Brain structure resolves the segmental affinity of anomalocaridid appendages

Abstract

Despite being among the most celebrated taxa from Cambrian biotas, anomalocaridids (order Radiodonta) have provoked intense debate about their affinities within the moulting-animal clade that includes Arthropoda. Current alternatives identify anomalocaridids as either stem-group euarthropods, crown-group euarthropods near the ancestry of chelicerates, or a segmented ecdysozoan lineage with convergent similarity to arthropods in appendage construction. Determining unambiguous affinities has been impeded by uncertainties about the segmental affiliation of anomalocaridid frontal appendages. These structures are variably homologized with jointed appendages of the second (deutocerebral) head segment, including antennae and 'great appendages' of Cambrian arthropods, or with the paired antenniform frontal appendages of living Onychophora and some Cambrian lobopodians. Here we describe Lyrarapax unguispinus, a new anomalocaridid from the early Cambrian Chengjiang biota, southwest China, nearly complete specimens of which preserve traces of muscles, digestive tract and brain. The traces of brain provide the first direct evidence for the segmental composition of the anomalocaridid head and its appendicular organization. Carbon-rich areas in the head resolve paired pre-protocerebral ganglia at the origin of paired frontal appendages. The ganglia connect to areas indicative of a bilateral pre-oral brain that receives projections from the eyestalk neuropils and compound retina. The dorsal, segmented brain of L. unguispinus reinforces an alliance between anomalocaridids and arthropods rather than cycloneuralians. Correspondences in brain organization between anomalocaridids and Onychophora resolve pre-protocerebral ganglia, associated with pre-ocular frontal appendages, as characters of the last common ancestor of euarthropods and onychophorans. A position of Radiodonta on the euarthropod stem-lineage implies the transformation of frontal appendages to another structure in crown-group euarthropods, with gene expression and neuroanatomy providing strong evidence that the paired, pre-oral labrum is the remnant of paired frontal appendages.

Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda

“…Although the VNC would have continued into the head region in life, our material does not preserve any anterior neurological structures that have been previously identified as the dorsal brain or nerves leading to the antennae and specialized postantennal appendages (8). The absence of fossilized brains in these otherwise exceptionally preserved specimens can be attributed to the small sample size and moderate postmortem disarticulation; likewise, other studies addressing neurological structures in Cambrian fossils rarely report the CNS preserved in its entirety (8)(9)(10)(11). The VNC also expresses a distinctive dark/light color banding throughout its length, with the dark bands varying from black to reddish-brown…”

“…The ventral nerve cord (VNC) reflects fundamental aspects of panarthropod body organization that complement the organization of the brain and together illuminate the evolution of the CNS (1-3, 5, 7, 12-16). The early evolutionary history of the panarthropod postcephalic CNS, however, remains obscure due to the exclusive preservation of brains in most available fossils (8,10,11). Moreover, the unresolved phylogenetic relationships within Panarthropoda complicate accurate reconstruction of the CNS ground pattern (16)(17)(18)(19)(20)(21)(22).…”

“…Identification of fossilized nervous tissues has provided a unique perspective on early euarthropod brain neuroanatomy and suggests that broad patterns of extant neurological diversity were already in place by the Cambrian (8)(9)(10)(11). The ventral nerve cord (VNC) reflects fundamental aspects of panarthropod body organization that complement the organization of the brain and together illuminate the evolution of the CNS (1-3, 5, 7, 12-16).…”

Hurdiid radiodontans from the middle Cambrian (Series 3) of Utah

“…Recent phylogenies (Cong et al, 2014;Van Roy et al, 2015) However, H. victoria specimens with straight proximal ventral spines and anteriorly curving distal ends are common (e.g. Daley et al, 2013, fig.…”

“…Further, we identify H. victoria in the Spence Shale for the first time. A 3D model of an idealized Hurdia appendage potentially allows characters used in previous phylogenetic analyses (e.g., Vinther et al, 2014;Cong et al, 2014;Van Roy et al, 2015) to be visualized and evaluated in the hopes of possibly inferring which characters might be influenced by taphonomic factors.…”