Register      Login
Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
REVIEW

The marsupial pouch: implications for reproductive success and mammalian evolution

Melanie J. Edwards A and Janine E. Deakin A B
+ Author Affiliations
- Author Affiliations

A Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.

B Corresponding author. Email: janine.deakin@anu.edu.au

Australian Journal of Zoology 61(1) 41-47 https://doi.org/10.1071/ZO12088
Submitted: 3 September 2012  Accepted: 18 October 2012   Published: 7 November 2012

Abstract

Extant mammals are divided into sub- and infraclasses that are distinguished by their mode of reproduction. The monotremes lay eggs, the marsupials give birth to altricial young that typically develop in a pouch, and the eutherians have prolonged in utero development, resulting in well developed young at birth. The three groups exhibit what appears to be a nice progression of evolution towards the well developed newborn young of eutherian mammals. However, marsupials do not represent a step in the progression of producing well developed young, but maintain a reproductive strategy that has evolved to prosper in their specific niche. The production of undeveloped young with increased development in the pouch (or counterpart) provides specific advantages to those species living in diverse environments. The evolution of this reproductive strategy provides a clever solution to the uncertain and often adverse conditions encountered by many species, and the survival of the developing young in a pouch containing potentially harmful microorganisms is truly remarkable. In this review, we explore the unique features of the pouch, highlight the research questions that remain unanswered regarding this unique marsupial attribute and discuss the advantages of the marsupial reproductive strategy and the potential role of the pouch in mammalian diversification.


References

Ambatipudi, K., Joss, J., and Deane, E. (2007). A comparative proteomic analysis of skin secretions of the tammar wallaby (Macropus eugenii) and the wombat (Vombatus ursinus). Comparative Biochemistry and Physiology D: Genomics and Proteomics 2, 322–331.
A comparative proteomic analysis of skin secretions of the tammar wallaby (Macropus eugenii) and the wombat (Vombatus ursinus).Crossref | GoogleScholarGoogle Scholar |

Ambatipudi, K., Joss, J., Raftery, M., and Deane, E. (2008). A proteomic approach to analysis of antimicrobial activity in marsupial pouch secretions. Developmental and Comparative Immunology 32, 108–120.
A proteomic approach to analysis of antimicrobial activity in marsupial pouch secretions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlyksbjK&md5=ee9560ca8acc505d1ebd0b0bf7a2cd78CAS |

Basden, K., Cooper, D. W., and Deane, E. M. (1997). Development of the lymphoid tissues of the tammar wallaby Macropus eugenii. Reproduction, Fertility and Development 9, 243–254.
Development of the lymphoid tissues of the tammar wallaby Macropus eugenii.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szlt1WmsQ%3D%3D&md5=bb00d46fb1261e49a91aec4f8ec9d74fCAS |

Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., and Purvis, A. (2007). The delayed rise of present-day mammals. Nature 446, 507–512.
The delayed rise of present-day mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsV2itb0%3D&md5=69199ce3ab157cb94a9e723dfb686f21CAS |

Block, M. (1960). Wound healing in the new-born opossum (Didelphis virginianam). Nature 187, 340–341.
Wound healing in the new-born opossum (Didelphis virginianam).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF3c7itF2iug%3D%3D&md5=c0435d6164cecc1a834a7d35d8ff3f80CAS |

Bobek, G., and Deane, E. M. (2001). Possible antimicrobial compounds from the pouch of the koala, Phascolarctos cinereus. Letters in Peptide Science 8, 133–137.
Possible antimicrobial compounds from the pouch of the koala, Phascolarctos cinereus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltV2nsbg%3D&md5=8f02e51ca26c035165bea8fae7fabb1bCAS |

Case, T. J. (1978). Endothermy and parental care in terrestrial vertebrates. American Naturalist 112, 861–874.
Endothermy and parental care in terrestrial vertebrates.Crossref | GoogleScholarGoogle Scholar |

