A quantitative model of temperature-dependent diapause progression

Proc Natl Acad Sci U S A. 2024 Sep 3;121(36):e2407057121. doi: 10.1073/pnas.2407057121. Epub 2024 Aug 28.

Abstract

Winter diapause in insects is commonly terminated through cold exposure, which, like vernalization in plants, prevents development before spring arrives. Currently, quantitative understanding of the temperature dependence of diapause termination is limited, likely because diapause phenotypes are generally cryptic to human eyes. We introduce a methodology to tackle this challenge. By consecutively moving butterfly pupae of the species Pieris napi from several different cold conditions to 20 °C, we show that diapause termination proceeds as a temperature-dependent rate process, with maximal rates at relatively cold temperatures and low rates at warm and extremely cold temperatures. Further, we show that the resulting thermal reaction norm can predict P. napi diapause termination timing under variable temperatures. Last, we show that once diapause is terminated in P. napi, subsequent development follows a typical thermal performance curve, with a maximal development rate at around 31 °C and a minimum at around 2 °C. The sequence of these thermally distinct processes (diapause termination and postdiapause development) facilitates synchronous spring eclosion in nature; cold microclimates where diapause progresses quickly do not promote fast postdiapause development, allowing individuals in warmer winter microclimates to catch up, and vice versa. The unveiling of diapause termination as one temperature-dependent rate process among others promotes a parsimonious, quantitative, and predictive model, wherein winter diapause functions both as an adaptation against premature development during fall and winter and for synchrony in spring.

Keywords: diapause; diapause termination; ecological predictions; insect; thermal performance curve.

MeSH terms

  • Animals
  • Butterflies* / physiology
  • Cold Temperature
  • Diapause / physiology
  • Diapause, Insect / physiology
  • Models, Biological
  • Pupa / growth & development
  • Pupa / physiology
  • Seasons*
  • Temperature*