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Non-ammocoete larvae of Palaeozoic stem lampreys

Abstract

Ammocoetes—the filter-feeding larvae of modern lampreys—have long influenced hypotheses of vertebrate ancestry1,2,3,4,5,6,7. The life history of modern lampreys, which develop from a superficially amphioxus-like ammocoete to a specialized predatory adult, appears to recapitulate widely accepted scenarios of vertebrate origin. However, no direct evidence has validated the evolutionary antiquity of ammocoetes, and their status as models of primitive vertebrate anatomy is uncertain. Here we report larval and juvenile forms of four stem lampreys from the Palaeozoic era (Hardistiella, Mayomyzon, Pipiscius, and Priscomyzon), including a hatchling-to-adult growth series of the genus Priscomyzon from Late Devonian Gondwana. Larvae of all four genera lack the defining traits of ammocoetes. They instead display features that are otherwise unique to adult modern lampreys, including prominent eyes, a cusped feeding apparatus, and posteriorly united branchial baskets. Notably, phylogenetic analyses find that these non-ammocoete larvae occur in at least three independent lineages of stem lamprey. This distribution strongly implies that ammocoetes are specializations of modern-lamprey life history rather than relics of vertebrate ancestry. These phylogenetic insights also suggest that the last common ancestor of hagfishes and lampreys was a macrophagous predator that did not have a filter-feeding larval phase. Thus, the armoured ‘ostracoderms’ that populate the cyclostome and gnathostome stems might serve as better proxies than living cyclostomes for the last common ancestor of all living vertebrates.

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Fig. 1: A growth series of Priscomyzon riniensis.
Fig. 2: Hatchlings of Pipiscius zangerli.
Fig. 3: Larval specimen of M. pieckoensis (FMNH PF8167).
Fig. 4: Time-calibrated phylogenetic tree of early vertebrate lineages shows a late evolutionary origin of a filter-feeding larva.

Data availability

The digitally reconstructed part and counterpart of Pipiscius (Fig. 2e, f) remain under the copyright of the FMNH, and are available at https://doi.org/10.6084/m9.figshare.13378628.v1. The original scan data are property of the FMNH (depository: https://emudata.fieldmuseum.org/) and are available upon request to the FMNH and the corresponding author. The cladistic dataset used for our analysis is available as Supplementary Information.

References

  1. 1.

    Haeckel, E. The Evolution of Man: A Popular Exposition of the Principal Points of Human Ontogeny and Phylogeny 3rd edn (Werner, 1876).

  2. 2.

    Gaskell, W. H. On the Origin of Vertebrates (Longmans, Green and Co., 1908).

  3. 3.

    Goodrich, E. S. Studies on the Structure and Development of Vertebrates (Dover, 1930).

  4. 4.

    De Beer, G. The Development of the Vertebrate Skull (Clarendon, 1937).

  5. 5.

    Romer, A. S. & Parsons, T. S. The Vertebrate Body 5th edn (Saunders, 1977).

  6. 6.

    Gee, H. Before the Backbone: Views on the Origin of the Vertebrates (Springer, 1996).

  7. 7.

    Janvier, P. Early Vertebrates (Clarendons, 1996).

  8. 8.

    Janvier, P. in Major Transitions in Vertebrate Evolution (eds. Anderson, J. S. & Sues, H.-D.) 57–121 (Indiana Univ. Press, 2007).

  9. 9.

    Delsuc, F., Brinkmann, H., Chourrout, D. & Philippe, H. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006).

    ADS  CAS  Article  Google Scholar 

  10. 10.

    Miyashita, T. et al. Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological–molecular conflict in early vertebrate phylogeny. Proc. Natl Acad. Sci. USA 116, 2146–2151 (2019).

    ADS  CAS  Article  Google Scholar 

  11. 11.

    Oisi, Y., Ota, K. G., Kuraku, S., Fujimoto, S. & Kuratani, S. Craniofacial development of hagfishes and the evolution of vertebrates. Nature 493, 175–180 (2013).

