Chelicerate neural ground pattern in a Cambrian great appendage arthropod

Nature volume 502, pages364–367(2013)Cite this article

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Abstract

Preservation of neural tissue in early Cambrian arthropods has recently been demonstrated1, to a degree that segmental structures of the head can be associated with individual brain neuromeres. This association provides novel data for addressing long-standing controversies about the segmental identities of specialized head appendages in fossil taxa2,3. Here we document neuroanatomy in the head and trunk of a ‘great appendage’ arthropod, Alalcomenaeus sp., from the Chengjiang biota, southwest China, providing the most complete neuroanatomical profile known from a Cambrian animal. Micro-computed tomography reveals a configuration of one optic neuropil separate from a protocerebrum contiguous with four head ganglia, succeeded by eight contiguous ganglia in an eleven-segment trunk. Arrangements of optic neuropils, the brain and ganglia correspond most closely to the nervous system of Chelicerata of all extant arthropods, supporting the assignment of ‘great appendage’ arthropods to the chelicerate total group4,5. The position of the deutocerebral neuromere aligns with the insertion of the great appendage, indicating its deutocerebral innervation and corroborating a homology between the ‘great appendage’ and chelicera indicated by morphological similarities4,6,7. Alalcomenaeus and Fuxianhuia protensa1 demonstrate that the two main configurations of the brain observed in modern arthropods, those of Chelicerata and Mandibulata, respectively8, had evolved by the early Cambrian.

Main

Cambrian ‘great appendage’ arthropods, collectively known as Megacheira9, are variously regarded as mono-, para- or polyphyletic and variously interpreted as stem-group chelicerates4,5,6,7 or as stem-group arthropods2,10. They are characterized by raptorial cephalic appendages with an ‘elbow joint’ between a proximal pedunculate part and a distal part bearing an elongate spine on each article7. Morphologically and taxonomically best understood are Leanchoiliidae, which have three long spine-bearing or spiniform articles on the great appendage, each with a flagellate distal part11,12.

YKLP 11075 is a leanchoiliid from the early Cambrian Chengjiang biota (Yu’anshan Member, Heilinpu Formation), Yunnan Province, southwest China13. It is preserved as part and counterpart in dorsoventral aspect, exhibiting the cephalic shield and 11 complete trunk segments (Figs 1a and 2a). It is assigned to Alalcomenaeus (Fig. 3a, b) rather than the closely allied Leanchoilia (Fig. 3c), abundantly represented in the Chengjiang biota by Leanchoilia illecebrosa. Distinction from Leanchoilia is based on the straight (rather than pointed) anterior margin of the cephalic shield and rounded, paddle-shaped (rather than lanceolate) telson14 (Fig. 3a). Studied specimens are similar to Alalcomenaeus cambricus from the Burgess Shale, Canada, having four rather than three pairs of cephalic appendages, as described for A. cambricus15. We describe them in open nomenclature, that is, Alalcomenaeus sp., because most of the Alalcomenaeus material from the Chengjiang biota has not been studied in detail.

Figure 1: Alalcomenaeus sp. from the Chengjiang Lagerstätte.
figure1

a, Incident light photograph, dorsal view of montaged part and counterpart YKLP 11075. b, Energy-dispersive X-ray fluorescence (EDXRF) Fe profile. Double-headed arrow indicates rostro-caudal extent of oesophageal foramen. c, MicroCT scan. d, Overlay of EDXRF Fe and microCT. e, Inverted white coincidence signal after isolated magenta (b) and green (c) removal. Arrowheads mark posterior margin of cephalic shield. f, Cephalon with superimposed EDXRF Cu (blue) and EDXRF Fe (red) profiles. g, Cephalon with superimposed EDXRF Cu (blue) and CT (green) profiles. C1, tritocerebrum; C2, C3, cephalic biramous segment neuropils; CA, cephalic segments; GA, great appendage neuropil = deutocerebrum (deu); Oe, oesophageal foramen; on1, first-order visual neuropil; pr, protocerebrum; T1–T8, trunk segment neuropils; T9–11, trunk segments lacking ganglia. Scale bar, 2 mm.

