Plasticity Through Canalization: The Contrasting Effect of Temperature on Trait Size and Growth in Drosophila.

Jeanne M C Mcdonald,Shampa M Ghosh,Alexander W Shingleton,Samuel J L Gascoigne

doi:10.3389/fcell.2018.00156

Abstract

In most ectotherms, a reduction in developmental temperature leads to an increase in body size, a phenomenon known as the temperature size rule (TSR). In Drosophila melanogaster, temperature affects body size primarily by affecting critical size, the point in development when larvae initiate the hormonal cascade that stops growth and starts metamorphosis. However, while the thermal plasticity of critical size can explain the effect of temperature on overall body size, it cannot entirely account for the effect of temperature on the size of individual traits, which vary in their thermal sensitivity. Specifically, the legs and male genitalia show reduced thermal plasticity for size, while the wings show elevated thermal plasticity, relative to overall body size. Here, we show that these differences in thermal plasticity among traits reflect, in part, differences in the effect of temperature on the rates of cell proliferation during trait growth. Counterintuitively, the elevated thermal plasticity of the wings is due to canalization in the rate of cell proliferation across temperatures. The opposite is true for the legs. These data reveal that environmental canalization at one level of organization may explain plasticity at another, and vice versa.

Highlights

Temperature impacts multiple aspects of biology through its influence on the rates of almost all biological processes
The elevated thermal plasticity of wing size relative to leg size arises through a reduction in the thermal plasticity of cell proliferation in the wing imaginal disk relative to the leg imaginal disk
Consistent with published results (Azevedo et al, 2002; Frazier et al, 2008; Shingleton et al, 2009), we found that wing size was significantly more thermally plastic than leg size or the size of any other trait we measured (Figure 1A)

Summary

Introduction

Temperature impacts multiple aspects of biology through its influence on the rates of almost all biological processes. There is still debate as to whether the TSR is a consequence of selection for mechanisms that reduce body size at higher temperatures or Plasticity Through Canalization due to the near-universal effects of temperature on the biophysical processes that regulate the rate of growth and development (Atkinson and Sibly, 1997; Angilletta and Dunham, 2003; Angilletta et al, 2004). That is, it is unclear whether or not the TSR is an adaptation

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