Thermal reactionomes reveal divergent responses to thermal extremes in warm and cool-climate ant species

Abstract

BackgroundThe distributions of species and their responses to climate change are in part determined by their thermal tolerances. However, little is known about how thermal tolerance evolves. To test whether evolutionary extension of thermal limits is accomplished through enhanced cellular stress response (enhanced response), constitutively elevated expression of protective genes (genetic assimilation) or a shift from damage resistance to passive mechanisms of thermal stability (tolerance), we conducted an analysis of the reactionome: the reaction norm for all genes in an organism’s transcriptome measured across an experimental gradient. We characterized thermal reactionomes of two common ant species in the eastern U.S, the northern cool-climate Aphaenogaster picea and the southern warm-climate Aphaenogaster carolinensis, across 12 temperatures that spanned their entire thermal breadth.ResultsWe found that at least 2 % of all genes changed expression with temperature. The majority of upregulation was specific to exposure to low temperatures. The cool-adapted A. picea induced expression of more genes in response to extreme temperatures than did A. carolinensis, consistent with the enhanced response hypothesis. In contrast, under high temperatures the warm-adapted A. carolinensis downregulated many of the genes upregulated in A. picea, and required more extreme temperatures to induce down-regulation in gene expression, consistent with the tolerance hypothesis. We found no evidence for a trade-off between constitutive and inducible gene expression as predicted by the genetic assimilation hypothesis.ConclusionsThese results suggest that increases in upper thermal limits may require an evolutionary shift in response mechanism away from damage repair toward tolerance and prevention.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2466-z) contains supplementary material, which is available to authorized users.

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 .…”

“…No species of Aphaenogaster , which are abundant ants that play key roles in the dispersal of understory plant species in North America and temperate Asia, have yet been sequenced. Previous studies have also shown that Aphaenogaster species’ ecological and physiological responses to climatic change appear to depend both on species identity and on the geographic region in which climatic change occurs (Warren and Chick, 2013; Stanton-Geddes et al, 2016).…”

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

“…Manuscript to be reviewed on species identity and on the geographic region in which climatic change occurs (Warren and Chick, 2013;Stanton-Geddes et al, 2016). To increase the number of genomes of temperate-zone ant species, we sequenced the genomes of Aphaenogaster species.…”

“…Multiple studies support the perspective that a more complete knowledge of ant genetics will increase our understanding of ant responses to environmental change (Diamond et al, 2012;Nygaard and Wurm, 2015;Stanton-Geddes et al, 2016;Boomsma et al, 2017;Penick et al, 2017). Studies of ant genomes have shed light on the evolution and social organization of ants (Libbrecht et al, 2013).…”