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.2020 Apr 21;117(16):8966-8972.
doi: 10.1073/pnas.1920733117. Epub 2020 Apr 6.

Aquatic stem group myriapods close a gap between molecular divergence dates and the terrestrial fossil record

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Aquatic stem group myriapods close a gap between molecular divergence dates and the terrestrial fossil record

Gregory D Edgecombe et al. Proc Natl Acad Sci U S A..

Abstract

Identifying marine or freshwater fossils that belong to the stem groups of the major terrestrial arthropod radiations is a longstanding challenge. Molecular dating and fossils of their pancrustacean sister group predict that myriapods originated in the Cambrian, much earlier than their oldest known fossils, but uncertainty about stem group Myriapoda confounds efforts to resolve the timing of the group's terrestrialization. Among a small set of candidates for membership in the stem group of Myriapoda, the Cambrian to Triassic euthycarcinoids have repeatedly been singled out. The only known Devonian euthycarcinoid,Heterocrania rhyniensis from the Rhynie and Windyfield cherts hot spring complex in Scotland, reveals details of head structures that constrain the evolutionary position of euthycarcinoids. The head capsule houses an anterior cuticular tentorium, a feature uniquely shared by myriapods and hexapods. Confocal microscopy recovers myriapod-like characters of the preoral chamber, such as a prominent hypopharynx supported by tentorial bars and superlinguae between the mandibles and hypopharynx, reinforcing an alliance between euthycarcinoids and myriapods recovered in recent phylogenetic analysis. The Cambrian occurrence of the earliest euthycarcinoids supplies the oldest compelling evidence for an aquatic stem group for either Myriapoda or Hexapoda, previously a lacuna in the body fossil record of these otherwise terrestrial lineages until the Silurian and Devonian, respectively. The trace fossil record of euthycarcinoids in the Cambrian and Ordovician reveals amphibious locomotion in tidal environments and fills a gap between molecular estimates for myriapod origins in the Cambrian and a post-Ordovician crown group fossil record.

Keywords: Arthropoda; Myriapoda; euthycarcinoid; molecular dating; terrestrialization.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
H. rhyniensis. (A) Reconstruction in dorsal view (modified from ref. 13). (B andC) Transverse section of head, NMS G.2014.11.1.1, showing compound eyes. Left eye magnified inC; arrows point to ommatidia. (Scale bars: 250 µm inB, 50 µm inC.) (D andE) Light microscopy (D) and confocal microscopy (E) images of isolated eye, NMS 1925.9.11.1. (Scale bars: 50 µm.) (F andG) Light microscopy (F) and confocal microscopy (G) images of isolated eye, GLAHM Kid2475. (Scale bar: 50 µm.) ey, eye; Md, mandible; te, cephalic tergite; st; sternite.
Fig. 2.
Fig. 2.
Preoral chamber ofH. rhyniensis in light microscopy (A) and confocal microscopy (B andF) and scanning electron micrographs of extant Myriapoda (C–E) for comparison. (A,B, andF)H. rhyniensis, NHM PI In 24658. (A) Transverse section of head, light microscopy photograph, with the buccal apparatus medially. (Inset) Corresponding to the confocal laser scan shown inB. (Scale bars: 100 µm inA, 25 µm inB.) (F) Confocal laser image of detail of proximal lobe of hypopharynx, showing sensilla coeloconica (arrows). (Scale bar: 10 µm.) (C)Polydesmus angustus (Diplopoda). (Scale bar: 50 µm.) (D andE)Hanseniella agilis (Symphyla). (D) Mouthparts, with left mandible removed to expose superlingua. (Scale bar: 25 µm.) (E) Hypopharynx and left superlingua. (Scale bar: 25 µm.) hy1, proximal lobe of hypopharynx; hy2, distal lobe of hypopharynx (lingua); la, labrum; Md, mandible; MxI, first maxilla; MxII, second maxilla (labium); Sl, superlingua.
Fig. 3.
Fig. 3.
Cuticular skeleton ofH. rhyniensis and corresponding structures in extant Myriapoda in light microscopy (A–D,G, andJ) and scanning electron microscopy (E andF) images. (A andB)H. rhyniensis, NMS G.2014.11.1.1. (A) Transverse section of the head (Scale bar: 200 µm.) (B) Transverse section of the trunk. (Scale bar: 250 µm.) (C)Dicellophilus carniolensis (Chilopoda: Geophilomorpha), transverse section of the head. (Scale bar: 200 µm.) The supramandibular arch of the tentorium (sat) continues into the posterior process (pp inA) more posteriorly. (D)Polydesmus angustus (Diplopoda: Polydesmida), transverse section of the head. (Scale bar: 250 µm.) (E andF)Orya almohadensis (Chilopoda: Geophilomorpha), scanning electron micrographs of pharynx (ph) and hypopharynx (hy).Inset inE shows cluster of spear-shaped sensilla near mouth (F). (Scale bars: 100 µm inE, 10 µm inF.) (G) Cuticular support of the hypopharynx inH. rhyniensis, NHM PI In 24658. (Scale bar: 20 µm.) (see also Fig. 2A,B, andF). (H–J) Cuticular support of the hypopharynx in Chilopoda. (H)Lithobius (Ezembius)giganteus (Sseliwanoff, 1881) (Lithobiomorpha). (Scale bar: 150 µm.) (I)Scolopocryptops spinicaudus Wood, 1862 (Scolopendromorpha). Arrowheads indicate a cluster of sensilla near the mouth. (Scale bar: 150 µm.) Reprinted with permission from ref. . (J)Thereuopodina queenslandica Verhoeff, 1925 (Scutigeromorpha). (Scale bar: 100 µm.) aa, appendicular apodeme; ba, basal part of appendage; df, distal fork; ey, eye; glt, mandibular gnathal lobe tendon; hb, hypopharyngeal bar of tentorium; hy1, proximal lobe of hypopharynx; la, labrum; lf, lateral flap of hypopharynx; mb, marginal bar; Md, mandible; mo, mouth; MxI, first maxilla; pf, proximal fork; pp, posterior process of tentorium; vlb, ventrolateral bar.E–F: Reprinted from ref. , by permission of Oxford University Press.
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