Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Free blastocyst and implantation stages in the European brown hare: correlation between ultrasound and histological data

Barbara Drews A B , Jennifer Ringleb A , Romy Waurich A , Thomas Bernd Hildebrandt A , Katharina Schröder A and Kathleen Roellig A
+ Author Affiliations
- Author Affiliations

A Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Strasse 17, 10315 Berlin, Germany.

B Corresponding author. Email: drews@izw-berlin.de

Reproduction, Fertility and Development 25(6) 866-878 https://doi.org/10.1071/RD12062
Submitted: 27 February 2012  Accepted: 23 July 2012   Published: 31 August 2012

Abstract

The European brown hare (Lepus europaeus) is the only species with superconception, whereby the maternal reproductive tract hosts two sets of conceptuses at different developmental stages. The embryonic development of the hare has not yet been described. To understand the mechanism of superconception, we studied oviduct transport and implantation stages by embryo flushing and live high-resolution ultrasound. Ultrasound data of implantation stages is correlated with histology. In the oviduct, a mucin coat is deposited on the zona pellucida. The blastocysts enter the uterine horns on Day 5, 1 day later than in the rabbit, and directly expand approximately threefold. Spacing is accompanied by peristaltic movement of the endometrium. The mucin coat disappears and the conceptuses attach. The yolk-sac expands in the blastocoel and syncytial knobs invade the antimesometrial endometrium. Maternal blood lacunae appear in the mesometrial endometrial folds, which are subsequently invaded by the syncytiotrophoblast. The haemochorial chorioallantoic placenta forms. The yolk-sac cavity is gradually replaced by the allantois and finally by the exocoel. The different reproductive strategies of the precocial hare and the altricial rabbit are discussed. We assume that the lagomorph-specific mucin coat and the hare-specific delay of the oviduct–uterine transition are prerequisites for superconception.

Additional keywords: Lagomorpha, mucin coat, prenatal development, superconception, syncytiotrophoblast.


References

Alliston, C. W., and Pardee, N. R. (1973). Variability of embryonic development in the rabbit at 19 to 168 hours after mating. Lab. Anim. Sci. 23, 665–670.
| 1:STN:280:DyaE2c%2Fis1Kltw%3D%3D&md5=1d06d9f91d246c410306cfb5d080a8a6CAS | 4356335PubMed |

Amoroso, E. C. (1961). Placentation. In ‘Marshall’s Physiology of Reproduction’. (Ed. A. S. Parks.) pp. 127–311. (Little Brown & Co: Boston.)

Beneden, E. V., and Julin, C. (1884). Recherches sur la formation des annexes foetales chez les Mammiferes (Lapin et Cheiropteres). Arch. Biol. , 369–438.

Blaise, S., de Parseval, N., Benit, L., and Heidmann, T. (2003). Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc. Natl Acad. Sci. USA 100, 13 013–13 018.
Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXoslKms70%3D&md5=490046890203c955d511a39a59744e03CAS |

Böving, B. G. (1957). Rabbit egg coverings. Anat. Rec. 127, 270.

Böving, B. G. (1962). Anatomical analysis of rabbit trophoblast invasion. Contrib. Embryol. 37, 33–55.

Boyd, J. D., and Hamilton, W. J. (1961). Cleavage, early development and implantation of the egg. In ‘Marshall’s Physiology of Reproduction’. (Ed. A. S. Parkers.) pp. 1–126. (Longmanns, Green & Co.: London.)

