Abstract

Ectotherms rely for their body heat on surrounding temperatures. A key question in biology is why most ectotherms mature at a larger size at lower temperatures, a phenomenon known as the temperature–size rule. Since temperature affects virtually all processes in a living organism, current theories to explain this phenomenon are diverse and complex and assert often from opposing assumptions. Although widely studied, the molecular genetic control of the temperature–size rule is unknown. We found that the Caenorhabditis elegans wild-type N2 complied with the temperature–size rule, whereas wild-type CB4856 defied it. Using a candidate gene approach based on an N2 × CB4856 recombinant inbred panel in combination with mutant analysis, complementation, and transgenic studies, we show that a single nucleotide polymorphism in tra-3 leads to mutation F96L in the encoded calpain-like protease. This mutation attenuates the ability of CB4856 to grow larger at low temperature. Homology modelling predicts that F96L reduces TRA-3 activity by destabilizing the DII-A domain. The data show that size adaptation of ectotherms to temperature changes may be less complex than previously thought because a subtle wild-type polymorphism modulates the temperature responsiveness of body size. These findings provide a novel step toward the molecular understanding of the temperature–size rule, which has puzzled biologists for decades.

Highlights

  • For many decades biologists have been intrigued by the relation between body size and temperature

  • Our results show that a polymorphism in a single gene may attenuate the thermal reaction norm for body size (TRB) in C. elegans

  • Concluding Remarks We have presented genetic and structural evidence that an single nucleotide polymorphism (SNP) in the gene tra-3 encoding a calpain-like protease is required for the regulation of the temperature–size rule in wild-type C. elegans

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Summary

Introduction

For many decades biologists have been intrigued by the relation between body size and temperature. It was discovered that ectotherms—animals that maintain their body temperature by absorbing heat from the surrounding environment such as fish and all invertebrates—reproduce later at a larger size when reared at lower temperatures [1,2,3]. This phenomenon is known as the temperature–size rule, and nearly 90% of ectothermic species studied so far follow this rule [4]. From the perspective of life-history evolution it is not well understood why growing bigger at lower temperatures is beneficial for organisms Because this thermal plasticity of body size is taxonomically widespread, the reasons are probably diverse and may vary among groups of organisms. Other explanations may be that a larger body size at maturity enables individuals to produce larger offspring or to provide better parental care [2]

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