Copulation in antiarch placoderms and the origin of gnathostome internal fertilization

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Abstract

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.

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Figure 1: Male reproductive structures in antiarchs and ptyctodontids.
Figure 2: Female reproductive structures in Middle–Late Devonian antiarchs.
Figure 3: Male and female sexual dimorphism in M. dicki.
Figure 4: Phylogeny of major lineages of gnathostomes, based on analysis of an expanded version of the data set from ref. 8.

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Acknowledgements

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.

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Contributions

The project was designed by J.A.L., with material examined and described by J.A.L., E.M.K., Z.J., K.T., B.C. and P.E.A. M.S.Y.L. performed phylogenetic analyses with input from J.A.L., G.C.Y. and B.C. M.N., J.D.B. and R.J. collected and prepared material, provided site information and input to the discussion. Illustrations were made by J.A.L. and B.C. with photography supplied for some specimens by the Natural History Museum, London, and by the Institute of Geology at Tallinn University of Technology. All authors contributed to data interpretation, figures and writing of the paper.

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Correspondence to John A. Long.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Location and stratigraphic position of Estonian specimens of Microbrachius.

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.

Extended Data Figure 3 Growth of claspers in M. dicki males.

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.

Extended Data Figure 4 New information on pelvic region anatomy in antiarchs.

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).

Extended Data Figure 9 Reconstruction showing hypothetical mating Microbrachius, with male to the right, female on left.

Artwork by B. Choo.

Supplementary information

Supplementary Information

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)

Supplementary Data

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)

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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

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