Is Phenotypic Evolution Affected by Spiders’ Construction Behaviors?

Abstract What happens when organisms actively modify their environment? Clarifying the role of construction behavior on a macroevolutionary scale is crucial to interpreting phenotypic evolution. Spiders, an extremely successful group of animals exhibiting a wide variety of functional, morphological, and behavioral diversity, are ideal candidates to test whether animal behaviors are related to their phenotypic evolution. Herein, we reconstructed the phylogenomic relationships of 303 spiders covering 105 families with 99 newly developed molecular markers that universally apply across Araneae, and explicitly tested the potential link between construction behavior and somatic evolution based on extensive morphological data from 3,342 extant species and 682 fossil species. Our dated molecular phylogeny provides the backbone for analyses, revealing the behavioral and ecological processes behind these spiders’ morphological adaptations. Evolutionary model analyses showed the artifacts constructed by spiders, especially the suspending webs, expand the spider’s ability to inhabit different habitats. These artifacts have more substantial impacts on their somatic traits than habitats and promote different trajectories of morphological evolution. Specifically, for spiders, silk-lined burrowing produced larger bodies, relatively shorter legs, and longer patellae, while web-building produced smaller bodies, relatively longer legs, and shorter patellae, and hunting promoted an intermediate morphological size. Molecular convergence analysis showed that genes related to morphogenesis or response to stimulus and stress are enriched in spiders with construction behavior. Our study demonstrated that the construction behavior of an animal plays a crucial role in determining the direction and intensity of the selection pressure imposed on it and provides strong evidence that construction behaviors are associated with phenotypic evolution on macroevolutionary timescales. [Araneae; body size; habitat change; molecular marker; leg length; phylogenomics.]