Charlick, J., Manessis, C., Stanley, N., Waring, H., and Cockson, A. (1981). Quantitative alterations of the aerobic bacterial flora of the pouch of Setonix brachyurus (quokka) during oestrus, anoestrus, pregnancy and lactating anoestrus (pouch young). The Australian Journal of Experimental Biology and Medical Science 59, 743–751.
Quantitative alterations of the aerobic bacterial flora of the pouch of Setonix brachyurus (quokka) during oestrus, anoestrus, pregnancy and lactating anoestrus (pouch young).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL387otFyktA%3D%3D&md5=130f5e453e442d8358f17d3595d88f27CAS |

Chhour, K., Hinds, L. A., Jacques, N. A., and Deane, E. M. (2010). An observational study of the microbiome of the maternal pouch and saliva of the tammar wallaby, Macropus eugenii, and of the gastrointestinal tract of the pouch young. Microbiology 156, 798–808.
An observational study of the microbiome of the maternal pouch and saliva of the tammar wallaby, Macropus eugenii, and of the gastrointestinal tract of the pouch young.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktFOksb8%3D&md5=042e364a1b9d7a896f379375a8216aadCAS |

Cockburn, A. (1989). Adaptive patterns in marsupial reproduction. Trends in Ecology & Evolution 4, 126–130.
Adaptive patterns in marsupial reproduction.Crossref | GoogleScholarGoogle Scholar |

Cooper, D. W., and Hope, R. M. (1989). Marsupial and monotreme phylogeny. Australian Journal of Zoology 37, 271–272.
Marsupial and monotreme phylogeny.Crossref | GoogleScholarGoogle Scholar |

Cooper, W. J., and Steppan, S. J. (2010). Developmental constraint on the evolution of marsupial forelimb morphology. Australian Journal of Zoology 58, 1–15.
Developmental constraint on the evolution of marsupial forelimb morphology.Crossref | GoogleScholarGoogle Scholar |

Deakin, J. E., and Cooper, D. W. (2004). Characterisation of and immunity to the aerobic bacteria found in the pouch of the brushtail possum Trichosurus vulpecula. Comparative Immunology, Microbiology and Infectious Diseases 27, 33–46.
Characterisation of and immunity to the aerobic bacteria found in the pouch of the brushtail possum Trichosurus vulpecula.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3srns1KltA%3D%3D&md5=bfbf7b754f6e7fd18634035532f8b463CAS |

Deane, E. M., and Cooper, D. W. (1988). Immunological development of pouch young marsupials. In ‘The Developing Marsupial: Models for Biomedical Research’. (Eds C. H. Tyndale-Biscoe and P. A. Janssens.) pp. 190–199. (Springer-Verlag: Berlin.)

Deane, E. M., Cooper, D. W., and Renfree, M. B. (1990). Immunoglobulin G levels in fetal and newborn tammar wallabies (Macropus eugenii). Reproduction, Fertility and Development 2, 369–375.
Immunoglobulin G levels in fetal and newborn tammar wallabies (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlt1er&md5=c413234b99e79ffa07014b86e923242aCAS |

Edwards, M. J., Hinds, L. A., Deane, E. M., and Deakin, J. E. (2011). Physical mapping of innate immune genes, mucins and lysozymes, and other non-mucin proteins in the tammar wallaby (Macropus eugenii). Cytogenetic and Genome Research 135, 118–125.
Physical mapping of innate immune genes, mucins and lysozymes, and other non-mucin proteins in the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlKkt7rF&md5=c65416c3c3d936520ac47ad5ad50352eCAS |

Edwards, M. J., Hinds, L. A., Deane, E. M., and Deakin, J. E. (2012). A review of complementary mechanisms which protect the developing marsupial pouch young. Developmental and Comparative Immunology 37, 213–220.
A review of complementary mechanisms which protect the developing marsupial pouch young.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xms12rsr0%3D&md5=8ce0b242f2a6fa36a4cf7b1530cdf9f3CAS |

