Urban areas are hot. The urban heat island effect causes urbanized regions to be significantly warmer than nearby forested areas, and the tropical islands of the Caribbean are no exception to this pattern. Just spend a few minutes in the noon heat in San Juan, Puerto Rico, and you will beg for the cool reprieve of a forest breeze, an air-conditioned building, or dip in the ocean. For the non-human animals of cities, the urban heat can push them dangerously close to their thermal limits, and they must either behaviorally adjust to avoid the heat, or physiologically adapt to tolerate higher temperatures.
In our recent paper in Nature Ecology & Evolution, Parallel selection on thermal physiology facilitates repeated adaptation of city lizards to urban heat islands, I collaborated with my friend, Shane Campbell-Staton, to investigate how the Puerto Rican Crested Anole (Anolis cristatellus) is responding to the thermal conditions of urban environments. Shane and I headed to Puerto Rico in 2016 together with a great team of field techs (Inbar Maayan and Jason Fredette) to quantify the thermal habitat and thermal tolerance of lizards from paired urban and forest sites in four municipalities across the island. We combined these field data with data collected on lizards we reared in captivity and lizards de-acclimated over several weeks in the laboratory. In addition, we collected muscle tissue from lizards in each population after exposing them to different thermal treatments in order to examine gene expression patterns. After collecting our field and laboratory data, Shane brought on a crew of genomics researchers (Nicholas Rochette, Rena Schweizer, Julian Catchen) to help investigate the genetic underpinnings of the thermal responses.
Urban lizards tolerate elevated temperatures
We hypothesized that exposure to elevated thermal environments in urban areas would lead to adaptive physiological responses in urban lizards. We first set out to establish that urban lizards do in fact experience different thermal environments than forest lizards using a combination of GIS data (BIOCLIM) and field data. We found that urban habitats were characterized by higher temperatures throughout year, including warmer winters and hotter summers. The microhabitat used by the lizards differed between urban and forest habitats as well. Perches used by lizards in urban areas and environmental temperature at the perch site (operative temperature, an estimate of the lizard body temperature at that location in the absence of thermoregulating behavior) were also warmer. Under these warm conditions, it is unsurprising then that we also found urban lizards experience elevated body temperatures.
We next conducted a series of thermal tolerance trials to determine the maximum temperature (CTmax) the lizards could withstand while maintaining function. These non-lethal experiments help us to understand the physiological limits of the lizards (with test temperatures not exceeding those experienced in the wild). These experiments revealed to us that urban lizards could withstand significantly higher temperatures compared to forest lizards in the same municipality. In some cases urban lizards could handle temperatures greater than 40°C, and on average urban populations tolerated temperatures of 0.8°C higher than nearby forest populations.
A genetic basis of thermal plasticity
Using RNAseq, we analyzed patterns of gene expression and transcriptomic signatures of selection, contrasting urban and forest pairs within each municipality. We found a single peak of genetic divergence in 3 of our 4 urban-forest pairs, corresponding to a genomic region around the RARS locus. This genomic region is associated with resilience under high-stress situations, such as elevated temperatures. We found that the urban lizards had a distinct genotype from the forest lizards across all municipalities: urban lizards tended to be homozygous at a SNP within RARS while forest lizards tended to be heterozygous at this site. When we examined phenotype-genotype correlations, we found that lizards with the homozygous genotype exhibited greater plasticity in their thermal responses and were able to tolerate higher maximum temperatures compared to heterozygotes. This elevated frequency of the homozygous genotype in urban populations and the correlation with thermal performance suggests that natural selection is shaping patterns of thermal tolerance in urban lizards.
But differences in thermal tolerance are likely attributable to more than just this single gene variant. When we looked at transcriptome-wide patterns of gene expression, we also found patterns of regulatory divergence between urban and forest populations in genomic regions associated with thermal performance. Parallel signatures of selection across several of these divergently expressed genes suggest that natural selection is acting on multiple genes and physiological networks in similar ways across urban populations. Interestingly, we also found that the common garden animals from the urban population displayed reduced expression variance compared to forest lizards after heat exposure, suggesting an adaptive refinement of gene expression in urban lineages.
A “hidden superpower”
The high-plasticity genotype that urban lizards possess is likely involved in a heat-hardening response that is environmentally dependent. The lizards with the high-plasticity genotype in urban environments are primed to respond to elevated temperatures appropriately because of the high thermal stress they endure in their habitat. As my co-author, Shane, explains, it is like “a hidden superpower that only presents itself in the right environment”. While tolerating an extra ~1°C might not seem like a superpower, this might mean life or death for a lizard out at noon in an urban environment. This 1°C difference might enable them to use urban habitat for more hours out of the day, or to use hot substrates like metal fences as perches instead of restricting habitat use to vegetation. This spatial and temporal expansion of habitat use translates to more mating opportunities, more time to forage, and more habitat space to occupy.
Check out the full paper here:
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