Skip to main content
Log in

Sexual differentiation of the urogenital system of the fetal and neonatal tammar wallaby, Macropus eugenii

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

In male tammar wallabies, the scrotum is the first organ to become sexually differentiated, 4–5 days before birth (day 22 of gestation). This is followed by enlargement of the gubernaculum and processus vaginalis one day before birth. However the indifferent gonad does not show any signs of testicular cord formation or androgen production until later, at around the time of birth; this is more pronounced at 2 days post-partum (p.p.), when the testis takes on a characteristic rounded appearance. Primordial germ cells proliferate throughout the testis at this time, although the testis does not become significantly heavier than the ovary until around 80 days p.p.. In females, the appearance of the mammary glands is the first sign of sexual differentiation 4–5 days before birth. The indifferent gonad first shows signs of developing an ovarian cortex and medulla 7 days after birth. The migrating germ cells are confined to the cortex, and first start to enter meiosis about 25 days after birth. The Wolffian (mesonephric) ducts are patent to the urogenital sinus in fetuses at day 21 of gestation. In the female they have started to regress by 10 days p.p. and only rudiments remain by day 25 p.p.. The Müllerian (paramesonephric) ducts develop adjacent to the cranial pole of the mesonephros at about day 25 of gestation and grow caudally to meet the urogenital sinus between days 2 and 7 p.p.. The Müllerian duct of the female develops a prominent ostium abdominale by day 9 p.p., but this structure has completely regressed in males by day 13 p.p.. The testis and ovary both migrate caudally, together with the adjacent mesonephros, at about day 10 p.p.. The ovaries remain around the level of lumbar vertebra 4 after about day 7 p.p., while the testes continue to descend. The testes enter the internal inguinal ring at about day 25 p.p., about the time that prostatic buds first appear in the urogenital sinus, and are in the inguinal canal from days 25 to 36 p.p.. They enter the scrotum at around day 36 p.p., and testicular descent is complete by days 65–72 p.p.. Melanin develops in the tunica vaginalis 72 days after birth. The overall development of the urogenital system in this marsupial is similar to that of eutherians but the sequence of events differs, with some aspects of genital differentiation preceding gonadal differentiation, apparently because they are directly controlled by X-linked genes, rather than indirectly controlled by gonadal steroids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alcorn GT (1975) Development of the ovary and urogenital ducts in the tammar wallaby, Macropus eugenii (Desmarest, 1817). PhD thesis, Macquarie University, Sydney NSW

    Google Scholar 

  • Alcorn GT, Robinson ES (1983) Germ cell development in female pouch young of the tammar wallaby (Macropus eugenii). J Reprod Fertil 67: 319–325

    Google Scholar 

  • Baker PJ, Moore HDM, Penfold LM, Burgess AMC, Mittwoch U (1990) Gonadal sex differentiation in the neonatal marsupial, Monodelphis domestica. Development 109: 699–704

    Google Scholar 

  • Baxter JS (1935) Development of the female genital tract in the American opossum. Carnegie Contribut Embryol 25: 15–35

    Google Scholar 

  • Bolliger A (1944) An experiment on the complete transformation of the scrotum into a marsupial pouch in Trichosurus vulpecula. Med J Aust 2: 56–58

    Google Scholar 

  • Bolton PM (1983) Gonadal development in Antechinus stuartii (Marsupialia: Dasyuridae). MSc thesis, Macquarie University, Sydney, NSW

    Google Scholar 

  • Bresslau E (1912) Die Entwickelung des Mammarapparates der Monotremen Marsupialier und einiger Placentalier. In: Semon R (ed) Zoologische Forschungreisen in Australien, vol 4. Gustav Fischer, Jena, pp 653–874

    Google Scholar 

  • Buchanan G, Fraser EA (1918) The development of the urogenital system in the Marsupialia, with special reference to Trichosurus vulpecula. J Anat 53: 35–95

    Google Scholar 

  • Burns RK (1939a) The differentiation of sex in the opossum (Didelphys virginiana) and its modification by the male hormone testosterone propionate. J Morphol 65: 79–199

    Google Scholar 

  • Burns RK (1939b) Sex differentiation during the early pouch stages of the opossum (Didelphys virginiana) and a comparison of the anatomical changes induced by male and female sex hormones. J Morphol 65: 497–547

    Google Scholar 

  • Burns RK (1939c) Affect of testosterone propionate on sex differentiation in pouch young of opossum. Proc Soc Exp Biol Med 41: 60–62

    Google Scholar 

  • Burns RK (1961) Role of hormones in the differentiation of sex. In: Young WC (ed) Sex and internal secretions, vol 1. Williams and Wilkins, Baltimore, pp 76–158

