Evolutionary kinematics of spinneret movements for rapid silk thread anchorage in spiders

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ORIGINAL PAPER

Evolutionary kinematics of spinneret movements for rapid silk thread anchorage in spiders Jonas O. Wolff1  Received: 25 August 2020 / Revised: 22 October 2020 / Accepted: 24 October 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Many organisms secrete structural materials from their bodies to enhance protection, foraging or signalling. The function of such secretion products can be further extended by their assembly into complex structures, so-called extended phenotypes, such as shells, nests and biofilms. Understanding the variation in the efficacy of such assembly processes could help to explain why extended phenotypes are common on some lineages and rare in others. Here, I comparatively studied the assembly of sticky silk fibres into thread anchorages by the innate ‘printing’ behaviour in 92 species of spiders from 45 families, representing the so-far largest comparative study of construction-related motion patterns. I found a global evolutionary trend towards a faster production of silk thread anchorages, in both web builders and hunting spiders. The slowest producers of silk anchors belong to a clade with an ancestral configuration of respiratory organs, suggesting that a major constraint to the evolution of spinning speed is the efficiency of oxygen uptake. Motion patterns were found to contain a high phylogenetic signal, but did not correlate with spinning speeds. These results help to explain the variation in diversity and ecological success among the spider fauna and showcase the value of comparative kinematics in biodiversity studies. Keywords  Spider web · Piriform silk · Evolution of behaviour · Construction behaviour · Geometric morphometrics

Introduction Many organisms secrete structural materials from their bodies to enhance protection, foraging or signalling (Barnes 1972; Tavener-Smith and Williams 1972; Dalgetty and Kennedy 2010; Nadell et al. 2016; Wolff and Gorb 2016). The function of such secretions can be further extended by their assembly into complex structures (Hansell 2005; Wolff et al. 2016; Waite 2017; Grannemann et al. 2019). A prime example are spider webs built from fibrous and adhesive secretions. Spider web structure is the result of a set of stereotypic behaviours, the morphology of the spinning apparatus and the physiological characteristics of the silk secretion process (Harmer et al. 2011). Of these processes, the behavioural Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0035​9-020-01453​-3) contains supplementary material, which is available to authorized users. * Jonas O. Wolff [email protected] 1



Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia

routine is one of the hardest to quantify and compare. Therefore, our knowledge on how construction behaviour evolves and how much it correlates with the architecture of the product is still rudimentary. Here, I studied the kinematics of spinneret movements during the production of silk thread anc