Society for Reproductive Biology Founders’ Lecture 2006. Life in the pouch: womb with a view
Marilyn B. RenfreeDepartment of Zoology, The University of Melbourne, Vic. 3010, Australia. Email: m.renfree@unimelb.edu.au
Reproduction, Fertility and Development 18(7) 721-734 https://doi.org/10.1071/RD06072
Submitted: 28 June 2006 Accepted: 11 July 2006 Published: 18 August 2006
Abstract
Marsupials give birth to an undeveloped altricial young after a relatively short gestation period, but have a long and sophisticated lactation with the young usually developing in a pouch. Their viviparous mode of reproduction trades placentation for lactation, exchanging the umbilical cord for the teat. The special adaptations that marsupials have developed provide us with unique insights into the evolution of all mammalian reproduction. Marsupials hold many mammalian reproductive ‘records’, for example they have the shortest known gestation but the longest embryonic diapause, the smallest neonate but the longest sperm. They have contributed to our knowledge of many mammalian reproductive events including embryonic diapause and development, birth behaviour, sex determination, sexual differentiation, lactation and seasonal breeding. Because marsupials have been genetically isolated from eutherian mammals for over 125 million years, sequencing of the genome of two marsupial species has made comparative genomic biology an exciting and important new area of investigation. This review will show how the study of marsupials has widened our understanding of mammalian reproduction and development, highlighting some mechanisms that are so fundamental that they are shared by all today’s marsupial and eutherian mammals.
Acknowledgments
I owe a special debt to my close colleagues Geoff Shaw, Andrew Pask and my husband Roger Short as well as to my collaborators past and present: Hugh Tyndale-Biscoe, Jean Wilson, Richard Behringer, Anne McLaren, Jenny Graves and Fumi Ishino. Much of this work has been aided and abetted by my many capable post-doctoral fellows and graduate students who have joined me in the excitement of discovery of all things marsupial.
Arlt, W. , Walker, E. A. , Draper, N. , Ivison, H. E. , and Ride, J. P. , et al. (2004). Congenital adrenal hyperplasia caused by mutant P450 oxidoreductase and human androgen synthesis: analytical study. Lancet 363, 2128–2135.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gordon, K. , Fletcher, T. P. , and Renfree, M. B. (1988). Reactivation of the quiescent corpus luteum and diapausing embryo after temporary removal of the sucking stimulus in the tammar wallaby (Macropus eugenii). J. Reprod. Fertil. 83, 401–406.
| PubMed |
Griffiths, M. , Elliot, M. A. , and Leckie, R. M. C. (1972). The mammary glands of the red kangaroo, with observations on the fatty acid components of the milk triglycerides. J. Zool. 166, 265–275.
Jacobs, P. A. , and Strong, J. A. (1959). A case of human intersexuality having a possible XXY sex-determining mechanism. Nature 183, 302–303.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
New, D. A. T. , and Mizell, M. (1972). Opossum fetuses grown in culture. Science 175, 533–536.
| PubMed |
Nicholas, K. , Simpson, K. , Wilson, M. , Trott, J. , and Shaw, D. (1997). The tammar wallaby: a model to study putative autocrine-induced changes in milk composition. J. Mammary Gland Biol. Neoplasia 2, 299–310.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Renfree, M. B. , Meier, P. , Teng, C. , and Battaglia, F. C. (1981). Relationship between amino acid intake and accretion in a marsupial, Macropus eugenii: I. Total amino acid composition of the milk throughout pouch life. Biol. Neonate 40, 29–37.
| PubMed |
Renfree, M. B. , Wilson, D. , Short, R. V. , Shaw, G. , and George, F. W. (1992). Steroid hormone content of the gonads of the tammar wallaby during sexual differentiation. Biol. Reprod. 47, 644–647.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wakefield, M. J. , and Graves, J. A. M. (2003a). The kangaroo genome – Leaps and bounds in comparative genetics. EMBO Rep. 4, 143–147.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Whitworth, D. J. (1998). XX germ cells: the difference between an ovary and a testis. Trends Endocrinol. Metab. 9, 2–6.
| Crossref | GoogleScholarGoogle Scholar |
Whitworth, D. J. , Shaw, G. , and Renfree, M. B. (1996). Gonadal sex reversal of the developing marsupial ovary in vivo and in vitro. Development 122, 4057–4063.
| PubMed |
Wilson, J. D. , Shaw, G. , Leihy, M. L. , and Renfree, M. B. (2002a). The marsupial model for male phenotypic development. Trends Endocrinol. Metab. 13, 78–83.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wilson, J. D. , Leihy, M. W. , Shaw, G. , and Renfree, M. B. (2002b). Androgen physiology: unsolved problems at the millennium. Mol. Cell. Endocrinol. 198, 1–5.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wilson, J. D. , Auchus, R. J. , Leihy, M. W. , Guryev, O. L. , Estabrook, R. W. , Osborn, S. M. , Shaw, G. , and Renfree, M. B. (2003a). 5α-Androstane-3α,17β-diol is formed in tammar wallaby pouch young testes by a pathway involving 5α-pregnane-3α,17α-diol-20-one as a key intermediate. Endocrinology 144, 575–580.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wilson, J. D. , Leihy, M. W. , Shaw, G. , and Renfree, M. B. (2003b). Unsolved problems in male physiology: studies in a marsupial. Mol. Cell. Endocrinol. 211, 33–36.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Woodburne, M. O. , Rich, T. H. , and Springer, M. S. (2003). The evolution of tribospheny and the antiquity of mammalian clades. Mol. Phylogenet. Evol. 28, 360–385.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Xu, K. P. , Yadav, B. R. , King, W. A. , and Betteridge, K. J. (1991). Sex-related differences in developmental rates of bovine embryos produced and cultured in vitro. Mol. Reprod. Dev. 31, 249–252.
| Crossref | GoogleScholarGoogle Scholar |
Yousef, A. , and Selwood, L. (1993). Embryonic development in culture of the marsupials Antechinus stuartii (Macleay) and Sminthopsis macroura (Spencer) during preimplantation stages. Reprod. Fertil. Dev. 5, 445–458.
| Crossref | GoogleScholarGoogle Scholar | PubMed |