Cambrian comb jellies from Utah illuminate the early evolution of nervous and sensory systems in ctenophores

Abstract

Ctenophores are a group of predatory macroinvertebrates whose controversial phylogenetic position has prompted several competing hypotheses regarding the evolution of animal organ systems. Although ctenophores date back at least to the Cambrian, they have a poor fossil record due to their gelatinous bodies. Here, we describe two ctenophore species from the Cambrian of Utah, which illuminate the early evolution of nervous and sensory features in the phylum. Thalassostaphylos elegans has 16 comb rows, an oral skirt, and an apical organ with polar fields. Ctenorhabdotus campanelliformis has 24 comb rows, an oral skirt, an apical organ enclosed by a capsule and neurological tissues preserved as carbonaceous films. These are concentrated around the apical organ and ciliated furrows, which connect to a circumoral nerve ring via longitudinal axons. C. campanelliformis deviates from the neuroanatomy of living ctenophores and demonstrates a substantial complexity in the nervous system of Cambrian ctenophores.

Keywords: biological sciences; evolutionary biology; phylogenetics.

Graphical abstract

Figure 1

Holotype specimen of Thalassostaphylos elegans gen. et sp. nov. from the Drumian Marjum Formation in Utah (A) Whole specimen UMNH.IP.6086 photographed underwater using cross polarized light. (B) Interpretative drawing of whole specimen showing main body regions and anatomy. (C) Details of comb row, white arrows indicate position of transverse bars interpreted as the cushion plates that underlie the comb rows. (D) Detail of apical organ polar fields. (E) Close up of the oral skirt and the comb rows closest to the oral region. Abbreviations: cr – comb row, os – oral skirt, pf – polar fields.

Figure 2

Holotype specimen of Ctenorhabdotus campanelliformis sp. nov. from the Drumian Marjum Formation in Utah (A and B) Counterpart and part (mirrored) of UMNH.IP.6125, photographed immersed in water under cross polarized light; dotted line in panel (A) indicates area examined for elemental analysis. (C) Energy-dispersive spectroscopy (EDS) elemental map of carbon in the counterpart. (D) Interpretative drawing of whole specimen, colors as in Figure 1 and as shown.

Figure 3

Anatomical details of Ctenorhabdotus campanelliformis sp. nov (A and B) Close up of the aboral region and ciliary grooves shown in UMNH.IP.6125b under cross polarized light (A) and in EDS carbon map (B). (C) Interpretative drawing of region shown in (A and B) based on both the part and counterpart. (D) Close-up of the apical organ and the capsule surrounding it in UMNH.IP.6125a, white arrows indicate the carbon film lining the apical organ. (E and F) Details of the comb rows and nerves in the oral region of UMNH.IP.6125a (E) and UMNH.IP.6125b (F), arrowheads indicate the position of giant axons. (G) EDS carbon map in the region shown in (F), and white arrows show the transverse ctenes. (H and I) Details of the comb rows and nerves from the oral to aboral regions of part of UMNH.IP.6125a (H) and UMNH.IP.6125b (I). (J) EDS carbon map for the region shown in I, white arrows show the transverse ctenes. (K–N) Details of the oral nerve ring of UMNH.IP.6125b (M) and UMNH.IP.6125a (K). (L) EDS carbon map in the region shown in (K). (N) Interpretative drawing of region shown in (K and L) based on features preserved in both the part and counterpart. The images of UMNH.IP.6125b have been mirrored to facilitate easier comparison between the part and counterpart.

Figure 4

Reconstruction of Thalassostaphylos elegans and Ctenorhabdotus campanelliformis (A and B) Technical drawings showing major anatomical features of T. elegans (A) and C. campanelliformis (B). (C) Life reconstructions of T. elegans (bottom) and C. campanelliformis (top). Artwork in all panels by Holly Sullivan.

Figure 5

Phylogeny and ancestral state reconstruction incorporating Ctenorhabdotus campanelliformis and Thalassostaphylos elegans Phylogenetic inferred from a character matrix of animals consisting of 285 characters. Note that the tree has been truncated at the node subtending Siphusauctum (see Figures S3 and S4 for full results). Numbers at nodes are posterior probabilities for the unconstrained analysis (top) and an analysis where Euplokamis is constrained as the sister group of all extant ctenophores (bottom). Tile plots illustrate posterior probabilities of ancestral states at selected nodes from Bayesian analysis of both the constrained and unconstrained analysis.