Tuatara: Volume 15, Issue 1, May 1967
Marsupials (Part 2)
Marsupials (Part 2)
The Following Description of the male has been based mainly on Owen (1841), who covered comparative anatomy more widely than later authors. Other references are Huggins and Potter (1959) and Pavaux (1962).
The vasa deferentia pass the ureters laterally and posteriorly to join the anterior end of the urethra. There are no vesiculae seminales, but the epididymes are large. The prostate is larger than that of placentals. It forms a single body, the urethral bulb, which is enclosed in a sheath containing mainly transverse muscle fibres. Two or three parts, arranged serially, can be distinguished macroscopically by structure or by colour. Its secretions discharge into the urethra through many pores. There are two or three pairs of Cowper's glands which communicate with the urethra by a common duct on each side.
The corpora spongiosa originate in two distinct muscular bulbs (placentals have one). The bulbs of the corpora cavernosa are enclosed by the erector penis muscles which are attached to the pubes (Fig. 3). Retractor penis muscles arise near the middle of the sacrum. A levator penis muscle is found in some species as a branch arising on each side from the fascia of the crus penis and converging ventrally to form a single tendon which joins the penis.
The glans may be bifurcated or single. In the former case each lobe is transversed by a seminal groove or an enclosed duct (Biggers 1966).
The main parts of the generalised female reproductive system are shown in Fig. 4. Names of the organs are not completely standardised, but those chosen conform to known functions. Like the prostate of the male, the vagina is large.
Fig. 3: The male reproductive system (Hypsiprymnodon). Dorsal aspect after removal of the sacrum. Redrawn from Owen (1841).
The median canal is usually a simple unlined slit which forms late in pregnancy and closes soon after parturition. In some species, mostly the Macropodidae, this birth canal may remain permanently open and it is then lined with epithelium. Infrequently, a temporary median canal may be lined similarly (Kean et al. 1964).
Fig. 4: Generalised diagram of the female reproductive system. The peripheral remains of a perforate median septum are shown anteriorly and posteriorly in the vaginal sac. The vaginal canals are shown open, see text. Expansion of both the sac and lateral canals anteriorly would not be expected in one species. In some species the sac has an anterior extension between the uteri.
In many species the lateral canals are occluded posteriorly by epithelial proliferation* after parturition and during anoestrus but data are scanty (Kean 1961).
The pattern of the marsupial vagina is varied by differences in expansions either of the lateral canals anteriorly, or of the median sac. Lateral canals are long in the Caenolestidae and the whole vagina tends to be long in the Australian marsupials.
In most marsupials placentation is of the yolk sac type (chorio-vitelline). In early stages there is a bilaminar omphalopleure. Mesoderm expands progressively to varying degrees between the two layers. In some marsupials at least (Flynn 1938-39; Sharman 1965a) close apposition of the placenta with the uterine wall during much of the gestation period is prevented by an apparently attenuated shell membrane. A syncytium derived from foetal and maternal cells, or sometimes possibly from maternal cells only, occurs in some species. An allantoic placenta is found in Perameles and Thylacis (Hill 1899) and in Phascolomis and Phascolarctos (Amoroso 1955), but detail for the last two species is not available.
Classification of marsupial placentation (discussed by Sharman 1959b, 1965) is subject to difficulties because type of placentation is not evidently associated either with neonatal size or with evolutionary status of the species, but the situation in placentals is equally unsatisfactory. Young (1957) pointed out that in the Placentalia the evidently primitive diffuse and epithelio-chorial type of placentation occurs among the most specialised mammalian orders. If types of placentation were used as a basis for taxonomy, lemurs should be combined with ungulates (because their placentation is epithelio-chorial) and the hyraxes with the insectivores, primates and other haemo-chorial types.
* Short term closure of the lateral canals does not necessarily depend on cellular growth. Valves are present in some Macropodidae (Owen 1841). In Trichosurus the canals are usually blocked after copulation by an acellular plug derived mainly from the prostate (Kean et al. 1964), and the presence of an additional ring of circular muscles at the posterior ends of the lateral canals in this species suggests alternative muscular occlusion. Vaginal occlusion occurs in many placentals (Asdell 1946; Kean 1961).
