Reproduction in jawed vertebrates (gnathostomes) involves either external or internal fertilization1. It is commonly argued that internal fertilization can evolve from external, but not the reverse. Male copulatory claspers are present in certain placoderms2,3,4, fossil jawed vertebrates retrieved as a paraphyletic segment of the gnathostome stem group in recent studies5,6,7,8. This suggests that internal fertilization could be primitive for gnathostomes, but such a conclusion depends on demonstrating that copulation was not just a specialized feature of certain placoderm subgroups. The reproductive biology of antiarchs, consistently identified as the least crownward placoderms5,6,7,8 and thus of great interest in this context, has until now remained unknown. Here we show that certain antiarchs possessed dermal claspers in the males, while females bore paired dermal plates inferred to have facilitated copulation. These structures are not associated with pelvic fins. The clasper morphology resembles that of ptyctodonts, a more crownward placoderm group7,8, suggesting that all placoderm claspers are homologous and that internal fertilization characterized all placoderms. This implies that external fertilization and spawning, which characterize most extant aquatic gnathostomes, must be derived from internal fertilization, even though this transformation has been thought implausible. Alternatively, the substantial morphological evidence for placoderm paraphyly must be rejected.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Blackburn, D. G. Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J. Morphol. http://dx.doi.org/10.1002/jmor.20272 (2014)
Miles, R. S. Observations on the ptyctodont fish, Rhamphodopsis Watson. Zool. J. Linn. Soc. 47, 99–120 (1967)
Ahlberg, P. E., Trinajstic, K., Johanson, Z. & Long, J. A. Pelvic claspers confirm chondrichthyan-like internal fertilization in arthrodires. Nature 460, 888–889 (2009)
Trinajstic, K. M., Boisvert, C., Long, J. A., Maksimeko, A. & Johanson, Z. Pelvic and reproductive structures in placoderms (stem gnathostomes). Biol. Rev. http://dx.doi.org/10.1111/brv.12118 (2014)
Brazeau, M. D. The braincase and jaws of a Devonian ‘acanthodian’ and modern gnathostome origins. Nature 457, 305–308 (2009)
Davis, S. P., Finarelli, J. A. & Coates, M. I. Acanthodes and shark-like conditions in the last common ancestor of modern gnathostomes. Nature 486, 247–250 (2012)
Zhu, M. et al. A Silurian placoderm with osteichthyan-like marginal jaw bones. Nature 502, 188–193 (2013)
Dupret, V., Sanchez, S., Goujet, D., Tafforeau, P. & Ahlberg, P. E. A primitive placoderm sheds light on the origin of the jawed vertebrate face. Nature 507, 500–503 (2014)
Freitas, R., Zhang, G. & Cohn, M. J. Biphasic Hoxd gene expression in shark paired fins reveals an ancient origin of the distal limb domain. PLoS ONE 2, e754 (2007)
Meyer, A. & Lydeard, C. The evolution of copulatory organs, internal fertilization placentae and viviparity in killifishes (Cyprinodontiformes) inferred from a DNA phylogeny of the tyrosine kinase gene X-src . Proc. R. Soc. Lond. B 254, 153–162 (1993)
Parenti, L. R., LoNostro, F. L. & Grier, H. J. Reproductive histology of Tomeurus gracilis Eigenmann, 1909 (Teleostei: Atherinomorpha: Poeciliidae) with comments on evolution of viviparity in atherinomorph fishes. J. Morphol. 271, 1399–1406 (2010)
Miles, R. S. & Young, G. C. Placoderm interrelationships reconsidered in the light of new ptyctodontids from Gogo, Western Australia. Linn. Soc. Symp. Ser. 4, 123–198 (1977)
Downs, J. P., Criswell, K. E. & Daeschler, E. B. Mass mortality of juvenile antiarchs (Bothriolepis sp.) from the Catskill Formation (Upper Devonian, Famennian Stage), Tioga county, Pennsylvania. Proc. Acad. Nat. Sci. Philad. 161, 191–203 (2011)
Hemmings, S. K. The Old Red Sandstone antiarchs of Scotland: Pterichthyodes and Microbrachius . Palaeontogr. Soc. Monogr. 131 (551),. 1–64 (1978)
Pan, J. A new species of Microbrachius from the Middle Devonian of Yunnan. Vertebr. Palasiat. 22, 8–13 (1984)
Wang, J.-Q. & Zhang, G.-R. New material of Microbrachius from the Lower Devonian of Qujing, Yunnan, China. Vertebr. Palasiat. 37, 200–211 (1999)
Stensiö, E. A. On the Placodermi from the Upper Devonian of East Greenland. II. Antiarchi: subfamily Bothriolepinae. With an attempt at a revision of the previously described species of the family. Medd. Grønl. 139, 1–622 (1948)
Long, J. A. & Werdelin, L. A new Late Devonian bothriolepid (Placodermi, Antiarcha) from Victoria, with descriptions of others from the state. Alcheringa 10, 355–399 (1986)
Lysarkaya, L. A. Baltic Devonian Placodermi. Asterolepididae [in Russian] 1–152 (Zinatne, 1981)
Johanson, Z. New Remigolepis (Placodermi; Antiarchi) from Canowindra, New South Wales, Australia. Geol. Mag. 134, 813–846 (1997)
Zhu, M., Yu, X., Choo, B., Wang, J. & Jia, L. An antiarch placoderm shows that pelvic girdles arose at the root of jawed vertebrates. Biol. Lett. 8, 453–456 (2012)
Leigh-Sharpe, H. The comparative morphology of the secondary sexual characters of elasmobranch fishes. The claspers, clasper siphons, and clasper glands. Memoir III–V. J. Morphol. 36, 190–240 (1922)
Goodrich, E. S. Studies on the Structure and Development of Vertebrates Vol. 1, 1–486 (Dover Publications, 1958)
Rouse, G. W. Broadcasting fables: is external fertilization really primitive? Sex, size, and larvae in sabellid polychaetes. Zool. Scr. 23, 271–312 (1994)
Brazeau, M. D. & Friedman, M. The characters of Palaeozoic jawed vertebrates. Zool. J. Linn. Soc. 170, 779–821 (2014)
Mark-Kurik, E. Psammosteid microremains from the Middle Devonian (Givetian) of Estonia. Mod. Geol. 24, 1–21 (1999)
For access to collections we thank E. Bernard, D. Pickering, E. Fitzgerald, L. Grande, W. Simpson and H.-D. Sues. For photography we thank P. Hurst, G. Baranov and D. Hubert. We thank M. Brazeau for reviewing an earlier version of the paper. Travel to Tallinn, London and Washington for J.A.L. to examine specimens was supported by Flinders University. G.C.Y., J.A.L. and K.T. acknowledge support from the Australian Research Council.
