Reproduction with giant sperm occurs in distinct groups scattered over the animal kingdom. Although experiments in Drosophila assessed the influence of different selection pressures on this character, no information was available on its long-term stability. Sub-micrometer-resolution synchrotron quantitative phase tomography (holotomography) of exceptionally well-preserved three-dimensional Cretaceous ostracode fossils from the Brazilian Santana Formation indicates that ostracode reproduction with giant sperm persisted for at least over the past 100 million years. Remnants of the male sperm pumps as well as giant, inflated female sperm receptacles evidence that, despite high costs, reproduction with giant sperm can be an evolutionary successful strategy.

Ostracods of the superfamily Cypridoidea have giant spermatozoa. However, little data exist on the sperm-egg interaction in this group: only two publications have so far given the most ambiguous indication that the entire sperm enters the egg on fertilization. These assumptions have not yet been tested with modern techniques, nor has their putative value for developmental and evolutionary investigations been realized. The present paper gives the first, clear, light- and scanning electron microscopical evidence of the entire giant ostracod spermatozoon being incorporated into the egg. Coiling of the sperm underneath the egg shell is shown in the early zygotes of the species Mytilocypris praenuncia and Pseudocandona marchica. Additionally, data on the morphology of female and male reproductive tracts are given for M. praenuncia. Hypotheses on the evolution of giant filiform sperm in the Animal Kingdom are reviewed, and their applicability to ostracods is discussed. The demonstrated ingression of the entire sperm implies the entry of the two giant paternal mitochondrial derivates into the zygote in Cypridoidea and potentially casts doubt upon the dogma of strict maternal inheritance of mitochondrial DNA. Evidence of paternal inheritance of mtDNA in several organisms has recently given rise to a controversial debate on this issue; the possible significance of this phenomenon for molecular studies on ostracod phylogeny and evolution is discussed.

Cypridoidean ostracods are one of a number of animal taxa that reproduce with giant sperm, up to 10 000 mm 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 MatzkeKarasz 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.

Smith, R.J., Matzke-Karasz, R., Kamiya, T., De Deckker, P. 2016. Sperm lengths of non-marine cypridoidean ostracods (Crustacea). -Acta Zoologica (Stockholm) 97: 1-17.

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