Measurement of the heat output from animals had its beginnings just over two hundred years ago. Adair Crawford in Glasgow measured the rise in temperature of a water jacket surrounding an animal chamber and, at about the same time, Lavoisier in Paris measured the heat output from a guinea-pig by recording the quantity of ice melted inside an insulated chamber which contained the ice and the animal. There is some doubt as to whether Crawford or Lavoisier made the first of these measurements (Mendelsohn, 1964; Blaxter, 1978). From the earlier work by Boyle, Hooke, Mayow and Priestley it was known that ‘pure air’ was necessary to support both animal life and the flame of a candle, and it was believed that both the animal and the candle ‘phlogisticated’ the air, thus gradually rendering it unfit for the continuing support of either. Both Crawford and Lavoisier compared the amount of heat given off by their animals with that given off by a lighted candle. Crawford believed that both animal heat and the heat produced by ‘combustible bodies’ was evolved from the air as phlogiston was formed but it was Lavoisier who made the breakthrough by recognising that the vital process involved was not the production of phlogiston, but the consumption of a new element which he named ‘oxygene’. The heat from living animals, like that from the burning candle, was evolved during the oxidation of carbon and the formation of carbon dioxide gas.

Marsupials give birth to small altricial young after a gestation period which lasts only 12–38 days (Table 2.2). The young then spends a much longer period within a pouch or nest nurtured by milk while it completes its growth and development to the stage of independence at weaning. In recent years there has been much written about the relative merits of marsupial reproduction compared to eutherian reproduction (Lillegraven 1969; 1975; 1979; Sharman, 1970; Cox, 1977; Kirsch, 19776; Renfree, 1981b; Padykula & Taylor, 1982). We will enter this debate in Chapter 10 but here we attempt to present a straightforward account of pregnancy and parturition in marsupials uncluttered, so far as possible, by preconceived notions of evolutionary relationships. The process from ovulation to parturition in marsupials can be divided into 10 fairly discrete stages, which are described below.

Sperm transport and fertilisation

Development of the spermatozoa and their maturation in the epididymis have been discussed in Chapter 4 and the varieties of courtship and copulatory behaviour in the several orders of marsupials was considered in Chapter 2. The fate of the spermatozoa after their deposition in the female genital tract and the process of fertilisation itself are less well known. There is a number of isolated observations on different aspects of the phenomena in many species but there are detailed, timed observations on only three species, Didelphis virginiana (Rodger & Bedford, 1982a,b), Macropus eugenii (Tyndale-Biscoe & Rodger, 1978) and Antechinus stuartii (Selwood, 1982b) (Fig. 7.1).

The unusual nature of the anatomy of the female marsupial was first recognised by Tyson (1698), when he described the paired vascular ‘cornuauteri’ of Didelphis virginiana, each leading into a vaginal cul de sac and then to separate lateral vaginae. The paired uteri are invariably separate and open by separate cervices (Fig. 5.1) unlike in many species of Eutheria, which have a single chambered uterus and a single cervix. The lateral vaginae open posteriorly into a urogenital sinus, which also receives the urethra.

Anatomy of the urogenital tract

The oviduct

Study of the oviduct in marsupials has been neglected, possibly because the eggs pass through it so rapidly. Nevertheless, as in other mammals, it is a complex structure with a transport and secretory function. The oviducts vary considerably between species in length and in the degree of convolution but the transport of sperm and eggs must involve muscular contractions. The musculature consists of inner circular and outer longitudinal layers which allow peristaltic movement (Hartman, 1924).

The mucosal lining of the mammalian oviduct consists of an intricately folded, simple ciliated columnar epithelium which is interspersed with mucus-secreting cells (Nalbandov, 1969). A similar arrangement of cells occurs in the few marsupials examined (Hughes, 1974; Arnold & Shorey, 1985; Armati-Gulson & Lowe, 1985; Figs 4.22 and 5.2). Four regions of the mammalian oviduct can be distinguished according to the structure of the epithelium (Nilsson & Reinius, 1969), and the suggested classification of these authors is largely followed here.

The pre-ampulla includes both the fimbria and the infundibulum which pass into the ampulla, where fertilisation occurs in most mammals.

