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A Lamprey from the Devonian Period of South Africa

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A Lamprey from the Devonian Period of South Africa Vol 000 | 00 Month 2006 | doi:10.1038/nature05150 LETTERS ; A lamprey from the Devonian period of South Africa < Robert W. Gess1, Michael I. Coates2 & Bruce S. Rubidge1 Lampreys are the most scientifically accessible of the remaining and the disc is proportionately larger than those of similarly sized, jawless vertebrates, but their evolutionary history is obscure. In post-metamorphic, living forms (Fig. 2). In contrast, the oral disc of contrast to the rich fossil record of armoured jawless fishes, all of the Late Carboniferous lamprey Mayomyzon7,8, if present, is much which date from the Devonian period and earlier1–3, only two smaller9, and no remnant of a disc is preserved in the Early Palaeozoic lampreys have been recorded, both from the Carboniferous lamprey Hardistiella10. The lamprey identity of the Carboniferous period1. In addition to these, the recent report of putative oral disc of Pipiscus11 is uncertain12. an exquisitely preserved Lower Cretaceous example4 demonstrates Priscomyzon displays a set of 14 evenly spaced teeth surrounding that anatomically modern lampreys were present by the late the mouth. These are the first teeth to be discovered in any fossil Mesozoic era. Here we report a marine/estuarine fossil lamprey lamprey, and resemble the circumoral arrangements of 19 or more from the Famennian (Late Devonian) of South Africa5,6, the iden- teeth present in modern forms such as Ichthyomyzon, Petromyzon, tity of which is established easily because many of the key specia- Caspiomyzon and Geotria13.InPriscomyzon, the posterior circumoral lizations of modern forms are already in place. These teeth appear to be more elongate than the remainder, whereas in specializations include the first evidence of a large oral disc, the modern forms lateral or anterior teeth tend to be largest. Modern first direct evidence of circumoral teeth and a well preserved bran- lamprey circumoral teeth usually display specialized shapes, and such chial basket. This small agnathan, Priscomyzon riniensis gen. et sp. teeth are often the largest of multiple series radiating to the oral disc nov., is not only more conventionally lamprey-like than other perimeter. In comparison, the circumoral teeth of Priscomyzon are Palaeozoic examples7,8, but is also some 35 million years older. very simple, and in this respect probably primitive. Irregularly shaped This finding is evidence that agnathans close to modern lampreys objects in the centre of the mouth (oesophageal opening, Fig. 1c) had evolved before the end of the Devonian period. In this light, might be traces of teeth from the apical cartilage of the ‘tongue’ lampreys as a whole appear all the more remarkable: ancient spe- complex, as in living hagfishes and lampreys14. cialists that have persisted as such and survived a subsequent 360 Several rod-like structures are preserved posterior to the oral disc. million years. These include a possible styliform cartilage and parts of further car- Hyperoartia Mu¨ller, 1844 tilages from the underside of the neurocranium (Fig. 1). Ovoid Petromyzontiformes Berg, 1940 patches flanking the midline are interpreted as the otic capsules. Priscomyzon riniensis gen. et sp. nov. The lighter colour of these indicates denser mineralization, but otherwise the capsule material resembles that of surrounding skeletal Etymology. Generic name from Latin prisco (ancient) and myzon remains. Otic capsules overlap the anterior of the branchial skeleton, (a lamprey). Specific name from Rini, the Xhosa name for a condition also seen in Mayomyzon7,8 but restricted to larval stages in Grahamstown and the surrounding valley. living forms9 and absent from Mesomyzon4 (the reconstruction in Holotype. Albany Museum, Grahamstown, Eastern Cape, cata- Fig. 2a illustrates the difference in cranial layout). The position of logue number AM5750. the orbits is less clear because there are no darkened areas indicative Locality and horizon. Waterloo Farm, Grahamstown, South of eye locations, as in Mayomyzon7,8, Hardistiella10 and Mesomyzon4. Africa; Witpoort Formation, Witteberg Group, Famennian, Late The branchial skeleton of Priscomyzon is preserved in greater detail Devonian5,6. than that of Mesomyzon4; gill arrangements in Mayomyzon are pre- Diagnosis. A small lamprey differing from all other living and served only as dark imprints7,8, whereas evidence of the branchial fossil lampreys in having a large oral disc, the diameter of which apparatus in Hardistiella10 is fragmentary15.InPriscomyzon, much approximately equals the length of the branchial region, and of the right and parts of the left branchial baskets are preserved. accounts for around one-half of total head length. A circumoral ring The posterior five branchial arches are well defined, including evid- of 14 simple teeth is present, the posterior members of which are ence of at least two sets of horizontal bars (further bars may be largest; there are no associated radiating series or plates of supple- obscured