    ADS  CAS  Article  Google Scholar 

  12. 12.

    Janvier, P. Facts and fancies about early fossil chordates and vertebrates. Nature 520, 483–489 (2015).

    ADS  CAS  Article  Google Scholar 

  13. 13.

    Evans, T. M., Janvier, P. & Docker, M. F. The evolution of lamprey (Petromyzontida) life history and the origin of metamorphosis. Rev. Fish Biol. Fish. 28, 825–838 (2018).

    Article  Google Scholar 

  14. 14.

    Gans, C. in The Skull. Volume 2. Patterns of Structural and Systematic Diversity (eds. Hanken, J. & Hall, B. K.) 1–35 (The Univ. of Chicago Press, 1993).

  15. 15.

    Mallatt, J. Ventilation and the origin of jawed vertebrates: a new mouth. Zool. J. Linn. Soc. 117, 329–404 (1996).

    Article  Google Scholar 

  16. 16.

    Northcutt, R. G. The new head hypothesis revisited. J. Exp. Zool. B Mol. Dev. Evol. 304B, 274–297 (2005).

    Article  Google Scholar 

  17. 17.

    Cattell, M., Lai, S., Cerny, R. & Medeiros, D. M. A new mechanistic scenario for the origin and evolution of vertebrate cartilage. PLoS ONE 6, e22474 (2011).

    ADS  CAS  Article  Google Scholar 

  18. 18.

    Jandzik, D. et al. Evolution of the new vertebrate head by co-option of an ancient chordate skeletal tissue. Nature 518, 534–537 (2015).

    ADS  CAS  Article  Google Scholar 

  19. 19.

    Chang, M. M., Wu, F., Miao, D. & Zhang, J. Discovery of fossil lamprey larva from the Lower Cretaceous reveals its three-phased life cycle. Proc. Natl Acad. Sci. USA 111, 15486–15490 (2014).

    ADS  Article  Google Scholar 

  20. 20.

    Sansom, R. S., Gabbott, S. E. & Purnell, M. A. Atlas of vertebrate decay: a visual and taphonomic guide to fossil interpretation. Palaeontology 56, 457–474 (2013).

    Article  Google Scholar 

  21. 21.

    Gess, R. W., Coates, M. I. & Rubidge, B. S. A lamprey from the Devonian period of South Africa. Nature 443, 981–984 (2006).

    ADS  CAS  Article  Google Scholar 

  22. 22.

    Sansom, R. S., Freedman, K., Gabbott, S. E., Aldridge, R. J. & Purnell, M. A. Taphonomy and affinity of an enigmatic Silurian vertebrate, Jamoytius kerwoodi White. Palaeontology 53, 1393–1409 (2010).

    Article  Google Scholar 

  23. 23.

    Hardisty, M. W. in The Biology of Lampreys Vol. 3 (eds. Hardisty, M. W. & Potter, I. C.) 118–124 (Academic, 1981).

  24. 24.

    Renaud, C. B. Lampreys of the World. An annotated and Illustrated Catalogue of Lamprey Species Known to Date (Food and Agriculture Organization of the United Nations, 2011).

  25. 25.

    Bardack, D. & Richardson, E. S. New agnathous fishes from the Pennsylvanian of Illinois. Fieldiana Geol. 33, 489–510 (1977).

    Google Scholar 

  26. 26.

    Janvier, P. Early jawless vertebrates and cyclostome origins. Zoolog. Sci. 25, 1045–1056 (2008).

    Article  Google Scholar 

  27. 27.

    Gabbott, S. E. et al. Pigmented anatomy in Carboniferous cyclostomes and the evolution of the vertebrate eye. Proc. R. Soc. Lond. B 283, 20161151 (2016).

    Google Scholar 

  28. 28.

    Bardack, D. & Zangerl, R. in The Biology of Lampreys Vol. 1 (eds. Hardisty, M. W. & Potter, I. C.) 1–65 (Academic, 1971).