    Google Scholar 

  • Butler CM, Shaw GS, Renfree MB (1995) Delayed virilization of the reproductive system of the male tammar wallaby. J Reprod Fertil Abstr Ser 15: 52

    Google Scholar 

  • Byskov AG (1986) Differentiation of mammalian embryonic gonad. Physiol Rev 66: 71–117

    Google Scholar 

  • Chase EB (1939) The reproductive system of the male opossum, Didelphis virginiana Kerr and its experimental modification. J Morphol 65: 215–240

    Google Scholar 

  • Cooper DW (1993) The evolution of sex determination, sex chromosome dimorphism, and X-inactivation in therian mammals: a comparison of metatherians (marsupials) and eutherians (“placentals”). In: Reed KC, Marshall Graves JA (eds) Sex chromosomes and sex-determining genes. Harwood, Chur, Switzerland, pp 183–200

    Google Scholar 

  • Cooper DW, Johnston PG, Vandeberg JL, Robinson ES (1990) X-chromosome inactivation in marsupials. Aust J Zool 37: 411–417

    Google Scholar 

  • Eusterschulte B, Reisert I, Pilgrim Ch (1992) Absence of sex differences in size of the genital ducts of the rat prior to embryonic day 15.5–16.0. Tissue and Cell 24: 483–489

    Google Scholar 

  • Fadem BH, Harder JD (1992) Evidence for high levels of androgen in peripheral plasma during postnatal development in a marsupial: the gray short-tailed opossum (Monodelphis domestica). Biol Reprod 46: 105–108

    Google Scholar 

  • Fadem BH, Tesoriero JV (1986) Inhibition of testicular development and feminization of the male genitalia by neonatal estrogen treatment in a marsupial. Biol Reprod 34: 771–776

    Google Scholar 

  • Fadem BH, Tesoriero JV, Whang M (1992) Early differentiation of the gonads in the gray short-tailed opossum (Monodelphis domestica). Biol Neonate 61: 131–136

    Google Scholar 

  • Fletcher TP, Jetton AE, Renfree MB (1988) Influence of progesterone and oestradiol 17β on blastocysts of the tammar wallaby during seasonal diapause. J Reprod Fertil 83: 193–200

    Google Scholar 

  • Foster JW, Brennan FE, Hampikian GK, Goodfellow PN, Sinclair AH, Lovell-Badge R, Selwood L, Renfree MB, Cooper DW, Marshal Graves, JA (1992) Evolution of sex determination and the Y chromosome: SRY-related sequences in marsupials. Nature 359: 531–533

    Google Scholar 

  • Fraser EA (1919) The development of the urogenital system in the Marsupialia, with special reference to Trichosurus vulpecula. II. J Anat 53: 97–129

    Google Scholar 

  • George FW, Hodgins MB, Wilson JD (1985) The synthesis and metabolism of gonadal steroids in pouch young of the opossum, Didelphis virginiana. Endocrinology 116: 1145–1150

    Google Scholar 

  • Goh DW, Momose Y, Middlesworth W, Hutson JM (1993) The relationship among calcitonin gene-related peptide, androgens and gubernacular development in 3 animal models of cryptorchidism. J Urol 150: 574–576

    Google Scholar 

  • Griffiths AL, Middlesworth W, Goh DW, Hutson JM (1993a) Exogenous calcitonin gene-related peptide causes gubernacular development in neonatal (Tfm) mice with complete androgen resistance. J Pediatr Surg 28: 1028–1030

    Google Scholar 

  • Griffiths AL, Renfree MB, Shaw G, Watts LM Hutson JM (1993b) The tammar wallaby (Macmpus eugenii) and the SpragueDawley rat: comparative anatomy and physiology of inguinoscrotal testicular descent. J Anat 183: 441–450

    Google Scholar 

  • Huhtaniemi IT, Warren DW, Catl KJ (1984) Functional maturation of rat testis Leydig cells. Ann NY Acad Sci 438: 283–303

    Google Scholar 

  • Hutson JM, Shaw G, O W-S, Short RV, Renfree MB (1988) Müllerian inhibitory substance production and testicular migration and descent in the pouch young of a marsupial. Development 104: 549–556

    Google Scholar 

  • Josso N (1979) Development and descent of the fetal testis. In: Bierch JR, Gairola A (eds) Cryptorchidism. Academic Press, New York London, pp 7–20

    Google Scholar 

  • Jost A (1970) Hormonal factors in the sex differentiation of the mammalian foetus. Philos Trans R Soc Lond Biol 259: 119–130

    Google Scholar 

  • Jost A (1972) Donneés préliminaires sur les stades initiaux de la différenciation du testicle chez le rat. Arch Anat Microsc Morphol Exp 61: 415–438

