Cypridoidean ostracods are one of a number of animal taxa that reproduce with giant sperm, up to 10 000 µm in length, but they are the only group to have aflagellate, filamentous giant sperm. The evolution and function of this highly unusual feature of reproduction with giant sperm are currently unknown. The hypothesis of long-term evolutionary persistence of this kind of reproduction has never been tested. We here report giant sperm discovered by propagation phase contrast X-ray synchrotron micro- and nanotomography, preserved in five Miocene ostracod specimens from Queensland, Australia. The specimens belong to the species Heterocypris collaris Matzke-Karasz et al. 2013 (one male and three females) and Newnhamia mckenziana Matzke-Karasz et al. 2013 (one female). The sperm are not only the oldest petrified gametes on record, but include three-dimensional subcellular preservation. We provide direct evidence that giant sperm have been a feature of this taxon for at least 16 Myr and provide an additional criterion (i.e. longevity) to test hypotheses relating to origin and function of giant sperm in the animal kingdom. We further argue that the highly resistant, most probably chitinous coats of giant ostracod sperm may play a role in delaying decay processes, favouring early mineralization of soft tissue.

Department of Earth and Environmental Sciences Palaeontology and Geobiology Ludwig Maximilian University and GeoBio Center Richard Wagner Strasse 10 80333 Munich Germany

Department of Zoology Faculty of Science Charles University Viničná 7 12844 Praha Czech Republic

European Synchrotron Radiation Facility 38043 Grenoble France

Lake Biwa Museum Oroshimo 1091 Kusatsu Shiga 525 0001 Japan

School of Biological Earth and Environmental Sciences University of New South Wales Sydney New South Wales 2052 Australia

School of Civil Engineering and Physical Sciences La Trobe University PO Box 199 Bendigo Victoria 3552 Australia

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Pitnick S, Hosken DJ, Birkhead TR. 2009. Sperm morphological diversity. In Sperm biology, an evolutionary perspective (eds Birkhead TR, Hosken DJ, Pitnick S.), pp. 69–149. Amsterdam, The Netherlands: Elsevier.

Bauer H. 1940. Über die Chromosomen der bisexuellen und der parthenogenetischen Rasse des Ostracoden DOI

Matzke-Karasz R. 2005. Giant spermatozoon coiled in small egg: fertilization mechanisms and their implications for evolutionary studies on Ostracoda (Crustacea). J. Exp. Zool. Part B 304, 129–149. ( 10.1002/jez.b.21031) PubMed DOI

Wingstrand KG. 1988. Comparative spermatology of the Crustacea Entomostraca. 2. Subclass Ostracoda. Biol. Skr. Dan. Vid. Sel. 32, 1–149.

Lowndes AG. 1935. The sperms of freshwater ostracods. Proc. Zool. Soc. Lond. 1935, 35–48. ( 10.1111/j.1469-7998.1935.tb06231.x) DOI

Gupta BL. 1968. Aspects of motility in the non-flagellate spermatozoa of freshwater ostracods. In Aspects of cell motility (ed. Miller PL.). PubMed

Smith RJ. 2000. Morphology and ontogeny of Cretaceous ostracods with preserved appendages from Brazil. Palaeontology 43, 63–68. ( 10.1111/1475-4983.00119) DOI

Matzke-Karasz R, Horne DC, Janz H, Griffiths HI, Hutchinson WF, Preece RC. 2001. 5,000 year-old spermatozoa in Quaternary Ostracoda (Crustacea). Naturwissenschaften 88, 268–272. ( 10.1007/s001140100234) PubMed DOI

Matzke-Karasz R, Smith RJ, Symonova R, Miller CG, Tafforeau P. 2009. Sexual intercourse involving giant sperm in Cretaceous ostracode. Science 324, 1535 ( 10.1126/science.1173898) PubMed DOI

Siveter DJ, Sutton MD, Briggs DEG, Siveter DJ. 2003. An ostracode crustacean with soft parts from the Lower Silurian. Science 302, 1749–1751. ( 10.1126/science.1091376) PubMed DOI

Siveter DJ, Siveter DJ, Sutton MD, Briggs DEG. 2007. Brood care in a Silurian ostracod. Proc. R. Soc. B 274, 465–469. ( 10.1098/rspb.2006.3756) PubMed DOI PMC

Siveter DJ, Briggs DEG, Siveter DJ, Sutton MD, Joomun SC. 2013. A Silurian myodocope with preserved soft-parts: cautioning the interpretation of the shell-based ostracod record. Proc. R. Soc. B 280, 1471–2954. ( 10.1098/rspb.2012.2664) PubMed DOI PMC

Keyser D, Weitschat W. 2005. First record of ostracods (Crustacea) in Baltic amber. Hydrobiologia 538, 107–114. ( 10.1007/s10750-004-5941-5) DOI

Williams M, Siveter DJ, Ashworth AC, Wilby PR, Horne DJ, Lewis AR, Marchant DR. 2008. Exceptionally preserved lacustrine ostracods from the Middle Miocene of Antarctica: implications for high-latitude palaeoenvironment at 77° south. Proc. R. Soc. B 275, 2449–2454. ( 10.1098/rspb.2008.0396) PubMed DOI PMC

Wilkinson IP, Wilby PR, Williams M, Siveter DJ, Page AA, Leggitt L, Riley DA. 2010. Exceptionally preserved ostracodes from a Middle Miocene palaeolake, California, USA. J. Geol. Soc. Lond. 167, 817–825. ( 10.1144/0016-76492009-178) DOI

Nordqvist O. 1885. Beitrag zur Kenntniss der inneren männlichen Geschlechtsorgane der Cypriden. Act. Soc. Sci. Fenn. 15, 129–168.