  29. 29.

    Bardack, D. & Zangerl, R. First fossil lamprey: a record from the Pennsylvanian of Illinois. Science 162, 1265–1267 (1968).

    ADS  CAS  Article  Google Scholar 

  30. 30.

    Hardisty, M. W. Biology of the Cyclostomes (Springer, 1979).

  31. 31.

    Lund, R. & Janvier, P. A second lamprey from the Lower Carboniferous (Namurian) of Bear Gulch, Montana (U.S.A.). Geobios 19, 647–652 (1986).

    Article  Google Scholar 

  32. 32.

    Janvier, P. & Lund, R. Hardistiella montanensis n. gen. et sp. (Petromyzontida) from the Lower Carboniferous of Montana, with remarks on the affinities of the lampreys. J. Vertebr. Paleontol. 2, 407–413 (1983).

    Article  Google Scholar 

  33. 33.

    Janvier, P., Lund, R. & Grogan, E. D. Further consideration of the earliest known lamprey, Hardistiella montanensis Janvier and Lund, 1983, from the Carboniferous of Bear Gulch, Montana, U.S.A. J. Vertebr. Paleontol. 24, 742–743 (2004).

    Article  Google Scholar 

  34. 34.

    Lund, R. Chondrichthyan life history styles as revealed by the 320 million years old Mississippian of Montana. Environ. Biol. Fishes 27, 1–19 (1990).

    Article  Google Scholar 

  35. 35.

    Grogan, E. D. & Lund, R. Soft tissue pigments of the Upper Mississippian chondrenchelyid, Harpagofututor volsellorhinus (Chondrichthyes, Holocephali) from the Bear Gulch Limestone, Montana, USA. J. Paleontol. 71, 337–342 (1997).

    Article  Google Scholar 

  36. 36.

    Lund, R., Greenfest-Allen, E. & Grogan, E. D. Habitat and diversity of the Bear Gulch fish: life in a 318 million year old marine Mississippian bay. Palaeogeogr. Palaeoclimatol. Palaeoecol. 342–343, 1–16 (2012).

    Article  Google Scholar 

  37. 37.

    Sallan, L. C. & Coates, M. I. The long-rostrumed elasmobranch Bandringa Zangerl, 1969, and taphonomy within a Carboniferous shark nursery. J. Vertebr. Paleontol. 34, 22–33 (2014).

    Article  Google Scholar 

  38. 38.

    Gess, R. W. & Whitfield, A. K. Estuarine fish and tetrapod evolution: insights from a Late Devonian (Famennian) Gondwanan estuarine lake and a southern African Holocene equivalent. Biol. Rev. 95, 865–888 (2020).

    Article  Google Scholar 

  39. 39.

    Hardisty, M. W. in The Biology of Lampreys Vol. 4b (eds. Hardisty, M. W. & Potter, I. C.) 165–259 (Academic, 1982).

  40. 40.

    Youson, J. H. & Sower, S. A. Theory on the evolutionary history of lamprey metamorphosis: role of reproductive and thyroid axes. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129, 337–345 (2001).

    CAS  Article  Google Scholar 

  41. 41.

    Ogasawara, M., Di Lauro, R. & Satoh, N. Ascidian homologs of mammalian thyroid peroxidase genes are expressed in the thyroid-equivalent region of the endostyle. J. Exp. Zool. 285, 158–169 (1999).

    CAS  Article  Google Scholar 

  42. 42.

    Ogasawara, M., Shigetani, Y., Suzuki, S., Kuratani, S. & Satoh, N. Expression of Thyroid transcription factor-1 (TTF-1) gene in the ventral forebrain and endostyle of the agnathan vertebrate, Lampetra japonica. Genesis 30, 51–58 (2001).

    CAS  Article  Google Scholar 

  43. 43.

    Gess, R. W. High Latitude Gondwanan Famennian Biodiversity Patterns: Evidence from the South African Witpoort Formation (Cape Supergroup, Witteberg Group) (Univ. of Witwatersrand, 2011).