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Figure 2: Details of eye pairs and visual neuropils in Alalcomenaeus sp. YKLP 11075.
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a, Cephalic region; boxed areas refer to panels b–d. b, Left cornea of left eye pair showing lenses (arrowed) surmounting pigmented area. c, Lens rows (arrowed: left eye of right pair). d, Enlargement of left eye (ey) pair showing trace of retinula axon bundle (r) extending to rust-coloured first-order optic neuropil (on1) separate from the brain, but connected to it by an optic nerve (op n) terminating in a similarly coloured domain (on2) integrated in the protocerebrum. e, Superimposition of EDXRF Fe (red) showing strict coincidence of detected iron at the first-order optic neuropil (on1) and underlying protocerebral areas. Outlines of on1 and on2 are superimposed. Scale bar, 2 mm.

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Figure 3: Leanchoiliid megacheiran arthropods from the Chengjiang Lagerstätte.
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Lateral views. Arrowheads mark posterior margin of cephalic shield. a, b, Alalcomenaeus sp. a, YKLP 11076. b, YKLP 11077. c, Leanchoilia illecebrosa. YKLP 11078. C1–C3, biramous cephalic appendages 1–3; ey, eye; GA, great appendage; T1–T3, biramous limbs of trunk segments 1–3. Scale bars, 2 mm.

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Paired eyes, well separated by exoskeleton, are preserved each side of the midline at the anterior margin of the cephalic shield (Fig. 2a). Each eye is approximately 0.75 mm wide, composed of approximately 15 μm diameter facets (Fig. 2b, c) spaced as 20–25 rows. Each comprises 8–10 vertically arranged elements, equipping each eye with 160–250 facets. Facets surmount a dark zone contiguous with centrally extending traces of the retinula nerve from each eye (Fig. 2d). Nerves from a lateral pair of eyes converge to an obcordate rust-brown area identified as the first visual neuropil (Fig. 2d, left). A single optic nerve connects it to a similarly rust-brown strip interpreted as the second optic neuropil integrated in the rostral volume of the protocerebrum (Fig. 2d). The extent of these neuropils is resolved by superimposition of iron distribution detected by energy-dispersive X-ray fluorescence (EDXRF Fe) over the relevant region (Figs 1f and Fig. 2e, and Extended Data Fig. 1).

Outlines of contiguous cerebral and thoracic neuromeres were resolved by combining EDXRF Fe with computed tomography (CT). The EDXRF copper (blue) signal (Extended Data Fig. 1) corresponds to much of the internal volume of the specimen. Overlaying the EDXRF Fe (magenta) signal demonstrates a highly constrained distribution of iron to the putative nervous system (Fig. 1f). Overlaying the CT signal (Fig. 1c, green) and EDXRF Fe (Fig. 1b, magenta) signal in Fig. 1d, then subtracting isolated greens and magentas and inverting the white coincidence signal, resolves highly constrained segmental neuromeres (Fig. 1e). In the head, EDXRF Fe and CT overlie the protocerebrum and first-order visual neuropil (Fig. 1f, g), which receives its input from the two eyes (Fig. 2a, d, e), followed by an elongated neuromere corresponding to the deutocerebral origin of the great appendage (Fig. 1e–g, GA; Extended Data Fig. 1). Two smaller swellings indicate fused neuromeres corresponding to the segmental origins of the first and second pairs of biramous cephalic appendages (C1, C2) (Fig. 1e). These three neuromeres (GA, C1, C2) flank the extended oesophageal foramen reaching rostrally to the caudal margin of the protocerebrum (Fig. 1e). Neuropils lateral to the foramen converge between the second (C2) and third post-GA neuromere (C3), which is at the midline (Fig. 1e). Each neuromere aligns with the segment of the head defined by the attachment points of the corresponding member of the first four appendage pairs. All are resolved anterior to the posterior margin of the head shield (open arrowheads in Figs 1e and 3a–c).

In contrast to discrete ganglia linked by elongated connectives3, the robust post-cephalic neuromeres T1–T8 are effectively contiguous, without intervening connectives. Segments 9–11 show no detectable signal indicative of ganglia. These most caudal segments are equipped with successively smaller appendages until the broad, ovoid telson (Fig. 3a), which is attached to the eleventh segment. Telson flexion, such as would elicit reflex escape behaviours, requires power from longitudinal muscles within the last few trunk segments. These were probably specialized in segments 8–11, driven by motor neurons in ganglion T8, a similar arrangement existing in the extant crustacean order Mystacocarida in which the last four trunk segments lack ganglia but are innervated from post-cephalic segment T8 (ref. 16).

