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Sexual Intercourse Involving Giant Sperm in Cretaceous Ostracode

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Science  19 Jun 2009:
Vol. 324, Issue 5934, pp. 1535
DOI: 10.1126/science.1173898

Abstract

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.

The microcrustacean ostracodes are the most abundantly preserved arthropods in the fossil record dating from at least the Ordovician (450 million years ago) (1). However, their body and appendages are only rarely preserved. One example of high-quality soft parts preservation is Harbinia micropapillosa (Bate, 1972) (2) (Cyprididae, Cypridoidea) from the Cretaceous Santana Formation of Brazil. Because scanning electron microscopy (3) cannot view internal features, we performed holotomography of five H. micropapillosa specimens, three males and two females, revealing the morphology of their internal reproductive system.

We compared submicrometer inline quantitative phase x-ray synchrotron tomography (holotomography) (4) on the beamline ID19 of the ESRF (Grenoble, France) on specimens of H. micropapillosa and of the extant species Eucypris virens (Jurine, 1820) (5). Phase contrast–based microtomographic techniques have been applied to nondestructively image microfossils (6), but application of phase retrieval on dense and complex fossils is a recent and powerful approach in paleontology (4). Extant cypridoidean ostracodes possess an intricate reproductive system comprising about a third of the volume of the body. In both genders, the reproductive organs are divided into two separately functioning systems on both sides of the body. The males have two large sperm pumps (Zenker organs), modified from the posterior section of the vas deferens (fig. S1A). The females possess epithelial recipients (seminal receptacles) at the end of long ducts originating in the two vaginal openings. Empty seminal receptacles of virgin females are folded up; the volume of transferred sperm gives the receptacles their shape and size after mating. These specialized reproductive systems are required for maneuvering the giant sperm: aflagellate, but filiform sperm cells. Sperm lengths range across species from several hundred micrometers to millimeters and thus are often longer than the ostracodes themselves (fig. S1, B and C). Their resistant sheaths allow fossil sperm to be recovered from 5000-year-old ostracodes from Neolithic excavations (7).

Three-dimensional processing of holotomographic data (movies S1 to S3) revealed that three male specimens of H. micropapillosa contained paired hollow tubes in the posterior part of the body (Fig. 1, B to D) suggestive of Zenker organs. Two female specimens had paired cavities near the midpoint of the body (Fig. 1F), corresponding to the seminal receptacles in recent Cyprididae (Fig. 1E), which are only known from ostracodes reproducing with giant sperm. The receptacles must have been filled with sperm in order to be preserved as two cavities. Thus, giant sperm had developed in cypridoidean ostracodes by ~100 million years ago.

Fig. 1

Partial reconstruction of E. virens (extant) and H. micropapillosa (fossil). Anterior is to the left. Orange structures indicate central tubes of Zenker organs in males or seminal receptacles in females; brown, esophagus; turquoise, mandible; purple, upper lip; pink, lower lip; green, valves; and gray scales, whole-body reconstruction. All scale bars indicate 100 μm. (A) Lateral view of male E. virens with several organs included for comparison. (B) Male H. micropapillosa in lateral view with several organs in context of whole-body reconstruction. (C and D) Ventral views of several organs including tubes of Zenker organs of male H. micropapillosa. (E) Lateral view of female E. virens with several organs included for comparison. (F) Female H. micropapillosa in lateral view with several organs in context of whole-body reconstruction, including seminal receptacles.

Reproduction with giant sperm, mainly studied in Drosophila species, occurs in distinct groups scattered over the animal kingdom. The influence of different selection pressures on this character has been examined, but its long-term stability was unknown. In spite of potential costs, this trait appears to be long-lived even in geological time scales. The wide occurrence of giant sperm in living members of suborder Cypridocopina, coupled with our fossil evidence, suggests that it evolved only once in the group, unlike in Drosophila (8). Given that sperm size provides an assay “for comparative analyses of the strength of sexual selection in … species without postmating parental investment” (9), the persistence of reproduction with giant sperm through geological time may add a criterion to test for the pressure of sexual selection with holotomography recovering data from the past through exceptionally preserved (micro)fossils.

Supporting Online Material

www.sciencemag.org/cgi/content/full/324/5934/1535/DC1

Materials and Methods

Fig. S1

Reference

Movies S1 to S3

References and Notes

  1. Materials and methods are available as supporting material on Science Online.
  2. Supported by the ESRF (proposal ec-274), the European Union Marie Curie RTN SexAsex (FP6-512492), LMU Palaeontology, the Lake Biwa Museum (Japan), and the Natural History Museum (by loan of fossil specimens). Holotomographies are available online at http://paleo.esrf.eu.
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