“Extreme insolation: climatic variation shapes the evolution of thermal tolerance at multiple scales”

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Kaitlin M. Baudier, Catherine L. D’Amelio, Rumaan Malhotra, Michael P. O’Connor, and Sean O’Donnell (Sep 2018)

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Insolation predicts thermal tolerance from microclimate to elevational clines

When the mean misses the point: An analysis of thermal selection at multiple scales

An army ant of species Eciton mexicanum following a pheromone trail up and over a moss-covered rock in Monteverde.
(Credit: Kaitlin M. Baudier)

Most tests of animal adaptation to local thermal environments use correlations of thermal physiology with local mean temperatures across latitudes or over elevation gradients. Such approaches ignore potentially important sources of ambient temperature variation, introducing confounds and potentially complicating interpretation of the geography of thermal adaptation. Baudier and co-authors in the O’Donnell Lab at Drexel University conducted a study to test whether temperature extremes or temperature means are a bigger factor in the evolution of thermal tolerance limits. This within-latitude comparative study of Costa Rican army ants’ insolation adaptations examined multiple scales of thermal variation: across elevations, in seasonal versus aseasonal forests, and in subterranean versus surface microhabitats.

Photo taken at the start and one week after the onset of the rainy season in a tropical rain shadow. Santa Rosa National Park, Guanacaste, Costa Rica.
(Credit: Kaitlin M. Baudier)

Baudier and co-authors found that thermally-buffered subterranean species had narrower thermal tolerance ranges compared to surface-active species, and also found that the relationship between heat tolerance and elevation differed by species surface activity level: heat tolerance decreased with elevation for subterranean species, but heat tolerance didn’t differ across elevations for above-ground species. The relationship between cold tolerance and elevation did not differ across species microhabitat use. Greater seasonal temperature variation in dry forests caused improved heat tolerance but did not affect cold tolerance. These patterns suggest that upper and lower thermal tolerances respond to different selective pressures in the environment. Heat tolerance likely evolves under selection from extreme warming events more than mean temperature, and cold tolerance in the tropics seems to be more selected for by mean annual temperature. Extreme heat spikes are predicted to become more common because of anthropogenic climate change. These changes may have most dangerous consequences for tropical species adapted to historically stable conditions.


Looking east at sunrise from San Gerardo research station, towards the Atlantic plain fed by more reliable year-round precipitation.
(Credit: Kaitlin M. Baudier)

Abstract

The climatic variability hypothesis (CVH) is a cornerstone of thermal ecology, predicting the evolution of wider organismal thermal tolerance ranges in more thermally variable environments. Thermal tolerance ranges depend on both upper and lower tolerance limits (critical thermal maxima: CTmax, and critical thermal minima: CTmin), which may show different responses to environmental gradients. To delineate the relative effects of mean and extreme temperatures on thermal tolerances, we conducted a within-latitude comparative test of CVH predictions for army ants (Dorylinae) at multiple scales: across elevations, in seasonal versus aseasonal forests, and in subterranean versus surface microhabitats. Consistent with the CVH, thermally-buffered subterranean species had narrower thermal tolerance ranges. Both CTmin and CTmax decreased with elevation for subterranean species. In contrast, aboveground species (those exposed to insolation) showed a decrease in CTmin but no change in CTmax across elevations. Furthermore, greater seasonal temperature variation in dry forests correlated with increased CTmax, but not CTmin These patterns suggest CTmax and CTmin respond to different abiotic selective forces: habitat-specific exposure to extreme insolation corresponds to CTmax differences, but not to CTmin variation. We predict increasingly frequent heat spikes associated with climate change will have habitat-specific physiological consequences for ectothermic animals. Models predicting climate change impacts should account for species microhabitat uses and within-latitude differences in temperature seasonality.