Sex chromosomes

The chromosome number and morphology is known for 112 species of marsupials representing all families (see Sharman, 1973a; Hayman & Martin, 1974; Hayman & Rofe, 1977; Hsu & Benirschke, 1977). While the total DNA content of marsupial nuclei is approximately the same as those of eutherian species (Hayman & Martin, 1974), it is contained within fewer, larger chromosomes (Sharman, 1973a). The total chromosome number ranges from 2n = 10 in Wallabia bicolor to 2n = 32 in Aepyprymnus rufescens, but the distribution is bimodal around 2n = 14 and 2n = 22 (Fig. 3.1). There is lack of agreement as to which is the primitive number as species with both the modal numbers occur in South America and Australasia but there is not much doubt that 2n = 14 is the primitive karyotype for the Australian radiation from South American ancestors (Sharman, 1982). Whatever the origin may be, the large size and small number has meant that individual chromosomes, including the sex chromosomes, can usually readily be identified.

With the exception of four species, all known marsupials possess the sex chromosome pattern XY male:XX female as found in the great majority of eutherian mammals. The four exceptions have either extra X or extra Y chromosomes but their respective conditions have probably been derived from an XY:XX system by fusion of a sex chromosome with an autosome. In the macropodids Potorous tridactylus and Wallabia bicolor and in the bandicoot Macrotis lagotis the X chromosomes are large and metacentric and there are two Y chromosomes.

All discussions about the origin and evolution of mammalian reproduction are constrained by the time frame of the fossil record and rely to a considerable extent on comparisons between the modes of reproduction in living representatives of the Prototheria (monotremes), Metatheria (marsupials) and Eutheria (placentals). Such comparisons are limited by the degree to which the processes of reproduction are understood in each group and by the assumption that the living species resemble their remote ancestors in essential features. In comparing living mammals there is now little dissension from the view that the Monotremata share fewer characters in common with the Metatheria than the Metatheria do with the Eutheria. This applies to characters controlled by structural genes, such as serum proteins (Kirsch, 1977a), amino acid sequence of haemoglobin and myoglobin (Whittaker & Thompson, 1974), chromosome number and sex-determining mechanisms (VandeBerg et al., 1983) which probably reveal true evolutionary affinities, as well as anatomy and reproduction (Griffiths, 1978). Where the differences of opinion occur are in how the living mammals are to be related to Mesozoic mammals and what evolutionary lines are to be drawn therefrom.

Discussion of evolutionary relationships has been enhanced by the theory of cladism but the power of cladistic analysis is only as great as the knowledge of the character states available. For fossils these are necessarily the characters controlled by regulatory genes which produce phenotypic changes in response to local environmental demands, and are limited to teeth, bones and the impressions of other organs left on them, and may be of little evolutionary significance in the cladogram, a point raised by Kemp (1983). Nevertheless, fossils provide the essential time frame for any evolutionary hypothesis.

The most recent checklist of living marsupials is that of Kirsch & Calaby (1977) and their nomenclature is used throughout this book except for more recent revisions in the Dasyuridae reported by Archer (1982). Kirsch & Calaby (1977) recognise 249 species in 16 families. Sixty species live in the Americas and the rest in Australia or the New Guinea islands. They range in size from 7 g to 90 kg and occupy rainforest, dry woodlands, open grasslands and semi-desert from sea level to altitudes of 3000 m in New Guinea and South America. Some are carnivorous, some insectivorous, others are arboreal folivores and others grazers or browsers (see Hume, 1982). Of these species there is now substantial information about the reproduction of 32 species representing 6 families and moderate or slight information about a further 45 species (Tables 2.1 and 2.2). In compiling the material for this chapter we have drawn extensively on the reviews of Collins (1973), Hunsaker (1977), Hunsaker & Shupe (1977) and Charles-Dominique (1983) for neotropical marsupials, Strahan (1983) for Australian marsupials, Archer (1982) for Dasyuridae, Smith & Hume (1984) for Phalangeroidea and Tyndale-Biscoe, Hearn & Renfree (1974) and Tyndale-Biscoe (1984) for the Macropodidae.

Russell (1982a) has provided a fine review of the maternal contribution to reproduction in marsupials, which emphasises the importance of adult body size in reproduction and the constraints it imposes on the strategies adopted by various species. For marsupials there are other constraints as well, which need to be borne in mind when reviewing reproductive patterns systematically.

