Ladder webs in orb-web spiders: ontogenetic and evolutionary patterns in Nephilidae

Spider web research bridges ethology, ecology, functional morphology, material science, development, genetics, and evolution. Recent work proposes the aerial orb web as a one-time key evolutionary innovation that has freed spider-web architecture from substrate constraints. However, the orb has repeatedly been modified or lost within araneoid spiders. Modifications include not only sheet- and cobwebs, but also ladder webs, which secondarily utilize the substrate. A recent nephilid species level phylogeny suggests that the ancestral nephilid web architecture was an arboricolous ladder and that round aerial webs were derived. Because the web biology of the basalmost Clitaetra and the derived Nephila are well understood, the present study focuses on the webs of the two phylogenetically intervening genera, Herennia and Nephilengys, to establish ontogenetic and macroevolutionary patterns across the nephilid tree. We compared juvenile and adult webs of 95 Herennia multipuncta and 143 Nephilengys malabarensis for two measures of ontogenetic allometric web changes: web asymmetry quantified by the ladder index, and hub asymmetry quantified by the hub displacement index. We define a 'ladder web' as a vertically elongated orb exceeding twice the length over width (ladder index ≥ 2) and possessing (sub)parallel rather than round side frames. Webs in both genera allometrically grew from orbs to ladders, more so in Herennia. Such allometric web growth enables the spider to maintain its arboricolous web site. Unexpectedly, hub asymmetry only increased significantly in heavy-bodied Nephilengys females, and not in Herennia, challenging the commonly invoked gravity hypothesis. The findings obtained in the present study support the intrageneric uniformness of nephilid webs, with Herennia etruscilla webs being identical to H. multipuncta. The nephilid web evolution suggests that the ancestor of Nephila reinvented the aerial orb web because the orb arises at a much more inclusive phylogenetic level, and all intervening nephilids retained the secondarily acquired substrate-dependent ladder web.