Cambrian bivalved arthropod reveals origin of arthrodization

Abstract

Extant arthropods are diverse and ubiquitous, forming a major constituent of most modern ecosystems. Evidence from early Palaeozoic Konservat Lagerstätten indicates that this has been the case since the Cambrian. Despite this, the details of arthropod origins remain obscure, although most hypotheses regard the first arthropods as benthic predators or scavengers such as the fuxianhuiids or megacheirans ('great-appendage' arthropods). Here, we describe a new arthropod from the Tulip Beds locality of the Burgess Shale Formation (Cambrian, series 3, stage 5) that possesses a weakly sclerotized thorax with filamentous appendages, encased in a bivalved carapace, and a strongly sclerotized, elongate abdomen and telson. A cladistic analysis resolved this taxon as the basal-most member of a paraphyletic grade of nekto-benthic forms with bivalved carapaces. This grade occurs at the base of Arthropoda (panarthropods with arthropodized trunk limbs) and suggests that arthrodization (sclerotization and jointing of the exoskeleton) evolved to facilitate swimming. Predatory and fully benthic habits evolved later in the euarthropod stem-lineage and are plesiomorphically retained in pycnogonids (sea spiders) and euchelicerates (horseshoe crabs and arachnids).

Figure 1.

Nereocaris exilis gen. et sp. nov. from the Cambrian (Stage 3) of British Columbia. (a) Holotype, Royal Ontario Museum (ROM) 61831. (b) Paratype ROM 61832. (c) Paratype ROM 61833. (d) Details of ocular region located in top box of (c), immersed in water. (e) Details of the appendicular region located in box of (a). (f) Details of the posterior part of the gut located in the posterior box of (c), showing three-dimensional preservation. All specimens were photographed using low-angle cross-polarized light. Accompanying camera lucida drawings in electronic supplementary material S1, figure S1. ah, anterior hook-like processes; as1–62, abdominal somites 1–62; cs, corneal surface; dk, dorsal keel; en, endopod; ep, eye peduncle; ex, exopod; fl, fluke; gut, gut; le, lateral eyes; ltp1–3, lateral telson processes 1–3; lv, left valve; mg, midgut glands; mtp, medial telson process; pm, photoreceptive material; sf, setal fringe; ts, thoracic segments.

Figure 2.

Reconstruction of Nereocaris exilis. A detailed reconstruction of the appendages can be found in the electronic supplementary material S1, figure S2.

Figure 3.

The phylogenetic position of Nereocaris and the origin of key innovations in Arthropoda. Summary of three most parsimonious trees (MPTs) of 91.98 steps (implied character weighting, k = 3; CI = 0.565; RI = 0.863; all nodes in the arthropod stem group are identical under equal weights). Complete phylogeny in electronic supplementary material S1, figure S4. Numbers in parentheses are the number of terminal taxa within supra-generic clades. Column at right is locomotory habit (B, benthic; N-B, nekto-benthic). Key innovations include: 1 compound eyes (as figured for Odaraia), although this character has disappeared and ‘re-evolved’ a number of times with Arthropoda; 2 arthropodized limbs (Anomalocaris)— it is unclear if the arthropodized cephalic limbs of radiodontans (Anomalocaris and Hurdia) are homologous to the arthropodized trunk limbs of arthropods; 3 (a) arthropodization and (b) biramy of the trunk appendages (Fuxianhuia), and (c) arthrodization of the trunk exoskeleton (Nereocaris); 4 specialization of the cephalic appendages into raptorial ‘great-appendages’ (Yohoia); 5 (a) division of trunk somites into distinct ventral sternites (Misszhouia) and (b) dorsal tergites with (c) paratergal folds (Shankouia); 6 (a) reduction in the number of trunk limb podomeres associated with (b) the acquisition of a rigid gnathobasic protopodite (Alalcomenaeus); 7 modification of the anterior (deutocerebral) appendages into antennae (Olenoides); 8 the origin of mandibular mastication (Locusta).