Reconstruction of neuromeric topology shows critical correspondences with the nervous systems of chelicerates, exemplified by the horseshoe crab Limulus polyphemus and scorpion Centruroides sculpturatus (Fig. 4). In all three taxa a single optic neuropil, which is separate from the brain, serves each eye (Fig. 2a, d), and all taxa have an extended oesophageal foramen flanked by the fused proto-, deuto- and tritocerebral neuromeres (Fig. 1e). As in Limulus, the fourth rostral neuromere also participates in this flanking arrangement. Although distinct entities, the ganglia in the trunk of Alalcomenaeus show partial fusion, as in Limulus.

Figure 4: Nervous systems of Chelicerata.
figure4

a–c, Reconstruction of ‘great appendage’ arthropod and Chelicerata nervous systems. a, Alalcomenaeus sp. b, Larval Limulus polyphemus (Xiphosura). c, Centruroides sculpturatus (Scorpiones). d–f, Enlargements of corresponding segmental neuromeres and optic neuropils (shown in navy blue). Each eye supplies its first optic neuropil (on1) outside the protocerebral mass; second order optic neuropils (on2) are integrated within the protocerebrum (pr). The oesophageal foramen (Oe) reaches the caudal margin of the protocerebrum; second and third neuromeres flank the foramen. In Centruroides, the protocerebrum is recurved over the cheliceral (ch) and pedipalp (pp) neuromeres (homologues of Alalcomenaeus great appendage neuromere (GA) and first cephalic appendage neuromere (C1), and Limulus cheliceral and pedipalp neuromeres). C1–C3, first–third cephalic neuromeres; deu, deutocerebrum; L1–L4, first to fourth leg ganglia; op1, op2, first and second opisthosomal neuromeres; T1–T8, trunk ganglia 1–8; tri, tritocerebrum. Eyes shown in brown, faceted eyes indicated by radial divisions.

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The great appendage of Megacheira has variously been regarded as proto-2, deuto-3 or tritocerebral4. A deutocerebral identity is consistent with a structural homology between the great appendage and chelicera with respect to the elbow joint and arrangement of fixed and movable fingers4,7. Chelicerae are demonstrably deutocerebral based on Hox gene expression domains17. The arrangement of neural structures in Alalcomenaeus favours a deutocerebral innervation of the great appendage. The position of its ventral point of origin corresponds to that of the second largest neuromere, immediately posterior to the protocerebrum, itself defined by its connection with the separate optic neuropil. Although the great appendage is incomplete in YKLP 11075, its attachment point in other specimens of Alalcomenaeus (Fig. 3b) and in Leanchoilia (Fig. 3c) best corresponds to the position of the prominent deutocerebral neuromere in YKLP 11075.

The distribution of neuromeres in the head of YKLP 11075 conforms to the presence of three pairs of biramous limbs posterior to the great appendage, although only two pairs have been described from the Burgess Shale Alalcomenaeus cambricus15. Two pairs had likewise been documented in Leanchoilia superlata18, but a small first pair was subsequently identified in that species12. The presence of three pairs in the present Chengjiang Alalcomenaeus (Fig. 3a, b) suggests that this is a diagnostic feature of leanchoiliids generally, and brings this group into line with the ground pattern of crown-group euarthropods as well as trilobites, which possess paired uniramous antennae and three biramous post-antennal head segments19.

