Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda

Abstract

Panarthropods are typified by disparate grades of neurological organization reflecting a complex evolutionary history. The fossil record offers a unique opportunity to reconstruct early character evolution of the nervous system via exceptional preservation in extinct representatives. Here we describe the neurological architecture of the ventral nerve cord (VNC) in the upper-stem group euarthropod Chengjiangocaris kunmingensis from the early Cambrian Xiaoshiba Lagerstätte (South China). The VNC of C. kunmingensis comprises a homonymous series of condensed ganglia that extend throughout the body, each associated with a pair of biramous limbs. Submillimetric preservation reveals numerous segmental and intersegmental nerve roots emerging from both sides of the VNC, which correspond topologically to the peripheral nerves of extant Priapulida and Onychophora. The fuxianhuiid VNC indicates that ancestral neurological features of Ecdysozoa persisted into derived members of stem-group Euarthropoda but were later lost in crown-group representatives. These findings illuminate the VNC ground pattern in Panarthropoda and suggest the independent secondary loss of cycloneuralian-like neurological characters in Tardigrada and Euarthropoda.

Keywords: Cambrian Explosion; Onychophora; Xiaoshiba Lagerstätte; phylogeny; stem-group Euarthropoda.

Fig. 1.

VNC in C. kunmingensis. Anterior at top. (A) YKLP 12023 (Holotype), complete specimen preserved in dorsal view with taphonomically dissected head shield (hs) showing internal organization of anterior region. (B) YKLP 12324, complete specimen preserved in dorsolateral view showing preserved VNC extending throughout the almost the entire length of the body. (C) YKLP 12324, magnification of VNC on the anterior trunk region showing the differential preservation of the condensed ganglia (ga) and longitudinal connectives (cn) as dark and light colored bands, respectively, and one-to-one correspondence between the ganglia and the walking legs (wl) (upper box in B). (D) YKLP 12024, magnification of the VNC on the posterior trunk region showing the progressive reduction of size of the ganglia and connectives toward the rear end of the body (lower box in B). Dotted lines highlight the anterior and posterior tergal borders of T15 for comparative purposes with the number of preserved ganglia. ant, antennae; SPA, specialized postantennal appendage; Tn, trunk tergites.

Fig. 2.

Fine neurological organization of the VNC in C. kunmingensis, YKLP 12026. Anterior is to the left. (A) Completely articulated specimen preserved in laterodorsal orientation with displaced head shield exposing VNC on anterior trunk region. (B) VNC showing the presence of seven sets of condensed ganglia (ga) linked by longitudinal connectives (cn) (box in A). (C) Composite fluorescence photograph of VNC (box in A). (D) Magnification of the VNC (box in B) showing regularly spaced peripheral nerve roots (arrowheads) emerging from the condensed ganglia and connective. (E) Composite fluorescence photograph magnification of the VNC (box in C).

Fig. S1.

Detail of well-preserved VNC in C. kunmingensis, specimen YKLP 12026. (A) Preserved VNC with seven sets of condensed ganglia. (B) Magnification of four posterior ganglia and their respective connectives. (C) Magnification of three anterior ganglia and their respective connectives, including the fine preservation of regularly spaced peripheral nerve roots (arrowheads) emerging at either side of the VNC. Abbreviations as in Fig. 1.

Fig. S2.

VNC preservation in C. kunmingensis. (A) YKLP 12322, complete articulated specimen preserved in dorsolateral view with exposed VNC on the posterior trunk region. (B) YKLP 12324a, articulated specimen in lateral view with exposed VNC on posterior trunk region, showing correlation between condensed ganglia and the walking legs. (C) YKLP 12324b, preservation of VNC on anterior trunk region, showing light coloration due to the advanced degree of weathering (compare with Fig. 2). Abbreviations as in Fig. 1. hs, head shield.

Fig. S3.

Morphological reconstruction of C. kunmingensis. (A) Complete exoskeletal morphology in ventral view showing arrangement of walking legs (wl) and their attachment sites to the body (wlas) relative to the preserved VNC (purple) and tergites (Tn); note that only T1–T5 have a one-to-one correspondence with the walking legs. (B) Overall view of the CNS, including the VNC and dorsal brain (the latter extrapolated from Fuxianhuia protensa; sensu 8); the gap between the VNC and brain reflects lack of paleontological data pertaining this region. (C) Magnification of the CNS; note the one-to-one correlation between the ganglia (ga) and T1–T5, and the presence of up to four ganglia on the remaining trunk tergites. (D) Neurological reconstruction of two condensed ganglia. Other abbreviations as in Figs. 1 and 3.

