Chaperones, Canalization, and Evolution of Animal Forms

Abstract

Over half a century ago, British developmental biologist Conrad Hal Waddington proposed the idea of canalization, that is, homeostasis in development. Since the breakthrough that was made by Rutherford and Lindquist (1998), who proposed a role of Hsp90 in developmental buffering, chaperones have gained much attention in the study of canalization. However, recent studies have revealed that a number of other molecules are also potentially involved in canalization. Here, I introduce the emerging role of DnaJ chaperones in canalization. I also discuss how the expression levels of such buffering molecules can be altered, thereby altering organismal development. Since developmental robustness is maternally inherited in various organisms, I propose that dynamic bet hedging, an increase in within-clutch variation in offspring phenotypes that is caused by unpredictable environmental challenges to the mothers, plays a key role in altering the expression levels of buffering molecules. Investigating dynamic bet hedging at the molecular level and how it impacts upon morphological phenotypes will help our understanding of the molecular mechanisms of canalization and evolutionary processes.

Keywords: DNAJs; bet hedging; developmental robustness; epigenetic landscape; heat shock proteins; maternal inheritance.

Figure 1

Measurement of canalization using seam cell numbers as a read-out in Caenorhabditis elegans. Most wild type worms have 16 seam cells in the lateral side of the body at L4 larval stage (A). If a gene is involved in phenotypic construction [18], knockdown of the gene alters the mean seam cell number (B). However, if a gene is involved in the canalization of seam cells, knockdown of the gene would increase the variance of seam cell numbers (C). See details of the experiments in Section 2.3.

Figure 2

Hypothesis on the role of bet hedging in altering developmental robustness that leads to evolution of organismal forms. Increased variation by maternal environment controls expression levels of buffering molecules such as chaperones. If the level of expression increases, developmental robustness will increase, allowing the accumulation of background mutations. On the other hand, if the level of expression decreases, developmental robustness will decrease, increasing the susceptibility to genetic variations and all the epistatic interactions involved, resulting in a change in the ‘epigenetic landscape’.