Descriptions of the Leanchoilia midgut show a uniformly broad, contiguous and segmentally convoluted organ system of associated glands distinct from segmental ganglia3, originating at the level of C3 and terminating at trunk segment T8 (ref. 20), whereas a more tubular gut tract is seen in Alalcomenaeus cambricus15. A gut identity can be ruled out for the nerve cord in Alalcomenaeus because of its continuity with the brain and the obvious intersegmental constrictions between segmental ganglia (Fig. 1e). In Alalcomenaeus the oesophageal foramen reaches forward to the caudal margin of the protocerebral neuromere (Figs 1e and 2a), demonstrating that in this taxon only the protocerebrum is supraoesophageal, a condition typifying Limulus and Centruroides and suggested as ancestral for chelicerates8. Chelicerate brains differ from those of mandibulates in that only the first-order visual neuropil of each eye lies separate from the brain, connected by relays to second- and third-order visual centres integrated within the protocerebrum. This organization, shared by pycnogonids21, xiphosurans22 and arachnids23, contrasts with mandibulates, in which three (Malacostraca, Insecta) or two (Scutigeromorpha) nested optic neuropils reside separate from, but connected to, the mid-brain proper1,8. Furthermore, other than in pycnogonids, all extant chelicerates, including Limulus, show fusion of cerebral and trunk ganglia. Alalcomenaeus shares these crucial elements of the chelicerate central nervous system ground pattern. Phylogenetic analysis of a comprehensive data set of neural characters24 (Supplementary Tables 1 and 2) resolves fusion of cerebral and trunk ganglia, and the single optic neuropil outside the protocerebrum, as apomorphies of Chelicerata s.l. (sensu lato; Pycnogonida and Euchelicerata), including Alalcomenaeus. The only arthropod outside the chelicerates known to possess a nervous system condensed into a single mass is the hemipteran water strider (Gerridae), but as in other mandibulates the three nested optic lobes extend laterally from the protocerebrum8. Segmentation of the postoral nervous system in Alalcomenaeus is a shared derived character of Euarthropoda rather than an indicator of affinity to a particular euarthropod clade.

Mandibulate arthropods possess just one pair of compound eyes, except where the upper and ventral halves are specialized to serve different perceptual functions, as in Bibionidae and Gyrinidae25,26. Multiple pairs of eyes typifies chelicerates. Possession of paired eyes disposed laterally and relaying to their optic neuropils fits the cladogram (Extended Data Fig. 2) as a derived character of Chelicerata s.l. including Alalcomenaeus. We infer this character to also apply to Leanchoilia where four visual units (as in Alalcomenaeus sp.) have been unambiguously described for L. superlata and L. persephone12,18. Structures in Leanchoilia interpreted as paired pendulous eyes ‘structured like a bunch of grapes’27 are likely cuticular features of the great appendages12.

The utility of computed synchrotron and phase-contrast radiation X-ray tomography for resolving soft tissue preservation has precedents in studies of ancient soft tissue from Cambrian Orsten trilobites28 and crustaceans29, including data on the gut, connective tissue and possible segmental muscle. For this account, computed tomography was achieved on a specimen that, unlike most Chengjiang specimens, showed considerable preservation in depth. Resolving nervous tissue resulted from scanning conjoined part and counterpart and subtracting contaminants of other tissue fragments (see Methods). Such combinatorial approaches should yield comparable internal details for other Burgess-Shale-type fossils that show appropriate dimensionality.

Methods Summary

Part and counterpart of the specimen (YKLP 11075) were precisely aligned for X-ray computed tomography (see Methods, Supplementary Information). Elemental distribution analyses were obtained using energy-dispersive X-ray fluorescence (EDXRF) microscopy. Light microscopy images were processed with Adobe Photoshop Elements 10 (Adobe Systems) using enhance functions for colour correction, balance, overlays, subtractions and inversions (see Methods, Supplementary Information and Figs 1d–g, 2e and Extended Data, Fig. 1).

Online Content Any additional Methods, Extended Data display items and Source Data are available in the online version of the paper; references unique to these sections appear only in the online paper.