Early establishment of the yolk-sac did not affect placental development. Where the yolk-sac intervened between the allantois and the uterus the intervening yolk-sac tissues — glandular epithelium with mesoderm and endoderm — soon degenerated, giving way to allantoic placentation (Weekes 1935).
Weekes (1935) suggested that in reptiles the first function of the yolk-sac placenta was the absorption of fluid, to facilitate yolk conversion following reduction of albumen in uterine eggs. Since blood vessels were not increased in the absorptive yolk-sac, the vascular allantois came to form the main placenta in the third (nutritive) stage described. But among mammals, in a fourth step, vascularisation of the placentary surface of the yolk-sac has occurred, either by the distal half of the placenta developing blood vessels, as in most placentals, or by this half becoming eroded, so permitting the vascular inner surface of the yolk-sac to be applied to the maternal endometrium, as in the inverted yolk-sac placenta of rodents (Young 1957).
Although the respiratory allantois, by its contact with the inner surface of the shell membrane and by its external vascularisation, was pre-adapted for placentation, the yolk-sac placenta became equally efficient after it had developed external vascularisation. Reduction in size of the marsupial embryo would have reduced placentary requirements and then the yolk-sac placenta, because of its earlier development in ontogeny, would have been retained rather than the allantoic one which, in most genera, has reverted to its initial primitive function as a receptacle for urinary waste.
Oestrus, Gestation and Lactation
Marsupials, with the possible exception of Dasyurus (see Hill and O'Donoghue 1913) are polyoestrous. Ovulation is spontaneous.
Lactation at the end of the oestrous cycle can be induced in virgin females by the stimulus of suckling more readily in marsupials than in placentals, indicating little physiological difference between the oestrous cycle and pregnancy in marsupials in regard to lactation (Sharman 1962). It has been suggested (Sharman 1955) that the corpus luteum formed when post-partum oestrus occurs has a lactational function, but most marsupials do not have such ‘corpora lutea of lactation’. In general, it seems that the minor difference in lactation between marsupials and placentals arises from the short gestation typical of the former group and results in early lobule and alveolar development of the mammary glands.page 30
In view of lactational similarities, Sharman (1965a) suggested that gestation in marsupials required only the hormones present during the oestrous cycle. This is doubtful since in pregnancy the post-ovulatory Graafiian follicles disappear insted of continuing on to ovulation, and the reduced vagina does not undergo pro-oestrous expansion (except in species specialised for post-part oestrus).
In Didelphis failure of pregnancy ofter ovariectomy (Hartman 1925) suggested that marsupial embroyos did not produce, from the placenta or elsewhere, hormones which could augment those of the corpus luteum, but Tyndale-Biscoe (1963b) found in Setonix that ovariectomy after the sixth day from coition did not prevent full development and retention of the embryo although parturition was unsuccessful. These results await further work for adequate explanation.
Post-partum oestrus occurs in many of the Macropodidae (Sharman 1955, 1963; Hughes 1962a) and probably in the phalanger Cercaertes concinnus (Bowley 1939). In such macropods parturition is immediately followed by another pregnancy in which intra-uterine development is suspended at an early blastocyst stage, but growth is resumed if suckling young leave the pouch. Decline of reproductivity to anoestrus may cause the blastocyst to be resorbed (Sharman 1955) or it may simply prolong suspension of growth until conditions are favourable for reproduction (Berger 1966).
Prolonged gestation in macropods is a favourable specialisation for unpredictable climatic aridity (Ealey 1963; Newsome 1965). During drought, females of Megaleia lose youch young before they are forced into anoestrus, and presence of a uterine blastocyst increases the number of successive young which can be produced in adverse conditions. Such young require a minimum of maintenance because of their minute initial size.
The reason for prolonged gestation in Cercaertes is unknown, and it is uncertain whether it conforms to the macropod pattern.
Viable sperm are not retained in the marsupial vagina, but Hill and O'Donoghue (1913) found sperm closely packed in parallel formation in gland lamina of the Fallopian tubes of Dasyurus. It is not known where spermatozoa are held similarly in other marsupials, but the method of sperm storage described by Hill and O'Donoghue was illustrated by Fox (1956) in photomicrographs of gland lumina of oviducts anterior to the uteri of snakes. (Captive lizards, snakes and turtles, in the absence of parturition, could retain viable sperm for several years.)
