Unlocking the early fossil record of the arthropod central nervous system

Abstract

Extant panarthropods (euarthropods, onychophorans and tardigrades) are hallmarked by stunning morphological and taxonomic diversity, but their central nervous systems (CNS) are relatively conserved. The timing of divergences of the ground pattern CNS organization of the major panarthropod clades has been poorly constrained because of a scarcity of data from their early fossil record. Although the CNS has been documented in three-dimensional detail in insects from Cenozoic ambers, it is widely assumed that these tissues are too prone to decay to withstand other styles of fossilization or geologically older preservation. However, Cambrian Burgess Shale-type compressions have emerged as sources of fossilized brains and nerve cords. CNS in these Cambrian fossils are preserved as carbon films or as iron oxides/hydroxides after pyrite in association with carbon. Experiments with carcasses compacted in fine-grained sediment depict preservation of neural tissue for a more prolonged temporal window than anticipated by decay experiments in other media. CNS and compound eye characters in exceptionally preserved Cambrian fossils predict divergences of the mandibulate and chelicerate ground patterns by Cambrian Stage 3 (ca 518 Ma), a dating that is compatible with molecular estimates for these splits.

Keywords: Arthropoda; Burgess Shale; Cambrian; Chengjiang; brains.

Figure 1.

Entombment experiment with Nereis virens compared with fossilized CNS in the Cambrian euarthropod Chengjiangocaris. (a) N. virens after compression and desiccation in clay. Inset shows ventral nerve cord. (b) Chengjiangocaris kunmingensis [28], showing ventral nerve cord with segmental ganglia in the trunk (image courtesy of J. Yang, J. Ortega-Hernández and X. Zhang). Scale bar, 1 mm.

Figure 2.

Experimental flattening of cockroach brain. (a) Fresh excised brain of Periplaneta americana. (b) Brain embedded in slurry of wet clay. (c) Compacted, drying brain in clay. (d) Flattened brain removed from clay. spr, superior protocerebrum; de, deutocerebrum; tri, tritocerebrum; ol, optic lobe; an, antennal nerve; vnc, ventral nerve connective.

Figure 3.

Cambrian Burgess Shale-type fossils preserving traces of the CNS. (a) Ottoia prolifica, USNM 188635, showing ventral nerve cord (vnc) as paired strands. (b) Waptia fieldensis, USNM 83948j, anterior part of head with inverted light. (c) Odaraia expansa, ROM 60746, anterior cephalic structures in cross-polarized light (image from http://burgess-shale.rom.on.ca/en/index.php, courtesy of Jean-Bernard Caron, Royal Ontario Museum). (d,e) Lyrarapax unguispinus, YKLP 13305, anterior part of head: (d) SEM-EDX carbon map; (e) light photograph. (f) Fuxianhuia protensa, YKLP 15006a, anterior cephalic structures, micro X-ray fluorescence iron map (lavender). (g) Alalcomenaeus sp., YKLP 11075, head, neural traces in inverted white coincidence signal of micro-CT (green) and SEM-EDX iron map (magenta). a1, antennal (deutocerebral) tract; a2, tritocerebral tract; an, antenna; br, brain; e, eye; frg, frontal ganglion; lp, lateral protocerebrum; mp, median photoreceptor; of, oesophaegeal foramen; on, optic neuropil; opt, optic tract; pl, protocerebral lobe; pr, protocerebrum. Scale bars, 2 mm except a, 5 mm.

Figure 4.

Neural tissue preservation in Fuxianhuia protensa. (a) Carbon on nerve track from deutocerebral region (YKLP 15006b, counterpart); (b) pyrite framboids and crystals from eye region (YKLP 15006a, part). Scale bars, 20 µm.