Christie, G. A. (1967). Histochemistry of implantation in the rabbit. Histochemie 9, 13–29.
Histochemistry of implantation in the rabbit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXktVWgtrk%3D&md5=9fc27922b86edc60ae5a34798a1bddb7CAS | 5586440PubMed |

Daniel, J. C. (1964). Early growth of rabbit trophoblast. Am. Nat. 98, 85–93.
Early growth of rabbit trophoblast.Crossref | GoogleScholarGoogle Scholar |

Denker, H. W., and Hafez, E. S. E. (1975). Proteases and implantation in rabbit: role of trophoblast vs uterine secretion. Cytobiologie 11, 101–109.
| 1:CAS:528:DyaE2MXltFWlurk%3D&md5=a30716d8b86a153db224c6c935243b73CAS | 1140497PubMed |

Dupressoir, A., Marceau, G., Vernochet, C., Benit, L., Kanellopoulos, C., Sapin, V., and Heidmann, T. (2005). Syncytin-A and syncytin-B, two fusogenic placental envelope genes of retroviral origin conserved in Muridae. Proc. Natl. Acad. Sci. USA 102, 725–730.
| 1:CAS:528:DC%2BD2MXis1CqsL4%3D&md5=e6bbf13e4c7adf495f27deda6980353cCAS | 15644441PubMed |

El-Gayar, M., and Holtz, W. (2009). Coating of objects introduced into the oviduct of pseudopregnant rabbit does. Reprod. Domest. Anim. 44, 326–330.
Coating of objects introduced into the oviduct of pseudopregnant rabbit does.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3jsVOjug%3D%3D&md5=34a9f4ba40eb6ccb886a5215748daec7CAS | 18992096PubMed |

Enders, A. C., and Schlafke, S. (1969). Cytological aspects of trophoblast–uterine interaction in early implantation. Am. J. Anat. 125, 1–29.
Cytological aspects of trophoblast–uterine interaction in early implantation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF1M7oslOisA%3D%3D&md5=2b42ca8dc107cbe8000fc3db0c07ca0bCAS | 5770161PubMed |

Enders, A. C., and Schlafke, S. (1971). Penetration of the uterine epithelium during implantation in the rabbit. Am. J. Anat. 132, 219–239.
Penetration of the uterine epithelium during implantation in the rabbit.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE38%2FisVSrtA%3D%3D&md5=e139281c6014b82665ac601a867afc63CAS | 5165258PubMed |

Fischer, B., Mootz, U., Denker, H. W., Lambertz, M., and Beier, H. M. (1991). The dynamic structure of rabbit blastocyst coverings. 3. Transformation of coverings under nonphysiological developmental conditions. Anat. Embryol. 183, 17–27.
| 1:STN:280:DyaK3M3ntlamtQ%3D%3D&md5=14a8270e36715a0f55e383c4bee9eda6CAS | 2053707PubMed |

Fukuda, M., and Fukuda, K. (1994). Uterine endometrial cavity movement and cervical mucus. Hum. Reprod. 9, 1013–1016.
| 1:STN:280:DyaK2M%2FltFemsg%3D%3D&md5=115feb5171d58de47e76dd9fa76f4d34CAS | 7962368PubMed |

Gottschewski, G. H. M., and Zimmermann, W. (1973). ‘Die Embryonalentwicklung des Hauskaninchens: Normogenese und Teratogenese.’ (M. and H. Schaper: Hannover.)

Hafez, E. S. E. (1964). Growth and survival of blastocysts in the domestic rabbit II. Quantitative effects of exogenous progesterone following ovariectomy. J. Reprod. Fertil. Suppl. 7, 241–249.
Growth and survival of blastocysts in the domestic rabbit II. Quantitative effects of exogenous progesterone following ovariectomy.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2c%2FpslGiug%3D%3D&md5=d29e59878aba0db43fa3691daea563feCAS |

Hamilton, W. J., Boyd, J. D., and Mossmann, H. J. (1972). ‘Human Embryology. Prenatal Development of Form and Function.’ (Heffer: Cambridge.)

Hediger, H. (1984). Die Zucht des Feldhasen (Lepus europaeus PALLAS) in Gefangenschaft. Physiol. Comp. Oecol. 1, 6–63.

