Adelophthalmus pyrrhae: A new species of Eurypterid 'Sea Scorpion' from the Carboniferous of Montagne Noire, France, which may have been capable of breathing air.

Arachnids are the second most successful terrestrial animal group after Insects and were one of the first Arthropod clades to successfully invade land. Fossil evidence for this transition is limited, with the majority of Arachnid clades first appearing in the terrestrial fossil record. Furthermore, molecular clock dating has suggested a Cambrian-Ordovician terrestrialization event for Arachnids, some 60million years before their first fossils in the Silurian, although these estimates assume that Arachnids evolved from a fully aquatic ancestor. Eurypterids or 'Sea Scorpions', the sister clade to terrestrial Arachnids, are known to have undergone major macroecological shifts in transitioning from marine to freshwater environments during the Devonian. Discoveries of apparently subaerial eurypterid trackways have led to the suggestion that Eurypterids were even able to venture on land and possibly breathe air. However, modern Horseshoe Crabs undertake amphibious excursions onto land to reproduce, rendering trace fossil evidence alone inconclusive.

In a paper published in the journal Current Biology on 10 September 2020, James Lamsdell of the Department of Geology and Geography at West Virginia University, Victoria McCoy of the Department of Geosciences at the University of Wisconsin-Milwaukee, Opal Perron-Feller of the Department of Geology at Oberlin College, and Melanie Hopkins of the Division of Paleontology (Invertebrates) at the American Museum of Natural History, present details of the respiratory organs of a new species of Eurypterid 'Sea Scorpion' from the Carboniferous of Montagne Noire, France.

The new species is placed in the genux Adelophthalmus, and given the specific name pyrrhae, after Pyrrha of Thessaly, daughter of Epimetheus and Pandora in Greek mythology, who along with her husband Deucalion cast stones that turned into babies to repopulate the earth after a great flood, which is a reference to the nodular mode of preservation of the holotype. It is described from a single specimen in the collection of the Hunterian Museum, University of Glasgow, (GLAHM) A23113, an almost complete specimen lacking the telson.

 

Photographs and Digital Segmentation of Adelophthalmus pyrrhae. (A) and (B) Photograph of the part (A) and counterpart (B) of the phosphatic nodule containing Adelophthalmus pyrrhae. (C) and (D) Digital segmentation of Adelophthalmus pyrrhae specimen in ventral (C) and left lateral (D) view. Labels show major aspects of the morphology, with Roman numerals indicating the prosomal appendage pair and Arabic numerals the body segment. Lamsdell et al. (2020).

The specimen is from the Lower Carboniferous (Middle to Late Tournaisian) Lydiennes Formation(?) of the St. Nazaire Group in the Montagne Noire region of France. Specific details about the source locality for the specimen are lacking; however, the Lydiennes Formation is the only geological unit in the region to produce fossil-bearing phosphatic nodules. The Lydiennes Formation is made up of black siliceous rocks, primarily described as radiolarian cherts, as well as black shales, and is characterized by abundant phosphate nodules, typically about
5 to 6 cm long, bearing exceptionally preserved, permineralized fossils. The localities of the Lydiennes Formation range from classic localities, interpreted as an offshore basin with well-formed nodules, to more recently described nearshore localities typically with poorly formed nodules. The fossils in the Lydiennes phosphatic nodules include Cephalopods, Arthropods, and abundant plants, which are in situ in the lower Lydiennes Formation.

The fossil is preserved within a phosphate nodule approximately 71 mm long and 55 mm wide and is visible where the nodule has been split medially, exposing the eurypterid along its dorsal plane. Almost the entire Eurypterid is preserved, with the exception of the telson. Externally, a portion of the book gills is visible on the sixth body segment, where the split has crossed through the operculum into the branchial chamber, revealing six overlapping lamellae that appear semicircular in shape attaching obliquely to the midline of the body. A more complete view of the eurypterid’s morphology is afforded through micro computed tomography scanning, permitting digital reconstruction of the entire specimen preserved within the nodule. This reveals details of the external ventral morphology, including prosomal appendages, the metastoma, genital appendage, and opercula, as well as the structure of the respiratory organs and gut. The specimen is interpreted as a carcass based on the retracted position of the prosomal appendages and the lack of opisthosomal curvature or telescoping.

 

Micro computed tomography scanning images of Adelophthalmus pyrrhae. (A) Lateral view along specimen midline. (B) dorsal view of specimen across the frontal plane. Enlarged images of proximal and distal trabeculae are shown in the lower right inset. Lamsdell et al. (2020).

All six pairs of prosomal appendages are preserved, including the chelicera, which are short and robust, and the distally expanded paddle of appendage VI. Appendages II–V all bear a pair of spines ventrodistally on each podomere; this, combined with the presence of postabdominal epimera and the lack of any lateral reduction in the anterior opisthosomal segment, indicates that Adelophthalmus pyrrhae has a close affinity to the American species Adelophthalmus mazonensis and Adelophthalmus mansfieldi. As in other Eurypterids, the mesosomal opisthosomal appendages of somites VIII–XIII are highly modified into broad, medially fused opercular plates that cover the entirety of the ventral sternites. The first two opercula are further fused into a single functional unit called the genital operculum, which bears the genital appendage. Posterior to the genital operculum are four more opercula, although the penultimate operculum, corresponding to the fifth dorsal tergite, is absent from the specimen and appears to have been lost due to taphonomic processes, potentially having broken off separately when the nodule was opened and subsequently been lost.

 

Digital segmentation of Adelophthalmus pyrrhae. (A) View of dorsal morphology. (B) Oblique view of ventral morphology. (C) Lateral view showing internal gut tract. The midgut is poorly preserved, but the morphology of the foregut and hindgut is clearly visible. Critically, the foregut is turned downwards to the ventrally oriented mouth, a position identical to that of aquatic feeding Xiphosurans. Lansdell et al. (2020).

The opercula enclose the book gills within a branchial chamber that is defined dorsally by the abdominal sternites. The opercula enclose the book gills within a branchial chamber that is defined dorsally by the abdominal sternites, indicating a total of five pairs of book gills in life, as in Xiphosura. The genital operculum bears only a single pair of book gills, located on the posteriormost of the two fused opercula, representing the appendages of somite IX. The book gills are horizontally oriented and fragmentary, with only the book gills of the sixth operculum preserved in their entirety; these are oval, attach close to the midline of the body, and consist of six lamellae. The number of lamellae in the anterior gills is unclear; however, the amount of fragmentary material within the branchial chamber indicates a higher lamella count and that these lamellae also bore trabeculae. Further evidence that the anterior book gills had more lamellae comes from a specimen of the Ordovician Eurypterid Onychopterella augusti that exhibits four sets of book gills (interpreted here as belonging to segments 2–5), each with 45 lamellae. The gills in Onychopterella were interpreted as being vertically stacked rather than horizontally oriented, as indicated by Adelophthalmus pyrrhae. This apparent difference, however, is taphonomic; the lamellae of Adelophthalmus pyrrhae are deflected into a more vertical orientation laterallyby the curvature of the opercula, and specimens of the Cretaceous Xiphosurid Tachypleus syriacus show that the lateral margins of the book gills can be preserved so as to appear vertically stacked. Although the gill macrostructure is Xiphosuran in appearance, the microstructure is markedly Arachnid in nature. The dorsal surface of each lamella is covered with regularly spaced 0.15-mm-tall, 0.05-mm-wide pillar-like trabeculae projecting up into the media space between lamellae, with a clear hemolymph space within each lamella. Trabeculae are commonly found in pulmonate arachnids and are a terrestrial adaptation for air breathing, serving to keep the lung lamellae from collapsing together and eliminating the media space, which would suffocate the organism. Trabeculae are absent in Horseshoe Crabs, the gills of which collapse out of water and are not efficient at air oxygen transfer, rendering them incapable of subaerial breathing, nor have trabeculae been described in any of the fossil Xiphosurans or stem Euchelicerates preserving gills. The presence of trabeculae in Adelophthalmus pyrrhae is therefore direct evidence that Eurypterids were able to breathe in subaerial environments through their main respiratory organs. The trabeculae exhibit regular spacing and possess a morphology comparable to the trabeculae found in arachnids, which comprise a conical base extending into a narrow pillar. The majority of the trabeculae within the specimen are represented by the broad conical base, with very few retaining the pillar structure; however, this preservation is identical to that of the trabeculae in an exceptionally preserved Devonian Trigonotarbid, which also preferentially preserves the base of the trabeculae but preserves the pillars in irregular shapes and widths. When sufficiently preserved, the trabeculae of Adelophthalmus pyrrhae exhibit a differentiation into anterior proximal trabeculae attached to both lamellar surfaces and posterior distal trabeculae attached only to the dorsal surface of the ventral lamella, a distribution also observed in modern Arachnids.

