A Quantitative Analysis of Growth and Size Regulation in Manduca sexta: The Physiological Basis of Variation in Size and Age at Metamorphosis

PLoS One. 2015 May 26;10(5):e0127988. doi: 10.1371/journal.pone.0127988. eCollection 2015.

Abstract

Body size and development time are important life history traits because they are often highly correlated with fitness. Although the developmental mechanisms that control growth have been well studied, the mechanisms that control how a species-characteristic body size is achieved remain poorly understood. In insects adult body size is determined by the number of larval molts, the size increment at each molt, and the mechanism that determines during which instar larval growth will stop. Adult insects do not grow, so the size at which a larva stops growing determines adult body size. Here we develop a quantitative understanding of the kinetics of growth throughout larval life of Manduca sexta, under different conditions of nutrition and temperature, and for genetic strains with different adult body sizes. We show that the generally accepted view that the size increment at each molt is constant (Dyar's Rule) is systematically violated: there is actually a progressive increase in the size increment from instar to instar that is independent of temperature. In addition, the mass-specific growth rate declines throughout the growth phase in a temperature-dependent manner. We show that growth within an instar follows a truncated Gompertz trajectory. The critical weight, which determines when in an instar a molt will occur, and the threshold size, which determines which instar is the last, are different in genetic strains with different adult body sizes. Under nutrient and temperature stress Manduca has a variable number of larval instars and we show that this is due to the fact that more molts at smaller increments are taken before threshold size is reached. We test whether the new insight into the kinetics of growth and size determination are sufficient to explain body size and development time through a mathematical model that incorporates our quantitative findings.

Publication types

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

MeSH terms

  • Age Distribution
  • Animals
  • Body Size*
  • Food
  • Genetic Variation
  • Larva / genetics
  • Larva / growth & development
  • Larva / physiology
  • Manduca / genetics
  • Manduca / growth & development*
  • Manduca / physiology
  • Metamorphosis, Biological*
  • Stress, Physiological*
  • Temperature

Grants and funding

National Science Foundation grants: IOS-0744952 EF-103859 and IOS-1121065. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.