Hildebrandt, T. B., Roellig, K., Goeritz, F., Fassbender, M., Krieg, R., Blottner, S., Behr, B., and Hermes, R. (2009). Artificial insemination of captive European brown hares (Lepus europaeus PALLAS, 1778) with fresh and cryopreserved semen derived from free-ranging males. Theriogenology 72, 1065–1072.
Artificial insemination of captive European brown hares (Lepus europaeus PALLAS, 1778) with fresh and cryopreserved semen derived from free-ranging males.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnmsFOguw%3D%3D&md5=0134ca4bdc4974ee2c6a67b7026c76a6CAS | 19740536PubMed |

Hoffman, L. H., Winfrey, V. P., and Hoos, P. C. (1990). Sites of endometrial vascular leakage during implantation in the rabbit. Anat. Rec. 227, 47–61.
Sites of endometrial vascular leakage during implantation in the rabbit.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3czhsVSjsA%3D%3D&md5=ead0f6239faed178b3b39f24f9d1c0ffCAS | 2368926PubMed |

Hohn, H. P., Donner, A. J., and Denker, H. M. (2003). Endometrial receptivity: selective adhesion competence of rabbit uterine epithelium for trophoblast but not for various tumor cells. Cells Tissues Organs 173, 204–216.
Endometrial receptivity: selective adhesion competence of rabbit uterine epithelium for trophoblast but not for various tumor cells.Crossref | GoogleScholarGoogle Scholar | 12766350PubMed |

Ijland, M. M., Evers, J. L. H., Dunselman, G. A. J., vanKatwijk, C., Lo, C. R., and Hoogland, H. J. (1996). Endometrial wavelike movements during the menstrual cycle. Fertil. Steril. 65, 746–749.
| 1:STN:280:DyaK283mslShsQ%3D%3D&md5=dab946fad83068102bc09df8d0f475b1CAS | 8654632PubMed |

Kane, M. T. (1975). Inhibition of zona shedding of rabbit blastocysts in culture by the presence of a mucin coat. J. Reprod. Fertil. 44, 539–542.
Inhibition of zona shedding of rabbit blastocysts in culture by the presence of a mucin coat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE28%2FkvVGmtA%3D%3D&md5=b495ebd74d5fbe323bde163f6efc5623CAS | 1181419PubMed |

Kaulenas, A., Parkington, H. C., and Coleman, H. A. (1991). Response of the rat myometrium to phenylephrine in early pregnancy and the effects of 6-hydroxydopamine. Br. J. Pharmacol. 103, 1429–1434.
Response of the rat myometrium to phenylephrine in early pregnancy and the effects of 6-hydroxydopamine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXksVamt7w%3D&md5=86e972f8b37290a236ede077db98542dCAS | 1909201PubMed |

Kirchner, C., and Mootz, U. (1969). Untersuchungen an uterusspezifischen Glykoproteinen während der frühen Gravidität des Kaninchens Oryctologaus cuniculus. Dev. Genes Evol. 164, 97–133.
Untersuchungen an uterusspezifischen Glykoproteinen während der frühen Gravidität des Kaninchens Oryctologaus cuniculus.Crossref | GoogleScholarGoogle Scholar |

Kirchner, C., and Seitz, K. (1972). Elektronenmikroskopische Untersuchungen über die Blastozyste des Kaninchens vor der Implantation in Bezug auf ihre Wechselbeziehung zur uterinen Umgebung. Dev. Genes Evol. 170, 221–233.
Elektronenmikroskopische Untersuchungen über die Blastozyste des Kaninchens vor der Implantation in Bezug auf ihre Wechselbeziehung zur uterinen Umgebung.Crossref | GoogleScholarGoogle Scholar |

Krespi, V., and Davies, J. (1963). Electric potential differences across the foetal membranes of the rabbit. J. Embryol. Exp. Morphol. 11, 167–174.
| 1:CAS:528:DyaF3sXkt1elur0%3D&md5=f9468e23bc33965916b3b9ab904caac2CAS | 14035732PubMed |

Larsen, J. F. (1961). Electron microscopy of the implantation site in the rabbit. Am. J. Anat. 109, 319–334.
Electron microscopy of the implantation site in the rabbit.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF38%2Fmtl2htg%3D%3D&md5=40987a89b981602d2f9e40500e8413fbCAS | 14462495PubMed |

McLaren, A., and Michie, D. (1959). Super pregnancy in the mouse I. Implantation and foetal mortality after induced superovulation in females of various ages. J. Exp. Biol. 36, 281–300.

