Canadia spinosa and the early evolution of the annelid nervous system

Abstract

Annelid worms are a disparate, primitively segmented clade of bilaterians that first appear during the early Cambrian Period. Reconstructing their early evolution is complicated by the extreme morphological diversity in early diverging lineages, rapid diversification, and sparse fossil record. Canadia spinosa, a Burgess Shale fossil polychaete, is redescribed as having palps with feeding grooves, a dorsal median antenna and biramous parapodia associated with the head and flanking a ventral mouth. Carbonaceously preserved features are identified as a terminal brain, circumoral connectives, a midventral ganglionated nerve cord and prominent parapodial nerves. Phylogenetic analysis recovers neuroanatomically simple extant taxa as the sister group of other annelids, but the phylogenetic position of Canadia suggests that the annelid ancestor was reasonably complex neuroanatomically and that reduction of the nervous system occurred several times independently in the subsequent 500 million years of annelid evolution.

Fig. 1. General anatomy of C. spinosa.

(A) USNM83929C, counterpart in dorsal view, polarized light, specimen underwater. (B) USNM277933, lateral view, note ventrally curved tips of notochaetae, polarized light, dry. (C) Elemental map for carbon of gill from USNM83929C part, position of equivalent gill of counterpart shown in (A). (D) Close-up view of head of USNM83929C, and anterior appendages, polarized light, dry. (E) Close-up view of anterior region of USNM83929D, polarized light, dry. (F) SEM backscatter image of median antenna of USNM83929D [area outlined in (E)]. (G) ROMIP65172.1 showing median antenna, reflected light, specimen under alcohol. (H and I) ROMIP65173, dorsal view. (H) Close-up view of palp and thick carbon band in palp, polarized light, specimen under ethanol. (I) SEM backscatter image showing carbon in the palp. Dashed boxes indicate positions of close up images. ma, median antenna; mo, mouth; nech, neurochaetae; noch, notochaetae; pa, palps; pagr, palp groove.

Fig. 2. Anterior nervous system of C. spinosa.

(A and B) USNM83929B, part in dorsal view. (A) Anterior region, polarized light, specimen under alcohol. (B) SEM-EDX map for carbon. (C) USNM83929B, counterpart, anterior region, cross-polarized light, specimen under alcohol. (D) USNM83929B, counterpart, SEM-EDX map for carbon. (E and F) Close-up view of region shown in box with dashed outline shown in (D). White arrowheads indicate carbonaceous preservation of the parapodial margin. (E) Cross-polarized light under ethanol. (F) SEM backscatter. (G to I) USNM275517, specimen in dorsal view. (G) Anterior segments, reflected light underwater. (H) Close-up view of head, SEM backscatter. (I) Close-up view of palp showing feeding groove/innervation. (J and K) Close-up view of anterior region of ROMIP65174, specimen in dorsal view. (J) Reflected light under ethanol. (K) SEM backscatter. (L and M) ROMIP65175, part, specimen in dorsal view. (L) Anterior region, polarized light, photographed under ethanol. (M) Close-up view of head, SEM-EDX map for carbon. (N and O) ROMIP65176, juvenile in dorsal view. (N) Anterior segments, cross-polarized light under ethanol. (O) Close-up view of head and three anterior segments, SEM backscatter [area outlined in (N)]. (P) Confocal microscope image of Neanthes arenaceodentata (Aciculata) acetylated α-tubulin immunoreactivity is red, and cell nuclei are blue, refigured and modified from (50). Dashed boxes indicate positions of close-up images. an, antenna; cc, circumoral connective; cs, commissure; mo, mouth; nech, neurochaetae; noch, notochaetae; nop, notopodium (numbered by chaetiger); nph, nephridia; pa, palp; pan, parapodial nerve (numbered by chaetiger); pn, palp nerve; pyc, pygidial cirrus; sog, supraesophogeal ganglion; tnc, tentacular cirrus.

Fig. 3. Preservation of nervous tissue in C. spinosa in specimens preserved in ventral view.

(A to H) ROMIP56972, specimen in ventral view. (A) Complete specimen, reflected light, specimen underwater. (B) Anterior region, SEM-EDX elemental map for carbon. (C) SEM backscatter image showing ventral and parapodial nerves. (D) SEM backscatter image showing palp and right circumoral connective. (E) SEM backscatter image showing palp nerve and left circumoral connective. (F) Posterior segments, photographed in reflected light underwater. (G) SEM EDX map for carbon of region shown in (F). (H) SEM backscatter of boxed region in (G), arrowheads demark the outline of the gut superimposed on the ventral nerve cord. (I to K) GSC8232A, specimen in ventral view. (J) SEM backscatter showing ventral nerves and ventral nerve cord of boxed region in (I). (K) Close-up view of parapodial nerve and parapodial outlines preserved carbonaceously, arrowheads indicate the body margin. cc, circumoral connective; ga, ganglion; pa, palp; pan, parapodial nerve; pn, palp nerve; sn, segmental nerve; vnc, ventral nerve cord.

Fig. 4. Reconstruction and schematic reconstructions of annelid nervous systems plotted on a simplified phylogeny.

(A) Reconstruction by M. Collins © Royal Ontario Museum, all rights reserved (see also movie S1). (B) Simplified phylogeny of Annelida with C. spinosa recovered in the annelid stem group (see also the Supplementary Materials for the full phylogenetic results). Topology is based on the analysis using phylogenetic constraints based on recent phylogenomic trees. Proposed nervous system synapomorphies are shown at nodes, and inferred losses are shown along branches as cross marks. cc, circumoral connectives; ga, segmental ganglion; ma, median antenna; pan, parapodial nerve; pa, palp; sn, segmental nerve; sog, supraesophegeal ganglion; vnc, ventral nerve cord.