Exceptional preservation of ancient sperm in Miocene ostracods from the Riversleigh fossil deposits (Queensland, Australia)

Freshwater ostracods, a class of mussel-like crustaceans, put a great deal of effort into the business of reproduction. Witness the fact that they produce giant sperm cells that are often much longer than the organisms themselves. Now Dr. Renate Matzke-Karasz, Privatdozentin for Geobiology in LMU’s Institute of Paleontology and Geobiology, has shown that this strategy must be highly successful, as it has deep evolutionary roots.

Specifically, she has directly demonstrated, for the first time, that giant sperm cells were already being produced by freshwater ostracods 16 million years ago. “We have been able to reconstruct the morphology of fossilized giant sperm at the cellular level. The cell nucleus, as well as a prominent invagination in the cell membrane, can be clearly discerned in the fossil specimens,” says Matzke-Karasz. Moreover, the preserved sperm look no different to those found in modern representatives of the class. “We can distinguish the typical helical organization of the organelles in the sperm cell, which makes its surface look like a hawser or cable. But the most astounding aspect of our findings is that it strongly suggests that the mode of reproduction in these tiny crustaceans has remained virtually unchanged to this day.”

The fossils had lain buried in sedimentary beds in Australia for approximately 16 million years when Matzke-Karasz and her colleagues used state-of-the-art technology to examine them. The team studied a total of 66 ostracod fossils at the European Synchrotron Radiation Facility (ESRF) in Grenoble, using synchrotron X-ray tomography, an imaging technique similar to medical computer tomography. In this case, however, the researchers were able to use a new high-resolution nanotomography procedure on their ancient specimens. “Using these methods, we can reconstruct the morphology of the fossil giant sperm cells in three dimensions,” says Matzke-Karasz. Most ostracods are only a few millimeters long, but their sperm cells can reach lengths in excess of 1 centimeter.

Ostracods have been around for the past 500 million years. Thanks to their bivalve-like calcareous shells, they are very frequently fossilized, often well preserved and easy to recognize. Indeed, their characteristic bivalved shells are used to date sediments, and also provide information on the environments in which they lived. Their soft parts, however, are very rarely conserved. However, Matzke-Karasz and colleagues had previously obtained indirect evidence for an early evolutionary origin of giant sperm. In 2009 they reported the identification of the characteristic organs required for the transfer of giant sperm in ostracod fossils from the famous Santana Formation in Eastern Brazil, which dates to Cretaceous times.

A highly elaborate organ system

The much younger fossils used in their new study were found by vertebrate paleontologists Professor Michael Archer and Dr. Suzanne Hand of the University of New South Wales. They were recovered from sediments that had been laid down in a cave in what is now the state of Queensland in Australia. “The extremely good state of preservation of these fossils is largely due to the very high level of phosphate in these sediments,” says Matzke-Karasz. Archer and Hand were able to reconstruct the environment inhabited by the ostracods. The animals lived in small bodies of water in a cave system, which was penetrated by sunlight. The cave was also frequented by bats, and their phosphate-rich droppings ensured the conservation of the minuscule ostracods by phosphatization. In this process, soft tissues are rapidly replaced by phosphatic minerals, preserving the fine morphological details which paleontologists prize but rarely find.

Freshwater ostracods have a highly elaborate reproductive system, which accounts for one-third of the volume of the mature adult. Indeed, in both males and females, the reproductive organs are duplicated. The males have extremely long seminal ducts, and sperm pumps, which provide for transfer of the giant sperm to the female. The females possess large seminal receptacles in which the sperm are stored prior to fertilization. The presence of these organ systems in the new fossils has also been confirmed by tomographic imaging. „Muschelkrebse müssen viel Energie in Produktion, Transport und Aufbewahrung der Riesenspermien einsetzen, was auf den ersten Blick etwas opulent wirkt“, sagt Matzke-Karasz. Ihre 3-D-Darstellungen zeigen nun, dass Spermien und Fortpflanzungstechnik vor 16 Millionen Jahren nicht anders waren als heute. „Das weist darauf hin, dass diese Fortpflanzungsart funktionell ein Erfolgsmodell darstellt – über Millionen Jahre hinweg “, sagt Matzke-Karasz. Weitere Untersuchungen sollen nun Aufschluss darüber geben, was diese bizarr anmutende Fortpflanzungsmethode so erfolgreich macht.

“Ostracods devote large amounts of energy to the production, transport and storage of giant sperm and, at first sight, the system might seem overelaborate,” says Matzke-Karasz. But her 3-D reconstructions show that sperm morphology and reproductive physiology in these organisms have remained virtually unchanged for tens of millions of years. “This suggests that their mode of reproduction represents a functionally successful model,” says Matzke-Karasz. Further studies will hopefully elucidate the reasons for the biological efficacy of such a bizarre system.

Contact

Dr. Renate Matzke-Karasz
Institute for Paleontology and Geobiology
GeoBioCenter der LMU
Tel.: 089/2180 6644
E-Mail: r.matzke@lrz.uni-muenchen.de

Publication

Renate Matzke-Karasz, John Neil, Robin Smith, Radka Symonová, Libor Morkovský, Michael Archer, Suzanne Hand, Peter Cloetens, Paul Tafforeau:
Subcellular preservation in giant ostracod sperm from an early Miocene cave deposit in Australia
In: Proceeding of the Royal Society B