Brain and eyes of Kerygmachela reveal protocerebral ancestry of the panarthropod head

Abstract

Recent discoveries of fossil nervous tissue in Cambrian fossils have allowed researchers to trace the origin and evolution of the complex arthropod head and brain based on stem groups close to the origin of the clade, rather than on extant, highly derived members. Here we show that Kerygmachela from Sirius Passet, North Greenland, a primitive stem-group euarthropod, exhibits a diminutive (protocerebral) brain that innervates both the eyes and frontal appendages. It has been surmised, based on developmental evidence, that the ancestor of vertebrates and arthropods had a tripartite brain, which is refuted by the fossil evidence presented here. Furthermore, based on the discovery of eyes in Kerygmachela, we suggest that the complex compound eyes in arthropods evolved from simple ocelli, present in onychophorans and tardigrades, rather than through the incorporation of a set of modified limbs.

Fig. 1

Kerygmachela kierkegaardi from the Cambrian Stage 3 of North Greenland. a–e MGUH 32048a. a Overview of part. b An interpretive drawing of a. c and d Magnified images of the head region of a. c Under high-angle polarized lighting. d Under low-angle lighting. e Interpretive drawing of c and d. f MGUH 32048b, the counterpart of MGUH 32048a; a wavelength dispersive X-ray elemental map of carbon of the head region. Carbon-rich region (red), superimposed upon the topographic map (blue), representing the frontal appendage nervous tracts and the anterior neural projections. al anterior lobe, el eye lobe, fpo outermost frontal process, inn non-neural impression, mo mouth opening, nap anterior neural projection, nfa frontal appendage nervous tract, npc protocerebrum, nop optic neuron, okl overprint of Kleptothule arthropod specimen, phr pharynx, rs rostral spine, ts tail spine

Fig. 2

Details of head structure in Kerygmachela kierkegaardi. a–d MGUH 32049. a Under high-angle polarized lighting. b Under low-angle lighting. c Wavelength dispersive X-ray elemental map of carbon of the head region. d Interpretive drawing of a and b. e–g MGUH 32050. e Under high-angle polarized lighting. f Under low-angle lighting. g Wavelength dispersive X-ray elemental map of carbon of the head region. h Interpretive drawing of e and f. eyd displaced eye structure, eyo original outline of eye lobe, inn non-neural impression, nap anterior neural projection, nc nerve cord, nfa frontal appendage nervous tract, npc protocerebrum, nop optic nerve, phr pharynx, rs rostral spine

Fig. 3

Reconstruction of Kerygmachela kierkegaardi. a Dorsal reconstruction of the head region with the central nervous system (orange), anterior neural projection (yellow), and muscular pharynx (blue). b Artistic reconstruction of K. kierkegaardi. el eye lobe, mo mouth opening, nap anterior neural projection, nb branching of nerve, nc nerve cord, nfa frontal appendage nervous tract, npc protocerebrum, nop optic nerve, phr pharynx. Artwork by Rebecca Gelernter (nearbirdstudios.com)

Fig. 4

A panarthropod phylogenetic tree with diagrammatic summary of central nervous system (CNS) and evolution of visual structures within Panarthropoda. a Diagrammatic representation of the CNS in panarthropod lineages, with the inferred CNS condition in the last common ancestor (LCA) of panarthropods. Although it is not unequivocal, the lack of segmental ganglia in the trunk of onychophorans and the stem-group euarthropod Lyrarapax suggests that segmental ganglia were absent in the LCA of panarthropods. b Visual structures of different panarthropod lineages. The diagrammatic representations of the visual organs of Tardigrada and Onychophora are modified from ref.. “Cambrian lobopodians” is also referred to as xenusians in the literature. The polytomy in this cladogram represents the unresolved phylogenetic relationship among Tardigrada, Onychophora, “Cambrian lobopodians,” and the total-group euarthropods