Repeated Evolution of Power-Amplified Predatory Strikes in Trap-Jaw Spiders

Small animals possess intriguing morphological and behavioral traits that allow them to capture prey, including innovative structural mechanisms that produce ballistic movements by amplifying power [1-6]. Power amplification occurs when an organism produces a relatively high power output by releasing slowly stored energy almost instantaneously, resulting in movements that surpass the maximal power output of muscles [7]. For example, trap-jaw, power-amplified mechanisms have been described for several ant genera [5, 8], which have evolved some of the fastest known movements in the animal kingdom [6]. However, power-amplified predatory strikes were not previously known in one of the largest animal classes, the arachnids. Mecysmaucheniidae spiders, which occur only in New Zealand and southern South America, are tiny, cryptic, ground-dwelling spiders that rely on hunting rather than web-building to capture prey [9]. Analysis of high-speed video revealed that power-amplified mechanisms occur in some mecysmaucheniid species, with the fastest species being two orders of magnitude faster than the slowest species. Molecular phylogenetic analysis revealed that power-amplified cheliceral strikes have evolved four times independently within the family. Furthermore, we identified morphological innovations that directly relate to cheliceral function: a highly modified carapace in which the cheliceral muscles are oriented horizontally; modification of a cheliceral sclerite to have muscle attachments; and, in the power-amplified species, a thicker clypeus and clypeal apodemes. These structural innovations may have set the stage for the parallel evolution of ballistic predatory strikes.