Enders, R. K. (1937). Panniculus carnosus and formation of the pouch in didelphids. Journal of Morphology 61, 1–26.
Panniculus carnosus and formation of the pouch in didelphids.Crossref | GoogleScholarGoogle Scholar |

Gemmell, R. T., Veitch, C., and Nelson, J. (2002). Birth in marsupials. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 131, 621–630.
Birth in marsupials.Crossref | GoogleScholarGoogle Scholar |

Graves, J. A. M., Hope, R. M., and Cooper, D. W. (1989). True beasts from pouches and eggs. Australian Journal of Zoology 37, 143–146.
True beasts from pouches and eggs.Crossref | GoogleScholarGoogle Scholar |

Griffiths, M., and Slater, E. (1988). The significance of striated muscle in the mammary glands of marsupials. Journal of Anatomy 156, 141–156.
| 1:STN:280:DyaL1czjtVKjsg%3D%3D&md5=ea13b70f8cd4a9b350100682b1f6ad26CAS |

Hopson, J. A. (1973). Endothermy, small size, and the origin of mammalian reproduction. American Naturalist 107, 446–452.
Endothermy, small size, and the origin of mammalian reproduction.Crossref | GoogleScholarGoogle Scholar |

Hughes, R. L., and Hall, L. S. (1988). Structural adaptations of the newborn marsupial. In ‘The Developing Marsupial: Models for Biochemical Research’. (Eds C. H. Tyndale-Biscoe and P. A. Janssens.) pp. 8–27. (Springer-Verlag: Berlin.)

Hulbert, A. J. (1988). Metabolism and the development of endothermy. In ‘The Developing Marsupial: Models of Biomedical Research’. (Eds C. H. Tyndale-Biscoe and P. A. Janssens.) pp. 148–161. (Springer-Verlag: Berlin.)

Johnson, K. A. (1995). Order Notoryctemorphia. In ‘The Mammals of Australia’. (Ed. R. Strahan.) pp. 409–411. (Reed Books: Sydney.)

Joss, J. L., Molloy, M. P., Hinds, L., and Deane, E. (2009). A longitudinal study of the protein components of marsupial milk from birth to weaning in the tammar wallaby (Macropus eugenii). Developmental and Comparative Immunology 33, 152–161.
A longitudinal study of the protein components of marsupial milk from birth to weaning in the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWrsbnP&md5=cdff0d8b50b09b7efcfdfdfc63a82301CAS |

Kelly, E. M., and Sears, K. E. (2011). Limb specialization in living marsupial and eutherian mammals: constraints on mammalian limb evolution. Journal of Mammalogy 92, 1038–1049.
Limb specialization in living marsupial and eutherian mammals: constraints on mammalian limb evolution.Crossref | GoogleScholarGoogle Scholar |

Kirsch, J. A. W. (1977a). Biological aspects of the marsupial–placental dichotomy: a reply to Lillegraven. Evolution 31, 898–900.
Biological aspects of the marsupial–placental dichotomy: a reply to Lillegraven.Crossref | GoogleScholarGoogle Scholar |

Kirsch, J. A. W. (1977b). The six-percent solution: second thoughts on the adaptedness of the Marsupialia. American Scientist 65, 276–288.
| 1:STN:280:DyaE2s3hvF2rsg%3D%3D&md5=bde02138c0a6d243f74c46d3dc041e01CAS |

Kubota, K., Shimizu, T., Shibanai, S., Nagae, K., and Nagata, S. (1989). Histological properties and biological significance of pouch in red kangaroo (Macropus rufus). Anatomischer Anzeiger 168, 169–179.
| 1:STN:280:DyaL1M3is1CnsA%3D%3D&md5=5729989e31b4f95c5dc45e5d9298e941CAS |

Lee, A. K., and Cockburn, A. (1985). ‘Evolutionary Ecology of Marsupials.’ (Cambridge University Press: Cambridge.)