 

Respiratory Organs in Adelophthalmus pyrrhae and Other Chelicerates. (A) Digital segmentation showing the location of the preserved gill lamellae. (B) Anterodorsal view of gill lamellae above the opercula. (C) Scan image of Adelophthalmus pyrrhae showing lamellae with trabeculae of the sixth body segment in lateral view. (D) Scan image of Adelophthalmus pyrrhae showing trabeculae of lamellae located on the fourth and sixth body segments in dorsal view. (E) Scan image of transverse cross section of Adelophthalmus pyrrhae showing fragments of the lamellae of the third body segment displaying trabeculae. (F) Digital segmentation of the lamellae of book gills of Adelophthalmus pyrrhae located on the sixth body segment. (G) and (H) Digital segmentation showing the trabeculae on two lamellae of Adelophthalmus pyrrhae book gills located on the sixth body segment. (I) Scanning electron microscope image showing the book gills of the extant Xiphosurid Limulus polyphemus. The trabeculae-like structures visible inside the hemolymph space are pillar cells, which are also found in arachnid book lungs. (J) Scanning electron microscope image showing the book lungs of the extant Spider Aculepeira ceropegia. (K) Scanning electron microscope image showing book lungs of the extant Scorpion Euscorpius carpathicus. (L) Digital segmentation of the book lungs of the Devonian Trigonotarbid Arachnid Palaeocharinus sp. Landsell et al. (2020).

Eurypterids are known to utilize a dual respiratory system, with gills on the opercula supplemented by vascular structures located on the ventral surface of the body wall termed Kiemenplatten. These Kiemenplatten have been tentatively suggested to act as ancillary respiratory structures for putative amphibious excursions. The occurrence of trabeculae on the book gills indicates that these too were active respiratory organs in air and confirms that Eurypterids were fully capable of persisting in terrestrial environments for extended periods. The low number of respiratory lamellae in the posterior book gills of Adelophthalmus pyrrhae is puzzling but may be a desiccation resistance strategy to reduce overall surface area while promoting subaerial gas exchange as seen in amphibious and terrestrial Crustaceans. Interestingly, amphibious Crustaceans also maintain some gills with a higher surface area for aquatic respiration. Despite these adaptations for subaerial breathing, Eurypterids had a predominantly aquatic life habit, as indicated by the diversity of species (including Adelophthalmus pyrrhae) with their posterior pair of prosomal appendages modified into a broad swimming paddle and their abundant aquatic fossil record. It has also been suggested that the Eurypterid’s method of masticating food via appendicular gnathobases would have been unable to function on land, thereby limiting the amount of time that Eurypterids could have spent out of their usual aquatic environment. Instead, the semi-terrestriality may have allowed Eurypterids to move between ephemeral pools to reproduce in sheltered creche environments, as indicated by the spatial segregation between adults and juveniles observed in the fossil record. Further support for this interpretation comes from the discovery that eurypterids, like Arachnids, possessed spermatophores. Spermatophore-mediated reproduction may have permitted female eurypterids to store sperm for up to several months as in modern Arachnids, permitting time for migration to creche environments to reproduce after mating. The presence of spermatophores also opens up the possibility that Eurypterids were capable of transferring sperm in terrestrial environments.

 

Respiratory Organ Structures in Eurypterids and Other Chelicerates (A) Reconstruction in lateral cross section of the respiratory system of Eurypterids as exemplified by Adelophthalmus pyrrhae. (B) Inferred evolution of terrestrialisation and respiratory structures in Euchelicerates, with simplified phylogeny for a monophyletic Arachnida. (C) Alternative hypothesis for the evolution of terrestrialisation and respiratory structures in Euchelicerates with a polyphyletic Arachnida. Note that, in this scenario, spermatophores would have to be secondarily lost in Xiphosura. Landsell et al. (2020).

Molecular divergence estimates indicate that Arachnids occupied terrestrial environments during the early Ordovician or late Cambrian. Until now, such a time frame for terrestrialisation would have required an almost saltationist transition from an aquatic to terrestrial life habit. Some Silurian Scorpions have been proposed to be aquatic and exhibit a stepwise acquisition of terrestrial characteristics; however, this would necessitate two terrestrialisation events within Arachnida, and the aquatic nature of these Scorpions has been debated. Similar disconnects between molecular estimates and the fossil record of myriapods were recently resolved by the recognition that the aquatic Cambrian-Triassic Euthycarcinoids are stem Myriapods. Similarly, the solution to the discrepancies in the projected and observed timing of Arachnid terrestrialisation may lie within their stem lineage. The discovery of air-breathing adaptations in the Eurypterids, the Arachnid sister group, indicates that terrestrial adaptations accrued in a stepwise pattern along the Arachnid stem lineage, culminating in the modifications for preoral digestion, including a preoral cavity formed from the basal articles of the pedipalp and anteroventrally directed mouth that characterise Arachnids (which Adelophthalmus pyrrhae lacks). Critically, the occurrence of subaerial breathing can be inferred across all Eurypterids based on trackway evidence of terrestrial excursions in Stylonurina; the occurrence of Kiemenplatten across Eurypterida, including records from the early Silurian; and the morphological evidence from Adelophthalmus pyrrhae, indicating that terrestrial adaptations were likely inherited from the common ancestor of Eurypterids and Arachnids. The Cambrian-early Ordovician ancestor of Arachnids and Eurypterids would therefore have been semi-terrestrial, corresponding to the molecular clock estimates for terrestrialisation within the group, with the radiation and diversification of Arachnids occurring fully within a terrestrial setting.

 

Artistic reconstruction of Adelophthalmus pyrrhae. Individuals of Adelophthalmus pyrrhae undertake amphibious excursions around freshwater pools in a Carboniferous forest. While the structure of the respiratory organs indicate that Eurypterids were capable of respiring on land, the external morphology, including the expanded swimming paddle, is indicative of a predominantly aquatic mode of life. Lansdell et al. (2020).

Recent molecular phylogenetic work has suggested that Xiphosurans are in-group Arachnids and are secondarily aquatic, but has been rebutted based on further molecular analyses and assessment of whole-genome duplication events. Eurypterids have not been considered in these studies and were assumed to have a life habit similar to Horseshoe Crabs. As such, our revised understanding of Eurypterid respiration has important ramifications for the suggestion that Horseshoe Crabs (and Eurypterids) are secondarily aquatic. The semi-aquatic nature of Eurypterids could be indicative of a lineage in the process of either leaving or returning to the water; however, other aspects of their morphology, including the lack of terrestrial feeding capabilities and the absence of paired apoteles, are more indicative of an organism with greater affinity to the aquatic rather than terrestrial realm. Crucially, the ancillary respiratory Kiemenplatten, which would not have functioned in subaqueous media, are distinct to any respiratory structure in Arachnida. This strongly indicates that Eurypterids were experimenting with modes of terrestrial respiration and were in the process of terrestrialising rather than returning to aquatic environments. This in turn suggests that Horseshoe Crabs evolved from fully aquatic ancestors. Assuming a single terrestrialisation event for Arachnida therefore necessitates that non-pulmonate Arachnids lost their book lungs, with tracheae evolving multiple times among non-pulmonates, as indicated by their occurrence on different body segments in different groups. Alternatively, Arachnids may have invaded land multiple times; however, this scenario still necessitates that non-pulmonates lost their respiratory lamellae and independently developed tracheae. Nevertheless, the discovery of trabeculae in the book gills of Eurypterids demonstrates that terrestrialization in at least pulmonate Arachnids occurred as the final step of a protracted series of character acquisitions within the Arachnid stem lineage and that eurypterids represent a truly unique example of semiterrestriality as part of a broader evolutionary trajectory toward the invasion of land.

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Undestanding the evolution of feeding apparatus within the Euchelicerata.

The origin of Euarthropoda, including the extant groups Myriapoda, Insecta, Eucrustacea, and Chelicerata and different fossil representatives, lies more than half a billion years ago. In this long time, an enormous species richness and morphological diversity evolved in the different ingroups. Within Euarthropoda, the lineage of Chelicerata is often somehow treated as the more ‘basal’ or ‘primitive’ side of the tree and is thought to be more ancestral, especially in comparison to Mandibulata, the other major lineage within Euarthropoda. This view is most extremely applied to Xiphosurida (Horseshoe ‘Crabs’) but also to now extinct groups such as Eurypterida (Sea Scorpions) or the Spider-like group of Trigonotarbida. Horseshoe ‘Crabs’ (though the old fashioned ‘Sword Tails’ would be less ambiguous) have often been treated as ‘living fossils’ (a very unscientific term). They have also been assumed to be a kind of proxy for the early terrestrialisation within Euchelicerata. Yet, this interpretation is most likely incorrect. It is unlikely that the stem species of Euchelicerata was already amphibious, hence the terrestrial behaviour of modern representatives of Xiphosurida has most probably evolved independently. It needs to be emphasised that modern representatives of Xiphosurida are not direct proxies for the ancestor of Euchelicerata, but possess their own specialisations (as all living groups do). 

One reason why the lineage of Chelicerata is assumed to be primitive might be the organisation of the feeding apparatus in most representatives. In different textbooks, the impression is given that these forms lack ‘proper’ mouthparts, while ingroups of Mandibulata have a ‘full’ set of mouthparts. One important German text book states that representatives of Chelicerata bear structures for acting in feeding but would lack true antagonistic jaws. He also states that mostly only the second pair of appendages and rarely the third and fourth one is incorporated in the feeding apparatus in most forms. This statement most likely refers to the state in Scorpions and other arachnids, but appears to ignore the state in Xiphosurida where appendage pairs 1–7 are involved in the feeding apparatus. In other cases the description of the feeding apparatuses appears to refer to only certain ingroups. For example the statement that there are always three pairs of mouthparts in Mandibulata is clearly correct for Insecta, but ignores maxillipeds in Chilopoda or Decapoda, or complex thoracic feeding apparatuses as for example in Branchiopoda (Fairy Shrimps). Hence, such textbook statements are at best oversimplified and tend to be based more on general assumptions than on direct observations.

In a paper published in the journal PeerJ on 13 August 2020, Carolin Haug of the Department of Biology and GeoBio-Center at Ludwig-Maximilians-Universität München, provides functional morphological interpretations of the feeding apparatuses (i.e. all external structures involved in feeding) of two supposedly ‘primitive’ Chelicerate groups, namely of Eurypterida and of Trigonotarbida and present them in the context of evolution in Euchelicerata. With this, she aims at providing a framework to evaluate the presumed ‘primitiveness’ of the feeding apparatuses of modern representatives of Euchelicerata.

For this study, fossil material from different museum collections was investigated, including the invertebrate palaeontology collection of the Yale Peabody Museum of Natural History, New Haven, the Natural History Museum, London, the Naturhistoriska riksmuseet, Stockholm, the Harvard Museum of Comparative Zoology, Cambridge, Massachusetts, and the Royal Ontario Museum, Toronto. Every specimen of Eurypterida and Trigonotarbida in these collections was briefly inspected, and those preserving morphological details of interest for this study were documented.

The specimens of Eurypterida in the Yale Peabody Museum of Natural History collections had been collected by a private collector, Samuel Ciurca, from late Silurian deposits in New York State, USA, and southern Ontario, Canada, and donated by him to the Yale Peabody Museum; it is by far the largest collection of Sea Scorpions worldwide. The Sea Scorpions in the Natural History Museum collections originate from different late Silurian deposits: few specimens come from New York State and from Scotland. Also one Sea Scorpion from the Harvard Museum of Comparative Zoology collections comes from the Silurian of Scotland. Most specimens in the Natural History Museum collections come from Estonia, more precisely from the village Rootsiküla on the island of Saaremaa (also called Ösel). From the same Estonian locality, also many specimens of Eurypterida in the Naturhistoriska riksmuseet collections and most in the Harvard Museum of Comparative Zoology collections originate, as well as from the island of Gotland, Sweden. The specimens from Saaremaa/Ösel and Gotland are insofar exceptional as of most of these the surrounding limestone matrix had been dissolved already in the 19th century by Gerhard Holm, resulting in isolated specimens with only their cuticle being preserved. Subsequently, the specimens had either been mounted between two large cover slips, or between a microscopic slide and a cover slip (dry or with Canada balsam), or they have been fully embedded in resin. All these methods allow to access dorsal as well as ventral structures.

The specimens of Trigonotarbida in the Royal Ontario Museum collections come from the Upper Carboniferous Mazon Creek, Carbondale Formation, IL, USA. The Natural History Museum collections houses specimens of Trigonotarbida preserved in Rhynie Chert, Lower Devonian of Scotland, the rest of the material stems from the British Coal Measures, Upper Carboniferous. 

Comparative material of extant species came from the former teaching collection of the University of Ulm (now at the University of Rostock) and the teaching collection of Ludwig-Maximilians-Universität München.

The appendages of seven segments clearly contribute to the feeding apparatus in Eurypterida: chelicerae, five subsequent pairs of legs (often called walking legs), and the plate-like appendage pair of the seventh post-ocular segment, the metastoma. The appendages are arranged in a circle around the central area of the feeding apparatus, with their median parts being very close together. The basipods (coxae in chelicerate terminology) of the appendages of post-ocular segment 6 (the leg pair right in front of the metastoma) are much larger than those of the other appendages, forming roughly a rectangle, but additionally with a pronounced endite. The metastoma covers part of these basipods as well as the median gap between the left and right appendage.

 

Feeding apparatus of YPM_IP_216689, Eurypterus lacustris (Eurypteridae, Eurypterida), Ontario, Welland County; images colour-inverted to enhance contrast. (A) Overview. (B)–(G) Close-ups. (B) Stout spine on appendage 2. (C) Spines and setae on appendages 3 and 4. (D) and (E) Surface ornamentation on basipods. (F) Setae on appendages 2 and 3. (G) Spines and setae on (presumably) appendages 4 and 5. Haug (2020).

Post-ocular appendages 2–6, that is all post-cheliceral legs, bear a more or less pronounced armature on the endites protruding from the median edges of their basipods. The armature differs between the appendages. The spines on some of the basipods (probably of the further anterior ones, but there appear to be species-specific differences) are thinner than on others. The basipods of post-ocular appendage 6 bear the stoutest spines, the entire basipodal median edge appearing strongly sclerotised, recognisable from its very dark colour.

 

Feeding apparatus of NHM I3406_2, Eurypterus fischeri (Eurypteridae, Eurypterida), Rootsiküla, Saaremaa, Estonia. (A) Overview. (B) Stereo image of central area, colour-inverted; use red-cyan glasses to view. (C) Colour-marked version of one half image of B; pink, chelicerae and setae; blue and green, basipods of appendages 2–6; cyan, metastoma (appendage 7); orange, spines. Abbreviations: a3–a7, post-ocular appendages 3–7. Haug (2020).

Also the armature on the same basipod is differentiated (also here with species–specific differences). The spines closer to the anterior edge of the basipod (in relation to the orientation of the body of the animal) are stouter and partly also longer, while those closer to the posterior edge of the basipod are thinner and smaller. This differentiation can be very pronounced, with very stout and large teeth, elongate and pointed spines, and thin setae on the same basipod. The armature on the median edge of the basipods can occur in two (or possibly three?) rows. The remaining surface of the basipods can be covered with setae of other surface structures.

 

Feeding apparatus of NRM Ar 35344, Eurypterus fischeri (Eurypteridae, Eurypterida), Rootsiküla, Saaremaa, Estonia. (A) Overview. (B) Close-up of median edges of basipods. (C) Further close-up of the differentiated armature of the basipods. Haug (2020).

In Trigonotarbida, the appendages of three segments contribute to the feeding apparatus: chelicerae, pedipalps and first pair of walking legs. The proximal parts of these appendages sit close together. The pedipalps are proximally armed with a row of short spines. The basipods of the first pair of walking appendages bear a prominent endite medially, which again bear setae. The endites are in some fossils positioned very closely together, in others further apart, which may point to a high movability during life. Additionally, there are two distinct oval fields of densely arranged short setae next to each other in the area between chelicerae and pedipalps. Another less distinct field of similar setae appears to be positioned slightly posteriorly to the two oval fields. Based on the three-dimensional position information, these fields are probably situated on the hypostome (though often termed ‘labrum’).

 

Feeding apparatus of Eurypterus fischeri (Eurypteridae, Eurypterida), Rootsiküla, Saaremaa,Estonia. (A) and (B) NRM Ar35343. (A) Overview over central area. (B) Close-up of median edges of basipods with differentiated armature and very strongly sclerotised edges of post-ocular appendage 6. (C) and (D) NRM Ar48883. (C) Overview over anterior part of feeding apparatus; posterior part not preserved. (D) Close-up of differentiated armature on basipods, including broader and blunt teeth, pointed spines of different sizes and thin setae. Haug (2020).

While Haug's study focused on the feeding apparatus of different groups of Euchelicerata, a proper character polarisation demanded an outgroup comparison. For this purpose it wss especially important to include now extinct groups as those may exhibit character states no longer present in the extant fauna.

 

Parts of feeding apparatuses of Eurypterida. (A)–(C) MCZ PALI 131326, Erettopterus bilobus (Pterygotidae, Eurypterida), Lesmahagow, Lanarkshire, Scotland. (A) Overview of a series of basipods with pronounced armature and metastoma. (B) Colour-marked version of (A). (C) Close-up of basipod armature with differentiation between different basipods; colour-inverted to enhance contrast. (D)–(F) Isolated leg of post-ocular segment 6 of MCZ PALI 185687, Erettopterus osiliensis (Pterygotidae, Eurypterida), Saaremaa, Estonia. (D) Overview; note pronounced endite with spines. (E) Close-up of spines. (F) Close-up of surface structure of basipod. Haug (2020).

The supposed sister group to Euchelicerata is Pycnogonida (Sea Spider), these together forming the Chelicerata. While being quite speciose today, the general body organisation is the same in all extant species of Pycnogonida, with a highly reduced posterior body area (the terms pro- and opisthosoma cannot be applied) and a strongly modified feeding apparatus adapted to suctionfeeding. The fossil record of the Pycnogonida dates back to the Cambrian, so more than half a billion years ago. However, as already at this time the morphology appears derived (and partly also as the Cambrian representatives of Pycnogonida are exclusively larvae), it does not provide relevant information about the evolution of the feeding apparatus in the lineage towards Euchelicerata. It is necessary to take a look at the feeding apparatus in supposed early representatives of Megacheira, the so-called ‘short great-appendage Arthropods,’ among which the sister group to Chelicerata is assumed by some authors. 

 

Isolated basipod, presumably of leg of post-ocular segment 6, of NRM Ar31829, undetermined representative of Eurypterida, Visby, Gotland, Sweden. (A) Overview. (B) Close-up of spines; note different spine sizes and arrangement in different rows. (C) Further close-up of smaller spines with apparent row arrangement. Haug (2020).

Recent reinvestigations of different of these species as well as older publications provide a sound basis for the reconstruction of the feeding apparatus in the ground pattern of Megacheira. At this evolutionary stage, the entire set of appendages was included into the feeding apparatus (possibly including the hypostome). While the first pair of appendages was specialised for grasping the prey, the second to last pair of appendages all exhibit the same general morphology, serving for swimming and feeding at the same time. While slight modifications in the size of the second appendage pair of Leanchoilia superlata might indicate a starting specialisation to a mouthpart, the ‘whole-body-feeding’ method represents the original condition in Megacheira and presumably in Chelicerata.

 

Feeding apparatus of NHM In24671, Palaeocharinus sp. (Trigonotarbida), Rhynie Chert, Scotland. (A)–(C) Stereo images, use red-cyan glasses to view. (A) Overview of entire specimen. (B) Same as (A), but with background virtually removed. (C) Close-up of feeding apparatus. (D) Colour-marked version of one half image of (C). Abbreviations: a3, appendage of post-ocular segment 3; ch, chelicera; ed, endite; pp, pedipalp; st, setae. Haug (2020).

This also holds true if assuming that short great-appendage Arthropods branched off earlier along the evolutionary lineage. The polarisation of characters remains the same. Also several other early representatives of Euarthropoda possess similar characters in their feeding apparatuses, most prominently opposing basipods with strong spines, but are not discussed further by Haug.

 

Parts of feeding apparatuses of Trigonotarbida. (A)–(E) Palaeocharinus sp., Rhynie Chert, Scotland. (A) and (B) NHM RC_019; ventro-lateral view on feeding apparatus. (B) Colour-marked version of one half image of (A). (C) and (D) NHM In27357; cross section through body at position of first walking appendages (appendages of post-ocular segment 3) with prominent endites. (D) Close-up of endites of (C). (E) NHM In24687; close-up of endite of first walking appendages. (F)–(I) NHM In31241, Trigonotarbus johnsoni, Coal Measures, UK. (F) and (G) Overview of entire specimen. (H) Stereo image of feeding apparatus. (I) Colour-marked version of one half image of H. Images (A), (C)–(E), (G) and (H) are stereo images, use red-cyan glasses to view. Abbreviations: a3, appendage of post-ocular segment 3; ch, chelicera; ed, endite; pp, pedipalp. Haug (2020).

The feeding apparatus of Pycnogonida is adapted to suction feeding and highly derived already in the fossil forms. This specialised feeding apparatus is an autapomorphy of Pycnogonida.

In Euchelicerata the systematic affinities are still in a certain state of flux and the feeding apparatus cannot be properly reconstructed for all early fossil representatives. The feeding apparatus and in general the tagmosis pattern can be reconstructed to a certain extent for the species Offacolus kingi, Dibasterium durgae, and Weinbergina opitzi, successively splitting off the evolutionary lineage towards the remaining representatives of Euchelicerata.

 

Feeding apparatus of ROMIP45532, undetermined Trigontarbidan, Mazon Creek, USA. (A) and (B) Overview of entire specimen. (B) and (C) Stereo images, use red-cyan glasses to view. (C) and (D) Close-up of feeding apparatus and further walking appendages. (D) Colour-marked version of one half image of (C). Abbreviations: a3–6, appendages of post-ocular segments 3–6; ch, chelicera; ed, endite; pp, pedipalp; ste, sternum. Haug (2020).

At the level of Euchelicerata, a characteristic division into an anterior and a posterior tagma usually termed prosoma and opisthosoma appears for the first time, supposedly as an autapomorphy for this group. The subdivision into these two distinct tagmata is characterised by dorsal and ventral structural changes.

 

Feeding apparatus of NHM In24702, Palaeocharinus sp. (Trigonotarbida), Rhynie Chert, Scotland. (A) and (B) Overview. (A) Stereo image. (B) Colour-marked version of one half image of (A). (C) and (D) Close-up of fields with setae. (C) Stereo image. (D) Colour-marked version of one half image of (C); red, chelicerae; green, pedipalps; blue, first walking appendages; yellow , fields with setae. Haug (2020).

Dorsally, the segments of the anterior tagma form a uniform shield without any visible segmental borders. The segments of the posterior tagma possess separate tergites in the ground pattern of Euchelicerata. Ventrally, the tagmatisation is characterised by a ‘division of labour’ between the different appendages. While in short great-appendage Arthropods all appendages were still involved in feeding, in the ground pattern of Euchelicerata the feeding apparatus becomes shorter; only the appendages of the anterior tagma contribute to the feeding apparatus, in addition to their locomotory (walking) function. The more posterior appendages serve for swimming; if they also possessed structures for oxygen exchange remains currently unclear.

 

Coarse phylogenetic overview of the groups discussed. Haug (2020).

The appendage of post-ocular segment 7 (the pre-genital segment) differs morphologically in Offacolus kingi, Dibasterium durgae, and Weinbergina opitzi, being significantly smaller in the first two species. Yet, as Weinbergina opitzi possesses an appendage on this segment similar to the preceding ones with apparently locomotory function, this was presumably the ground pattern condition for Euchelicerata. Hence, the feeding apparatus in the ground pattern of Euchelicerata most likely consists of (possibly the hypostome and) chelicerae and six pairs of walking appendages.

 

Schemes of feeding apparatuses and general body organisation in the ground pattern of different evolutionary levels. (A) Megacheira. (B) Euchelicerata. (C) Neochelicerata. Grey background shadings mark different tagmata. Colour coding: black = appendages of first post-ocular segment (great appendages resp. chelicerae) and hypostome (‘labrum’); dark grey, basipod; light grey, endopod; white. exopod and (possibly) limbless segments. Presence of specific respiratory structures not known for the ground patterns of Megacheira and Euchelicerata. Haug (2020).

Neochelicerata is an ingroup of Euchelicerata, the ‘crown group’ (most inclusive group with extant representatives). It has been characterised as certain aspects of body organisation have not evolved in Euchelicerata yet, but are present in the ground pattern of Neochelicerata. The ground pattern condition of Neochelicerata is mainly reconstructed based on the morphology of Xiphosurida. 

The body organisation in general and the feeding apparatus in particular are very similar in the ground pattern of Neochelicerata to that of Euchelicerata. Also here the anterior tagma dorsally bears a uniform shield. The tergites of the posterior tagma are fused into an entire dorsal shield, the thoracetron, in Xiphosurida. However, this condition appears to be an autapomorphy of Xiphosurida, while in the ground pattern of Neochelicerata the tergites were most probably still separate.

Also ventrally, the ground pattern condition of Neochelicerata is largely the same as that of Euchelicerata. The appendages of the anterior tagma, (possibly the hypostome and) chelicerae and the following six pairs of appendages, are incorporated into the feeding apparatus. However, the last of these appendage pairs, the chilaria (appendages of the pre-genital segment or post-ocular segment 7), consists of only the shovel-shaped most proximal part (basipod in neutral euarthropodan terminology, usually called coxa in Chelicerate terminology); the walking part (endopod) is lacking. With this, the appendages of post-ocular segment 7 no longer perform a combined feeding-and-walking function, but instead close the feeding apparatus from its posterior end to reduce the loss of food in Xiphosurida. This condition is possibly already present earlier as it looks very similar in a species splitting off the evolutionary lineage before the node of Neochelicerata, Venustulus waukashensis. Therefore, in the ground pattern of Neochelicerata (or slightly earlier) the feeding apparatus became further specialised, consisting of (possibly the hypostome,) chelicerae, five pairs of walking appendages and chilaria.

The exact relationships of Eurypterida, Arachnida, Xiphosurida, and other exclusively fossil groups such as Chasmataspidida are still not entirely The feeding apparatus of Eurypterida (and possibly already of Metastomata if this is a natural group) shows a stronger specialisation than that in the ground pattern of Neochelicerata, but is still composed of (possibly the hypostome and) the appendages of the same segments (chelicerae, following five pairs of appendages, metastoma). The further posterior segments are also here not involved in feeding or locomotion; the corresponding appendages most probably became (partly) internalised and fulfilled respiratory function.

 

Feeding apparatuses of different extant representatives of Arachnida. (A) Araneae. (B) Amblypygi. (C) Schizomida. (D) Thelyphonida. (E) Phalangida (Opiliones). (F) Cyphophthalmi (Opiliones). (G) Solifugae. (H) Pseudoscorpiones. (I) Palpigradi. (J) Ricinulei. (K) Mesostigmata (Acari). (L) Ixodoidea (Acari). Haug (2020).

Also in Sea Scorpions, feeding and locomotion appears to be performed by the same appendages. However, Paul Seldon, who described the functional morphology of Eurypterus tetragonophthalmus in great detail, assumed that only the posterior appendages were used for locomotion to avoid coordination problems between the differently long appendages (though this assumption does not have to account for all species of Eurypterida due to their morphological differences). He also assumed that there is a task differentiation in food handling between the anterior and posterior legs, the anterior ones gathering food, while especially the last pair crushed hard food particles. This differentiation is corroborated by the specimens investigated in this study, as the basipods of the different appendages are equipped with different types of teeth on their median edges, best visible when (almost) the entire feeding apparatus is preserved in situ. In some specimens the teeth on the basipods of the further anterior appendages are thinner and appear less robust than those on the basipods of the fifth (last) pair of walking legs (appendage pair of post-ocular segment 6). The antero-median edges of the latter are equipped with strong teeth and reach under the metastoma. They are also significantly elongated in anterior-posterior axis, probably to achieve a larger biting force. With this, sea scorpions possessed fully functional antagonistic jaws comparable to the condition in many Crustaceans, but convergently evolved.

In addition to the differentiation of armature on the basipods of different appendages, on the same basipod the armature is also differentiated. The teeth further anterior on the median edge of the basipod appear stronger than the further posterior ones on the same basipod. Paul seldon described this differentiation for Eurypterus tetragonophthalmus, and discussed that some of the teeth or spines would have been movable while others were not. The presence of movable teeth may be species specific based on the observations in this study, but the general pattern of differentiated armature on the same basipod apparently occurs in different species of Eurypterida. This differentiation appears very similar to the situation in Mandibulata, in which the mandibles bear the pars incisivus and the pars molaris, that is two regions with rather different armature. Apparently, also this specialisation evolved convergently.

The metastoma (appendage of pre-genital segment or post-ocular segment 7) in representatives of Eurypterida basically fulfils the same function as the chilaria in representatives of Xiphosurida, it closes the feeding apparatus from posteriorly. Yet, in Sea Scorpions this is only a single plate (but which can have various shapes), so most probably the conjoined basipods of formerly free appendages. Some species show a notch in the anterior area of the metastoma, which may represent a remnant of the not completed fusion process. Unfortunately, no extremely early ontogenetic stages are preserved (late embryos to hatchlings, at least not well enough to allow investigation of the development of the metastoma.

In addition to the closing of the feeding apparatus, the metastoma appears to provide a kind of guide rail for the movements of the basipods of the appendage pair right in front of it. This function is comparable to that of the paragnaths in Eucrustaceans, which are elevations of the sternite of the mandible segment and guide the movement of the mandibles/ Again, this morphological similarity evolved most likely convergently. 

The condition of the metastoma as a single plate and its covering of the proximal area of the posterior appendages leads to a more tightly closed feeding apparatus in comparison to that in Xiphosurida and the ground pattern condition of Euchelicerata. Considering that representatives of Eurypterida may have had an amphibious lifestyle, a more closed feeding apparatus could have been a predisposition for going on land, as food may get lost more easily on land than in the water, where it sinks slower when it is not grabbed tightly enough. The specialised feeding apparatus of Sea Scorpions in its highly differentiated morphology is probably best interpreted as an autapomorphy of Eurypterida or even of an ingroup.

In the following, Scorpions are taken as a first example for Arachnida. Scorpions have been assumed to be the sister group to the remaining groups of Arachnida. Yet, in recent studies, Scorpions resulted as sister group to Megoperculata; in these analyses Sea Sorpions were not included (which was mostly not possible due to the type of analysed characters). This deep ingroup position of Scorpions may be an artefact resulting from the lack of proper character polarisation due to the absence of Eurypterida, but this problem cannot be further discussed here.

In Arachnida, the posterior border of the feeding apparatus lies further anteriorly than in the previously discussed groups. In modern Scorpions (Scorpiones), only the first four appendage-bearing segments (and possibly the hypostome) are involved in the feeding apparatus: chelicerae, pedipalps, and two pairs of walking appendages. The basipods of these two pairs of walking appendages are antero-medially elongated into a pronounced endite, which reaches far anteriorly, closing the feeding apparatus from the posterior end. The median areas of the basipods of walking appendage pairs 3 and 4 are oriented almost anteriorly, but apparently not included into the feeding apparatus. Also the sternum, most likely the embryonically fused appendages of the seventh post-ocular (pre-genital) segment, is oriented anteriorly, but not involved in the feeding apparatus. Dorsally, the shield extends further posteriorly, including the segments bearing chelicerae, pedipalps, all walking appendages and possibly also the sternum-bearing segment. Hence, the posterior border of the feeding apparatus in Scorpiones no longer corresponds to the posterior border of the dorsal shield, in contrast to the presumed ground pattern condition in Euchelicerata, Neochelicerata, and Metastomata.

However, the condition of the feeding apparatus in modern Scorpions differs from that in early fossil Scorpions. In early Scorpions, the feeding apparatus extends posteriorly only to the pedipalps. The walking appendages do not bear enditic protrusions, hence do not appear to have been involved in the feeding process. If this condition is the ground pattern condition of Scorpionida, the group including Scorpiones and different fossil Scorpions, the feeding apparatus in modern Scorpions would be an autapomorphy of Scorpiones.

In Trigonotarbida, the Chelicerae, pedipalps and first pair of walking appendages contribute to the feeding apparatus. The basipods of the pedipalps and especially of the first pair of walking appendages possess endites medially, which were probably used for food manipulation. This condition is unknown from other Arachnids.

The phylogenetic position of Trigonotarbida is still unclear. In different analyses, they have already resolved, for example, as sister group to Ricinulei or as closely related to Megoperculata. Similarities to the one respectively the other group occur, for example, in the filtering structures on the mouthpart, details on the pedipalps, or the general body organisation.

The feeding apparatus does not provide clear arguments for placing Trigonotarbida near the one or the other group of Arachnida. In most representatives of Arachnida, the feeding apparatus only consists of (possibly a hypostome,) chelicerae and pedipalps. In some of them, the basipods of the pedipalps are more or less closely connected medially. The basipods of the pedipalps are in many Web Spiders involved in the feeding process, using median projections for mastication (sometimes referred to as gnathocoxae or maxillae). In certain cases, a lower lip contributes to the feeding apparatus from posteriorly. In some groups, all these structures form a single, tightly connected unit. If this short condition of the feeding apparatus would be present in all representatives of Arachnida besides Trigonotarbida, two options for the ground pattern of Arachnida would be possible: either the feeding apparatus of Trigonotarbida would represent the ground pattern condition of Arachnida, or the very short condition of the other representatives of Arachnida would be the ground pattern condition and Trigonotarbida autapomorphically elongated the feeding apparatus.

However, the entire situation is more complicated due to the feeding apparatus of Opiliones (Harvestmen). In Harvestmen, the feeding apparatus includes also the first pair of walking legs, which bears endites on the basipods. Also the second pair of walking legs bears endites, at least in certain Harvestmen, which may have a supporting function in the feeding process. The presence of a preoral chamber, stomotheca, formed by all these endites in Opiliones and Scorpionida has led to the suggestion a sister group relationship between these two groups (together forming Stomothecata). The endites of the first pair of walking appendages in Harvestmen look rather similar to those in Trigonotarbida, and in general also the composition of the feeding apparatus would be similar between the two groups/However, the morphology in Harvestmen is highly variable, and it is unclear how the feeding apparatus in the ground pattern of Opiliones looks. This together with the still unresolved phylogenetic position of Opiliones does not allow to make a reliable assumption about the feeding apparatus in the ground pattern of Arachnida.