In the early pouch young, marsupials are clearly differentiated from placentals, in both sexes, by the Wolffian ducts, which pass the ureters laterally instead of mesially.page 31
The Wolffian ducts develop early in both male and female embryos. The ureters arise later, in apposition to the metanephric blastema, as dorsal or lateral buds (Fig. 5)t on the Wolffian ducts (Buchanan and Fraser 1918; Hill and Hill 1955) and become extended as embryonic growth carries the kidneys to relatively anterior positions. Müllerian ducts form subsequently as infundibula which extended posteriorly from the mesonephric region. Pearson (1947) pointed out that the Müllerian ducts reach the urogenital sinus by following along the route already established by the Wolffian ducts, as described by Baxter (1935), and he suggested that their positions in marsupials and placentals was a consequence of the positions of the Wolffian ducts. His hypothesis was supported by re-examination of material used by Buchanan and Fraser, and by further reseach, which showed than in many, if not all, marsupials the Wolffian ducts contributed posteriorly to the actual formation of the lateral canals (de Bavay and Pearson 1949).
Since there is no apparent reason for differences in the placement of marsupial and placental Wolffian ducts in males, the positions of the Wolffian ducts seem to have been determined by the respective female requirements.
Fig. 5: Development of the ureter from the Wolffian duct in Trichosurus, second stage. The metanephric blastema and the Wolffian duct have separated. The Wolffian duct can be seen entering the cloaca, right. The medullary tube lies dorsally. The relative positions of the metanephric blastema and the Wolffian ducts are not constant. Redrawn from Buchanan and Fraser 1918. (X 20)
Fig. 6: Pouch young of Didelphis virginiana, head length of 9.0 mm. The Mullerian ducts have grown along the Wolffian ducts and have just joined the sinus horns. (Redrawn from Baxter (1935)) by permission of the Carnegie Institution.)
A further change of form occurs in the female: the Müllerian ducts approximate mesially and together extend a short distance posteriorly, but they do not communicate with the urogenital sinus until the approach of sexual maturity or parturition. Posterior mesenchyme of the uterine embryo and the early pouch young becomes differentiated into the muscles of the lateral canals and the sac, and into connective tissue and muscle fibres of the urogenital strand. The ureters also move laterally and leave unoccupied the connective tissue which accommodates the later extension of the median vaginal canal or birth passage.
Fig. 7: Pouch young, slightly older than in Fig. 7, showing looping and mesial convergence of the Mullerian ducts. There is antero-lateral and postero-mesial expansion. The lumina of the Mullerian ducts are separated from the urogenital sinus by solid tissues — of the sinus cords laterally and the urogenital strand mesially. Detail of lumina omitted. (Redrawn from Baxter (1935) by permission of the Carnegie Instition.)
In the Phalangeridae the gut and caecum become relatively longer with increase in body size and decrease of insects in the diet. In the anomalous Phascolarctos, which has affinites with both the Phalangeridae and Vombatidae, the caecum is very large and presumably digests cellulose efficiently. Pseudocheirus, with a sacculated caecum having two very strong taenia, is probably also efficient. Trichosurus has a relatively simple caecum divided partially by constrictions into four pockets. It is still large although relative to body size only half the length found in Pseudocheirus. It appears to digest parenchymatous leaf substance but not the more fibrous tissues (Lonnberg 1902). Honigmann (1941) reported high values for absorption of crude fibre by Trichosurus when tested on banana and carrot, but such material would conform only to the parenchymatous material mentioned by Lonnberg, and over-all digestion of fibre found in more natural foods is probably relatively poor since this species in the wild state avoids fibrous material (unpublished data). Petaurus, which supplements vegetable material with insects, screens all large particles from entering the caecum (Lonnberg 1902).
In Trichosurus it is likely that rate of caecal digestion is slow, resulting in a high proportion of food material being passed directly from the small intestine to the colon because of closure of the ileocaecal valve. D. Gilmore (personal communication) found that food was eliminated in from eight to more than 120 hours, with 80% passage in thirty-six to ninety-two hours.