    Google Scholar 

  • Krause WJ, Cutts JH, Leeson CR (1979a) Morphological observations on the mesonephros in the postnatal opossum Didelphis virginiana. J Anat 129: 377–397

    Google Scholar 

  • Krause WJ, Cutts JH, Leeson CR (1979b) Morphological observations on the metanephros in the postnatal opossum Didelphis virginiana. J Anat 129: 459–77

    Google Scholar 

  • Lister JJ, Fletcher JJ (1881) On the condition of the median portion of the vaginal apparatus in the Macropodidae. Proc Zool Soc London 1881: 976–96

    Google Scholar 

  • Maitland P, Ullmann SL (1993) Gonadal development in the opossum, Monodelphis domestica: the Rete ovarii does not contribute to the steroidogenic tissues. J Anat 183: 43–56

    Google Scholar 

  • Magre S, Jost A (1980) The initial phases of testicular organogenesis in the rat. An electron microscope study. Arch Anat Microsc Morphol Exp 69: 297–318

    Google Scholar 

  • Mittwoch U (1986) Males, females and hermaphrodites. Ann Hum Genet 50: 103–121

    Google Scholar 

  • Mittwoch U, Burgess AMC (1991) How do you get sex? J Endocrinol 128: 329–331

    Google Scholar 

  • McCrady E (1938) The embryology of the opossum. Am Anat Mem 16: 1–233

    Google Scholar 

  • Moore CR (1939) Modification of sexual development in the opossum by sex hormones. Proc Soc Exp Biol Med 40: 544–546

    Google Scholar 

  • Moore HDM, Thurstan SM (1990) Sexual differentiation in the grey short-tailed opossum, Monodelphis domestica, and the effect of oestradiol benzoate on development in the male. J Zool 221: 639–658

    Google Scholar 

  • Morgan CF (1943) The normal development of the ovary of the opossum from birth to maturity and its reactions to sex hormones. J Morphol 72: 27–85

    Google Scholar 

  • National Health and Medical Research Council of Australia (1990) Australian code of practice for the care and use of animals for scientific purposes. Australian Government Printer, Canberra Australia

    Google Scholar 

  • Nurse SC, Renfree MB (1994) Pubertal development of the pouch and teats in a marsupial. J Reprod Fertil 101: 279–285

    Google Scholar 

  • O W-S, Short RV, Renfree MB, Shaw G (1988) Primary genetic control of sexual differentiation in a mammal. Nature 331: 716–717

    Google Scholar 

  • Poole WE, Simms NG, Wood JT, Lubulwa M (1991) Tables for age determination of the Kangaroo Island wallaby (tammar), Macropus eugenii from body measurements. CSIRO Technical Memorandum 32, CSIRO Division of Wildlife and Ecology, Canberra, Australia

    Google Scholar 

  • Renfree MB (1972) Embryo-maternal relationships in the tammar wallaby Macropus eugenii. PhD thesis, Australian National University, Canberra

    Google Scholar 

  • Renfree MB (1973) The composition of fetal fluids of the marsupial Macropus eugenii. Dev Biol 33: 62–79

    CAS  PubMed  Google Scholar 

  • Renfree MB (1992a) The role of genes and hormones in marsupial sexual differentiation. J Zool 226: 165–173

    Google Scholar 

  • Renfree MB (1992b) Ontogeny, genetic control and phylogeny of female reproduction in monotreme and therian mammals. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammal phylogeny. Princeton University Press, Princeton NJ, pp 4–20

    Google Scholar 

  • Renfree MB (1994) Sexual dimorphisms in the gonads and reproductive tract of marsupial mammals. In: Balaban E, Short RV (eds) The differences between the sexes. Cambridge University Press, Cambridge, 213–230

    Google Scholar 

  • Renfree MB, Short RV (1988) Sex determination in marsupials: evidence for a marsupial-eutherian dichotomy. Philos Trans R Soc Lond Biol 322: 41–54

    Google Scholar 

  • Renfree MB, Shaw G, Short RV (1987) Sexual differentiation in marsupials. In: Haseltine FP, McClure ME, Goldberg EH (eds) NIH workshop on genetic markers of sex differentiation. Plenum Press, New York, pp 27–41

    Google Scholar 

  • Renfree MB, Fletcher TP, Blanden DR, Lewis PR, Shaw G, Gordon K, Short RV, Parer-Cook E, Parer D (1989) Physiological and behavioural events around the time of birth in macropodid marsupials. In: Jarman P, Hume ID, Grigg G (eds) Kangaroos, wallabies and rat kangaroos. Surrey Beatty, Sydney, pp 323–337

