Take a deep breath… The evolution of the respiratory system of symphytognathoid spiders (Araneae, Araneoidea)

Spiders are unique in having a dual respiratory system with book lungs and tracheae, and most araneomorph spiders breathe simultaneously via book lungs and tracheae, or tracheae alone. The respiratory organs of spiders are diverse but relatively conserved within families. The small araneoid spiders of the symphytognathoid clade exhibit a remarkably high diversity of respiratory organs and arrangements, unparalleled by any other group of ecribellate orb weavers. In the present study, we explore and review the diversity of symphytognathoid respiratory organs. Using a phylogenetic comparative approach, we reconstruct the evolution of the respiratory system of symphytognathoids based on the most comprehensive phylogenetic frameworks to date. There are no less than 22 different respiratory system configurations in symphytognathoids. The phylogenetic reconstructions suggest that the anterior tracheal system evolved from fully developed book lungs and, conversely, reduced book lungs have originated independently at least twice from its homologous tracheal conformation. Our hypothesis suggests that structurally similar book lungs might have originated through different processes of tracheal transformation in different families. In symphytognathoids, the posterior tracheal system has either evolved into a highly branched and complex system or it is completely lost. No evident morphological or behavioral features satisfactorily explains the exceptional variation of the symphytognathoid respiratory organs.

Sequence Capture Phylogenomics of True Spiders Reveals Convergent Evolution of Respiratory Systems

The common ancestor of spiders likely used silk to line burrows or make simple webs, with specialized spinning organs and aerial webs originating with the evolution of the megadiverse “true spiders” (Araneomorphae). The base of the araneomorph tree also concentrates the greatest number of changes in respiratory structures, a character system whose evolution is still poorly understood, and that might be related to the evolution of silk glands. Emphasizing a dense sampling of multiple araneomorph lineages where tracheal systems likely originated, we gathered genomic-scale data and reconstructed a phylogeny of true spiders. This robust phylogenomic framework was used to conduct maximum likelihood and Bayesian character evolution analyses for respiratory systems, silk glands, and aerial webs, based on a combination of original and published data. Our results indicate that in true spiders, posterior book lungs were transformed into morphologically similar tracheal systems six times independently, after the evolution of novel silk gland systems and the origin of aerial webs. From these comparative data, we put forth a novel hypothesis that early-diverging web-building spiders were faced with new energetic demands for spinning, which prompted the evolution of similar tracheal systems via convergence; we also propose tests of predictions derived from this hypothesis.[Book lungs; discrete character evolution; respiratory systems; silk; spider web evolution; ultraconserved elements.]

The evolution of air-breathing respiratory faculties in invertebrates

This chapter aims at piecing together the evolution of air breathing in invertebrates, the main conclusion here being that it evolved independently several times. In molluscs alone, air breathing has evolved several times, but almost exclusively among snails. Among crustaceans, several groups of crabs have also independently developed terrestrial representatives and transitional stages, particularly in the control of breathing, are evident. Analysis of insects shows few recognizable evolutionary progressions: air sacs and different stigmatal closure mechanisms have appeared and disappeared numerous times, even within closely related groups. But other tracheate groups such as myriapods show an interesting correlation between the presence of tracheal lungs, which end in an open circulatory system, and tracheae that invade the tissue as in insects, and the presence or reduction of respiratory proteins. In arachnids a similar tendency is seen, and the most interesting developments were the (partial) replacement of a ‘perfectly good’ air-breathing organ (book lungs) by another one (tracheae).

Microanatomy of Early Devonian book lungs

The book lungs of an exceptionally preserved fossil arachnid (Trigonotarbida) from the Early Devonian (approx. 410 Myr ago) Rhynie cherts of Scotland were studied using a non-destructive imaging technique. Our three-dimensional modelling of fine structures, based on assembling successive images made at different focal planes through the translucent chert matrix, revealed for the first time fossil trabeculae: tiny cuticular pillars separating adjacent lung lamellae and creating a permanent air space. Trabeculae thus show unequivocally that trigonotarbids were fully terrestrial and that the microanatomy of the earliest known lungs is indistinguishable from that in modern Arachnida. A recurrent controversy in arachnid evolution is whether the similarity between the book lungs of Pantetrapulmonata (i.e. spiders, trigonotarbids, etc.) and those of scorpions is a result of convergence. Drawing on comparative studies of extant taxa, we have identified explicit characters (trabeculae, spines on the lamellar edge) shared by living and fossil arachnid respiratory organs, which support the hypothesis that book lungs were derived from a single, common, presumably terrestrial, ancestor.