by matrix): the hypobranchials and either hypo- or epitre- mentary teeth. The first gill pouch is ventral to the otic capsule. Total matic bars (Fig. 1). Anterior to these, areas of lesser mineral concen- body length is little more than 4.2 cm, post-branchial body shape is tration suggest the presence of seven branchial pouches in total. Of elongate and tapering, and only 1.5 times the head length. The dorsal the two Carboniferous lamprey species, Mayomyzon displays five fin extends from the immediate posterior of the branchial region. pairs of gill pouches with indications of a further two7, and a possible Description. The 4.2-cm-long specimen of Priscomyzon is pre- juvenile specimen of Hardistiella shows at least six branchial units16. served in ventral view, in part (Fig. 1a) and counterpart (Fig. 1b) In Priscomyzon a bi-lobed structure posterior to the branchial skel- on a natural bedding plane. No post-depositional distortion is appar- eton corresponds to the expected position of the heart. However, it is ent in associated plant axes. The most striking feature of Priscomyzon not clear that this is evidence of a pericardial cartilage capsule, as in is its large oral disc, edged with a soft outer lip, supported by an modern lampreys. annular cartilage, and surrounding a circular mouth (Fig. 1c). This The post-branchial body of Priscomyzon is much narrower than is the first clear evidence of a Palaeozoic lamprey with an oral disc, the head and tapers posteriorly (Fig. 1). It is also exceptionally short: 1Bernard Price Institute (Palaeontology), School for Geosciences, University of Witwatersrand, Johannesburg 2050, South Africa. 2Department of Organismal Biology, University of Chicago, Chicago, Illinois 60637, USA. 1 Nature nature05150.3d 12/9/06 17:13:19 LETTERS NATURE | Vol 000 | 00 Month 2006 ac abc cm ol ct od sc brb 1 or 2 3 bra 4 5 oc h/eb 6 7 hyb blb df 10 mm Figure 1 | Holotype of Priscomyzon riniensis gen. et sp. nov. This 360- cartilage; blb, bi-lobed structure; bra, branchial arch; brb, branchial basket; million-year-old lamprey is the earliest example known in the fossil record, cm, circular mouth; ct, circumoral teeth; df, dorsal fin; hyb, hypobranchial showing most of the specialized feeding structures present in modern forms. bar; h/eb, hypotrematic/epitrematic bar; oc, otic capsule; od, oral disc; ol, a, b, Part (a) and counterpart (b) of holotype AM5750. The total length of outer lip; or, orbital region; sc, styliform cartilage; 1–7, positions of gill the specimen is 42 mm. c, Interpretive drawing of the holotype. ac, annular pouches. a b Figure 2 | Reconstruction of Priscomyzon riniensis, illustrating tadpole-like positioned in front of the branchial region. The total length of the specimen body proportions and large oral disc, compared with post-metamorphic is 116 mm. Drawings in a and b are scaled to show equivalent head lengths: modern lamprey, Lampetra fluviatilis.a, Reconstruction of Priscomyzon in from anterior limit of the oral disc to rear of the branchial region. Horizontal dorsal (top) and left lateral (bottom) views. b, Macropthalmia stage of bars indicate the anterior–posterior span of the oral disc in each species. Lampetra28 showing anterior location of orbit and smaller oral disc, both 2 Nature nature05150.3d 12/9/06 17:13:34 NATURE | Vol 000 | 00 Month 2006 LETTERS Jawed vertebrates Jawed vertebrates Figure 3 | Cladograms showing the hypothesized position of Priscomyzon from analysis of re-weighted character set: cyclostomes (hagfishes and among early craniates. a, Strict consensus of 42 shortest trees: length, 211 lampreys) are paraphyletic; Euphanerops1,3 is a stem lamprey on the basis of steps; consistency index, 0.63; homoplasy index, 0.37; retention index, 0.7; homoplastic synapomorphies. Time axis (million years) and temporal rescaled consistency index, 0.44. Priscomyzon lies within a polytomy of fossil ranges of taxa (bold lines) are from refs 1, 3, 4, 12, 18, 23. Numbered brackets and modern lampreys. Bremer support values are circled at nodes (compare indicate major monophyletic groups: 1, Craniata; 2, Myxiniformes; 3, with refs 2, 18; see Supplementary Information for details). b, Single tree Vertebrata; 4, Petromyzontiformes; 5, Gnathostomata. only 1.5 times the length of the head, compared to 3.3 times head Euphanerops3 to the base of a lamprey stem group. This result echoes length in the similarly sized Mayomyzon. Faint impressions of small previous suggestions about the relationships of these clades1,20. lunate ridges are present, but their significance is unknown. Details of The discovery of Priscomyzon within a Late Devonian marginal the dorsal fin are limited, although it is evident that it originates marine estuarine environment5,6 pushes the minimum date of lam- immediately behind the branchial region and extends as a continuous prey-like fishes back by some 35 million years, and provides a new fold towards the caudal extremity. This resembles conditions in an minimum date for molecular-clock-based estimates of the cyc- ammocoete rather than in modern adult lampreys, in which separate lostome crown node.
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