  44. 44.

    Sansom, R. S., Gabbott, S. E. & Purnell, M. A. Decay of vertebrate characters in hagfish and lamprey (Cyclostomata) and the implications for the vertebrate fossil record. Proc. R. Soc. Lond. B 278, 1150–1157 (2011).

    Google Scholar 

  45. 45.

    Sansom, R. S., Gabbott, S. E. & Purnell, M. A. Non-random decay of chordate characters causes bias in fossil interpretation. Nature 463, 797–800 (2010).

    ADS  CAS  Article  Google Scholar 

  46. 46.

    Purnell, M. A. et al. Experimental analysis of soft-tissue fossilization: opening the black box. Palaeontology 61, 317–323 (2018).

    Article  Google Scholar 

  47. 47.

    Swofford, D. L. PAUP*. (Sinauer, 2017).

  48. 48.

    State of New York Conservation Department. A Biological Survey of the Oswego River System. Supplemental to Seventeenth Annual Report. (J. B. Lyon, 1928).

Download references

Acknowledgements

We thank J.-B. Caron, J. Hanken, J. Hurum, P. Janvier, G. Clement, Z. Johanson, O. Matton, K. Moore, T. Mörss, M. Purnell, S. Gabbott, T. Schossleitner, K. Seymour, W. Simpson, and S. Walsh for collections access; M. Bronner, A. Chinsammy-Turan, S. Gess, S. Green, D. Hockman, K. Miyashita, H. Parker, and R. Prevec for logistical support; J. Pardo for reporting UMPC 10210; K. Seymour and D. Evans for reporting ROM 78122; and R. Plotnick for the access to the D. Bardack slide collections. Funding was provided by Chicago Fellows Program, Vanier Canada Graduate Scholarship, I. W. Killam Memorial Scholarship, Commonwealth Science Conference Follow-on Grant (T.M.); NSF DEB-1541491 (M.I.C.); Millennium Trust, South African DSI-NRF Centre of Excellence in Palaeosciences, National Research Foundation, and the South African Natural Science Collections Facility (R.W.G.).

Author information

Affiliations

Authors

Contributions

T.M. designed the study, performed morphological and phylogenetic analyses, prepared figures, and wrote the manuscript; R.W.G. conceptualized the study of Priscomyzon, performed the fieldwork in the Waterloo Farm lagerstätte, discovered the specimens of Priscomyzon, and contributed to the morphological analysis of Priscomyzon and drafting the manuscript; K.T. performed the computed tomography scan of Pipiscius and provided reconstructions; M.I.C. coordinated the study, identified the specimens of Pipiscius, and contributed to drafting the manuscript.

Corresponding author

Correspondence to Tetsuto Miyashita.

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Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature thanks Philippe Janvier, Shigeru Kuratani and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Comparison of the specimens of P. riniensis to the same scale in reverse ontogenetic order.

a, b, An adult (AM 5750), photograph (a) and interpretive drawing (b). c, d, A juvenile (AM 7538), photograph (c) and interpretive drawing (d). e, f, A large late larva (AM 5816), photograph (e) and interpretive drawing (f). g, h, A small late larva (AM 5815), photograph (g) and interpretive drawing (h). i, j, A small late larva (AM 7539), photograph (i) and interpretive drawing (j). k, l, A large early larva (AM 5817), photograph (k) and interpretive drawing (l). m, n, A small early larva (AM 5814), photograph (m) and interpretive drawing (n). o, p, A hatchling (AM 5813), photograph (o) and interpretive drawing (p). Scale bar, 2 mm. q, Reconstruction of three individuals of Priscomyzon, each representing a different ontogenetic stage. Clockwise from the right: a hatchling carrying a yolk sac (based on AM 5813), tucked in the meadow of the charophyte Octochara crassa; a juvenile (based on AM 7538), attached to the substrate in the foreground; and an adult (based on AM 5750), looming over the other individuals and showing its feeding apparatus. In the background, a school of the coelacanth Selenichthys kowiensis swim above the charophyte meadow. Artwork by K.T.

