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A Paleozoic Stem Hagfish Myxinikela Siroka — Revised Anatomy and Implications for Evolution of the Living Jawless Vertebrate Lineages

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A Paleozoic Stem Hagfish Myxinikela Siroka — Revised Anatomy and Implications for Evolution of the Living Jawless Vertebrate Lineages Canadian Journal of Zoology A Paleozoic stem hagfish Myxinikela siroka — Revised anatomy and implications for evolution of the living jawless vertebrate lineages Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0046.R1 Manuscript Type: Article Date Submitted by the 24-Aug-2020 Author: Complete List of Authors: Miyashita, Tetsuto; University of Chicago, Organismal Biology and Anatomy Is your manuscript invited for Draft consideration in a Special Zoological Endeavors Inspired by A. Richard Palmer Issue?: Myxinoidea, cyclostomes, Mazon Creek, Francis Creek Shale, Keyword: Pennsylvanian, Carboniferous, soft tissue preservation © The Author(s) or their Institution(s) Page 1 of 47 Canadian Journal of Zoology 1 2 A Paleozoic stem hagfish Myxinikela siroka — Revised anatomy and implications 3 for evolution of the living jawless vertebrate lineages1 4 5 Tetsuto Miyashita*, † 6 7 *Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, Ontario, Canada K1P 6P4 8 †Department of Organismal Biology and Anatomy, the University of Chicago. Chicago, IL 60637 USA 9 10 Email: [email protected] 11 Draft 12 Running title: Anatomy of a stem hagfish 13 14 1This article is one of a series of invited papers arising from the symposium “Zoological Endeavours 15 Inspired by A. Richard Palmer” that was co-sponsored by the Canadian Society of Zoologists and the 16 Canadian Journal of Zoology and held during the Annual Meeting of the Canadian Society of 17 Zoologists at the University of Windsor, Windsor, Ontario, 14–16 May 2019. 18 19 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 2 of 47 20 Abstract 21 22 Hagfishes and lampreys comprise cyclostomes, the earliest branching and sole surviving clade of the 23 once diverse assemblage of jawless crown-group vertebrates. Lacking mineralized skeletons, both of 24 the crown cyclostome lineages have notoriously poor fossil record. Particularly in the hagfish total 25 group, Myxinikela siroka Bardack, 1991 from the Late Carboniferous estuarine system of Illinois 26 represents the only definitive stem taxon. Previously known from a single specimen, Myxinikela has 27 been reconstructed as a short-bodied form with pigmented eyes but otherwise difficult to distinguish 28 from the living counterpart. With a new, second specimen of Myxinikela reported here, I re-evaluate the 29 soft tissue anatomy and formulate diagnosis for the taxon. Myxinikela has a number of general features 30 of cyclostomes, including cartilaginous branchialDraft baskets, separation between the esophageal and 31 branchial passages, and a well-differentiated midline finfold. In effect, these features give more 32 lamprey-like appearance to this stem hagfish than previously assumed. Myxinikela still has many traits 33 that set modern hagfishes apart from other vertebrates (e.g., nasohypophyseal aperture, large velar 34 cavity, and cardinal heart) and some intermediate conditions of modern hagfishes (e.g., incipient 35 posterior displacement of branchial region). Thus, Myxinikela provides an important calibration point 36 with which to date origins of these characters. 37 38 Keywords: Myxinoidea, cyclostomes, Mazon Creek, Francis Creek Shale, Pennsylvanian, 39 Carboniferous, soft tissue preservation, hagfishes, Myxinikela siroka 40 41 © The Author(s) or their Institution(s) Page 3 of 47 Canadian Journal of Zoology 42 Introduction 43 44 When Carl Linnaeus described a hagfish as an “intestinal worm” (vermes intestina) (Linnaeus 1758; 45 Fänge 1998), he misclassified the animal but perhaps had a grasp of its strange morphology distinct 46 from any other living fish lineages. Boneless, sightless, and jawless, there is little to the external 47 morphology of hagfish that reveals its vertebrate affinity. The single nasohypophyseal canal has an 48 open aperture at the anterior end of the animal; the excurrent branchial ducts open in the mid-portion of 49 the trunk; and the flaccid skin covers a massive subcutaneous sinus (Marinelli and Strenger 1956; 50 Jørgensen et al. 1998). A hagfish appears even more puzzling internally, having anatomical traits such 51 as: a single semicircular canal; single midline choana; absence of the lateral wall of the braincase; an 52 enormous feeding apparatus occupying theDraft region that would otherwise house the branchial apparatus; 53 and kidneys consisting of segmentally organized glomeruli (Marinelli and Strenger 1956; Jørgensen et 54 al. 1998). The cladistic consensus now has hagfish firmly nested within vertebrates (Mallatt and 55 Sullivan 1998; Kuraku et al. 1999; Near 2009; Heimberg et al. 2010; Miyashita et al. 2019a), and the 56 comparative anatomical, embryological, and physiological research has offered explanations to these 57 peculiar traits (Ota and Kuratani 2006; Oisi et al. 2013b; Miyashita and Coates 2016; Kuratani et al. 58 2016; Higuchi et al. 2019). However, the evolutionary history of the distinct hagfish morphology 59 remains poorly documented or calibrated. This lack of understanding is due to the poor quality of 60 hagfish fossil record. 