    Google Scholar 

  • Renfree MB, Robinson ES, Short RV, VandeBerg JL (1990) Mammary glands in male marsupials 1. Primordia in neonatal opossums, Didelphis virginiana and Monodelphis domestica. Development 110: 385–390

    Google Scholar 

  • Renfree MB, Wilson JD, Short RV, Shaw G, George FW (1992a) Steroid hormone content of the gonads of the tammar wallaby during sexual differentiation. Biol Reprod 47: 644–647

    Google Scholar 

  • Renfree MB, Shaw G, Clark J, Short RV, Kerr JB (1992b) Morphology of the developing urogenital system of the tammar wallaby, Macropus eugenii. J Reprod Fertil Abstr Ser 9: 134

    Google Scholar 

  • Renfree MB, Harry JL, Shaw G (1995) The marsupial male: a role model for sexual development. Philos Trans R Soc Lond Biol 350: 243–251

    Google Scholar 

  • Robinson ES, Renfree MB, Short RV, VandeBerg JL (1991) Mammary glands in male marsupials 2. Development and regression of mammary primordia in Monodelphis domestica and Didelphis virginiana. Reprod Fertil Dev 3: 295–301

    Google Scholar 

  • Samarakkody UK, Hutson JM (1992) Intrascrotal CGRP 8–37 causes a delay in testicular descent in mice. J Pediatr Surg 27: 874–875

    Google Scholar 

  • Sharman GB, Hughes RL, Cooper DW (1990) The chromosomal basis of sex differentiation in marsupials. Aust J Zool 37: 451–466

    Google Scholar 

  • Shaw G, Renfree MB, Short RV, O W-S (1988) Experimental manipulation of sexual differentiation in wallaby pouch young with exogenous steroids. Development 104: 689–701

    Google Scholar 

  • Shaw G, Renfree MB, Short RV (1990) Primary genetic control of sexual differentiation in marsupials. Aust J Zool 37: 443–50

    Google Scholar 

  • Shaw G, Harry JL, Whitworth DJ, Renfree MB (1995) Sexual determination and differentiation in the marsupial. In: Saunders NA, Hinds LA (eds) Recent advances in marsupial biology. University of New South Wales Press (in press)

  • Short RV, Renfree MB, Shaw G (1988) Sexual development in marsupial pouch young. In: Tyndale-Biscoe CH, Janssens PA (eds) The developing marsupial, models for biomedical research. Springer, Berlin Heidelberg New York, pp 200–210

    Google Scholar 

  • Tyndale-Biscoe CH, Renfree MB (1987) Reproductive physiology of marsupials Cambridge University Press, Cambridge

    Google Scholar 

  • Ullmann SL (1981) Sexual differentiation of the gonads in bandicoots (Permelidae: Marsupialia). In: Byskov AG, Peters H (eds) Proc Vth Workshop on the development and function of the reproductive organs. Int Congr Ser 559, Excerpta Medica, Amsterdam, pp 41–50

    Google Scholar 

  • Ullmann SL (1984) Early differentiation of the testis in the native cat, Dasyurus viverrinus (Marsupialia). J Anat 138: 675–688

    Google Scholar 

  • Ullmann SL (1989) Ovary development in bandicoots: sexual differentiation to follicle formation J Anat 165: 45–60

    Google Scholar 

  • Ullmann SL (1993) Differentiation of the gonads and initiation of the mammary gland and scrotum development in the brushtail possum Trichosurus vulpecula (Marsupialia). Anat Embryol 187: 475–484

    Google Scholar 

  • Warren DW, Haltmeyer GC, Eik-Nes KB (1973) Testosterone in the fetal rat testis. Biol Reprod 8: 560–565

    Google Scholar 

  • Wilkes GE (1984) The development of structure and function of the kidney in the tammar wallaby, Macropus eugenii. PhD thesis, Australian National University, Canberra

    Google Scholar 

  • Wilkes GE, Janssens PA (1988) The development of renal function. In: Tyndale-Biscoe CH, Janssens PA (eds) The developing marsupial. Models for biomedical research. Springer, Berlin Heidelberg New York, pp 176–189

    Google Scholar 

  • Williams SC (1990) Control of puberty in the female tammar wallaby. PhD Thesis, Monash University, Victoria

    Google Scholar 

  • Yoshinaga K, Hess DL, Hendrickx AG, Zamboni L (1988) The development of the sexually indifferent gonad in the prosimian, Galago crassicaudatus crassicaudatus. Am J Anat 181: 89–105

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Renfree, M.B., O, WS., Short, R.V. et al. Sexual differentiation of the urogenital system of the fetal and neonatal tammar wallaby, Macropus eugenii . Anat Embryol 194, 111–134 (1996). https://doi.org/10.1007/BF00195006

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00195006

Key words

Navigation