Lactation is a fundamental characteristic of all mammals and has been a major factor in the evolution of mammalian patterns of reproduction (Pond, 1977, 1983). Despite their separate evolution the cellular processes of mammary development appear to be very similar in monotremes, marsupials and eutherians (Bresslau, 1912, 1920; Griffiths et al., 1972; Griffiths et al., 1973; Griffiths, 1978; Cowie, 1984), although the particular lactational strategies of each taxon differ. The young of monotremes and of marsupials are much less developed than the most altricial young of eutherian species and lactation is proportionally much longer. Monotremes lack teats, the galactophores opening on two areolae, and both the mammary glands secrete milk during lactation; among marsupials, however, each young initially has exclusive use of one teat and only the mammary glands associated with these teats lactate. After the first phase of continuous attachment the young begin to release and reattach to the teat and littermates may move from one to another of these teats. During this phase the young may be carried in the pouch or left in a nest, depending on the species (Russell, 1982a).

The composition of the milk of marsupials, unlike that of eutherians, changes substantially through lactation (Green, 1984) and the size of the lactating mammary gland enlarges manyfold, these changes being, presumably, necessary for the considerable growth and development that the young undergoes during this phase of its life.

Reproduction in the male marsupial has been less well studied than reproduction in the female, perhaps because there are fewer obvious differences between marsupial and eutherian patterns in this sex. However, on closer scrutiny, many unique features emerge, including, as in the female, the anatomy of the genital tract. As Edward Tyson wrote when introducing Cowper's (1704) paper – ‘the organs of generation in the male are no less surprising and remarkable than in the female; and in both they are different from any other animal that I have met with’ (Fig. 1.1).

Anatomy and physiology of the male genitalia

The genital tract consists of paired testes, epididymides and vasa deferentia which open into the anterior end of the large prostate gland. A thin membraneous urethra extends from the posterior end of the prostate, and bulbo-urethral (or Cowper's) glands are present (Figs 4.1 and 4.2). There are no seminal vesicles, ampullae or coagulating glands. The only apparent exceptions to this are found in Caenolestes obscurus (Rodger, 1982)and in Burramysparvus(P. D. Temple-Smith,unpublished), which each have a convoluted secretory segment of the distal portion of the vas, which resembles the eutherian ampulla. The glans penis is cleft in some species, and the scrotum is anterior to the penis in all species (Stirling, 1891; Sweet, 1907).

The scrotum, testes and epididymides

The testes of adult marsupials are generally ellipsoid in shape, (Setchell, 1977) and, in all except two fossorial species, are permanently scrotal.

The three sub-classes of living mammals are distinguished most clearly by their modes of reproduction, which have developed independently during the past 100 million years of their separate evolution. Study of the differences in reproduction between monotremes, marsupials and eutherians helps to throw light on the origins of mammalian reproduction, especially the origin of mammalian viviparity. More importantly, comparisons between these three groups elucidates general principles by disclosing the different means that each has used to achieve the same ends. The central control of ovarian function, the nature and the role of the corpus luteum, the transport and fate of the germ cells at fertilisation, maternal recognition of pregnancy, the initiation and control of lactation, and the neuroendocrine control of seasonal reproduction are all topics that interest the student of reproduction and to which the results of studies on marsupials are contributing new insights.

This is the first attempt to bring the wealth of material, old and new, on marsupial reproduction within one book. In attempting to do this we have been greatly helped by our many colleagues who have generously read those parts that cover their speciality and given us the benefit of their criticism. While we accept responsibility for what is written we thank Des Cooper, Brian Green, Mervyn Griffiths, Lyn Hinds, Jim Kenagy, Russell Jones, Steve McConnell, Kevin Nicholas, Jeremy O'Shea, John Rodger, Lynne Selwood, Brian Setchell, Geoff Sharman, Geoff Shaw and Peter Temple-Smith for reading particular chapters, and we especially thank John Calaby and Roger Short for giving us the benefit of their wide experience on all aspects of the book.

The three sub-classes of living mammals are distinguished most clearly by their modes of reproduction. Many other features set the oviparous Monotremata apart (see Griffiths, 1978) but no other function so distinguishes the Marsupialia from the Eutheria as the manner of their reproduction. This has been recognised since the first marsupials came to the attention of scientists almost 500 years ago and has remained the predominant interest in their study ever since.

