction is so important for understanding how or if species are vulnerable to extinction.

Field Research in Arid Desert Grassland in Arizona

The researchers write in their article about how “changes in ambient temperature due to anthropogenic climate change are altering species activity patterns, raising field-active body temperatures, and modifying performance capacities. There are four mechanisms of response to these novel conditions: shift geographical range to track current niches, adapt genetically to accommodate novel thermal niches, adjust physiological or behavioural traits through plasticity, or go extinct. For species with limited dispersal capabilities, the ability to adapt genetically to climate change may be the only mechanism of long-term persistence.”

“Determining the patterns of natural selection operating on thermal physiology is a critical first step to understand the evolutionary responses to rising temperatures,” they write. “Yet, the fitness consequences of among-individual variation in thermal traits, either through survival or reproductive success, have received limited attention.”

For their study, the researchers captured 206 adult lizards at Appleton-Whittell Research Ranch of the National Audubon Society, an arid desert grassland in Arizona. They measured field-active body temperatures as they captured each lizard. They also constructed models using PVC pipe and painted to match the lizards’ spectral reflectivity to sample the habitat’s operative thermal environment. This provides an estimate of what potential body temperatures lizards have available to them as they move around the habitat. Lizards are ectothermic, meaning they maintain their body temperatures entirely from their environment, and is one reason they are so threatened by rising temperatures caused by climate change.

Since lizards must move to avoid predators, capture prey and defend territories, the researchers studied the lizards’ sprint speed relative to body temperature—because their body temperature affects their speed and how well they are able to do things in their environment. They used a one-meter long track and a high-speed digital camera to measure speed and a heated chamber to represent the increase of 4 degrees Centigrade projected for this area by the Intergovernmental Panel on Climate Change.

After the measurements, each lizard was marked with a four-digit toe clip and released. That allowed the researchers to conduct a census seven weeks later through the breeding season.

“We resampled for surviving individuals over such a short timescale for three reasons. First, the period between late May and mid-July in the Sonoran Desert is the hottest and driest period of the year. This is also during the reproductive season when male activity is the highest and females initiate reproduction. Males patrol and defend their territories from rival males during this period. Because the fitness consequences of sustained activity should be greatest during the reproductive season, we predict that the fitness consequences of variation in thermal physiological traits should be most evident when the activity season coincides with the most thermally extreme portion of the year,” the researchers write.

“Second, this period of time marks the production of the first clutch of offspring. Not all females may have the energy reserves to attempt a second clutch, so survival to the first clutch of offspring is a major selective event. Third, the onset of the monsoonal weather pattern characteristic of the arid southwestern USA during early July is a proximate cue for female U. ornatus to initiate oviposition. We estimated viability selection by resampling for surviving individuals for a period of 10 days at the end of July once the monsoons ceased.”

Surviving Lizards Had Warmer Thermal Preference and Faster Speed

To gather their data, the researchers walked daily through the study site to find lizards who survived the deserts’ hot sun and cooling monsoons.

Analyzing their data, the researchers found that the lizards’ body size and condition was not associated with survival, but they did find that surviving lizards had a warmer thermal preference and faster speed than the population mean. “Survivors also had a somewhat broader thermal tolerance range, meaning that they could tolerate both warmer and colder temperatures than the lizards we did not find during the censuses,” Gilbert said.

“Understanding how selection operates across all traits related to the thermal biology of a species is crucial if we are to determine the potential for organisms to adapt to altered thermal niches over a rapid timescale,” they write, noting that for lizards this could include using energy to sprint between shaded and open microhabitats to regulate their body temperature. “Individuals preferring warmer (temperatures) are not relegated to shaded microhabitats as often and as a result can be active in open microhabitats longer to exploit more foraging or reproductive opportunities…. Lizards with greater performance capacities at higher temperatures will have a strong advantage for accommodating altered thermal niches.

“We also provide the first evidence of correlational selection on thermal biological traits,” they write. They discussed thermal specialists and thermal generalists, with generalists having a more difficult time adapting to warmer environments.

“We detected negative correlational selection on the combination of (temperature preference) and (maximum body temperature). Surviving lizards exhibited higher (temperature preferences) and lower (maximum body temperatures) than did non-survivors, which is interesting given a lack of a negative phenotypic correlation between the two traits. Because daily (temperature) often exceeds the (maximum body temperature) threshold, selection should favor those that could tolerate hotter temperatures, but what we might have characterized is selection operating on the degree of thermal specialization,” they write.

“The narrowness of an individual’s thermal performance breadth, or how close (optimal temperature) is to (maximum body temperature) are two estimates of the degree of thermal specialization. Thermal specialists are predicted to have a more difficult time coping with rising temperatures compared with thermal generalists. In theory, thermal specialists benefit in that they can maintain higher performance capacities at a narrower range of body temperatures.

“Surviving lizards had a higher performance capacity in addition to warmer (temperature preferences) and cooler (maximum body temperatures). These individuals are perhaps more specialized with respect to their thermal biology,” they conclude.

“Lastly, we found multiple traits had statistically significant selection differentials (minimum body temperatures and thermal performance) that were not the actual targets of natural selection (statistically weak selection gradients). This highlights that multiple physiological and thermal traits for lizards have some degree of phenotypic integration, and may co-evolve in response to strong selective pressures. The degree of integration and the constraints on the co-evolution of these traits should be determined a priori before predicting how multiple suites of traits will evolve in response to climate change.”

In short, “evolutionary adaptation in altered thermal environments could be more probable than current models forecast,” the researchers conclude.

Abstract: Climate change is resulting in a radical transformation of the thermal quality of habitats across the globe. Whereas species have altered their distributions to cope with changing environments, the evidence for adaptation in response to rising temperatures is limited. However, to determine the potential of adaptation in response to thermal variation, we need estimates of the magnitude and direction of natural selection on traits that are assumed to increase persistence in warmer environments. Most inferences regarding physiological adaptation are based on interspecific analyses, and those of selection on thermal traits are scarce. Here, we estimate natural selection on major thermal traits used to assess the vulnerability of ectothermic organisms to altered thermal niches. We detected significant directional selection favouring lizards with higher thermal preferences and faster sprint performance at their optimal temperature. Our analyses also revealed correlational selection between thermal preference and critical thermal maxima, where individuals that preferred warmer body temperatures with cooler critical thermal maxima were favoured by selection. Recent published estimates of heritability for thermal traits suggest that, in concert with the strong selective pressures we demonstrate here, evolutionary adaptation may promote long-term persistence of ectotherms in altered thermal environments.


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