Ancestral morphology of Ecdysozoa constrained by an early Cambrian stem group ecdysozoan

Abstract

Background: Ecdysozoa are the moulting protostomes, including arthropods, tardigrades, and nematodes. Both the molecular and fossil records indicate that Ecdysozoa is an ancient group originating in the terminal Proterozoic, and exceptional fossil biotas show their dominance and diversity at the beginning of the Phanerozoic. However, the nature of the ecdysozoan common ancestor has been difficult to ascertain due to the extreme morphological diversity of extant Ecdysozoa, and the lack of early diverging taxa in ancient fossil biotas.

Results: Here we re-describe Acosmia maotiania from the early Cambrian Chengjiang Biota of Yunnan Province, China and assign it to stem group Ecdysozoa. Acosmia features a two-part body, with an anterior proboscis bearing a terminal mouth and muscular pharynx, and a posterior annulated trunk with a through gut. Morphological phylogenetic analyses of the protostomes using parsimony, maximum likelihood and Bayesian inference, with coding informed by published experimental decay studies, each placed Acosmia as sister taxon to Cycloneuralia + Panarthropoda-i.e. stem group Ecdysozoa. Ancestral state probabilities were calculated for key ecdysozoan nodes, in order to test characters inferred from fossils to be ancestral for Ecdysozoa. Results support an ancestor of crown group ecdysozoans sharing an annulated vermiform body with a terminal mouth like Acosmia, but also possessing the pharyngeal armature and circumoral structures characteristic of Cambrian cycloneuralians and lobopodians.

Conclusions: Acosmia is the first taxon placed in the ecdysozoan stem group and provides a constraint to test hypotheses on the early evolution of Ecdysozoa. Our study suggests acquisition of pharyngeal armature, and therefore a change in feeding strategy (e.g. predation), may have characterised the origin and radiation of crown group ecdysozoans from Acosmia-like ancestors.

Keywords: Cambrian; Cycloneuralia; Ecdysozoa; Palaeobiology; Panarthropoda; Phylogenetics.

Fig. 1

RCCBYU 10233 Acosmia maotiania in lateral orientation. a Polarized light photograph. b Digitised Camera Lucida. c Close up of the oral and pharyngeal morphology, showing the mouth, lip, and pharyngeal ridges connecting to the associated elements in the anterior portion of the pharynx. Black triangles indicate possible oral spines. d Close up of the posterior trunk cuticle, showing posterior papillae and infilled gut. an annulations, ap anterior papillae, g gut, l lip, pe pharyngeal elements, phx pharynx, pp posterior papillae, pr pharyngeal ridges, sc sclerotized tissue, si sediment infill, tm terminal mouth. Extent of the gut (pink) and pharynx (red) highlighted

Fig. 2

RCCBYU 10235 Acosmia maotiania in lateral orientation. a Polarized light photograph. b Digitised Camera Lucida. 1 = first individual, 2 = second individual (unidentified), vnc ventral nerve cord, other abbreviations as in Fig. 1. Extent of the gut (pink) and pharynx (red) highlighted

Fig. 3

RCCBYU 10234 two individuals of Acosmia maotiania in lateral orientation. a Polarized light photograph of individual “a”. b Polarized light photograph of individual “b”. c Digitised Camera Lucida of individual “a”. d Digitised Camera Lucida of individual “b”. Abbreviations as for Fig. 1. Extent of the gut (pink) and pharynx (red) highlighted in both individuals

Fig. 4

YKLP 11410 Acosmia maotiania in lateral orientation. a Polarized light photograph. b Digitised Camera Lucida. Abbreviations as for Fig. 1. Extent of the gut (pink) and pharynx (red) highlighted

Fig. 5

Summary of tree searches, showing simplified topology of each optimality criterion. TGE total group Ecdysozoa, CGE crown group Ecdysozoa. See Methods for explanation of nodal support values. See supplementary material for full topologies. Silhouettes from phylopic.org. Acosmia life reconstruction credited to Franz Anthony

Fig. 6

Visualization of ancestral character state reconstructions. TGE total group Ecdysozoa, CGE crown group Ecdysozoa. Percentages in pie charts represent posterior probability of the state of presence (1) for that character. Silhouettes from phylopic.org. Acosmia life reconstruction credited to Franz Anthony

Fig. 7

Optimisation of well-supported ancestral characters on topology, with fossil exemplars. a Anterior terminal mouth of Acosmia maotiania (RCCBYU 10233) in lateral orientation (normal light). b Annulated trunk of Acosmia maotiania (RCCBYU 10235) in lateral orientation (polarized, low angle). c Circumoral structures (scalids) and pharyngeal armature (teeth) of Cricocosmia jinningensis (YKLP 11412) in lateral orientation (polarized, low angle). d Circumoral structures (plates) of Peytoia nathorsti (USNM 57538) in ventral orientation (polarized, low angle). cos circumoral structures; pha pharyngeal armature. Photograph D credited to Allison Daley, all others to Richard Howard. Silhouettes from phylopic.org. Acosmia life reconstruction credited to Franz Anthony