Iepure S, Namiotko T, Valdecasas AG, Magyari EK. 2012. Exceptionally well-preserved giant spermatozoa in male and female specimens of an ostracod PubMed DOI

Poinar G. 2000. First fossil record of stalked spermatophores with sperm (Collembola: Hexapoda). Hist. Biol. 14, 229–234. ( 10.1080/10292380009380570) DOI

Hand SJ, Archer M. 2005. A new hipposiderid genus (Microchiroptera) from an Early Miocene bat community in Australia. Palaeontology 48, 371–383. ( 10.1111/j.1475-4983.2005.00444.x) DOI

Archer M, Hand SJ, Godthelp H. 1994. Riversleigh: the story of animals in ancient rainforests of inland Australia. Sydney, Australia: Reed Books.

Paganin D, Mayo SC, Gureyev TE, Miller R. 2002. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J. Microsc. 206, 33–40. ( 10.1046/j.1365-2818.2002.01010.x) PubMed DOI

Langer M, Pacureanu A, Suhonen H, Grimal Q, Cloetens P, Peyrin F. 2012. X-Ray phase nanotomography resolves the 3D human bone ultrastructure. PLoS ONE 7, e35691 ( 10.1371/journal.pone.0035691) PubMed DOI PMC

Yamada S, Matzke-Karasz R. 2012. How is a giant sperm ejaculated? Anatomy and function of the sperm pump, or ‘Zenker organ’, in PubMed DOI

Matzke-Karasz R, Neil JV, Smith RJ, Godthelp H, Archer M, Hand SJ. 2013. Ostracods (Crustacea) with soft part preservation from Miocene cave deposits of the Riversleigh World Heritage Area, NW Queensland, Australia. J. Syst. Palaeontol. 11, 789–819. ( 10.1080/14772019.2012.760007) DOI

Thomas DB, McGoverin CM, Fordyce RE, Frew RD, Gordon KC. 2011. Raman spectroscopy of fossil bioapatite: a proxy for diagenetic alteration of the oxygen isotope composition. Palaeogeogr. Palaeocol. 310, 62–70. ( 10.1016/j.palaeo.2011.06.016) DOI

Ozerov IA, Zhinkina NA, Efimov AM, Machs EM, Rodionov AV. 2006. Feulgen-positive staining of the cell nuclei in fossilized leaf and fruit tissues of the Lower Eocene Myrtaceae. Bot. J. Linn. Soc. 150, 315–321. ( 10.1111/j.1095-8339.2006.00471.x) DOI

Bomfleur B, McLoughlin S, Vajda V. 2014. Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in royal ferns. Science 343, 1376–1377. ( 10.1126/science.1249884) PubMed DOI

Taylor TN, Millay MA. 1977. Structurally preserved fossil cell contents. Trans. Am. Microsc. Soc. 96, 390–393. ( 10.2307/3225870) DOI

Li CW, Chen JY, Hua TE. 1998. Precambrian sponges with cellular structures. Science 279, 879–882. ( 10.1126/science.279.5352.879) PubMed DOI

Schopf JM. 1975. Modes of fossil preservation. Rev. Palaeobot. Palynol. 20, 27–53. ( 10.1016/0034-6667(75)90005-6) DOI

Voigt E. 1935. Die Erhaltung von Epithelzellen mit Zellkernen, von Chromatophoren und Corium in fossiler Froschhaut aus der mitteleozänen Braunkohle des Geiseltales. Nova Act. L. C. NF 3, 340–360.

Voigt E. 1988. Preservation of soft tissues in the Eocene lignite of the Geiseltal near Halle/S. Cour. Forsch. Senck. 107, 325–343.

Martill DM. 1990. Macromolecular resolution of fossilized muscle tissue from an elopomorph fish. Nature 346, 171–172. ( 10.1038/346171a0) DOI

Huldtgren T, Cunningham J, Yin C, Stampanoni M, Marone F, Donoghue PCJ, Bengtson S. 2011. Fossilized nuclei and germination structures identify Ediacaran ‘animal embryos’ as encysting protists. Science 334, 1696–1699. ( 10.1126/science.1209537) PubMed DOI

Schiffbauer JD, Xiao S, Sharma KS, Wang G. 2012. The origin of intracellular structures in Ediacaran metazoan embryos. Geology 40, 223–226. ( 10.1130/G32546.1) DOI

Pitnick S, Markow TA, Spicer GS. 1995. Delayed male maturity is a cost of producing large sperm in PubMed DOI PMC

Miller GT, Pitnick S. 2002. Sperm–female co-evolution in PubMed DOI