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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 Aquatic stem group myriapods close a gap between molecular divergence dates and the terrestrial fossil record Gregory D. Edgecombea,1, Christine Strullu-Derriena,b, Tomasz Góralc,d, Alexander J. Hetheringtone, Christine Thompsonf, and Markus Kochg,h aDepartment of Earth Sciences, The Natural History Museum, London SW7 5BD, United Kingdom; bInstitut de Systématique, Evolution, Biodiversité, UMR 7205, Muséum National d’Histoire Naturelle, 75005 Paris, France; cImaging and Analysis Centre, The Natural History Museum, London SW7 5BD, United Kingdom; dCentre of New Technologies, University of Warsaw, 02-097 Warsaw, Poland; eDepartment of Plant Sciences, University of Oxford, Oxford OX1 2JD, United Kingdom; fDepartment of Natural Sciences, National Museums Scotland, Edinburgh EH1 1JF, United Kingdom; gSenckenberg Society for Nature Research, Leibniz Institution for Biodiversity and Earth System Research, 60325 Frankfurt am Main, Germany; and hInstitute for Evolutionary Biology and Ecology, University of Bonn, 53121 Bonn, Germany Edited by Conrad C. Labandeira, Smithsonian Institution, National Museum of Natural History, Washington, DC, and accepted by Editorial Board Member David Jablonski February 24, 2020 (received for review November 25, 2019) Identifying marine or freshwater fossils that belong to the stem (2–5). Despite this inferred antiquity, there are no compelling groups of the major terrestrial arthropod radiations is a long- fossil remains of Myriapoda until the mid-Silurian and no hexa- standing challenge. Molecular dating and fossils of their pancrus- pods until the Lower Devonian. In both cases, the oldest fossils tacean sister group predict that myriapods originated in the can be assigned to crown group lineages (Diplopoda in the case of Cambrian, much earlier than their oldest known fossils, but Silurian myriapods and Collembola in the case of Hexapoda) and uncertainty about stem group Myriapoda confounds efforts to the fossils have morphological characters shared by extant species resolve the timing of the group’s terrestrialization. Among a small that indicate terrestrial habits. The aquatic or terrestrial stem set of candidates for membership in the stem group of Myriapoda, groups of Myriapoda and Hexapoda remain unknown. the Cambrian to Triassic euthycarcinoids have repeatedly been Euthycarcinoidea, a group presently known from 18 species Heterocra- singled out. The only known Devonian euthycarcinoid, that span the mid-Cambrian to Middle Triassic, has repeatedly EVOLUTION nia rhyniensis from the Rhynie and Windyfield cherts hot spring been evoked as a candidate for filling this gap in knowledge about complex in Scotland, reveals details of head structures that con- myriapod or hexapod origins. That said, a vast range of alternative strain the evolutionary position of euthycarcinoids. The head cap- affinities have been suggested for euthycarcinoids, including a sule houses an anterior cuticular tentorium, a feature uniquely relationship to branchiopod crustaceans, merostomate chelicerates, shared by myriapods and hexapods. Confocal microscopy recovers trilobitomorphs, or the euarthropod stem group (reviewed in myriapod-like characters of the preoral chamber, such as a prom- ref. 6). More recent studies have restricted their systematic inent hypopharynx supported by tentorial bars and superlinguae position to Mandibulata (= Myriapoda and Pancrustacea), between the mandibles and hypopharynx, reinforcing an alliance based in part on the presence of mandibles as the main mouthpart between euthycarcinoids and myriapods recovered in recent phy- in several species (7). Some of these studies have more specifi- logenetic analysis. The Cambrian occurrence of the earliest euthy- cally proposed that euthycarcinoids are allied to hexapods or carcinoids supplies the oldest compelling evidence for an aquatic stem group for either Myriapoda or Hexapoda, previously a lacuna Significance in the body fossil record of these otherwise terrestrial lineages until the Silurian and Devonian, respectively. The trace fossil re- cord of euthycarcinoids in the Cambrian and Ordovician reveals Most arthropod diversity is now found on land, with hexapods amphibious locomotion in tidal environments and fills a gap be- (insects), arachnids, and myriapods being major terrestrial ra- tween molecular estimates for myriapod origins in the Cambrian diations. Molecular dating consistently predicts that these and a post-Ordovician crown group fossil record. groups have earlier evolutionary origins than are recorded by fossils. A reason for this difference between molecular- and fossil-based age estimates is that few candidates for marine or Arthropoda | Myriapoda | euthycarcinoid | terrestrialization | molecular