Extended Data Fig. 2 Adult and juvenile stages of P. riniensis.

ag, AM 5750. hn, AM 7538. a, b, Main slab of AM 5750. Photograph (a) with angled single-directional light (unlike the vertical polarized light in Fig. 1a); and photograph from Fig. 1a overlain with outlines of the anatomical structures identified in this study (b). For interpretive drawing, see Fig. 1b. c, d, Counterslab of AM 5750. Photograph (c) and interpretive drawing (d). e, Detailed, low-angle-light photograph of the oral funnel, showing the individual cusps of the circumoral feeding apparatus and ridges along the edge of the oral funnel. f, g, Detailed anatomy of the region surrounding the left (f) and right (g) eye, showing eye lenses and otic capsules. Owing to the thickness of the preserved body, some of the dorsal skeletal structures in the snout (for example, tectal cartilages) cannot be observed at the surface. h, i, Main slab of AM 7538. Photograph overlain with outlines of the anatomical structures identified in this study (h) and interpretive drawing (i). j, Detailed photograph of the branchial basket on main slab. k, Detailed photograph of the left eye, showing the periocular structure. l, Photograph of counterslab of AM 7538. m, n, Detailed low-angle-light photographs of the circumoral feeding apparatus, which consists of 14 grooved, petaliform plates. m, Main slab, showing cast. n, Counterslab, showing mould. Scale bar, 5 mm (ad), 2 mm (h, i, l). Definitions of abbreviations are provided in the legends of Figs. 13 and ‘Anatomical abbreviations’ in the Methods.

Extended Data Fig. 3 Late larval stages of P. riniensis.

af, AM 5816. gk, AM 5815. l, m, AM 7539. a, b, Main slab of a large late larva, AM 5816 (no counterslab was found). Photograph overlain with outlines of the anatomical structures identified in this study (a) and interpretive drawing (b). c, Detailed photograph of the head, showing potential preservation of the petaliform plates of the circumoral feeding apparatus (arrowhead) and additional soft tissue structures. d, Detailed photograph of the branchial basket and digestive tract. e, f, Detailed photographs of the posterior trunk, with broken lines showing partial outline of the tail. g, h, Main slab of AM 5815, a small late larva missing a large portion of the snout and posterior half of the trunk. Photograph overlain with outlines of the anatomical structures identified in this study (g) and interpretive drawing (h). i, Photograph of counterslab, which shows posterior extremity of the trunk. j, Detailed photograph of the head, showing arrangement of the branchial arches and positions of the snout structures. k, Detailed photograph of the snout and eyes, showing the small snout structures and otic capsules. l, m, Main slab of AM 7539, a small late larva (counterslab has no anatomically informative trace). Photograph overlain with outlines of the anatomical structures identified in this study (l), and interpretive drawing (m). Scale bars, 2 mm. Definitions of abbreviations are provided in the legends of Figs. 13 and ‘Anatomical abbreviations’ in the Methods.

Extended Data Fig. 4 Early larval stages of P. riniensis.

ac, AM 5817. dj, AM 5814. a, b, Main slab of AM 5817, a large early larva (no counterslab was found). Photograph overlain with outlines of the anatomical structures identified in this study (a) and interpretive drawing (b). c, Detailed photograph of the head region, showing individual branchial arches and surface erosion structures. d, e, Main slab of AM 5814, a small early larva. Photograph overlain with outlines of the anatomical structures identified in this study (d) and interpretive drawing (e). f, g, Counterslab. Photograph (f) and interpretive drawing (g), showing individual branchial arches. h, i, Detailed photographs of the oral region in main slab, with (h) or without (i) broken lines delineating the circumoral feeding apparatus. j, Detailed photographs of the head region in counterslab. Scale bars, 2 mm. Definitions of abbreviations are provided in the legends of Figs. 13 and ‘Anatomical abbreviations’ in the Methods.