Fig. S4.

Raman spectroscopy analysis of VNC in C. kunmingensis. (A) Carbon (1,360 cm⁻¹) and organic carbon (1,604 cm⁻¹) were detected in the dark stripes within the VNC of YKLP 12026. (B) No mineral or organic constituent are detected by Raman spectroscopy in the light areas within the VNC of YKLP 12026. (C) Carbon (1,370 cm⁻¹) and organic carbon (1,603 cm⁻¹) were detected in the dark stripes within the VNC of YKLP 12320. (D) No mineral or organic constituent detected by Raman spectroscopy in the light areas within the VNC of YKLP 12320.

Fig. 3.

Simplified cladogram showing the evolution of the postcephalic CNS in Panarthropoda. Detailed results of the phylogenetic analysis are provided in Fig. S6 and SI Text. The topology supports a single origin for the condensed ganglia (ga) in the VNC in a clade including Tardigrada and Euarthropoda; note that the presence of multiple intersegmental peripheral nerves (ipn) in C. kunmingensis represents an ancestral condition. Given the morphological similarity between peripheral and leg nerve roots, the presence of a single pair of leg nerves (lgn) in C. kunmingensis is hypothetical (dashed lines) and based on the condition observed in crown-group Euarthropoda. †, fossil taxa; ?, uncertain character polarity within total-group Euarthropoda. asn, anterior segmental nerve; cn, longitudinal connectives; co, commissure; dln, dorsolateral longitudinal nerve; ico, interpedal median commissure; irc, incomplete ring commissure; pn, peripheral nerve; psn, posterior segmental nerve; rc, ring commissure. Reconstruction of VNC in Onychophora adapted from ref. .

Fig. S5.

Diversity of VNC organization in extant Panarthropoda. (A) E. kanangrensis (Peripatopsidae, Onychophora). VNC confocal micrograph stained with a monoclonal antibody directed toward acetylated tubulin (Sigma). Reprinted with permission from ref. . (B) M. cf harmsworthi (Eutardigrada, Tardigrada). VNC confocal micrograph stained with combined antityrosinated and antiacetylated α-tubulin immunolabeling. Reprinted with permission from ref. . (C) S. tulumensis (Remipedia, Euarthropoda). VNC confocal micrograph labeled for acetylated α-tubulin immunoreactivity (TUB-IR, yellow). Reprinted with permission from ref. . (D) S. gregaria (Hexapoda, Euarthropoda). VNC confocal micrograph stained with 8b7 immunocytochemistry (46). Abbreviations as in Figs. 1 and 3.

Fig. S6.

Summary of results from phylogenetic analyses. See SI Text and Dataset S2. (A) Strict consensus of 546 most parsimonious trees (MPTs) under equal weights [178 steps; consistency index (CI) = 0.65; retention index (RI) = 0.88]. (B) Strict consensus of 160 MPTs under implied weights (k = 0.1; CI = 0.64; RI = 0.87); this topology is stable when 1 ≤ k ≥ 0.1, with some variation in the number of MPTs. (C) Strict consensus of 146 MPTs under implied weights (k = 3; CI = 0.65; RI = 0.88); this topology is stable when 10 ≤ k ≥ 3, with some variation in the number of MPTs. (D) Strict consensus of 58 MPTs under implied weights (k = 20; CI = 0.65; RI = 0.88); this topology is stable when k ≥ 20, with some variation in number of MPTs. Color coding: stem-group Panarthropoda (dark pink), total-group Onychophora (green), total-group Tardigrada (red), total-group Euarthropoda (blue).

Fig. S7.

Evolution of the nervous system in Panarthropoda under an alternative phylogenetic hypothesis grouping Onychophora and Euarthropoda as sister taxa. Note that that these scenarios for the evolution of the panarthropod nervous system are less parsimonious compared with the topology obtained in the present study (Fig. S6). (A) Evolutionary scenario favoring substantial convergent evolution of the VNC in Tardigrada and Euarthropoda. (B) Evolutionary scenario favoring the secondary simplification of the neurological organization in Onychophora, derived from ancestors with a ganglionated VNC (30). †, fossil taxa; ?, uncertain neurological character polarity within total-group Euarthropoda.