Morphological Evolution of Spiders Predicted by Pendulum Mechanics

Abstract

BackgroundAnimals have been hypothesized to benefit from pendulum mechanics during suspensory locomotion, in which the potential energy of gravity is converted into kinetic energy according to the energy-conservation principle. However, no convincing evidence has been found so far. Demonstrating that morphological evolution follows pendulum mechanics is important from a biomechanical point of view because during suspensory locomotion some morphological traits could be decoupled from gravity, thus allowing independent adaptive morphological evolution of these two traits when compared to animals that move standing on their legs; i.e., as inverted pendulums. If the evolution of body shape matches simple pendulum mechanics, animals that move suspending their bodies should evolve relatively longer legs which must confer high moving capabilities.Methodology/Principal FindingsWe tested this hypothesis in spiders, a group of diverse terrestrial generalist predators in which suspensory locomotion has been lost and gained a few times independently during their evolutionary history. In spiders that hang upside-down from their webs, their legs have evolved disproportionately longer relative to their body sizes when compared to spiders that move standing on their legs. In addition, we show how disproportionately longer legs allow spiders to run faster during suspensory locomotion and how these same spiders run at a slower speed on the ground (i.e., as inverted pendulums). Finally, when suspensory spiders are induced to run on the ground, there is a clear trend in which larger suspensory spiders tend to run much more slowly than similar-size spiders that normally move as inverted pendulums (i.e., wandering spiders).Conclusions/SignificanceSeveral lines of evidence support the hypothesis that spiders have evolved according to the predictions of pendulum mechanics. These findings have potentially important ecological and evolutionary implications since they could partially explain the occurrence of foraging plasticity and dispersal constraints as well as the evolution of sexual size dimorphism and sociality.

Silk elasticity as a potential constraint on spider body size

“…crab spiders within the RTA clade and Orbiculariae spiders). Because their morphology is unsuitable for walking along solid surfaces (Moya-Laraño et al, 2008), they are seldom seen walking on the ground and depend on bridging for their mid-range displacements. As we have seen, the elastic properties of minor ampulalte silk may make bridging an inefficient displacement mechanism for large spiders.…”

“…The morphological traits allowing efficient locomotion in spiders that spend most of their life hanging upside-down from their webs are very different from those favoured in spiders that must support their weights on their legs while walking on solid surfaces (Moya-Laraño et al, 2008). As a result, spiders adapted to moving along silk fibres are clumsy when moving on hard surfaces.…”

“…To use this displacement method, a spider releases a bridging line until it adheres to some substrate, spanning a gap in the vegetation. The spider then tightens the line (Moya-Laraño et al, 2008;Peters 1990) and crawls across the silk threads. Although bridging has received relatively little attention in the literature, in the only species that have been studied in detail (Linyphia triangularis and Araneus diadematus) the bridging line is composed of two minor ampullate silk filaments (Peters, 1990).…”

“…Although bridging has received relatively little attention in the literature, in the only species that have been studied in detail (Linyphia triangularis and Araneus diadematus) the bridging line is composed of two minor ampullate silk filaments (Peters, 1990). Bridging frees spiders at once from the need to support their own weight (Moya-Laraño et al, 2008) and the constraint to follow the complex, fractal-like three-dimensional structure of vegetation for their displacements. Bridging is widespread in the Orbicularia clade.…”

Intra-specific variability of hindlimb length in the palmate newt: an indicator of population isolation induced by habitat fragmentation?

“…The costs associated with dispersal are likely to limit resource allocation, which can cause covariations between dispersal capacities and life-history traits [3]. In particular, because selection for efficient displacement might lead to leg elongation, morphological adaptations to dispersal could be deduced from estimates of leg length [4]. Dispersal abilities may be associated with locomotor performance [5], which is in turn related to hindlimb length (hereafter HLL) through its effects on take-off speed, jump distance [5] and distance moved [6] in anurans and on running burst speed and endurance in salamanders [7].…”