Extended Data Fig. 5 Hatchling stage of P. riniensis, represented by AM 5813 carrying a yolk sac.

ac, Main slab. Photograph (a), photograph overlain with outlines of the anatomical structures identified in this study (b) and interpretive drawing (c). d, e, Detailed photographs of the head region in different light angles, highlighting different structures preserved by kaolinite mass. f, Detailed photograph of the branchial region. g, Detailed photograph of the circumoral feeding apparatus. hj, Counterslab. Photograph (h), interpretive drawing (i) and detailed photograph of the head region (j). Scale bars, 2 mm. Definitions of abbreviations are provided in the legends of Figs. 13 and ‘Anatomical abbreviations’ in the Methods.

Extended Data Fig. 6 Various growth stages of the Mazon Creek stem lampreys P. zangerli and M. pieckoensis.

av, Pipiscius (ah) and Mayomyzon (iv) show suites of characters that are compatible with the Priscomyzon series, including prominent eyes, an oral funnel, and short branchial baskets. a, b, ROM 56679, a hatchling carrying a yolk sac. Photograph overlain with outlines of the anatomical structures identified in this study (a) and photograph of the counterpart (b). c, d, FMNH PF16082, a hatchling carrying a yolk sac. Photograph overlain with outlines of the anatomical structures identified in this study (c) and photograph of the counterpart (d). eh, Comparison of the specimens of P. zangerli at the same scale reveals nearly identical suites of morphological characters between the hatchling and adult, except size and presence or absence of a yolk sac. e, f, Holotype FMNH PF8346 shown as a photograph (e) and interpretive drawing (f), representing the general adult morphology of the taxon and preserved in comparable orientations to the two hatchling specimens. g, The largest specimen known for Pipiscius (FMNH PF8344), showing the circumoral feeding apparatus in dorsal view. h, The smaller hatchling (ROM 56679), shown in interpretive drawing at the same scale as eg (two adult specimens). ip, A specimen referred to M. pieckoensis (FMNH PF8167), representing a larva. il, Main part. Photograph (i), photograph overlain with outlines of the anatomical structures identified in this study (j), interpretive drawing (k), and scanned photograph taken in the 1960s by D. Bardack to show the original state of tissue preservation in this specimen (l). The photograph in l was discovered in the slide collections of D. Bardack. A full view of the snout can be seen in figure 2 of ref. 28. The specimen was damaged in the snout, and the thin film of organic tissues has deteriorated across the entire specimen. mp, Detailed photographs and illustration of the head region. Photograph in low-angle lighting to reveal surface textures (m), interpretive drawing (n), photograph in high-angle lighting to reveal the film of preserved tissues (o) and photograph of counterpart in high-angle lighting for comparison (p). q, Scan of photograph taken in the 1960s by D. Bardack, to show original state of tissue preservation in the head region of FMNH PF5687, a juvenile of M. pieckoensis. The photograph in q was discovered in the slide collection of D. Bardack. Further details can be seen in figures 2–4 of ref. 28. rv, Comparison of the specimens of M. pieckoensis at the same scale reveals character transitions across ontogeny, including the decreasing relative proportions of branchial region. r, s, Holotype FMNH PF5687 shown as a photograph (r) and interpretive drawing (s), representing the juvenile stage. t, Interpretive drawing of FMNH PF8167 at the same scale as r, s (juvenile), u, v (adult). u, v, The largest known specimen (ROM 56787) shown as a photograph (u) and interpretive drawing (v), representing the adult stage. Scale bars, 2 mm (ad, il, mp), 5 mm (eh, rv). Definitions of abbreviations are provided in the legends of Figs. 13 and ‘Anatomical abbreviations’ in the Methods.

Extended Data Fig. 7 Growth series of H. montanensis.