Lillegraven, J. A. (1975). Biological considerations of the marsupial–placental dichotomy. Evolution 29, 707–722.
Biological considerations of the marsupial–placental dichotomy.Crossref | GoogleScholarGoogle Scholar |

Lombardi, J. (1998). ‘Comparative Vertebrate Reproduction.’ (Kluwer Academic Publishers: Norwell, MA.)

Low, B. S. (1978). Environmental uncertainty and the parental strategies of marsupials and placentals. American Naturalist 112, 197–213.
Environmental uncertainty and the parental strategies of marsupials and placentals.Crossref | GoogleScholarGoogle Scholar |

MacFarlane, P. M., Frappell, P. B., and Mortola, J. P. (2002). Mechanics of the respiratory system in the newborn tammar wallaby. The Journal of Experimental Biology 205, 533–538.
| 1:STN:280:DC%2BD387mtFKitA%3D%3D&md5=2fcada13372ec34190cb387a661abd87CAS |

Morimoto, Y., and Saga, K. (1995). Proliferating cells in human eccrine and apocrine sweat glands. The Journal of Histochemistry and Cytochemistry 43, 1217–1221.
Proliferating cells in human eccrine and apocrine sweat glands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpsFSqsLw%3D&md5=bdc1e364590da324138c765fa9a7ef98CAS |

Mortola, J. P., Frappell, P. B., and Woolley, P. A. (1999). Breathing through skin in a newborn mammal. Nature 397, 660.
Breathing through skin in a newborn mammal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1equ74%3D&md5=2c0a071e396d799d2dd45965fcd13667CAS |

Nicholas, K. R. (1988). Control of milk protein synthesis in the marsupial Macropus eugenii: a model system to study prolactin-dependent development. In ‘The Developing Marsupial Models for Biomedical Research’. (Eds C. H. Tyndale-Biscoe and P. A. Janssens.) pp. 68–85. (Springer-Verlag: Berlin.)

Old, J. M., and Deane, E. M. (1998). The effect of oestrus and the presence of pouch young on aerobic bacteria isolated from the pouch of the tammar wallaby, Macropus eugenii. Comparative Immunology, Microbiology and Infectious Diseases 21, 237–245.
The effect of oestrus and the presence of pouch young on aerobic bacteria isolated from the pouch of the tammar wallaby, Macropus eugenii.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1cvkvVCrsw%3D%3D&md5=ff9e85538c3079d4ef25a59e1bf8e771CAS |

Old, J. M., and Deane, E. M. (2003). The detection of mature T- and B-cells during development of the lymphoid tissues of the tammar wallaby (Macropus eugenii). Journal of Anatomy 203, 123–131.
The detection of mature T- and B-cells during development of the lymphoid tissues of the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3szlvFCltA%3D%3D&md5=08c35638c58d259b7990d8d021d069feCAS |

Old, J. M., Irving, M., and Deane, E. M. (2005). Histology of the pouch epithelium and the mammary glands during chemically induced oestrus in the brushtail possum (Trichosurus vulpecula). Journal of Anatomy 207, 97–102.
Histology of the pouch epithelium and the mammary glands during chemically induced oestrus in the brushtail possum (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar |

Parker, P. (1977). An ecological comparison of marsupial and placental patterns of reproduction. In ‘The Biology of Marsupials’. (Eds B. Stonehouse and D. Gilmore.) pp. 273–286. (University Park Press: Baltimore, MD.)

Pond, C. M. (1984). Physiological and ecological importance of energy storage in the evolution of lactation: evidence for a common pattern of anatomical organization of adipose tissue in mammals. Symposium of the Zoological Society of London 51, 1–32.

Pope, C. H. (1956). ‘The Reptile World: A Natural History of the Snakes, Lizards, Turtles and Crocodilians.’ (Alfred A. Knoff: New York.)