The feeding apparatus in different groups of Euchelicerata is far from primitive, but is in fact a highly specialised system in each group. During evolution, the feeding apparatus became progressively shorter in Euchelicerata, though the evolution within Arachnida remains still unclear due to unresolved phylogenetic relationships. The shortness of the feeding apparatus is not an ancestral character, but in fact a highly derived one, probably evolved in adaptation to new requirements resulting from habitat changes such as terrestrialisation. Sea scorpions possess true antagonistic mouthparts with differentiated armature and a guide rail system. These characters are all similar to the condition in the mandibles of Mandibulata, apparently as result of convergent evolution. Representatives of Trigonotarbida show similar specialisations concerning their feeding apparatuses to Harvestmen.In conclusion, the supposedly ‘primitive’ groups Eurypterida and Trigonotarbida are astonishingly specialised.

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Molecular clock data sugests the first Arachnids ventured onto land in the Cambrian or Odovician.

Arachnids are an important group of terrestrial Arthropods, including the familiar Ticks, Mites, Spiders, and Scorpions, together with Pseudoscorpions, Camel Spiders, Vinegaroons, Whip Spiders, and a few other groups. Arachnids are important predatory Arthropods across almost every conceivable terrestrial habitat. While Ticks are ectoparasites that affect Humans and livestock, Spiders are ecologically the most successful Arachnids and as predators consume vast quantities of Insects. Thus, understanding when Arachnids colonised land and diversified is of interest from a macroevolutionary and macroecological perspective. Arachnids are chelicerates, together with the marine Horseshoe Crabs (Xiphosura) and Sea Spiders (Pycnogonida). They are the most speciose clade in Chelicerata, with more than 112 000 described extant species. Together with Hexapods and Myriapods, Arachnids represent one of three distinct and ancient events of Arthropod terrestrialisation (terrestrial Isopods are a younger addition to the continental Arthropod biota). While Arachnids have traditionally been considered monophyletic and terrestrial (apart from secondarily marine Mites) this picture has been challenged at different times. Scorpions were long thought to be the sister group of all other extant Arachnids or most closely allied to the aquatic 'Sea Scorpions', the Eurypterids. Early fossil Scorpions have been interpreted as aquatic, and in some cases even as marine. These phylogenetic hypotheses and interpretations of fossil ecology have been seen as requiring independent events of terrestrialisation. Some of these views have been overturned by strong molecular and morphological evidence for Scorpions being nested within the Arachnida as the sister group of the other Arachnids with book lungs, the Tetrapulmonata. Indeed, detailed correspondences in book lung morphology between Scorpions and tetrapulmonates support their homology. The supposed aquatic mode of life of various fossil Scorpions has also been questioned on both morphological and geological grounds, Another challenge to a single terrestrialisation event in arachnids came from analyses of phylogenomic datasets, which have often recovered the marine Xiphosura to be nested within Arachnida. This remains a contentious issue, as other phylogenomic analyses have yielded trees in which Arachnida is monophyletic.

Most Chelicerate lineages are predatory components of a diverse range of ecosystems, and the rock record attests to their presence in both earlier Palaeozoic marine settings and through into the Mesozoic and Cainozoic, which witnessed a prolific diversification of Spiders and other terrestrial Arachnids. The terrestrial rock record prior to the Silurian is very sparse and has presented some apparent discordances when investigating Myriapod, Hexapod, and Plant divergence times. While the body fossil record of terrestrial Plants and Arthropods does not extend much further back than the Silurian (roughly 443–419 million years ago), molecular clock estimates go back to the Ordovician (485–443 million years ago) and Cambrian (538–485 million years ago). However, likely Plant spores with desiccation-resistant adaptations extend back to the middle Cambrian. The fossil record presents no unequivocal evidence for crown-group Arachnids before the Silurian. The oldest crown-group Arachnids are of Silurian age (stem-group Scorpiones in the Llandovery), followed by the extinct Trigonotarbida in the late Silurian (early Přídolí), Acariformes and Opiliones in the Early Devonian (Pragian), and Pseudoscorpiones in the Middle Devonian (Givetian). Several other Arachnid orders first appear in the Carboniferous, including Araneae, Uropygi, Amblypygi, and Ricinulei. In contrast to a picture of scattered branches of the Arachnid crown-group first appearing in the Siluro–Devonian, older representatives of the Arachnid lineage are stem-group Arachnida, and are marine shoreline or brackish water/estuarine forms rather than being terrestrial. These include Chasmataspida and Eurypterida, the earliest members of which date to the Miaolingian Series of the Cambrian (Drumian Stage) and the Late Ordovician (Sandbian), respectively. Xiphosura-like Chelicerates have a good fossil record, showing considerable morphological stasis, with marine stem-group representatives of Xiphosura such as Lunataspis being documented from the Late Ordovician, about 445 million years ago, and a species from the Early Ordovician (Tremadocian) of Morocco extends the lineage’s history even deeper. With such a deep history revealed by the fossil record, any inferred phylogenetic position for Xiphosura within terrestrial Arachnids would imply that the marine ecology of this lineage should be a secondary acquisition. Although such a scenario is palaeontologically unlikely, molecular studies have often recovered Horseshoe Crabs in highly derived clades of Arachnids, such as sister groups to Opiliones or Palpigradi, or Scorpiones and Araneae.

 

Cornupalpatum burmanicum, a fossil Hard Tick from Cretaceous Burmese Amber. Peñalver et al. (2017).

As with other terrestrial groups, molecular dating has recovered old dates for the origin and main diversification of Arachnids. As part of wider campaigns investigating Arthropods using just a few Arachnid representatives, several previous syudies have recovered dates for the origin of Arachnida with credibility intervals bracketed between the Cambrian, in the first two studies, and Ordovician in the latter. One recent study reported a Chelicerate molecular phylogeny in which when they constrained Arachnida to be monophyletic inferred an Ediacaran origin for the group. Consequently, there are significant geochronological discrepancies, particularly for terrestrial lineages, between the molecular clock-based studies and the younger dates suggested by the first appearances of fossils. As fossils do not inform on the age of origin of clades, but rather provide minimum ages of divergence, clock-based methods are required to approach an accurate evolutionary timescale.

In a paper published in the journal Frontiers in Genetics on 11 March 2020, Jesus Lozano-Fernandez of the School of Biological Sciences and School of Earth Sciences at the University of Bristol, Alastair Tanner, also of the School of Biological Sciences at the University of Bristol,  Mark Puttick of the Department of Biology and Biochemistry at the University of Bath, Jakob Vinther, again of the School of Biological Sciences and School of Earth Sciences at the University of Bristol, Gregory  Edgecombe of the Department of Earth Sciences at the Natural History Museum, and Davide Pisani, once again of the School of Biological Sciences and School of Earth Sciences at the University of Bristol, present the results of a study in which they estimate the divergence time of Arachnids, using a method which previously recovered both Arachnida and Acari as monophyletic groups.  To calibrate the molecular clock, Lozano-Fernandez et al. used a carefully selected and expanded set of 27 fossil constraints across the tree.

 

Carbolohmannia maimaiphilus, a fossil Oribatid Mite from the Carboniferous Tupo Formation of Ningxia Province, China. Robin et al. (2020).

The molecular supermatrix used by Lozano-Fernandez et al. is composed of 89 species, 75 of them being Chelicerates, with 14 other Panarthropod species as outgroups. This matrix is a concatenation of 233 highly conserved and slow-evolving genes retrieved from transcriptomic data (45,939 amino acid positions and 78,1% complete). To evaluate the robustness of the results to an alternative topology, Lozano-Fernandez et al. also performed a divergencedate analysis in which Arachnida was non-monophyletic, with Xiphosura nested inside the Arachnids. The phylogenetic trees were inferred using PhyloBayes MPI v.4.1 under the site-heterogeneous CAT–GTR C 0 model of amino acid substitution. Convergence was assessed by running two independent Markov chains and using the bpcomp and tracecomp tools from PhyloBayes to monitor the maximum discrepancy in clade support (maxdiff), the effective sample size (effsize), and the relative difference in posterior mean estimates (rel_diff) for several key parameters and summary statistics of the model. We ran the analysis for 10 000 cycles and discarded as 'burn-in' the first 3000 generations.

