A Natural Mutational Event Uncovers a Life History Trade-Off via Hormonal Pleiotropy

Curr Biol. 2020 Nov 2;30(21):4142-4154.e9. doi: 10.1016/j.cub.2020.08.004. Epub 2020 Sep 3.

Abstract

Environmental signals often control central life history decisions, including the choice between reproduction and somatic maintenance. Such adaptive developmental plasticity occurs in the nematode Caenorhabditis elegans, where environmental cues govern whether larvae will develop directly into reproducing adults or arrest their development to become stress-resistant dauer larvae. Here, we identified a natural variant underlying enhanced sensitivity to dauer-inducing cues in C. elegans: a 92-bp deletion in the cis-regulatory region of the gene eak-3. This deletion reduces synthesis or activity of the steroid hormone dafachronic acid (DA), thereby increasing environmental sensitivity for dauer induction. Consistent with known pleiotropic roles of DA, this eak-3 variant significantly slows down reproductive growth. We experimentally show that, although the eak-3 deletion can provide a fitness advantage through facilitated dauer production in stressful environments, this allele becomes rapidly outcompeted in favorable environments. The identified eak-3 variant therefore reveals a trade-off in how hormonal responses influence both the pace of developmental timing and the way in which environmental sensitivity controls adaptive plasticity. Together, our results show how a single mutational event altering hormonal signaling can lead to the emergence of a complex life history trade-off.

Keywords: C. elegans; adaptive developmental plasticity; dauer induction; eak-3; environmental sensitivity; genotype-by-environment interactions; hormonal pleiotropy; life history trade-off; natural variation; steroid hormones.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics
  • Alleles
  • Animals
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / genetics*
  • Caenorhabditis elegans Proteins / metabolism
  • Cholestenes / metabolism*
  • Gene Expression Regulation, Developmental*
  • Genetic Pleiotropy
  • Larva / genetics
  • Larva / growth & development*
  • Mutation
  • Regulatory Sequences, Nucleic Acid / genetics
  • Sequence Deletion
  • Signal Transduction

Substances

  • Caenorhabditis elegans Proteins
  • Cholestenes
  • dafachronic acid