In the allied Macropodidae specialisation for grazing has resulted in more complicated structure of the stomach and the adoption of ruminant-type microbial digestion. Moir et al. (1956), for Setonix, described partial division of the stomach into four parts. There is a sacculated fore-stomach (the putative rumen), a non-sacculated region to which a well defined groove leads from the oesophagus, a highly acidic region analogous to the ruminant abomasum, and a smaller fourth region of unknown function. Calaby (1958) found that Setonix digested fibre considerably less efficiently than did sheep and cattle. In protein assimilation the animals were much the same, but food residues were passed more quickly by Setonix. Foot and Romberg (1965) found that Megaleia rufa ate relatively more oat page 35 straw and less lucerne than sheep, with digestive co-efficients lower for lucerne but about the same as for straw, on which Megaleia assimilated less crude fibre but showed a higher total intake of nitrogen — apparently associated with a more rapid passage of food through the alimentary tract (as also in Setonix). This advantage appeared to be offset somewhat by a higher rate of nitrogen excretion, but Megaleia might have the lower basal metabolic rate since sheep were less successful in maintaining body weight on a diet of straw.
The utilisation of low protein foods was demonstrated in Western Australia where Macropus robustus lived in the Triodia covered hills while Ma. canguru was found on the plains where more nutritious grasses were available. Droughts and grazing by sheep resulted in Triodia, which has a low nitrogen content, becoming dominant on the plains, and this change permitted Ma. robustus to displace both Ma. canguru and sheep (Main et al. 1959). In competition with sheep, Ma. canguru would probably have been the more successful since, from preference or unselective feeding, it takes a higher proportion of coarse grass (Kirkpatrick 1965), but its minimum requirements seem to be greater than those of Ma. robustus.
Ma. robustus produces a urine of high concentration, and although the animal drank by preference, a proportion of the population was capable of surviving for long periods without free water if shade was available (Ealey et al. 1965). This faculty was an obvious advantage in an arid climate, but Ealey (1963b) suggested that it was also associated with an adaption for a diet low in proteins. Schmidt-Neilsen (1964), for the camel, confirmed earlier reports of high urea secretion falling when water supplies were limited and he found it as low as 1/50 of normal level. He suggested that this change resulted from the passing of urea to the stomach where the microflora re-converted it to protein. Similarly, in Macropus robustus increase in drinking water resulted in increase of nitrogen in the urine Ealey 1963a).
The macropods appear to differ from domesticated ruminants, not so much in digestive efficiency, as in adaption to the coarse forage of arid land.
Adequate treatment of brain structure and psychology would extend far beyond the scope of these notes. Literature on structure is extensive but mostly concerned with fine detail. Comparative morphology was covered by Owen (1841).
The brains of many marsupials are small, but some brains are large by equivalent placental standards. The most notable feature is the absence of a corpus callosum, the main inter-cerebral page 36 commissure of placentals (Abbie 1939). Diprotoronts have a different commissure, the fasciculus aberrans (Abbie 1941; Masai 1960) which might possibly be compensatory.
Such apparent commissural deficiency fostered a belief of marsupial primitiveness, but recent work (Sperry 1964; Gazzaniga 1965; Gazzaniga et al. 1965) showed that in placentals severance of the corpus callosum had little effect on intelligence. The commissure was associated with cerebral dominance and lateralisation, which is most highly developed in man. These terms denote specialisation of functions in one or other of the hemispheres — as speech on the left and spatial cognition on the rigtht. Visual perception and some tactile sensations are lateralised, but some stimuli are conveyed to both hemispheres, and there are traces of inter-cerebral communication even when all commissures have been cut. Accordingly, there is some need for lateral dominance, which is illustrated in a simple form by right handedness.
Among species, intelligence is largely proportional to cerebral size, and some marsupials could not be expected to score highly, but even small-brained marsupials have been greatly under rated because of comparisons with placentals, made without regard to marsupial specialisations (Hediger 1958). It now seems that the assumed deficiency of commissures in marsupials may not be primitive, but that it indicates bilateral organisation to a degree greater than found in placentals.
