The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): Evidence for homology and a single terrestrialisation event of a common arachnid ancestor

Scholtz, Gerhard; Kamenz, Carsten

doi:10.1016/j.zool.2005.06.003

Cited by 91 publications

(106 citation statements)

References 36 publications

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“…Overall, these fossil characters match in great detail the corresponding structures in both modern scorpions and tetrapulmonates (figure 1d,e; e.g. Scholtz & Kamenz 2006;Kamenz & Prendini in press). …”

Section: Resultssupporting

confidence: 59%

“…Hypotheses of respiratory organ evolution in spiders, including ways in which lung lamellae might have evolved into tracheal tubes, are summarized by Levi (1967). Second, a major controversy in arachnid evolution is whether their common ancestor was aquatic (Størmer 1976;Selden & Jeram 1989) or terrestrial (Scholtz & Kamenz 2006). The 'aquatic' hypothesis is based on the (disputed) notion that early scorpions were marine.…”

Section: Discussionmentioning

confidence: 99%

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Microanatomy of Early Devonian book lungs

et al. 2008

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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.

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Section: Resultssupporting

confidence: 59%

Section: Discussionmentioning

confidence: 99%

Microanatomy of Early Devonian book lungs

et al. 2008

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“…13 and 27, but see also ref. 28) and vertebrates (7) replaced gills with tracheae and lungs. This transition surely involved primitive lungs or analogous structures (27) that may have been inefficient for sufficient O 2 extraction at levels lower than present.…”

Section: Discussionmentioning

confidence: 99%

Confirmation of Romer's Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization

Ward

Labandeira

Laurin

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

133

104

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The first terrestrialization of species that evolved from previously aquatic taxa was a seminal event in evolutionary history. For vertebrates, one of the most important terrestrialized groups, this event was interrupted by a time interval known as Romer's Gap, for which, until recently, few fossils were known. Here, we argue that geochronologic range data of terrestrial arthropods show a pattern similar to that of vertebrates. Thus, Romer's Gap is real, occupied an interval from 360 million years before present (MYBP) to 345 MYBP, and occurred when environmental conditions were unfavorable for air-breathing, terrestrial animals. These model results suggest that atmospheric oxygen levels were the major driver of successful terrestrialization, and a low-oxygen interval accounts for Romer's Gap. Results also show that terrestrialization among members of arthropod and vertebrate clades occurred in two distinct phases. The first phase was a 65-million-year ( (1) indicates that arthropods, with species interpreted as fully land-based before 400 million years before present (MYBP) (2), preceded vertebrates onto land by tens of millions of years. The first body fossils identified as stegocephalians (limbed vertebrates) are known from strata Ϸ370 MYBP, such that the appearance of the limb with digits, the loss of the opercular apparatus, and the development of other characters that subsequently allowed a terrestrial lifestyle, presumably occurred during the 25-My interval between 385 and 360 MYBP (3, 4). Most of our understanding about these crucial vertebrate events comes from only a few freshwater deposits from Euramerican localities, with outcrops in Greenland producing the most prolific stegocephalian remains. Elginerpeton and Obruchevichthys were first, between 385 and 375 MYBP, followed several million years later by a modest radiation that included Ventastega, Ichythostega, Acanthostega, Tulerpeton, Metaxygnathus, and Hynerpeton. Although most of these taxa possessed limbs (although this is not certain for Elginerpeton and Obruchevichthys), all of these taxa have been interpreted as fully aquatic, rather than terrestrial (5-7). Their respiratory systems are poorly known, but osteology suggests that they were able to derive some amount of O 2 from water instead of being entirely air breathing (8). These stegocephalians disappeared soon thereafter, followed rapidly by rare appearances of limbed vertebrates. This temporal gap has long been called Romer's Gap, and until recently it was unknown whether this hiatus was due to a combination of unfavorable taphonomic conditions and collection failure or whether it represented an interval of intrinsically low diversity and an abundance of limbed vertebrates. Romer's Gap separates occurrences of the earliest (Late Devonian) aquatic stegocephalians from a much larger adaptive radiation that included the first terrestrial vertebrates that commenced during the Visean stage of the Early Carboniferous. Although new collections have partly filled Romer's Gap (9), including the d...

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“…Arthropod hemocyanins are composed of various subunits, each of which contains two copper moieties that reversibly bind oxygen molecules. In chelicerates, the presence of hemocyanins has been biochemically analyzed in horseshoe crabs (Xiphosura), spiders (Araneae), vinegaroons (Uropygi), tailless whip scorpions (Amblypygi), and scorpions (Scorpiones), all of which respire using book gills or book lungs, respiratory organs that are putatively homologous [26][27][28]. Most arachnids (terrestrial chelicerates) bear an archetypal 4 × 6 (24-mer) hemocyanin, whereas horseshoe crab hemocyanin consists of an 8 × 6 (48-mer) configuration [29].…”

Section: Introductionmentioning

confidence: 99%

Cross-bracing uncalibrated nodes in molecular dating improves congruence of fossil and molecular age estimates

Sharma

Wheeler

2014

Front Zool

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Introduction: The practice of molecular dating is an essential tool for hypothesis testing in evolutionary biology. Vagaries of fossilization and taphonomic bias commonly engender high uncertainty in molecular dating in taxonomic groups wherein few fossils can be unambiguously assigned to phylogenetic nodes. A recent and novel implementation in molecular dating, "cross-bracing", exploits gene duplications by formally linking calibrated node dates throughout the paralogous subtrees through hierarchical Bayesian models. An unexplored refinement of this method is cross-bracing nodes with unknown dates, in addition to calibrated nodes, such that all nodes representing the same cladogenetic events have linked priors. We applied such a refinement to molecular dating in chelicerates, one of the earliest groups of arthropods present in the fossil record, but whose molecular dating has been greatly inconsistent in the literature. We inferred divergence times using hemocyanin paralogs isolated from de novo assembled transcriptomic libraries, and multiple fossil calibrations. Results: We show that extending cross-bracing to uncalibrated nodes greatly reduced variance in estimates of divergence times throughout the phylogeny, particularly for estimated diversification ages of spiders and scorpions, whereas cross-bracing calibrated nodes alone did not affect age estimation for uncalibrated, derived clades. Comparing ages inferred with extended cross-bracing to the fossil record, we observe smaller gaps between diversification and the first appearance of crown group fossils than have previously been inferred, particularly for spiders. Our dating indicates that scorpions have a Silurian origin, but diversification of extant lineages occurred near the Triassic-Jurassic boundary, falsifying previous inference of Permian diversification age based on extant distribution alone. Conclusion: The significant reduction of variance in divergence time estimates upon extending cross-bracing to uncalibrated nodes makes this approach greatly suited for evolutionary inference in groups with poor fossil records, with particular reference to terrestrial arthropods.

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The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): Evidence for homology and a single terrestrialisation event of a common arachnid ancestor

Cited by 91 publications

References 36 publications

Microanatomy of Early Devonian book lungs

Microanatomy of Early Devonian book lungs

Confirmation of Romer's Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization

Cross-bracing uncalibrated nodes in molecular dating improves congruence of fossil and molecular age estimates

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