Online Methods

Matrix obscuring parts of the fossil was removed with a fine needle under a binocular microscope. Part and counterpart of the specimen (YKLP 11075; stored at the Yunnan Key Laboratory for Palaeobiology, Yunnan University) were precisely aligned, wrapped in cotton wool for stability and placed into a film case. For X-ray computed tomography (CT) the encased specimen was scanned using a ScanXmate-L system (Comscantecno) at 151 kV with a resolution of 28.8 μm (Fig. 1c) or 14.4 μm (Fig. 1g and Extended Data Fig. 1). Molcer Plus software (White Rabbit) was used to convert the two-dimensional CT image stacks into a three-dimensional (3D) image. For Fig. 1c, volume rendering was performed on a 1332 TIFF image stack (28.8 μm stack intervals). For Fig. 1g and Extended Data Fig. 1, volume rendering was performed on a 1264 TIFF image stack (14.4 μm stack intervals). Contrast and brightness of the 3D images were processed with Molcer Plus software. Elemental distribution analyses were obtained using energy-dispersive X-ray fluorescence (EDXRF) microscopy. HORIBA XGT-7000V (HORIBA) at 50 kV accelerated voltage and 1 mA probe current, using mono-capillary primary optics to focus the X-ray beam to a diameter of 100 μm. YKLP 11075 was attached to an aluminium stage using conductive carbon tape, its position in the vacuum chamber adjusted using a motorised xyz platform, and viewed using three integrated colour video cameras. An area of 25.6 mm × 7.2 mm was analysed under full vacuum using 50 μm steps and 200 × 74 frames to provide two-dimensional distribution maps of Fe and Cu recorded as high-resolution TIFF images. Light microscopy photographs were taken with a Leica DFC 500 digital camera attached to a Leica M205C microscope. Images were processed with Adobe Photoshop Elements 10 (Adobe Systems) using enhance functions for colour correction, balance, overlays, subtractions and inversions (Figs 1d–g, 2e and Extended Data Fig. 1).

Each reconstruction in Fig. 4 has been scaled up or down to aid comparison. Figure 4b is based on published immunocytological data21. Figure 4c is adapted from histological observations of scorpion central nervous system8.

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Acknowledgements

We thank N. Shimobayashi, H. Maeda, and T. Kogiso for arranging and performing EDXRF analyses, and D. Andrew for advice on cladistics. This work was supported by grants from the Natural Science Foundation of China (no. 40730211), Research in Education and Science from the Government of Japan (no. 21740370), a Leverhulme Trust Research Project Grant (F/00 696/T), by the Center for Insect Science, University of Arizona, and a grant from the Air Force Research Laboratories (FA8651-10-1-0001) to N.J.S.

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Affiliations

  1. Japan Agency for Marine-Earth Science and Technology, Yokosuka 2370061, Japan

    • Gengo Tanaka

  2. Yunnan Key Laboratory for Palaeobiology, Yunnan University, Kunming 650091, China

    • Xianguang Hou
    •  & Xiaoya Ma

  3. Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

    • Xiaoya Ma
    •  & Gregory D. Edgecombe

  4. Department of Neuroscience and Center for Insect Science, University of Arizona, Tucson, 85721, Arizona, USA

    • Nicholas J. Strausfeld

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Contributions

The project was conceived by G.T. Fossil data were analysed by all authors. G.D.E., N.J.S. and X.M. composed the text.

Corresponding authors

Correspondence to Xianguang Hou or Nicholas J. Strausfeld.

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Extended data figures and tables

Extended Data Figure 1 Cephalic region of Alalcomenaeus sp. YKLP 11075

All in dorsal view, composites of part and counterpart (upper left). Second left to right: CT scan (green); EDXRF Fe (red); superimposition of CT and EDXRF Fe. Lower row, left to right: EDXRF Cu (blue); superimposition of CT and EDXRF Cu; superimposition of EDXRF Fe and EDXRF Cu; superimposition of all scans. C1, first post-GA neuropil = tritocerebrum (tri); C2, second post-GA neuropil; GA, great appendage neuropil = deutocerebrum (deu); on1, first optic neuropil; pr, protocerebrum.

Extended Data Figure 2 Arthropod relationships based on neuroanatomical characters.

Strict consensus of 34 shortest cladograms based on 145 characters in Supplementary Information Table 2.

Supplementary information

Supplementary Information

This file contains Supplementary Tables 1-2, Phylogenetic Methods and Supplementary References. (PDF 249 kb)

Supplementary Data

This zipped file contains characters coded in phylogenetic analysis (in nexus format, it can be opened in freeware such as Mesquite and Nexus Data Editor). (ZIP 3 kb)

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Tanaka, G., Hou, X., Ma, X. et al. Chelicerate neural ground pattern in a Cambrian great appendage arthropod. Nature 502, 364–367 (2013) doi:10.1038/nature12520

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