Discussion and Conclusions
History of evolution is always tentative. Deductions are subject to the limitations of available evidence.
The early mammals are not shown to have differed greatly from reptiles in brain structure. Their main advance was endothermy, with which was associated insulating hair. A sweat gland system assisted in maintaining condition in hair and skin, and produced odours of social importance. Many mammals were too small to sustain the water loss required for evaporative cooling by sweat. Milk evolved from sweat glands and is itself evidence of pre-established socialisation in care of young.
Viviparity was almost certainly present in some reptiles, but it has not been shown for early mammals. It would have been advantageous to heliothermic animals, rather than to endothermic ones. In mammals it probably arose late, as a consequence of socialisation which afforded maternal protection to free young.
Such young would have been relatively large, preceded in evolution by heavily yolked eggs which produced the yolk-sac and respiratory allantois that were to form the placenta. Efficiency of a simple placenta depends on the relationship of placental surface to bulk of the embryo, decreasing as an embryo increases, and the page 37 primitive neonatus would accordingly have been small in absolute size. Viviparity would have evolved late and in the smaller of the therians.
A single functional oviduct is present in birds and monotremes. Probably analogous development of a median vagina occurred in oviparous therians during some 50 million years preceding separation of marsupials and placentals. Eggs were hard shelled according to the vestigial evidence of a caruncle on the marsupial embryo.
In many recent marsupials the lateral vaginal canals receive a large volume of semen which cannot be accommodated in the median passage. In the other marsupials, semen is transported to the median sac, probably as a secondary development which evolved simultaneously with anoestrous closure of a narrow median canal. The width of this canal in living marsupials is commensurate with neonatal size, suggesting reduction associated with that of the neonatus. But a small therian would have had a relatively large birth passage, able to accommodate semen.
Common therian inheritance would explain the presence of a median vaginal canal in both placentals and marsupials. This origin has not always been accepted. Sharman (1959a, 1965b) agreed that the median canal is not needed by recent marsupials, but stated that the ‘more posterior pseudo-vaginal canal is a new, purely marsupial, development’. No reason or phylogenetic antecedent was given for such new development, and similarity of lateral canals, median canal, and placental vagina was not explained. These canals of three types are all derived directly or indirectly from Müllerian ducts and the cloaca, with varying participation of the Wolffian ducts (Buchanan and Fraser 1918; Baxter 1935: Kean et al. 1964). Admittedly the posterior median canal originates anteriorly from the vaginal sac after it has become differentiated from the Müllerian ducts, and the canal is completed late, after sexual maturity, but late completion is somewhat misleading. Organisation for the canal is early, as shown by the lateral deflection of the lateral canal primordia and the ureters, which leave a clear path for the canal. The lateral canals require little explanation; phyletic antecedence is unnecessary since they are functional.
Sharman (1965b) erroneously cited Kean (1961) as claiming that marsupials differ from all other amniote animals in the course followed by their Wolffian and Müllerian ducts, and the statement (Sharman 1965b) ‘The ureters take a path between the Wolffian ducts in monotremes, reptiles and marsupials so this is the ancestral condition’ was also incorrect. In reptiles and monotremes the ureters lie dorsally and end in the wall of the uregenital sinus. Marsupials and placentals differ from all other amniotes in that their ureters cross from the dorsal position to a ventral one where they join the neck to the bladder. Since this feature is present in all therians, it must have been an early page 38 development, and it is simpler to postulate a single evolutionary step before marsupials and placentals diverged, rather than simultaneous parallel evolution in two closely allied groups, while other steps were taken by the more distantly related amniotes.
Differences between marsupials and placentals in the courses followed by the Wolffian ducts are readily explainable. From an early therian vagina with centrally united Müllerian ducts, marsupials would have required only to develop lateral canals. Their lateral positioning of the Wolffian ducts would then have been a simple case of neoteny—facilitation of female embryonic development — as already explained, of no selective consequence to the fully formed adult.
The parallel evolution of allantoic placentation in many reptiles, the absence of similar yolk sac placentation, and the pre-adaption of the externally vascularised allantois, indicates that the occasional allantoic placentation among marsupials is vestigial and not rudimentary.
