Enrico L. Rezende

Tolerance landscapes in thermal ecology

Summary 1. How thermal tolerance estimated in the laboratory can be extrapolated to natural settings remains a contentious subject. Here, we argue that the general premise that a single temperature can accurately describe upper or lower tolerance limits is incorrect. 2. Survival probability is determined by both the intensity and the duration of a thermal stress, and the association between these variables can be adequately conveyed by a thermal tolerance landscape. Employing this framework, we demonstrate that the temperature range that an organism can tolerate is expected to narrow down with the duration of the thermal challenge. 3. Analyses suggest that a trade-off exists between tolerances to acute and chronic exposition to thermal stress, and that changes in temperature means or extremes may result in drastically different selective pressures and subsequent evolutionary responses. 4. After controlling for the duration of the thermal challenge, we also uncover latitudinal effects on upper lethal temperatures in insects that remained unnoticed in previous broad-scale comparative analyses. 5. Ultimately, critical thermal limits have been adopted in the ecological literature for logistic reasons and are inadequate descriptors of thermal tolerance on conceptual grounds. We consider that tolerance landscapes provide a more suitable framework to study temperature tolerance and its potential impact in ecological settings.

Evolution and plasticity of anuran larval development in response to desiccation. A comparative analysis

Anurans breed in a variety of aquatic habitats with contrasting levels of desiccation risk, which may result in selection for faster development during larval stages. Previous studies suggest that species in ephemeral ponds reduce their developmental times to minimize desiccation risks, although it is not clear how variation in desiccation risk affects developmental strategies in different species. Employing a comparative phylogenetic approach including data from published and unpublished studies encompassing 62 observations across 30 species, we tested if species breeding in ephemeral ponds (High risk) develop faster than those from permanent ponds (Low risk) and/or show increased developmental plasticity in response to drying conditions. Our analyses support shorter developmental times in High risk, primarily by decreasing body mass at metamorphosis. Plasticity in developmental times was small and did not differ between groups. However, accelerated development in High risk species generally resulted in reduced sizes at metamorphosis, while some Low risk species were able compensate this effect by increasing mean growth rates. Taken together, our results suggest that plastic responses in species breeding in ephemeral ponds are constrained by a general trade-off between development and growth rates.

Hsp70 protein levels and thermotolerance in Drosophila subobscura: A reassessment of the thermal co-adaptation hypothesis

Theory predicts that geographic variation in traits and genes associated with climatic adaptation may be initially driven by the correlated evolution of thermal preference and thermal sensitivity. This assumes that an organism’s preferred body temperature corresponds with the thermal optimum in which performance is maximized; hence, shifts in thermal preferences affect the subsequent evolution of thermal‐related traits. Drosophila subobscura evolved worldwide latitudinal clines in several traits including chromosome inversion frequencies, with some polymorphic inversions being apparently associated with thermal preference and thermal tolerance. Here we show that flies carrying the warm‐climate chromosome arrangement O3+4 have higher basal protein levels of Hsp70 than their cold‐climate Ost counterparts, but this difference disappears after heat hardening. O3+4 carriers are also more heat tolerant, although it is difficult to conclude from our results that this is causally linked to their higher basal levels of Hsp70. The observed patterns are consistent with the thermal co‐adaptation hypothesis and suggest that the interplay between behaviour and physiology underlies latitudinal and seasonal shifts in inversion frequencies.

Thermal tolerance and climate warming sensitivity in tropical snails

Abstract Tropical ectotherms are predicted to be especially vulnerable to climate change because their thermal tolerance limits generally lie close to current maximum air temperatures. This prediction derives primarily from studies on insects and lizards and remains untested for other taxa with contrasting ecologies. We studied the HCT (heat coma temperatures) and ULT (upper lethal temperatures) of 40 species of tropical eulittoral snails (Littorinidae and Neritidae) inhabiting exposed rocky shores and shaded mangrove forests in Oceania, Africa, Asia and North America. We also estimated extremes in animal body temperature at each site using a simple heat budget model and historical (20 years) air temperature and solar radiation data. Phylogenetic analyses suggest that HCT and ULT exhibit limited adaptive variation across habitats (mangroves vs. rocky shores) or geographic locations despite their contrasting thermal regimes. Instead, the elevated heat tolerance of these species (HCT = 44.5 ± 1.8°C and ULT = 52.1 ± 2.2°C) seems to reflect the extreme temperature variability of intertidal systems. Sensitivity to climate warming, which was quantified as the difference between HCT or ULT and maximum body temperature, differed greatly between snails from sunny (rocky shore; Thermal Safety Margin, TSM = −14.8 ± 3.3°C and −6.2 ± 4.4°C for HCT and ULT, respectively) and shaded (mangrove) habitats (TSM = 5.1 ± 3.6°C and 12.5 ± 3.6°C). Negative TSMs in rocky shore animals suggest that mortality is likely ameliorated during extreme climatic events by behavioral thermoregulation. Given the low variability in heat tolerance across species, habitat and geographic location account for most of the variation in TSM and may adequately predict the vulnerability to climate change. These findings caution against generalizations on the impact of global warming across ectothermic taxa and highlight how the consideration of nonmodel animals, ecological transitions, and behavioral responses may alter predictions of studies that ignore these biological details.

Contrasting patterns of phenotypic variation linked to chromosomal inversions in native and colonizing populations of Drosophila subobscura

In fewer than two decades after invading the Americas, the fly Drosophila subobscura evolved latitudinal clines for chromosomal inversion frequencies and wing size that are parallel to the long‐standing ones in native Palearctic populations. By sharp contrast, wing shape clines also evolved in the New World, but the relationship with latitude was opposite to that in the Old World. Previous work has suggested that wing trait differences among individuals are partially due to the association between chromosomal inversions and particular alleles which influence the trait under consideration. Furthermore, it is well documented that a few number of effective individuals founded the New World populations, which might have modified the biometrical effect of inversions on quantitative traits. Here we evaluate the relative contribution of chromosomal inversion clines in shaping the parallel clines in wing size and contrasting clines in wing shape in native and colonizing populations of the species. Our results reveal that inversion‐size and inversion‐shape associations in native and colonizing (South America) populations are generally different, probably due to the bottleneck effect. Contingent, unpredictable evolution was suggested as an explanation for the different details involved in the otherwise parallel wing size clines between Old and New World populations of D. subobscura. We challenge this assertion and conclude that contrasting wing shape clines came out as a correlated response of inversion clines that might have been predicted considering the genetic background of colonizers.

Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits?

The potential of populations to evolve in response to ongoing climate change is partly conditioned by the presence of heritable genetic variation in relevant physiological traits. Recent research suggests that Drosophila melanogaster exhibits negligible heritability, hence little evolutionary potential in heat tolerance when measured under slow heating rates that presumably mimic conditions in nature. Here, we study the effects of directional selection for increased heat tolerance using Drosophila as a model system. We combine a physiological model to simulate thermal tolerance assays with multilocus models for quantitative traits. Our simulations show that, whereas the evolutionary response of the genetically determined upper thermal limit (CTmax) is independent of methodological context, the response in knockdown temperatures varies with measurement protocol and is substantially (up to 50%) lower than for CTmax. Realized heritabilities of knockdown temperature may grossly underestimate the true heritability of CTmax. For instance, assuming that the true heritability of CTmax in the base population is h2 = 0.25, realized heritabilities of knockdown temperature are around 0.08–0.16 depending on heating rate. These effects are higher in slow heating assays, suggesting that flawed methodology might explain the apparently limited evolutionary potential of cosmopolitan D. melanogaster.