Menkhorst, E., and Selwood, L. (2008). Vertebrate extracellular preovulatory and postovulatory egg coats. Biol. Reprod. 79, 790–797.
Vertebrate extracellular preovulatory and postovulatory egg coats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlSrtL3L&md5=d57d6d09f26927f44e7f30b30da434ceCAS | 18614703PubMed |

Murakami, H., and Imai, H. (1996). Successful implantation of in vitro cultured rabbit embryos after uterine transfer: a role for mucin. Mol. Reprod. Dev. 43, 167–170.
Successful implantation of in vitro cultured rabbit embryos after uterine transfer: a role for mucin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XpslWisA%3D%3D&md5=61433657ff744c294074349579e716a3CAS | 8824914PubMed |

Novak, R. M. (1991). Order Lagomorpha. In ‘Walkers Mammals of the World’. 5th edn. (Ed. R. M. Nowak.) pp. 539–560. (The John Hopkins University Press: Baltimore.)

Püschel, B., Daniel, N., Bitzer, E., Blum, M., Renard, J., and Viebahn, C. (2010). The rabbit (Oryctolagus cuniculus): a model for mammalian reproduction and early embryology. Cold Spring Harb. Protoc. 1, pdb.emol139.

Rexroad, C. E., and Guthrie, H. D. (1983). Alpha-adrenergic receptors in myometrium of pregnant and non-pregnant pics until Day 19 postestrus. Biol. Reprod. 29, 615–619.
Alpha-adrenergic receptors in myometrium of pregnant and non-pregnant pics until Day 19 postestrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXlsFars7o%3D&md5=36a5e6a29382e3f3bb993be60651e8e0CAS | 6313082PubMed |

Roellig, K., Goeritz, F., Fickel, J., Hermes, R., Hofer, H., and Hildebrandt, T. B. (2010a). Superconception in mammalian pregnancy can be detected and increases reproductive output per breeding season. Nat. Commun. 1, 1–7.
Superconception in mammalian pregnancy can be detected and increases reproductive output per breeding season.Crossref | GoogleScholarGoogle Scholar |

Roellig, K., Goeritz, F., and Hildebrandt, T. B. (2010b). Ultrasonographic characterisation of prenatal development in European brown hares (Lepus europaeus PALLAS, 1778): an evolutionary approach. Reprod. Fertil. Dev. 22, 448–458.
Ultrasonographic characterisation of prenatal development in European brown hares (Lepus europaeus PALLAS, 1778): an evolutionary approach.Crossref | GoogleScholarGoogle Scholar | 20047730PubMed |

Selwood, L. (2000). Marsupial egg and embryo coats. Cells Tissues Organs 166, 208–219.
Marsupial egg and embryo coats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ps1WrtA%3D%3D&md5=bfee11c1b8bfa2ce71cc03b313514ceaCAS | 10729728PubMed |

Strauss, F. (1957). Die Placenta des Feldhasen. Acta Anat. 30, 815–826.
Die Placenta des Feldhasen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG1c%2FitFSlsg%3D%3D&md5=2c69022d8d07ec1cf3668868b5fe7790CAS | 13478370PubMed |

Warner, S. M., Conlon, F. V., and Kane, M. T. (2003). Inositol transport in preimplantation rabbit embryos: effects of embryo stage, sodium, osmolality and metabolic inhibitors. Reproduction 125, 479–493.
Inositol transport in preimplantation rabbit embryos: effects of embryo stage, sodium, osmolality and metabolic inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOqt7k%3D&md5=88ffda63e3be227da3e3ce6488b22a6fCAS | 12683919PubMed |