Adaptive divergence in shoot gravitropism creates hybrid sterility in an Australian wildflower

Proc Natl Acad Sci U S A. 2021 Nov 23;118(47):e2004901118. doi: 10.1073/pnas.2004901118.

Abstract

Natural selection is responsible for much of the diversity we see in nature. Just as it drives the evolution of new traits, it can also lead to new species. However, it is unclear whether natural selection conferring adaptation to local environments can drive speciation through the evolution of hybrid sterility between populations. Here, we show that adaptive divergence in shoot gravitropism, the ability of a plant's shoot to bend upwards in response to the downward pull of gravity, contributes to the evolution of hybrid sterility in an Australian wildflower, Senecio lautus We find that shoot gravitropism has evolved multiple times in association with plant height between adjacent populations inhabiting contrasting environments, suggesting that these traits have evolved by natural selection. We directly tested this prediction using a hybrid population subjected to eight rounds of recombination and three rounds of selection in the field. Our experiments revealed that shoot gravitropism responds to natural selection in the expected direction of the locally adapted population. Using the advanced hybrid population, we discovered that individuals with extreme differences in gravitropism had more sterile crosses than individuals with similar gravitropic responses, which were largely fertile, indicating that this adaptive trait is genetically correlated with hybrid sterility. Our results suggest that natural selection can drive the evolution of locally adaptive traits that also create hybrid sterility, thus revealing an evolutionary connection between local adaptation and the origin of new species.

Keywords: hybrid sterility; intrinsic reproductive isolation; local adaptation; natural selection; speciation.

MeSH terms

  • Adaptation, Physiological / genetics
  • Adaptation, Physiological / physiology
  • Arabidopsis Proteins
  • Australia
  • Genetic Variation
  • Gravitropism / physiology*
  • Indoleacetic Acids / metabolism
  • Infertility*
  • Phenotype
  • Plant Shoots / physiology*
  • Selection, Genetic
  • Senecio / genetics
  • Senecio / physiology*
  • Sulfurtransferases

Substances

  • Arabidopsis Proteins
  • Indoleacetic Acids
  • Sulfurtransferases