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Cambrian Lobopodians and Extant Onychophorans Provide New Insights Into Early Cephalization in Panarthropoda

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Cambrian Lobopodians and Extant Onychophorans Provide New Insights Into Early Cephalization in Panarthropoda

Qiang Ou et al. Nat Commun.

Abstract

Cambrian lobopodians are important for understanding the evolution of arthropods, but despite their soft-bodied preservation, the organization of the cephalic region remains obscure. Here we describe new material of the early Cambrian lobopodian Onychodictyon ferox from southern China, which reveals hitherto unknown head structures. These include a proboscis with a terminal mouth, an anterior arcuate sclerite, a pair of ocellus-like eyes and branched, antenniform appendages associated with this ocular segment. These findings, combined with a comparison with other lobopodians, suggest that the head of the last common ancestor of fossil lobopodians and extant panarthropods comprized a single ocular segment with a proboscis and terminal mouth. The lack of specialized mouthparts in O. ferox and the involvement of non-homologous mouthparts in onychophorans, tardigrades and arthropods argue against a common origin of definitive mouth openings among panarthropods, whereas the embryonic stomodaeum might well be homologous at least in Onychophora and Arthropoda.

Figures

Figure 1
Figure 1. Anterior body region of the lobopodian O. ferox.
Amongst the most conspicuous structures are the feathery, antenniform appendages, the proboscis with a terminal mouth and the ocellus-like eye at the basis of each antenniform appendage.
Figure 2
Figure 2. Anatomy of the lobopodians O. ferox and A. pedunculata.
(ah) O. ferox. (a) Laterally compressed specimen ELEL-SJ101888A; anterior is right. (b) Dorsoventrally compressed specimen ELEL-EJ100329A; anterior is left. (c) Close-up of anterior end in a showing head structures and outline of bulbous pharynx (dotted lines). Arrow points to mouth. (d) Close-up of anterior end in b showing a pair of branched antenniform appendages (branches indicated by arrowheads). (e) Specimen ELEL-SJ102011A showing left antenniform appendage with branches. Note annulations of antenniform appendage (arrowheads) and claws on first walking lobopod. (f) Specimen ELEL-SJ100307B showing an eye with a lens-like structure. Arrow indicates mouth. (g,h) Specimens ELEL-SJ100635 and ELEL-SJ100546A showing anterior anatomy, notably proboscis, eye and branched antenniform appendages. (i) Anterior end of A. pedunculata. Note branched antenniform appendages, eye-like structure (arrowhead) and putative proboscis delineated from the rest of the body. as, arcuate sclerite; at, antenniform appendage; bt, buccal tube; cl, claw; ey, eye; gu, gut; le1–le12, walking lobopods 1–12; lu, pharyngeal lumen; pb, proboscis; ph, pharynx; sc, sclerotized plate; vp, ventral papillae. Scale bars, 1 cm in a and b; 2 mm in ci.
Figure 3
Figure 3. Mouth development in the onychophoran E. rowelli.
Note that three consecutive mouth openings arise during onychophoran ontogeny (indicated by green, red and white dotted lines, respectively). (ae) Confocal micrographs of embryos at subsequent developmental stages in ventral view, labelled with the DNA-marker Hoechst as described previously. Anterior is up. Presumptive jaws are coloured artificially in yellow. (a) Embryonic disc of a late stage 1 embryo. Note the first embryonic mouth (em) arising at the anterior end of the slit-like blastopore. Developing segments are numbered. Arrowheads point to closing blastoporal lips. (b) Anterior end of an early stage 4 embryo. Note the position of the stomodaeum (second mouth) at the posterior border of the antennal segment. (c) Anterior end of a late stage 4 embryo. Note the beginning formation of lips that originate from three different segments (white dotted lines). Asterisks indicate openings of presumptive salivary glands. (d) Anterior end of a stage 5 embryo showing the formation of the definitive (third) mouth. Note that the stomodaeum and the anlagen of jaws and tongue are incorporated into the mouth cavity. (e) Anterior end of a stage 7 embryo. Mouth development is completed and lips surround the circular mouth opening. (f) Diagram of an adult onychophoran illustrating regions of digestive tract that correspond to the three consecutive embryonic mouth openings (dotted lines with Roman numerals I–III). Dorsal is up, anterior is right. an, developing anus; at, antenna; em, first embryonic mouth (derivative of the blastopore); jw, jaw; le1–le4, legs 1–4; lp, developing lips; mc, mouth cavity; mg, midgut; oe, oesophagus; ph, pharynx; so, stomodaeum; sp, slime papilla; to, presumptive tongue. Scale bars, 200 μm in ae.
Figure 4
Figure 4. Alignment and homology of anterior appendages in the lobopodian O. ferox and among extant panarthropods.
Homologous appendages are depicted by corresponding colour. Vertical dotted lines indicate segmental borders. Black and checked ovals represent ocelli and compound eyes, respectively. Alignment of head segments in tardigrades is based on the assumption of serial homology of the stylet with distal leg portions. Note that segmental identity and homology of the arthropod labrum is discussed controversially. Dark-grey hatched area in the diagram on mandibulate arthropods indicates segments that do not contribute to adult mouth formation. Note that non-homologous segments and structures are involved in adult mouth apparatuses in O. ferox and different groups of extant panarthropods. af, antenniform appendage; at, antenna; at1, first antenna; at2, second antenna (indicated by a dotted line, as it occurs only in crustaceans); ch, chelicera; ic, intercalary segment (limbless in myriapods and hexapods); jw, jaw; lb, labrum (question mark highlights the uncertain segmental identity and homology of this structure); le, walking limbs/lobopods; md, mandible; mx, maxilla; pb, proboscis; pp, pedipalp; sp, slime papilla; st, stylet.

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