The architectural design of animal structures forms part of an individual's extended phenotype that can be subjected to strong selection pressures. We examined cocoon architectural dimorphism in robin moths (Hyalophora cecropia), which construct multilayered silk-woven cocoons that possess either a ‘baggy’ or ‘compact’ morphology. These dimorphic cocoons reflect extended phenotypes that can enable survival during a critical developmental period (pupal stage to adult emergence), with cocoons occurring either sympatrically or as monomorphic groups across different climatic regions in North America. We hypothesized that cocoon dimorphism is related to the cocoon's role as a mediating barrier for moisture. We predicted that the macro- and micro-architectural differences between the cocoon morphs would be consistent with this function. We compared the cocoon morphs in terms of their orientation when spun under natural field conditions, examined how these orientations affected cocoon water absorption under simulated rain trials, and performed material surface tests to compare the hydrophobicity of cocoons. We found that compact cocoons had traits that increased water resistance, as they had significantly greater hydrophobicity than baggy cocoons, because they absorbed less water and released water vapor faster. In contrast, the increased water absorptiveness of baggy cocoons can allow for greater moisture retention, a function related to the prevention of desiccation. Our study suggests that cocoon dimorphism in robin moths reflects distinct architectural syndromes, in which cocoons are spun to optimize either water resistance or retention. These different functions are consistent with strategies that act to respond to uncertain external environmental conditions that an individual might encounter during development.

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