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Central Nervous System of a 310-My-Old Horseshoe Crab

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Central Nervous System of a 310-My-Old Horseshoe Crab https://doi.org/10.1130/G49193.1 Manuscript received 2 March 2021 Revised manuscript received 26 April 2021 Manuscript accepted 2 June 2021 © 2021 The Authors. Gold Open Access: This paper is published under the terms of the CC-BY license. Central nervous system of a 310-m.y.-old horseshoe crab: Expanding the taphonomic window for nervous system preservation Russell D.C. Bicknell1*, Javier Ortega-Hernández2, Gregory D. Edgecombe3, Robert R. Gaines4 and John R. Paterson1 1 Palaeoscience Research Centre, School of Environmental and Rural Science, University of New England, Armidale, NSW 2351, Australia 2 Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA 3 Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK 4 Geology Department, Pomona College, 185 E. Sixth Street, Claremont, California 91711, USA ABSTRACT reconstructing the complex evolutionary history The central nervous system (CNS) presents unique insight into the behaviors and ecology of Euarthropoda (Lamsdell, 2016). Euproops of extant and extinct animal groups. However, neurological tissues are delicate and prone danae shares similar prosomal appendage or- to rapid decay, and thus their occurrence as fossils is mostly confined to Cambrian Burgess ganization with the extant Limulus polyphemus Shale–type deposits and Cenozoic amber inclusions. We describe an exceptionally preserved (Linnaeus, 1758) (Haug and Rötzer, 2018) and CNS in the horseshoe crab Euproops danae from the late Carboniferous (Moscovian) Mazon is one of the best-documented fossil xiphosurids Creek Konservat-Lagerstätte in Illinois, USA. The E. danae CNS demonstrates that the general both within Mazon Creek (Raymond, 1945) prosomal synganglion organization has remained essentially unchanged in horseshoe crabs and globally (Haug and Rötzer, 2018; Bicknell for >300 m.y., despite substantial morphological and ecological diversification in that time. and Pates, 2020). Therefore, these new data on Furthermore, it reveals that the euarthropod CNS can be preserved by molding in siderite E. danae inform on the internal anatomy of this and suggests that further examples may be present in the Mazon Creek fauna. This discov- major euchelicerate group, represent the first oc- ery fills a significant temporal gap in the fossil record of euarthropod CNSs and expands the currence of CNS preservation in a fossil horse- taphonomic scope for preservation of detailed paleoneuroanatomical data in the Paleozoic shoe crab, and shed new light on preservational to siderite concretion Lagerstätten of marginal marine deposits. modes for fossilized neural tissue. INTRODUCTION understanding of CNS evolution. Notable excep- MATERIALS AND METHODS The central nervous system (CNS) plays a tions include the putative brain described for the We reviewed E. danae specimens in the Yale critical role in animal functions, behavior, and Carboniferous Tullimonstrum gregarium Rich- Peabody Museum (New Haven, Connecticut, ecology, and contains valuable morphologi- ardson, 1966 (McCoy et al., 2016) and a phos- USA) Division of Invertebrate Paleontology cal data that inform the evolution of complex phatized ventral nerve cord in a Triassic insect (YMP IP). One specimen (YPM IP 168040) organisms (Schmidt-Rhaesa et al., 2015). Al- (Montagna et al., 2017), suggesting that paleo- showing evidence of preserved internal anatomy though the lipid-rich composition of the CNS neuroanatomical structures can be captured by was identified. This specimen was photographed makes it prone to rapid decay (Sansom, 2016), taphonomic pathways other than Burgess Shale– as a series of stacked images under normal LED recent research demonstrates that neurologi- type preservation in the Paleozoic (Butterfield, light using a Canon EOS 5DS digital SLR cam- cal tissues can be preserved as carbonaceous 1995; Gaines, 2014), albeit extremely rarely. era fitted with a Canon MP-E 65 mm macro compressions in Cambrian animal macrofossils We describe an exceptionally well-preserved lens (complete specimen) and a Canon MP-E from open- marine deposits (Edgecombe et al., CNS in the belinurid Euproops danae (Meek 65 mm 1×–5× macro lens (close-up on CNS) 2015; Strausfeld et al., 2016; Ortega-Hernán- and Worthen, 1865) from the Pennsylva- and a Cognisys StackShot 3X stacking system. dez et al., 2019; Table S1 in the Supplemen- nian (Moscovian) Mazon Creek Konservat- Photos were stacked and stitched using Helicon tal Material1). Paleoneuroanatomical remains Lagerstätte in Illinois, USA. The discovery of Focus 7 (https://www.heliconsoft.com/helicon- are extremely rare in younger deposits before paleoneuroanatomy in E. danae