Divergence time estimation was performed using PhyloBayes 3.3f (serial version). Lozano-Fernandez et al. compared the fit of alternative, autocorrelated and uncorrelated, relaxed molecular clock models generating ten different random splits replicates and performing cross-validation analyses. The tree was rooted on the Onychophora–Euarthropoda split. A set of 27 fossil calibrations and 1 node constrained by a maximum age was used. Lozano-Fernandez et al.imposed a soft maximum of 559 million years ago for the Onychophoran–Euarthropod split based on trace fossils in the White Sea/South Australian Ediacaran. This uses a radiometric date of 558 million years for strata at which body fossils such as Kimberella, a putative total-group Bilaterian Metazoan, occur. Metazoan trace fossils in the White Sea/South Australian Ediacaran indicate suitable preservation for Arthropod traces, were they present. Lozano-Fernandez et al. regard this to be a conservative soft maximum, as there is no body or trace fossil evidence for Arthropods in the Ediacaran. A minimum for the divergence of Onychophorans and Arthropods is set by the earliest Rusophycus traces (total-group Arthropoda), dated to a minimum of 528.8 million years ago. To allow the analysis to explore younger ages and prevent having posterior ages being much older than the fossil record, Lozano-Fernandez et al. also set maximum constraints on a few of the deepest calibrations within Euarthropoda. Lozano-Fernandez et al. infer that crown-group Mandibulata and Chelicerata do not predate the oldest fossil evidence for Arthropods (Rusophycus) and set soft maxima for each of this pair of sister taxa at the base of the Cambrian (538.8 million yars ago). Within Arachnida, Lozano-Fernandez et al. infer Acari and Arachnopulmonata do not predate the oldest body fossils of crown-group Chelicerata, using Wisangocaris barbarahardyae and its date of 509 million years old as a soft maximum. The amino acid substitution model used to estimate branch lengths was the CAT–GTR C 0 model.All analyses were conducted using soft bounds with 5% of the probability mass outside the calibration interval. A birth–death model was used to define prior node ages. Analyses were run under the priors to evaluate the effective joint priors induced by our choice of calibrations and root maxima. Convergence was considered achieved with tracecomp statistics dropping below 1 for all relative difference scores, and all effective sample sizes being above 50, for all chain parameters. The time-scaled phylogenies were plotted using the package MCMCtreeR, which allows the display of full posterior distributions on nodes and the inclusion of the geological timescale. We included as supplementary data the chronograms, the guiding trees and the calibration file used in PhyloBayes, the subset of sampled timescaled trees used to generate the posterior distributions shown on the figures.

 

Nephila jurassica, a Golden Orb-weaver Spider from the Middle Jurassic Daohugou Biota of Inner Mongolia, China. Scale bar is 5 mm. Selden et al. (2020).

Lozano-Fernandez et al. estimated rates of molecular evolution within Chelicerata using two different methods. For the first method, they modeled the rates of molecular evolution on a fixed tree topology constrained to the timetree relationships. On this tree they estimated relative branch lengths under the C60 model C 0 in IQTree. Lozano-Fernandez et al. then divided these relative branch lengths by the timetree lengths to provide an estimate of absolute molecular rates through time. For the second method, they inferred ancestral estimates of the amino acid sequence on the fixed timetree, again using the C60 model C 0 in IQTree. Lozano-Fernandez et al. divided the sum of gross amino acid changes between ancestral and descendant nodes by absolute time to obtain per-branch rates of change.

Lozano-Fernandez et al.  estimated speciation and extinction rates on the fixed timetree by using a Bayesian episodic diversification rate model in RevBayes 1.0.10. This model estimates piece-wise rates of speciation and extinction on a phylogeny through time. Within each bin, rates of speciation are equal but can differ between bins. The initial episodic speciation and extinction rate was sampled from a log-uniform distribution U(-10,10). Moving backward in time for each distinct time bin, the model samples speciation and extinction rate from a normal distribution with the mean inherited from the value of the previous bin so rates are autocorrelated. Each normal distribution has a standard deviation inferred from an exponential hyper-prior of mean 1. In this manner, the model follows a Brownian motion pattern of rate change through time. To incorporate incomplete sampling in the model, we provided estimates of the known extant species numbers to complement the diversity shown in the tree using empirical taxon sampling by providing estimate diversity represented by each tip on our incomplete time tree. This empirical taxon-sampling approach is believed to produce less biased estimates of speciation and extinction parameters compared to diversified taxon sampling. Lozano-Fernandez et al. used values of the described extant species: Pycnogonida (1346); Xiphosura (4); Ricinulei (77); Opiliones (6571); Solifugae (1116); Acariformes (42233); Parasitiformes (12385); Pseudoscorpiones (3574); Scorpiones (2109); Uropygi (119); Amblypygi (172); and Araneae (44863). As Lozano-Fernandez et al. tested for the presence of early high rates compared to later times rather than differences in geological time units. Lozano-Fernandez et al. assumed there were 10 equally sized time intervals which can potentially possess distinct speciation and extinction rates.

 

Parioscorpio venator, a Scorpion from the Silurian Brandon Bridge Formation of  Wisconsin, USA. Scale bar is 5 mm. Wendruff et al. (2020).

In the topology tree used for the molecular clock analyses by Lozano-Fernandez et al. Chelicerata and Euchelicerata are monophyletic, with the Horseshoe Crabs retrieved as the sister group of monophyletic Arachnida. Bayesian cross-validation indicates that the autocorrelated CIR model most optimally fits the data. Accordingly, divergence time estimation was performed using the Autocorrelated CIR model.

The age of the Euarthropoda root, given the taxonomic sample, is recovered near the end of the Ediacaran, 546 million years ago, with the 95% highest posterior density lying between 551 and 536 million years ago. Chelicerata are inferred to originate at 535 million years ago (with highest posterior density 540–527 million years ago), similar to the age retrieved for Mandibulata 535 million years ago (539–526 million years ago). The origin of Myriapoda comprises ages centered on the early Cambrian 516 million years ago (524–505 million years ago) and precedes that of Pancrustacea at 486 million years ago (501–471 million years ago). Hexapods are inferred to be much younger in age than Myriapods, ranging through the Late Ordovician to Early Devonian, 422 million years ago (448–400 million years ago).

 

Chelicerate divergence times in the molecular clock analysis (outgroups not shown). Divergence times shown are obtained under the CIR autocorrelated, relaxed molecular clock model. Nodes in the tree represent average divergence times. The density plots represent the posterior distributions from the considered node. The numbered blue circles represent the age of the fossil calibrations and are located at a height corresponding to the node they are calibrating. In the timescale on the X axis, numbers represent millions of years before the present. Lozano-Fernandez et al. (2020).

Arachnid terrestrialisation is inferred to date to the Cambrian to Ordovician, crown-group Arachnida having a mean at 485 million years ago (494–475 million years ago). Therefore, Lozano-Fernandez et al.'s results support a Cambrian or Early Ordovician origin of two of the three main terrestrial Arthropod lineages (Myriapods and Arachnids). The upper limit is consistent with fossil evidence for stem-group Arachnida (Chasmataspidid trackways) but is substantially older than any crown-group fossils. Within Arachnida, rapid cladogenesis then occurred during the 20 million years that followed their origin, with several crown-group supra-ordinal clades becoming established in this time interval. By around 450 million years ago, all 10 stem groups leading to extant orders of Chelicerates included in the analysis (out of 12 in total, Palpigrada and Schizomida are unsampled) were already established. Further cladogenesis is inferred to have involved a more gradual tempo of evolution, in particular for Arachnopulmonata and Acari, which originated at  470 million years ago but greatly expanded after the start of the Mesozoic (252 Ma to 66 million years ago). Lozano-Fernandez et al.'s dating suggests that the oldest crown-group Arachnid orders are Opiliones and Parasitiformes, with Silurian and Devonian origins, respectively. Crown-group Scorpions have a Devonian to Carboniferous origin, with the sampled extant lineages splitting more recently. For Araneae, the crown-group age is centered on the Devonian–Carboniferous boundary, with most extant Mygalomorph and Araneomorph lineages diversifying after the Jurassic.

In general, these Palaeozoic age estimates for deep nodes within the most intensely sampled Arachnid orders are similar to those inferred in other recent molecular dating analyses. For example, Lozano-Fernandez et al.'s estimates for crown-group Araneae is consistent with the Late Devonian or Early Carboniferous dates retrieved in other transcriptome-based analyses; likewise, a Carboniferous mean age for crown-group Opistothele Spiders is found in each of these studies. Lozano-Fernandez et al.'s estimates encompassing a Late Ordovician median age for crown-group Opiliones corresponds to that estimated using tip dating, whereas node calibration in that study recovered a Silurian median. In the case of Scorpiones, a Late Devonian to Carboniferous origin of the crown group is closely comparable to the date for the same node, but older than the strictly Carboniferous ages estimated by a previous study. However, in all cases mentioned the credibility intervals substantially overlap, indicating that these independent studies found results that, despite some differences, are not significantly different and corroborate each other. One exception is from a recent  phylotranscriptomic study of Pseudoscorpiones, which retrieved an Ordovician to Carboniferous origin for the group, significantly older than the Permian ages retrieved by Lozano-Fernandez et al. This may reflect the much more complete taxonomic coverage of Pseudoscorpion diversity in that study.

Electrochelifer balticus, a Pseudoscorpion from Eocene Baltic Amber. Scale bar is 1 mm. Harms & Dunlop (2017).

