Constraints, independence, and evolution of thermal plasticity: probing genetic architecture of long- and short-term thermal acclimation

Proc Natl Acad Sci U S A. 2015 Apr 7;112(14):4399-404. doi: 10.1073/pnas.1503456112. Epub 2015 Mar 24.


Seasonal and daily thermal variation can limit species distributions because of physiological tolerances. Low temperatures are particularly challenging for ectotherms, which use both basal thermotolerance and acclimation, an adaptive plastic response, to mitigate thermal stress. Both basal thermotolerance and acclimation are thought to be important for local adaptation and persistence in the face of climate change. However, the evolutionary independence of basal and plastic tolerances remains unclear. Acclimation can occur over longer (seasonal) or shorter (hours to days) time scales, and the degree of mechanistic overlap is unresolved. Using a midlatitude population of Drosophila melanogaster, we show substantial heritable variation in both short- and long-term acclimation. Rapid cold hardening (short-term plasticity) and developmental acclimation (long-term plasticity) are positively correlated, suggesting shared mechanisms. However, there are independent components of these traits, because developmentally acclimated flies respond positively to short-term acclimation. A strong negative correlation between basal cold tolerance and developmental acclimation suggests that basal cold tolerance may constrain developmental acclimation, whereas a weaker negative correlation between basal cold tolerance and short-term acclimation suggests less constraint. Using genome-wide association mapping, we show the genetic architecture of rapid cold hardening and developmental acclimation responses are nonoverlapping at the SNP and corresponding gene level. However, genes associated with each trait share functional similarities, including genes involved in apoptosis and autophagy, cytoskeletal and membrane structural components, and ion binding and transport. These results indicate substantial opportunity for short-term and long-term acclimation responses to evolve separately from each other and for short-term acclimation to evolve separately from basal thermotolerance.

Keywords: developmental acclimation; environmental stress; genome-wide association studies; rapid cold hardening; thermal acclimation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Acclimatization / genetics*
  • Acclimatization / physiology
  • Animals
  • Biological Evolution*
  • Climate Change
  • Cold Temperature
  • Drosophila melanogaster / genetics*
  • Female
  • Genome-Wide Association Study
  • Hot Temperature
  • Male
  • Mutation
  • Phenotype
  • Polymorphism, Single Nucleotide