dating freshwater stem groups of these terrestrial lineages have been identified. A Devonian euthycarcinoid arthropod preserves de- tails of the head shared by myriapods, adding support to the nowledge of the early fossil record of arthropods has made theory that they are each other’s closest relative. The fossil re- Kenormous advances in recent years, driven largely by new cord of euthycarcinoids in the Cambrian, including trackways discoveries in the Cambrian. Foremost among these are com- made on tidal flats, clarifies the marine-to-terrestrial transition in pression fossils from the Burgess Shale and sites of similar pres- the myriapod lineage and reconciles molecular and fossil-based ervation around the world, small carbonaceous fossils that record estimates for the timing of myriapod origins. minute details of crustacean mouthparts and other appendages, and phosphatized larval and juvenile remains (1). Taken together, Author contributions: G.D.E. and C.S.-D. designed research; G.D.E., C.S.-D., T.G., A.J.H., these fossils have allowed the early history of some pancrustacean C.T., and M.K. performed research; C.S.-D. and T.G. contributed new reagents/analytic lineages as well as chelicerates to be traced as far back as the tools; G.D.E. and M.K. analyzed data; and G.D.E. and M.K. wrote the paper. early Cambrian. The authors declare no competing interest. In contrast, Cambrian Konservat-Lagerstätten have remained This article is a PNAS Direct Submission. C.C.L. is a guest editor invited by the Editorial silent on the stem lineages of two major arthropod lineages, the Board. Myriapoda and Hexapoda. Fossil-calibrated molecular phyloge- Published under the PNAS license. nies predict that myriapods and hexapods both diverged from 1To whom correspondence may be addressed. Email: [email protected]. other extant arthropod lineages in the Cambrian, and there is This article contains supporting information online at https://www.pnas.org/lookup/suppl/ broad agreement from dated trees that Myriapoda and Hexapoda doi:10.1073/pnas.1920733117/-/DCSupplemental. began to diversify in the Cambrian and Ordovician, respectively www.pnas.org/cgi/doi/10.1073/pnas.1920733117 PNAS Latest Articles | 1of7 Downloaded by guest on October 2, 2021 myriapods. The former option drew on comparisons between Results ventral cephalic plates in Carboniferous euthycarcinoids and the New Anatomic Evidence from Heterocrania. Specimens of H. labrum of certain insects (8), and some phylogenetic analyses of fossil rhyniensis preserve cuticular parts of the head in clearer detail and extant Arthropoda resolved euthycarcinoids as a sister group to than in any other known euthycarcinoid. In what follows, we sum- Hexapoda (9). More recently, however, euthycarcinoids have been marize previously unknown anatomic features of euthycarcinoids. allied with the Cambrian fuxianhuiids in the mandibulate stem Eyes. The eyes of euthycarcinoids were described using a neutral group (10) or as a sister group of Myriapoda (11), with fuxianhuiids terminology as “sphaeroidal processes” (14), consistently situ- resolved immediately outside the mandibulate crown-group. ated beneath the border of the two cephalic tergites and usually Heterocrania rhyniensis from the Early Devonian Rhynie Chert projecting beyond the margin of those tergites. An interpretation of Scotland was originally interpreted as a possible eurypterid as eyes was cautiously endorsed (14) but later was implicitly (12), but documentation of more anatomically complete material rejected (e.g., coding for an absence of eyes in Euthycarcinoidea: from the overlying Windyfield Chert demonstrated that it is ref. 15). New specimens of Heterocrania demonstrate that the unquestionably a euthycarcinoid (13) (Fig. 1A). We have restudied “sphaeroidal processes” are compound eyes. NMS 1925.9.11.1 is known and new material of this species, drawing on new imaging an isolated eye from the Rhynie Chert with an ovoid, incomplete methods, in particular confocal laser scanning microscopy, to visual field composed of regularly patterned rows of round lenses elucidate morphological details that shed further light on the (Fig. 1 D and E). At least 90 lenses are preserved, 18 of which systematic position of euthycarcinoids (SI Appendix). We highlight have diameters measured from the central part of the visual field a set of previously undocumented features of the head skeleton in ranging from 19.2 to 24.7 μm (mean, 21.9 ± 1.7 μm). A narrow particular that reinforce a euthycarcinoid-myriapod alliance. marginal rim indicates that at least part of the outer edge of the Fig. 1. H. rhyniensis. (A) Reconstruction in dorsal view (modified from ref. 13). (B and C) Transverse section of head, NMS G.2014.11.1.1, showing compound eyes. Left eye magnified in C; arrows
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