To assess whether our joint prior assumptions were driving their posterior estimates, Lozano-Fernandez et al. also ran the analysis under the priors (i.e. they performed analyses without data) and found that the joint priors allowed a wide possible distribution of ages, for the most part encompassing but not enforcing the posteriors. Lozano-Fernandez et al. also performed a molecular clock analysis from a different matrix that resulted in a topology in which Xiphosura was nested within Arachnida, specifically as the sister group of Arachnopulmonata plus Pseudoscorpiones. Overall, the result it is in general agreement with the main analysis, with most significant discrepancies concerning the age of Pycnogonida, which encompasses Silurian to Devonian ages, whereas in the main analysis are centered on the Carboniferous.

Lozano-Fernandez et al. conducted estimations of molecular evolution and diversification rates based on their Chelicerate timetree in an attempt to clarify whether the explosive cladogenesis at the onset of the Arachnid radiation early in the Phanerozoic was matched by an increase in either of these rates. The analyses of rates of molecular evolution along the branches show a very high rate early in Chelicerate history, including at the origin of Euchelicerata. These rates remain high during the early radiation of the Arachnida until the end of the Cambrian. Molecular rate estimations using branch lengths or ancestral sequences under a non-clock model gave nearly identical results. Using the episodic model of speciation and extinction rates through time, Lozano-Fernandez et al. found no evidence of high rates of speciation during the Cambrian, the period that presents the highest rates of molecular evolution. Instead, there is evidence for higher rates of cladogenesis later, bracketed between the Permian and Early Cretaceous, but especially high in the Permian and Triassic.

 

Inferred rates of molecular evolution and diversification over time across chelicerates. Shown on the left Y axis are inferred amino acid substitutions per site per million years. On the right Y axis are diversification rates estimated with speciation rate as a proxy. Rates of molecular evolution are marked in green. Median speciation rates are marked in black with the highest posterior density of estimates shown in gray. In the timescale, numbers represent millions of years before the present. Lozano-Fernandez et al. (2020).

Molecular clocks allow the reconstruction of evolutionary timescales, but the reliability of these timescales depends on a variety of assumptions, which includes fossil data that have robust stratigraphic and phylogenetic justification, the use of a robust phylogenetic framework for the extant taxa, and the use of well-fitting models of both amino acid substitution and change in rate of molecular evolution. In this context, fossil calibrations then provide minimum ages for the origin of crown groups. Lozano-Fernandez et al. report divergence times on a well-sampled phylogeny, using the best-fitting molecular substitution and relaxed molecular clock models Fernandez et al. therefore contend that their findings provide the currently most robust insights into early Chelicerate evolution. In Fernandez et al.'s analysis, the ancestral Pycnogonid divergence from Euchelicerata is inferred to have happened early in the Cambrian. This does not greatly predate the oldest unequivocal total-group Pycnogonid, Cambropycnogon klausmuelleri, from the late Cambrian Orsten Konservat-Lagerstätte. The from the late Cambrian Orsten Konservat-Lagerstätte. The Pycnogonid–Euchelicerate divergence date suggests cryptic evolution of the Euchelicerate stem group in the early Cambrian. Chelicerate, and, indeed, Arthropod, body fossils are lacking in the earliest Cambrian, the Fortunian, the Arthropod fossil record in the first 20 million years of the Cambrian being limited to trace fossils. Subsequently, it is estimated that Xiphosurids diverged from Arachnids in the late Cambrian, followed soon after by the radiation of crown-group Arachnida. While revising this paper, a new study on Spider fossil calibrations came out and suggests that a few of the shallower calibrations used within Araneae treated as crown-groups may instead be stem-groups, so Fernandez et al. add this caveat when interpreting the age of Spiders.

There remain major geochronological discrepancies between the inferred molecular and fossil age of the various terrestrial Arthropod groups. While these discrepancies may be thought to question the accuracy of molecular clocks, the differences need to account for pervasive biases in the terrestrial sedimentary rock record. It has been noted that in Euramerica (from which much of the data on early terrestrial arthropods and early Plant megafossils are derived), terrestrial sediments are rare before the late Silurian, and first become widespread in the Early Devonian. This temporal bias in the rock record almost certainly affects the fossil records of terrestrial organisms, and likely accounts for a major component of the discordance between molecular and fossil dates. The common recovery of Horseshoe Crabs as ingroup Arachnids is perhaps unsurprising, given the short molecular branch lengths among these nodes in the tree, which also suggest short divergence times. With a reasonably good Xiphosurid and Pycnogonid fossil record, the molecular clock is well constrained among Euchelicerates. This is evidenced by the short credibility intervals among deep Arachnid nodes.

 

Cushingia ellenbergeri, a Camel Spider from Cretaceous Burmese Amber. Scale bar is 2 mm. Dunlop et al. (2015).

From an ecological context, it has been suggested that appreciably complex terrestrial ecosystems may have existed as far back as 1 billion years ago, with molecular dating suggesting that crown-group land plants were already present by the middle Cambrian. If it is indeed the case that Myriapods and Arachnids were on land so early, we speculate that the Animals may have been early grazers on littoral bacterial mats, or predated on other amphibious or terrestrial organisms. These ecologies represent habitats highly unfavorable to fossilisation, such as high-energy environments characterized by erosion rather than deposition. It is unsurprising that paleontological insight is thus limited, and inference of the
molecular kind as used here becomes more important as an investigative tool.

Fernandez et al. estimate that Arachnids colonised the land near the Cambrian–Ordovician boundary, and diversified soon after. Rates of molecular evolution were high at the onset of Arachnida, coinciding with rapid cladogenesis. High rates are concentrated on the branches leading to the major clades within Arachnida, representing major morphological and ecological partitions within the group. In unusually large and ancient clades, such as Chelicerates, it is expected to find high rates of molecular evolution in their early lineages and Fernandez et al. retrieved results in agreement with that expectation. In order to avoid biases related to that fact, they imposed on the molecular clock analyses several maxima on the deepest nodes to account for possible overestimations of divergence times. Arachnids are predominantly predators, which must reflect the presence of an already diverse ecosystem, which the slightly older divergence times for Myriapods and Embryophytes established in the middle Cambrian. Fernandez et al. therefore suspect that Arachnids primitively represent carnivorous Arthropods rather than having adapted to this mode of life convergently several times. The carnivorous Centipede (Chilopoda) crown group is separated from other Myriapods by a long branch estimated to be much younger in age than the detritivorous and/or fungal-feeding Progoneate Myriapods, allowing Arachnids to be potentially the first carnivorous Animals on land with early Myriapod lineages as a likely source of prey. Hexapod divergence estimates are generally younger, suggesting a colonisation of land no earlier than the Ordovician.

Mesoproctus rowlandi, a Whip Scorpion from the Cretaceous Santana Formation of Brazil. Scale bar is 1 cm. Dunlop (1998).

There is a clear contrast in evolutionary tempo after the explosive radiation of the Cambrian and Ordovician. More gradual cladogenesis characterises later Phanerozoic macroevolutionary dynamics of Chelicerates, as is seen in the origins of ordinal clades. Fernandez et al. 's diversification studies reveal an increase in speciation rates bracketed between the Permian and the Early Cretaceous, in the origin of most sub-ordinal clades, with no evidence of higher speciation rates coinciding with the early rapid Arachnid cladogenesis. A heightened diversification of Spiders during the Cretaceous has previously been detected, suggested to result from the rise of Angiosperms, stimulated by a warmer climate that led to the proliferation of Spiders’ main prey, Insects. Interestingly, Fernandez et al. did not observe an early burst of diversification at the origin of Chelicerates followed by a slowdown toward the present, a statistical bias usually found in large clades that survive to the present, the so-called 'push of the past'. Instead, it seems that speciation rates are decoupled from the rates of molecular change. The common origin of Arachnids giving rise to a plethora of adaptations, together with high molecular rates on the short internodes at the origin of the group suggests an ancient adaptive radiation shortly after colonising the land, but our diversification analyses have not detected higher speciation rates at that time, one of the key features signaling an adaptive radiation. Fernandez et al. acknowledge that the taxon sampling may not be the most adequate to infer speciation rates, as it was originally designed to maximize diversity, particularly at the deepest nodes to resolve the splits at the ordinal level.

Fernandez et al.'s analysis corroborates euchelicerates having radiated in the Cambrian and Arachnids having diversified rapidly in the latest Cambrian–Early Ordovician. While this radiation was rather fast, Fernandez et al. found no evidence that the speciation rates that underpinned it were explosive. The late Cambrian to Early Ordovician emergence of Arachnid stem groups onto land was soon followed by a rapid radiation near that same geological boundary, cladogenesis coinciding with high rates of molecular evolution during that time. A later phase of diversification within Arachnida is detected between the Permian and Early Cretaceous, during which the living arachnid orders exhibit heightened rates of speciation.

 

Limulus darwini, a Horseshoe Crab from the Jurassic Kcynia Formation of central Poland.  Fernandez et al. (2020).

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