61 Myxinikela siroka Bardack, 1991 from the Pennsylvanian Francis Creek Shale of Illinois (the 62 Mazon Creek fauna) (Bardack 1991) was the sole fossil hagfish until the discovery of Tethymyxine, a 63 crown-group hagfish from the Cretaceous of Lebanon (Miyashita et al. 2019a). Myxinikela remains the 64 only stem hagfish with cladistic support from multiple datasets (Gabbott et al. 2016; Miyashita et al. 65 2019a). In the original description, the holotype and only specimen of Myxinikela was illustrated with © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 4 of 47 66 nasohypophsyeal barbels, paired eyes, otic capsules, branchial skeletons, and heart (Bardack 1991, 67 1998). With the exception of the pigmented eyes, the soft tissues identified in Myxinikela have been 68 questioned but conditionally accepted in subsequent analyses (Janvier 1996, 2007, 2008; Sansom et al. 69 2011; Janvier and Sansom 2016; Gabbott et al. 2016; Miyashita et al. 2019a). The apparent rarity of 70 Myxinikela in the Mazon Creek localities presented another challenge to interpreting the anatomy, as 71 no other specimen of the taxon has been found to date. The Mazon Creek fauna has yielded another 72 potential stem hagfish, Gilpichthys greenei Bardack & Richardson, 1977 (Bardack and Richardson 73 1977). The hagfish affinity of Gilpichthys has ambiguous cladistic support. It is typically precluded 74 from cladistic analyses because it can be coded for only a fraction of characters (22.6% in Miyashita et 75 al. 2019a). Gilpichthys was placed on the lamprey stem recently (Miyashita et al. 2019a), but the re- 76 analysis of a modified dataset found it on theDraft hagfish stem, nested immediately outside the clade 77 (Myxinikela + the crown group) (Miyashita et al. in review). Gilpicithys may represent a different 78 preservation mode of the same animal with Myxinikela, which, again, cannot be reliably tested without 79 additional specimens of Myxinikela. 80 In this paper, I report a second specimen of Myxinikela and re-evaluate previous reconstruction 81 of the Carboniferous stem hagfish. The newly identified specimen represents a different mode of 82 preservation in which the overall body proportion appears more slender and the visceral imprints are 83 more prominent than the skeletal remains. The original descriptions of the holotype (Bardack 1991, 84 1998) over-interpreted its hagfish-like morphology, and my revision renders Myxinikela less like a 85 modern hagfish than previously considered. Nevertheless, Myxinikela shows an intermediate stage 86 between the presumed ancestral cyclostome and modern hagfishes and provides calibrations for 87 important characteristics of the crown group Myxinoidea. 88 89 Institutional abbreviations © The Author(s) or their Institution(s) Page 5 of 47 Canadian Journal of Zoology 90 FMNH, Field Museum of Natural History, Chicago, USA; ROM, Royal Ontario Museum, 91 Toronto, Canada. 92 93 Systematic Palaeontology 94 95 Vertebrata Linnaeus, 1758 96 Cyclostomi Duméril, 1806 97 Myxinoidea Müller, 1834 98 99 Myxinikela siroka Bardack, 1991 100 (Figs. 1–4) Draft 101 102 HOLOTYPE: FMNH PF15373 (Figs. 1, 2). Body length = 73.3 mm. 103 PARATYPE: FMNH PF8472 (Figs. 3, 4). Body length = 62.5 mm. 104 HORIZON: Francis Creek Shale, Moscovian, Middle Pennsylvanian. Both specimens were collected 105 from the site formerly known as Pit 11, Peabody Coal Company, Will-Kankakee Counties, 106 Illinois (Bardack 1997; Hay and Krutty 1997; Ledvina 1997). The abandoned pit is now in the 107 property of Braidwood Generating Station. This locality yields members of the ‘Essex fauna’ — 108 a nearshore estuarine marine habitat in the Pennsylvanian deltaic system of Mazon Creek (Baird 109 et al. 1986; Baird 1997a,b). 110 DIAGNOSIS: The original description (Bardack 1991) did not formulate diagnosis for this taxon. In 111 this paper, Myxinikela siroka is diagnosed as a myxinoid with a unique combination of the 112 following characters: pigmented eyes (symplesiomorphy for myxinoids); eyes close to midline 113 (autapomorphy within myxinoids); eyes and otic capsules close to each other (autapomorphy © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 6 of 47 114 within myxinoids); branchial region in postotic position (synapomorphy for myxinoids) but not 115 widely separated from the rest of head by lingual apparatus (autapomorphy within myxinoids); 116 branchial region shorter than preoptic length (autapomorphy
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