This series shows suites of characters that are compatible with those of other Palaeozoic stem lampreys, including prominent eyes, an oral funnel, and short branchial baskets. This series also documents gradual character transitions in the decreasing body depth, increasing interocular distance and progressively slender profile of the oral funnel. Comparison reveals size discrepancies across the juvenile–adult transition and between the sexually mature, gravid specimen and other adults (discussed in section A-3a of the Supplementary Information in comparison to modern lampreys). al, Hardistiella montanensis. a, b, Photograph (a) and interpretive drawing (b) of late larval stage represented by CM 4505, showing the deeper body than in any later ontogenetic stages. c, d, Juvenile stage, represented by ROM 78122, showing intermediate body depth. Photograph (c) and interpretive drawing (d). el, Adult stage represented by CM 63079 (e, f), UMPC 10210 (g, h) and UMPC 7696 (il). e, f, CM 63079—incomplete, but potentially the largest specimen—shown as a photograph (e) and interpretive drawing (f). g, h, UMPC 10210, showing an advanced stage of decay relative to other specimens, shown as a photograph (g) and interpretive drawing (h). il, UMPC 7696 associated with potential gonads (probably representing a gravid female with ovaries or eggs), shown as a photograph (i) and interpretive drawing (l). k, Detailed photograph of the abdominal region of the main part, showing the circular structures interpreted in ref. 32 as gonads. l, Tracing of the anatomical structures in k (in grey). mp, The abdominal structures were identified as gonads in the stem myxinoid Gilpichthys greenei from the Mazon Creek fauna, indicating a small number of large ovaries or eggs (white arrowheads) in this taxon. These examples, which are shown here in various forms of development and states of preservation, bolster the gonadal interpretation for the serial, circular abdominal structures in the holotype of the stem lamprey Hardistiella UMPC 7696 (k, l). In Gilpichthys, the structures appear to develop in a small number (3–5) of iron concretions as in ROM 56389 (m), or paired series of fewer than a dozen circular depressions as in FMNH PF23464 (n). o, p, FMNH PF8464 shows a seemingly mature state of development: 11 circular structures of iron-rich recrystallization, implying that the contents were encapsulated and chemically distinct from the rest of the body. The number agrees with the 11 present in FMNH PF23464, shown here as a photograph with low-angle lighting (o) and as a detailed photograph of the gonads in high-angle, high-exposure lighting (p). Scale bars, 5 mm. Definitions of abbreviations are provided in the legends of Figs. 13 and ‘Anatomical abbreviations’ in the Methods.

Extended Data Fig. 8 Comparison of anatomical traits preserved in the specimens of Palaeozoic stem lamprey described in this Article.

a, Modern decay series of ammocoetes and adult lampreys, after a previous publication20. Codes for these reference decay series are as follows. Yellow, pristine; orange, decaying; red, onset of loss; terminal point, complete loss. The x axis shows number of days, whereas y axis ranks decay stages. For each fossil specimen (bp), bars shown in original colours (yellow, orange, and red) represent characters preserved in the specimen; 50% transparent (brown) bars represent characters preserved in the specimen but in a different form than in the modern reference; grey bars represent characters missing in the specimen; no bars shown denotes that, in principle, characters cannot be assessed in the specimen (for example, ‘slanting gill openings’ cannot be determined in dorsoventrally compressed specimens, whereas ‘gill symmetry’ cannot be assessed in transversally compressed specimens). bi, Priscomyzon riniensis. b, AM 5750, representing the adult stage. c, AM 7538, representing the juvenile stage. df, AM 5816 (d), AM 5815 (e), and AM 7539 (f), all representing the late larval stage. g, h, AM 5817 (g) and AM 5814 (h), representing the early larval stage. i, AM 5813, representing the hatchling stage. j, k, Pipiscius zangerli. ROM 56679 (j) and FMNH PF16082 (k), both representing the hatchling stage. l, Mayomyzon pieckoensis. FMNH PF8167, representing the late larval stage. mq, Hardistiella montanensis. m, CM 4505, representing the late larval stage. n, ROM 78122, representing the juvenile stage. oq, CM 63079 (o), UMPC 10210 (p), and UMPC 7696 (q), all representing the adult stage. Interpretive drawings in bq are not to scale.

Extended Data Fig. 9 Determination of ontogenetic stages for the Palaeozoic stem lamprey specimens.

This comparison reveals gradual transitions of characters in each taxon, allowing the designation of ontogenetic stages and corroborating their taxonomic identity. Each ontogenetic series of stem lamprey shows an early expression of character states that, in modern lampreys, develop only in the adult phase (dark blue shades in cf), confirming the absence of the ammocoete phase in these stem taxa. a, Modern lampreys. Reference ontogenetic sequence and comparison of ontogenetically variable characters that are also preserved in the stem lamprey specimens, indicated in blue shades. Images are after a previous publication48 (adult, P. marinus) or courtesy of G. Kovalchuk (late larva and juvenile, Entosphenus tridentatus), except for the hatchling and early larva (photographs by T.M., P. marinus). b, Size variations among the specimens of P. riniensis. Principal component 1 is used as a composite size metric that correlates with ontogenetic stages (x axis), whereas the specimens are similar in body length from larval to juvenile stages (y axis). For methodological details, see the ‘A-3a. Size variations’ section of the Supplementary Information. For original measurements and principal component scores, see Supplementary Tables 3 and 4, respectively. cf, Ontogenetic series of four Palaeozoic stem lampreys: P. riniensis (c); P. zangerli (d); M. pieckoensis (e); and H. montanensis (f). In addition to the characters that vary in modern lamprey ontogeny (blue shades), the table compares characters that vary ontogenetically in Priscomyzon (red shades) and in Hardistiella and Mayomyzon (green shades). Each row represents a character; the lighter shade shows the immature state (described in the leftmost column) and the darker shade shows the mature state (described in the rightmost column). Intermediate shades indicate polymorphism within the stage (absence and presence mixed) or intermediate state (character describes a continuum). An empty box with a question mark denotes missing information. Each stage represented in the fossil record is linked to interpretive drawings of the specimens (representative specimens for nonlarval stages of Mayomyzon and Pipiscius). For detailed information and discussion of the characters, see the ‘A-3f. Definitions of ontogenetic characters’ section of the Supplementary Information.

Extended Data Fig. 10 Phylogenetic tree of early vertebrate lineages resulting from our analysis, showing the relationships of stem lampreys and other cyclostomes.

The tree shows strict consensus of 360 most parsimonious trees based on 52 taxa and 167 morphological characters, revised from a previous publication10. Topology is similar to the previously presented consensus tree10, but differs in: the deeply nested, stem-petromyzontiform position of Pipiscius; the stem-myxinoid affinity of Gilpichthys; the position of Myxineidus as outgroup to all the rest of petromyzontiforms; and the collapse of crown nodes into polytomies for both myxinoids and petromyzontiforms. Filled circles indicate crown nodes, and empty circles show total nodes or the most inclusive nodes of entirely extinct lineages. Black, nonvertebrate outgroups; green, stem vertebrates; magenta, stem cyclostomes; purple, anaspids (stem cyclostomes); red, myxinoids (hagfishes); orange, petromyzontiforms (lampreys); blue, gnathostomes (total group). For the methodology and analytical details, see the ‘Part B’ section of the Supplementary Information.

Supplementary information

Supplementary Information

This file contains supplementary text (Part A. Additional Descriptions and Comparison; Part B. Phylogenetic Analysis) and Tables S1–S5.

Reporting Summary

Supplementary Data

Data matrix: This file contains a taxon and character matrix used for phylogenetic analysis presented in Extended Data Figure 10.

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Miyashita, T., Gess, R.W., Tietjen, K. et al. Non-ammocoete larvae of Palaeozoic stem lampreys. Nature 591, 408–412 (2021). https://doi.org/10.1038/s41586-021-03305-9

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