is significant soft-products/helicon-focus/). Backscatter and Cenozoic ambers, leaving profound gaps in our because xiphosurids (horseshoe crabs) are the energy dispersive X-ray spectroscopy (EDS) only wholly aquatic extant order of euchelic- analyses were conducted to examine compo- *E-mail: [email protected] erates, and their fossil record is critical for sition of the CNS with a JEOL JSM-6010LA 1Supplemental Material. Figures S1 and S2, and Table S1. Please visit https://doi.org/10.1130/GEOL.S.14925225 to access the supplemental material, and contact [email protected] with any questions. CITATION: Bicknell, R.D.C., Ortega-Hernández, J., Edgecombe, G.D., Gaines, R.R., and Paterson, J.R., 2021, Central nervous system of a 310-m.y.-old horseshoe crab: Expanding the taphonomic window for nervous system preservation: Geology, v. 49, p. XXX–XXX, https://doi.org/10.1130/G49193.1 Geological Society of America | GEOLOGY | Volume XX | Number XX | www.gsapubs.org 1 Downloaded from http://pubs.geoscienceworld.org/gsa/geology/article-pdf/doi/10.1130/G49193.1/5367142/g49193.pdf by guest on 26 September 2021 scanning electron microscope (SEM) under low correspondence between the synganglia of CNS margin is sharp and the matrix is composed vacuum at a voltage of 20 kV. The specimen E. danae and L. polyphemus suggests close of siderite, as indicated by enrichment in iron, was not coated. functional and behavioral similarities between carbon, and oxygen (Figs. 1H and 1K; Fig. S2). modern and extinct xiphosurids, despite the The siderite surrounding the CNS has the same RESULTS substantial temporal and phylogenetic gaps composition and texture as the matrix of the Specimen YPM IP 168040 contains the first between their respective clades (Bicknell and concretion enveloping the specimen. known record of E. danae internal anatomy, as- Pates, 2020). This fossil shows that the funda- The preservation of the examined CNS re- pects of which are preserved on both the part mental organization of the xiphosurid CNS has quires that siderite grew rapidly around the de- and counterpart (Fig. 1; Fig. S1 in the Supple- essentially remained unchanged for >300 m.y. composing organism, molding the CNS in three mental Material). The specimen is a fully ar- Furthermore, close anatomical parallels between dimensions. The CNS was then lost to decay, ticulated individual in dorsal view, preserved the CNS organization of L. polyphemus, E. da- leaving a void inside its external mold that was with limited relief in a siderite concretion, as nae, and the great appendage stem-group che- stabilized by the siderite mineral matrix. This is typical for Mazon Creek fossils (Clements licerates (Tanaka et al., 2013; Ortega-Hernández void was subsequently filled by the precipita- et al., 2019). The prosoma is 6.9 mm long and et al., 2019) suggest that euchelicerates have tion of kaolinite (Fig. 2). Such a pathway has 16.8 mm wide, the opisthosoma is 7.3 mm long sustained this conserved neuroanatomy since two important implications. and 11.2 mm wide, and the telson is 7.9 mm the Cambrian. (1) The siderite matrix must have been em- long. Based on opisthosomal size, the speci- This unique E. danae specimen represents placed very quickly to capture neural tissue. men likely represents the third Euproops devel- the earliest unequivocal evidence of preserved While this rapid growth could be difficult to opmental stage (sensu Haug and Rötzer, 2018). euarthropod neuroanatomy from a brackish mar- account for (e.g., Berner, 1968; Yoshida et al., The axial region of the prosoma features a ginal-marine deposit (Clements et al., 2019). El- 2020), it is currently the accepted mode of ex- bilaterally symmetrical complex structure with a emental mapping indicates that the CNS—which ceptional preservation within the Mazon Creek white coloration (Figs. 1A, 1B, and 1G). Elemen- is white in visible light (Fig. 1G)—is enriched Konservat-Lagerstätte (Clements et al., 2019). tal mapping indicates that this feature is enriched in aluminum, silicon, and oxygen (Figs. 1I–1K). Such a preservational pathway is thought to in aluminum and silicon (Clements et al., 2019; Further, SEM imaging reveals that vermiform have produced the flattened composite molds Figs. 1I and 1J) and depleted in iron, potassium, stacks of platy, micron-sized crystallites com- observed in the Mazon Creek concretions, and magnesium relative to the siderite matrix pose the white material (Fig. 1F). These obser- particularly of dermal, cuticular, and other ex- (Figs. 1H, 1M, and 1N). The morphology of the vations, coupled with depletion in potassium and ternal structures (Baird et al., 1986; Clements internal structure consists of a fusiform ring ori- magnesium relative to matrix, indicate that the et al., 2019). However,
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