Reduction of neonatal size seems to be an inescapable conclusion. The 0.012g neonatus of Dasyurus would be improbably small for a primitive non-lactating therian, and the young to adult weight ratios of marsupials are clearly separable from placental ones. Sharman (1965b) postulated a present evolutionary trend for increasing neonatal size, but adequate published data are available for only three species other than macropod ones, and although neonatal size increases in macropods, relative neonatal size tends to decrease.
Reproductive hormones of marsupial females show considerable resemblance of those of placentals, with due allowance made for shortness of gestation. Oestrous cycles usually exceed gestation in length, except in Macropus canguru (Poole and Pilton 1964) and in Protemnodon bicolor (Sharman et al. 1966). Asynchrony of oestrous and gestational periods has been recorded for Potorous (Flynn 1922).
Prolonged gestation occurs in many macropods as an adaption to arid country with unpredictable rainfall. Embryonic development which follows postpartum oestrus is totally suspended at an early blastocyst stage but is resumed if youch young are lost while conditions are suitable for reproduction.
Regulation of body temperature is efficient. The main difference from placentals is that marsupials tend to have more definite active and resting temperatures, but there is no clear distinction between the two groups in this respect.
Digestive specialisation of marsupials are comparable to those of placentals. Grazing macropods have ruminant-like macrobial digestion, and they show a high degree of adaption to coarse grasses.
Many marsupials have small brains, but others are fully equivalent to placentals. The corpus callosum is absent. This feature page 39 is unlikely to affect intelligence, but it may indicate little cerebral dominance and lateralisation relative to placentals.
Marsupials have been widely adaptive. Much of their evolution has paralleled that of placentals, and in a number of respects they demonstrate alternative efficient methods methods of attaining the same ends.
I am indebted to Dr W. D. L. Ride and Mr J. M. de Bavay for discussion and assistance, to Dr R. A. Barbour for advice on musclature, to Mr and Mrs F. Farrar for German translation, and to Miss J. E. Corbett for illustrations.
Didelphis virginiana — Virginia opossum
Marmosa spp. — Murine opossums
Metachirus nudicaudata — Brown opossum
Dromicops sp. — Opossum
Antechinus flavipes — Yellow-footed marsupial mouse
Dasyurus (viverrinus) = quoll — Native cat
Dasycercus cristicaudata — Crest-tailed marsupial mouse
Myrmecobius fasciatus — Banded anteater
Phascogale tapoatafu — Black-tailed phascogale
Satanellus hallucatus — Little native cat
Sarcophilis harrisii — Tasmanian devil
Sminthopsis crassicaudata — Fat-tailed marsupial mouse
(Isoodon) = Thylacis macrourus — Brindled bandicoot
Macrotis lagotis — Rabbit bandicoot
Perameles nasuta — Long-nosed bandicoot
Cercaertus (= Cercartetus = Dromica) spp. — Pigmy opossums
Eudromicia spp. — Pigmy opossums
Pseudocheirus peregrinus — Ring-tailed opossum
Trichosurus vulpecula — Brush-tailed opossum. (Widespread in N.Z.)
Phascolarctos cinereus — Koala
Phascolomis mitchellii = Vombatus hirsutus — Common wombat
Hypsiprymnodon (= Hypsiprymnus) moschata — Musky rat kangaroo
Macropus canguru (= major) — Grey kangaroo
Macropus robustus — Euro
Megaleia rufa (= Macropus rufus) — Red kangaroo
Petrogale penicillata — Bushtailed rock wallaby. (Kawau and Rangitoto Islands, N.Z.)
Potorous tridactylus — Rat kangaroo
Protemnodon rufogrisea (= Macropus ruficollis) — Brush wallaby. (South Canterbury, N.Z.)
P. bicolor — Swamp wallaby. (Kawau Island, N.Z.)
P. eugenii — Tammar. (Kawau Island and Rotorua, N.Z.)
P. parma* — Parma wallaby. (Kawau Island, N.Z.)
Setonix brachyurus — Quokka
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Protemnodon dorsalis was previously rare on Kawau Island and is now likely to be extinct.