Modulation of the heat shock response is associated with acclimation to novel temperatures but not adaptation to climatic variation in the ants Aphaenogaster picea and A. rudis

Abstract

Ecological diversification into thermally divergent habitats can push species toward their physiological limits, requiring them to accommodate temperature extremes through plastic or evolutionary changes that increase persistence under the local thermal regime. One way to withstand thermal stress is to increase production of heat shock proteins, either by maintaining higher baseline abundance within cells or by increasing the magnitude of induction in response to heat stress. We evaluated whether environmental variation was associated with expression of three heat shock protein genes in two closely-related species of woodland ant, Aphaenogaster picea and A. rudis. We compared adult workers from colonies collected from 25 sites across their geographic ranges. Colonies were maintained at two different laboratory temperatures, and tested for the independent effects of environment, phylogeny, and acclimation temperature on baseline and heat-induced gene expression. The annual maximum temperature at each collection site (Tmax) was not a significant predictor of either baseline expression or magnitude of induction of any of the heat shock protein genes tested. A phylogenetic effect was detected only for basal expression of Hsp40, which was lower in the most southern populations of A. rudis and higher in a mid-range population of possible hybrid ancestry. In contrast, a higher acclimation temperature significantly increased baseline expression of Hsc70-4, and increased induction of Hsp40 and Hsp83. Thus, physiological acclimation to temperature variation appears to involve modulation of the heat shock response, whereas other mechanisms are likely to be responsible for evolutionary shifts in thermal performance associated with large-scale climate gradients.

Does social thermal regulation constrain individual thermal tolerance in an ant species?

“…In the case of A. iberica, workers only collect solid prey, and so the species' diet is relatively poor in carbohydrates. It is more likely that thermal tolerance is enhanced by mechanisms such as the production of heat shock proteins (Gehring & Wehner, 1995;Helms Cahan et al, 2017;Ślipiński, Pomorski, & Kowalewska, 2015;Willot et al, 2017), more efficient convective cooling or constrained cuticular transpiration (Cerdá & Retana, 2000;Gibbs & Pomonis, 1995). These differences could be the result of natural selection acting differentially on intermediate-elevation populations, creating a pattern of local adaptation.…”

DraftAphaenogastergenomes expand our view of ant genome size variation across climate gradients

“…Efforts such as The Global Ant Genomics Alliance (GAGA)(Boomsma et al, 2017), which aims to greatly increase the number of ant species sequenced from across the world, will provide additional resources for ecological genomics studies. Further work investigating the variation in genomic content and mapping of target coding regions from previous physiological (Nguyen et al, 2017), biochemical (Helms Cahan et al, 2017), and transcriptomic (Stanton-Geddes et al, 2016) studies of Aphaenogaster and other ant species will inform predictions of how these species, and the ecosystems that they inhabit, may respond to ongoing climatic change. For instance, determining the genomic factors underlying the temperature response of ant assemblages to climatic gradients (Warren and Chick, 2013; Diamond et al, 2016, 2017) could provide useful insights into the response of these important organisms to non-analog ecosystem states and idiosyncratic community responses (Bewick et al, 2014).…”

“…Although correlative, our genome analysis results are consistent with the hypothesis that ants from regions with more similar climates tend to have similar sized genomes. Previous studies have observed physiological and ecological responses of ants to climate gradients and shifting temperatures (Warren and Chick, 2013; Stanton-Geddes et al, 2016; Diamond et al, 2016; Nguyen et al, 2017; Helms Cahan et al, 2017; Diamond et al, 2017; Penick et al, 2017) that could act as agents of selection or as environmental filters. For example, Warren and Chick (2013) found that cold, but not warm, temperatures limited shifts in the distributions of A. picea and A. rudis .…”

Peer Review #2 of "Draft Aphaenogaster genomes expand our view of ant genome size variation across climate gradients (v0.1)"

“…Although correlative, our genome analysis results are consistent with the hypothesis that ants from regions with more similar climates tend to have similar sized genomes. Previous studies have observed physiological and ecological responses of ants to climate gradients and shifting temperatures (Warren and Chick, 2013;Stanton-Geddes et al, 2016;Diamond et al, 2016;Nguyen et al, 2017;Helms Cahan et al, 2017;Diamond et al, 2017;Penick et al, 2017) that could act as agents of selection or as environmental filters. For example, Warren and Chick (2013) found that cold, but not warm, temperatures limited shifts in the distributions of A. picea and A. rudis.…”

“…Further work investigating the variation in genomic content and mapping of target coding regions from previous physiological (Nguyen et al, 2017), biochemical (Helms Cahan et al, 2017), and transcriptomic (Stanton-Geddes et al, 2016) studies of Aphaenogaster and other ant species will inform predictions of how these species, and the ecosystems that they inhabit, may respond to ongoing climatic change. For instance, determining the genomic factors underlying the temperature response of ant assemblages to climatic gradients (Warren and Chick, 2013;Diamond et al, 2016Diamond et al, , 2017 could provide useful insights into the response of these important organisms to non-analog ecosystem states and idiosyncratic community responses (Bewick et al, 2014).…”