Russell, E. M. (1982a). Parental investment and desertion of young in marsupials. American Naturalist 119, 744–748.
Parental investment and desertion of young in marsupials.Crossref | GoogleScholarGoogle Scholar |

Russell, E. M. (1982b). Patterns of parental care and parental investment in marsupials. Biological Reviews of the Cambridge Philosophical Society 57, 423–486.
Patterns of parental care and parental investment in marsupials.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2FkvFCisw%3D%3D&md5=acd8904d47d4d5efeb9bd0874b2925bdCAS |

Sharman, G. B., and Calaby, J. H. (1964). Reproductive behaviour in the red kangaroo, Megaleia rufa in captivity. CSIRO Wildlife Research 9, 58–85.
Reproductive behaviour in the red kangaroo, Megaleia rufa in captivity.Crossref | GoogleScholarGoogle Scholar |

Shaw, G., Renfree, M. B., and Short, R. V. (1989). Primary genetic control of sexual differentiation in marsupials. Australian Journal of Zoology 37, 443–450.
Primary genetic control of sexual differentiation in marsupials.Crossref | GoogleScholarGoogle Scholar |

Smith, K. K. (2001). Early development of the neural plate, neural crest and facial region of marsupials. Journal of Anatomy 199, 121–131.
Early development of the neural plate, neural crest and facial region of marsupials.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotVGktA%3D%3D&md5=88e94fc59bdb971ea473d64aa726500eCAS |

Starck, J. M., and Ricklefs, R. E. (1998). Patterns of development: the altricial–precocial spectrum. In ‘Avian Growth and Development: Evolution within the Altricial–Precocial Spectrum’. (Eds J. M. Starck and R. E. Ricklefs.) pp. 3–30. (Oxford University Press: Oxford.)

Trevathan, W. R. (1987). ‘Human Birth: An Evolutionary Perspective.’ (Transaction Publishers: New Brunswick, NJ.)

Tyndale-Biscoe, C. H., and Renfree, M. B. (1987). ‘Reproductive Physiology of Marsupials.’ (Cambridge University Press: Cambridge.)

Tyndale-Biscoe, H. (2005). ‘Life of Marsupials.’ (CSIRO Publishing: Melbourne.)

Wang, J., Wong, E. S. W., Whitley, J. C., Li, J., Stringer, J. M., Short, K. R., Renfree, M. B., Belov, K., and Cocks, B. G. (2011). Ancient antimicrobial peptides kill antibiotic-resistant pathogens: Australian mammals provide new options. PLoS ONE 6, e24030.
Ancient antimicrobial peptides kill antibiotic-resistant pathogens: Australian mammals provide new options.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Wrt77N&md5=f5a41cf0e9dae0c6679691bbe0a0e429CAS |

Watson, C. M., and Cooper, D. W. (1995). Sex differentiation differs down under. Trends in Genetics 11, 385.
Sex differentiation differs down under.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXoslSqsb4%3D&md5=f5aecdce057499495295bdffbb98cc18CAS |

Watson, C. M., Johnston, P. G., Rodger, K. A., McKenzie, L. M., Waugh O’Neill, R. J., and Cooper, D. W. (1997). SRY and karyotypic status of one abnormal and two intersexual marsupials. Reproduction, Fertility and Development 9, 233–241.
SRY and karyotypic status of one abnormal and two intersexual marsupials.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVGgt7s%3D&md5=20ce92245bff9ea53ef1fd5b0db72485CAS |

Yadav, M., Stanley, N. F., and Waring, H. (1972). Microbial flora of gut of pouch-young and pouch of a marsupial Setonix brachyurus. Journal of General Microbiology 70, 437–442.
Microbial flora of gut of pouch-young and pouch of a marsupial Setonix brachyurus.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE383htVaktA%3D%3D&md5=8e5a46a34891c59ecc60ddc10eec601dCAS |

Young, L., Basden, K., Cooper, D. W., and Deane, E. M. (1997). Cellular components of the milk of the tammar wallaby (Macropus eugenii). Australian Journal of Zoology 45, 423–433.
Cellular components of the milk of the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar |