Can phenology and plasticity prevent adaptive clines in tolerance limits across temperate mountains?

Critical thermal limits (CTmax and CTmin) are predicted to decrease with elevation, with greater change in CTmin, and the risk to suffer heat and cold stress increasing at the gradient ends. A central prediction is that populations will adapt to the prevailing climatic conditions. Yet, reliable support for such expectation is scant because of the complexity of integrating phenotypic and molecular divergence. We propose that phenotypic plasticity and breeding phenology may hinder local adaptation cancelling the appearance of adaptive patterns. We examined intraspecific variation of CTmax/CTmin in 11 populations of an amphibian across an elevational gradient, and assessed (1) the existence of local adaptation through a PST-FST comparison, (2) the acclimation scope in both thermal limits, and (3) the vulnerability to suffer acute heat (CTmax–tmax) and cold (tmin–CTmin) thermal stress, measured at both macro- and microclimatic scales. Our study revealed significant microgeographic variation in CTmax/CTmin, and unexpected elevation gradients in pond temperatures. However, variation in CTmax/CTmin could not be attributed to selection because critical thermal limits were not correlated to elevation or temperatures. Differences in breeding phenology among populations resulted in exposure to higher and more variable temperatures at mid and high elevations. Accordingly, mid- and high-elevation populations had higher CTmax and CTmin plasticities than lowland populations, but not more extreme CTmax/CTmin. Thus, we confirm our prediction that plasticity and phenological shifts may hinder local adaptation, promoting thermal niche conservatism and a higher vulnerability to climate change. This contradicts some of the existing predictions on adaptive thermal clines.

Male fertility thermal limits predict vulnerability to climate warming

Forecasting which species/ecosystems are most vulnerable to climate warming is essential to guide conservation strategies to minimize extinction. Tropical/mid-latitude species are predicted to be most at risk as they live close to their upper critical thermal limits (CTLs). However, these assessments assume that upper CTL estimates, such as CTmax, are accurate predictors of vulnerability and ignore the potential for evolution to ameliorate temperature increases. Here, we use experimental evolution to assess extinction risk and adaptation in tropical and widespread Drosophila species. We find tropical species succumb to extinction before widespread species. Male fertility thermal limits, which are much lower than CTmax, are better predictors of species’ current distributions and extinction in the laboratory. We find little evidence of adaptive responses to warming in any species. These results suggest that species are living closer to their upper thermal limits than currently presumed and evolution/plasticity are unlikely to rescue populations from extinction.

Progeny of Xenopus laevis from altitudinal extremes display adaptive physiological performance

Environmental temperature variation generates adaptive phenotypic differentiation in widespread populations. We used a common garden experiment to determine whether offspring with varying parental origins display adaptive phenotypic variation related to different thermal conditions experienced in parental environments. We compared burst swimming performance and critical thermal limits of African clawed frog (Xenopus laevis) tadpoles bred from adults captured at high (∼ 2000 m above sea level) and low (∼ 5 m above sea level) altitudes. Maternal origin significantly affected swimming performance. Optimal swimming performance temperature had a >9°C difference between tadpoles with low altitude maternal origins (Topt: pure- and cross-bred 35.0°C) and high altitude maternal origins (Topt: pure-bred 25.5°C, cross-bred 25.9°C). Parental origin significantly affected critical thermal limits. Pure-bred tadpoles with low altitude parental origins had higher CTmax (37.8±0.8°C) than pure-bred tadpoles with high altitude parental origins and all cross-bred tadpoles (37.0±0.8 and 37.1±0.8°C). Pure-bred tadpoles with low altitude parental origins and all cross-bred tadpoles had higher CTmin (4.2±0.7 and 4.2±0.7°C) than pure-bred tadpoles with high altitude parental origins (2.5±0.6°C). Our study shows Xenopus laevis tadpoles’ varying thermal physiological traits is the result of adaptive responses to their parental thermal environments. This study is one of few demonstrating potential intraspecific evolution of critical thermal limits in a vertebrate species. Multi-generation common garden experiments and genetic analyses would be required to further tease apart the relative contribution of plastic and genetic effects to the adaptive phenotypic variation observed in these tadpoles.

The evolution of critical thermal limits of life on Earth

Understanding how species’ thermal limits have evolved across the tree of life is central to predicting species’ responses to climate change. Here, using experimentally-derived estimates of thermal tolerance limits for over 2000 terrestrial and aquatic species, we show that most of the variation in thermal tolerance can be attributed to a combination of adaptation to current climatic extremes, and the existence of evolutionary ‘attractors’ that reflect either boundaries or optima in thermal tolerance limits. Our results also reveal deep-time climate legacies in ectotherms, whereby orders that originated in cold paleoclimates have presently lower cold tolerance limits than those with warm thermal ancestry. Conversely, heat tolerance appears unrelated to climate ancestry. Cold tolerance has evolved more quickly than heat tolerance in endotherms and ectotherms. If the past tempo of evolution for upper thermal limits continues, adaptive responses in thermal limits will have limited potential to rescue the large majority of species given the unprecedented rate of contemporary climate change.

A high-throughput method for measuring critical thermal limits of leaves by chlorophyll imaging fluorescence

Plant thermal tolerance is a crucial research area as the climate warms and extreme weather events become more frequent. We developed and tested a high-throughput method for measuring photosynthetic critical thermal limits at low (CTMIN) and high (CTMAX) temperatures to achieve pragmatic and robust measures of thermal tolerance limits using a Maxi-Imaging fluorimeter and a thermoelectric Peltier plate temperature ramping system. Leaves exposed to temperature extremes accumulate damage to photosystem II (PSII). Temperature-dependent changes in basal chlorophyll fluorescence (T-F0) can be used to identify the critical temperature at which PSII is damaged. We examined how experimental conditions: wet vs dry surfaces for leaves and temperature ramp rate, affect CTMIN and CTMAX across four species. CTMAX estimates were not different whether measured on wet or dry surfaces, but leaves were apparently less cold tolerant when on wet surfaces. Temperature ramp rate had a strong effect on both CTMAX and CTMIN that was species-specific. We discuss potential mechanisms for these results and recommend settings for researchers to use when measuring T-F0. The system described and tested here allows high-throughput measurement of critical temperature thresholds of leaf photosynthetic performance for characterising plant function in response to thermal extremes.