Although the original inhabitants of South America and of Australia and the New Guinea islands knew of them, scientific interest began on 8 February 1500 when Vincente Yanez Pinzon collected a female opossum during his first voyage to Brazil. He was so impressed by its pouch and contained young that he took it back to Spain and presented it to King Ferdinand and Queen Isabella at Granada.

Most species of marsupial are seasonal breeders and, as shown in Chapter 2, the emergence of the young at the end of lactation coincides with the most favourable season of the year. For small species with a short gestation and pouch life (Russell, 1982a) the environmental factor that determines the mating season may be some component of favourable conditions such as increasing temperature or protein rich food (e.g. in the Peramelidae, see p. 53) although photoperiod may be an additional factor (e.g. in Sminthopsis crassicaudata (Godfrey, 1969b), see p. 41). For larger species with a longer pouch life, however, mating may occur at a time when environmental conditions are highly unfavourable (e.g. in Setonix brachyurus, see p. 85) and, for these species, photoperiod may be an important factor. By far the best-studied marsupial in this regard is Macropus eugenii and in this chapter we will discuss the evidence for control of seasonal breeding by daylength in this species.

The highly seasonal nature of breeding in M. eugenii was described in Chapter 2 (Fig. 2.26) and other aspects of the interrelationship between the corpus luteum, ovary and blastocyst were referred to in Chapters 6 and 7 respectively. Superficially the reproductive pattern resembles that of the domestic sheep in that both species mate during declining photoperiod; for that reason they are said to be ‘short-day’ breeders. During the period of increasing daylength the ewe is anoestrous (Legan, Karsch & Foster, 1977) and the ram has small testes in which spermatogenesis is much reduced or absent (Lincoln & Short, 1980).

The growth and development of ovarian follicles has been discussed in Chapter 5. In this Chapter we review the evidence for hormonal secretion and the several functions of the ovary in marsupials, as well as the evidence for endocrine control of the ovary. Because of its profound importance in the regulation of the oestrous cycle and pregnancy of marsupials, consideration of the functions and control of the corpus luteum forms a large part of this Chapter.

Serious study of the corpus luteum of marsupials dates from Sandes' (1903) paper on Dasyurus viverrinus and O'Donoghue's (1912, 1914, 1916) papers on this and nine other species. Sandes concluded that the corpus luteum is probably a gland of internal secretion with the functions of influencing the genital organs and of stopping further ovulation during pregnancy. O'Donoghue (1912) extended these conclusions to the corpus luteum of the non-pregnant female by showing that in its growth and development and in the related changes in the genital tract it was wholly equivalent to the corpus luteum of pregnancy, and this was subsequently shown to hold for almost all other marsupials (Sharman, 1970). During the past decade, the application of hormone-assay and surgical techniques has fully confirmed and extended Sandes' conclusion as to the importance of the corpus luteum in marsupial reproduction. There is now evidence that it is involved in the regulation of follicular growth and ovulation; in oestrous behaviour and, possibly, in male response; in embryo development and endometrial growth and secretion; and in the preparation of the genital tract for parturition and of the mammary gland for lactation.

Hitherto we have been concerned with the tactics adopted by individuals and the performance of populations, and we have demonstrated a number of applications of evolutionary theory to these levels of organisation. However, one of the most active areas of both theoretical and empirical ecological research concerns the interspecific interactions among individuals and populations. Such interactions fall within the ambit of community ecology or synecology. Most community properties are the sum of the properties of individuals and consequently reflect the separate adaptations of species. This causes difficulty in the application of evolutionary theory to explain the apparent structure and resilience exhibited by some communities with regard to phenomena such as species diversity (for an alternative view see Wilson (1980)). One type of individual selection which can increase the structure and stability of communities is evolutionary change in a trait of the individuals in one population in response to a trait exhibited by the individuals in a second population, followed by an evolutionary response by the second population to the change in the first. This process is called coevolution (Janzen, 1980), and may arise in a number of circumstances, depending on the nature of the effects of the interacting species on each other (Table 7.1).

Where two species interact to the benefit of both, the interaction is termed mutualism. Mutualism and other two-species interactions may arise without coevolution, but coevolution may enhance the relationship to the extent that the species become obligatorily interdependent (symbiosis). A more immediately obvious interaction is one where one species enhances its fitness to the detriment of another through predation or parasitism.