The authors declare no competing financial interests.
Extended data figures and tables
Top, map showing locality of the Essi Farm site, Estonia, and stratigraphical section where the fossils were found. Modified from ref. 26. Below, Microbrachius sp. plates from Essi Farm, Estonia. a, GIT 628-37, sample showing several small plates and fragments; b, GIT 628-9, right lateral plate, visceral view; c, 628-3, posterior median dorsal plate, dorsal view; d, GIT 628-25, right posterior ventrolateral plate, visceral view; e, GIT 628-18, anterior section of anterior ventrolateral plate, lateral view showing brachial process. All specimens held within the Institute of Geology at Tallinn University of Technology, Estonia, collection GIT 628.
Extended Data Figure 2 Location and stratigraphic position of new Scottish specimens of M. dicki described herein.
Top, map of the Orkney Islands with an asterisk marking the location where the specimens of M. dicki described in this paper were collected. Below, stratigraphical column of the upper part of the Middle Devonian in the Orkney Islands with the position of the Eday Flagstone Formation fish beds marked by a dotted line.
a, b, NHMUKVP P 77400, claspers only weakly developed, no lateral wing; close up of claspers in b; c, d, NHMUK VP P 77403 showing further caudally directed growth of claspers; d, close up of claspers showing fusion in midline. Scale bars, 1 cm.
Top, Yunnanolepis porifera, Xitun Formation, Yunnan, China. Specimen IVPP V19359) in (a) dorsal view, (b) ventral view and (c) showing posterior region of trunkshield prepared to show internal side of the PVL plates. p.ri, strong ridge on the dorsal surface of the posterior region of the PVL plates. Below, a, b, Bothriolepis sp., Gogo Formation, Western Australia (P223045, Museum Victoria, Melbourne); c, B. canadensis, Escuminac Formation, Quebec, Canada (UF 252, Field Museum, Chicago). Abbreviations: m.att?, muscle attachment area; ri.i, internal ridge, ri.o, outer ridge; pl, platform; sb.l, subanal lamina; tvr, transverse ridge ( = crista transversalis interna posterior, Stensiö 1948).
Extended Data Figure 5 Strict consensus tree from 7,039 trees (L = 640) from analysis of the expanded data set (85 taxa, 259 characters).
Numbers on branches denote Bremer and bootstrap support. Green squares denote presence of bony claspers (character 122), red squares denote presence of cartilaginous claspers (character 259) and white squares denote absence of both types of clasper. Circles denote gain/loss of the two types of clasper under the most-parsimonious optimization.
Extended Data Figure 6 Majority-rule consensus tree, and one of the most-parsimonious trees (length 640) from analysis of the expanded data set (85 taxa, 259 characters).
Numbers on branches indicate the percentage of most-parsimonious trees that contain a particular clade (100% unless otherwise indicated). Green squares denote presence of bony claspers (character 122), red squares denote presence of cartilaginous claspers (character 259) and white squares denote absence of both types of clasper. Circles denote gain/loss of the two types of clasper under the most-parsimonious optimization.
Extended Data Figure 7 Strict consensus tree from 808 trees (L = 611) from re-analysis of the data set in ref. 8.
Numbers on branches denote Bremer and bootstrap support.
Extended Data Figure 8 Majority-rule consensus tree, and one of the most-parsimonious trees (length 611) from analysis of the data in ref. 8.
Numbers on branches indicate percentage of MPTs that contain a particular clade (100% unless otherwise indicated).
This file contains Supplementary Text and Data, which includes Geological and Taxonomic Background Information, Further Discussion of antiarch reproductive structures, Phylogenetic analysis, Results and additional references (see Contents for more details). (PDF 622 kb)
This zipped file contains the new data matrix for phylogenetic analsyis (Placoderms_Long.nex) and the data matrix of Dupret et al 2014 for phylogenetic analsyis (Placoderms_Dupret.nex). Please note that a corrected version of Placoderms_Long.nex was uploaded on 24 November 2014. (ZIP 11 kb)
About this article
Cite this article
Long, J., Mark-Kurik, E., Johanson, Z. et al. Copulation in antiarch placoderms and the origin of gnathostome internal fertilization. Nature 517, 196–199 (2015). https://doi.org/10.1038/nature13825
The erroneous chondrichthyan egg case assignments from the Devonian: implications for the knowledge on the evolution of the reproductive strategy within chondrichthyans
The Science of Nature (2021)
BMC Biology (2017)
New findings in a 400 million-year-old Devonian placoderm shed light on jaw structure and function in basal gnathostomes
Scientific Reports (2017)
Nature Communications (2015)