The origin and early evolution of Panarthropoda

Abstract

Exceptionally-preserved fossils are key to reconstructing the origins of the modern animal body plans in the Cambrian radiation. The panarthropod phyla Euarthropoda, Onychophora, and Tardigrada have roots in a lobopodian grade of worm-like animals with fluid-filled appendages. From such forebears evolved Radiodonta, characterised by segmented frontal appendages; in turn, the Euarthropods have their roots in radiodont-like organisms. Whether these panarthropod phyla originated in the Cambrian or have a cryptic Precambrian origin is debated.

Early-diverging lobopodians have locomotory appendages. The evolutionary transition from a legless worm to a lobopodian is missing from the fossil record. By describing fine details of the ventral projections of the worm Cricocosmia jinningensis, I show that these projections are plausible precursors to lobopodian legs and their cone-in-cone claws. Phylogenetic tests confirm that Cricocosmia is a plausible morphological intermediate between legless worms and legged lobopodians, providing a robust model for the origin of panarthropod legs by the elongation of ventral projections.

Fully “arthropodized” appendages and cephalic armature also appear abruptly in the fossil record. Opabinia regalis could be pertinent to the origin of these features; however, its lack of characters shared with stem-group euarthropods has resulted in disagreements on the interpretation and phylogenetic significance of its morphology. My re-examination of fossils of Opabinia regalis from the Burgess Shale of British Colombia reveals the presence of trunk nodes, circumoral plates, a dorsal cephalic sclerite, and terminal spines on its frontal appendages. My analyses confirm that the combination of “lobopodian” characters (dorsal trunk nodes, terminal appendage spines, oral apparatus with equal sized plates) and “radiodontan” characters (dorsal sclerite, eye stalks) signifies an evolutionary position intermediate between these groups; Opabinia is one of the earliest stem-group euarthropods to exhibit cephalic sclerites and stalked eyes.

Further, my phylogenetic analyses consistently recover a paraphyletic Radiodonta, clarifying that the ancestral euarthropod exhibited anterior, downward directed, segmented, radiodont-like appendages. More derived euarthropods exhibit ventral, upward directed appendages – suggesting a 180° rotation and migration of anterior appendages. A similar transformation characterizes the euarthropod labrum during development. These fossil data corroborate the hypothesis that the labrum, a structure observed in almost all euarthropods, is derived from the first segment appendages (homologous to the onychophoran antennae).

These results give novel insights into the morphological transitions from worm to lobopodian to radiodont to euarthropod. To understand the timing of these transitions it is necessary to turn to fossil records which have a more complete stratigraphic range than Lagerstätten. I thus integrated the shelly and carbonaceous microfossil records with the trace fossil record to assess the earliest occurrences of Panarthropoda and its major sub-clades such as Euarthropoda. My review of the trace fossil record suggests that Fortunian (Cambrian Stage 1) Rusophycus cannot be considered a euarthropod trace fossil, given that lophotrochozoans make similar traces under experimental conditions. On this basis, my review of the early panarthropod body fossil record demonstrates a consistent picture in the trace, shelly, and carbonaceous fossil records: lobopodians and stem-group panarthropods first occur in Cambrian Stage 2, and the first appearance of stem-group euarthropods is in the terminal Stage 2, closely followed by the crown group. Body fossils of higher euarthropod orders (e.g., Pancrustacea) are found in Stage 3 and younger strata.

My assessment of key taxa fills some of the outstanding gaps in panarthropod evolution, particularly regarding the origins of legs and “arthropodized” appendages. Further, my examination of the fossil record suggests that by integrating various fossilization modes and robust experimentally-led interpretations, a reasonable timeline of panarthropod evolutionary transitions can be uncovered. Together, these data provide a more complete picture of the evolutionary origin of the crown group panarthropod phyla and elucidate the morphological changes underpinning their radiation.