A fundamental difference between the eutherians and metatherians stems from the development of their urinogenital structures. During development, the ureters in metatherians attach to the bladder in a more central position, threading through the middle of the two lateral vaginae (Figure 1). As a consequence to this, the lateral vaginae are unable to fuse together to form a central chamber, or uterus. Despite the positioning of the ureters, a central canal can form during a female’s first pregnancy, and is able to be lost and reformed accordingly. The position of the ureters is unable to wholly account for the reason why metatherians have small, altricial young, not only because of the ability to form a central canal, but not all eutherians have the two vaginal horns joining to form a uterus.
One can compare this chance alteration of structure to the systemic arches retained by birds and mammals. In birds, the right systemic arch is predominant, whereas mammals preserved the right systemic arch. Which arch is maintained is embedded within the development of the embryo. There is, however, no functional consequence evident, and so it matters little which arch was lost.
In comparison, there seems to be significant structural complications arising from the seemingly random placement of the ureters between the metatheria and eutheria. These structural implications may result in the consequences we are familiar with, such as shorter gestation times and altricial neonates.
Figure 1: The ureters thread through the middle of the vaginae to meet the bladder in metatherians, whereas in eutherians, the ureters encircle the horns, enabling them the capability to fuse. (From Bradshaw 2003a)
I hypothesise that the positioning of the ureters occurred purely by chance, with implicit complications, which were not initially selected against. As the climate of Australia changed, becoming more unpredictable, an extreme form of the metatherian mode of reproduction arose, characterising the macropods. The perhaps more ancestoral exploitations of this method of reproduction still persist to this day, demonstrating the vigorous nature of the metatherians. In this essay, I examine the plausibility of some of the proposed selective pressures favouring the metatherian mode of reproduction, such as the ease of termination of investment in offspring; the metatherians low basal metabolic rate and the unpredictability of conditions.
Consequences of the urinogenital structure of the Metatheria
Shorter gestation times may have occurred because having a larger foetus present within the central canal could place stress upon the ureters as it developed. Shorter gestation times would therefore be favoured within the metatheria. This would result in altricial neonates, and the female would be obligated to direct energies into a longer period of lactation to compensate for the lack of development in the young.
Conversely, it could be entirely coincidental that the gestation period of a metatherian does not often interrupt the continuation of an oestrus cycle. This may then have been selected for under certain conditions and environments. The fact that the metatheria have altricial young may simply be a consequence of the short gestation period.
I hypothesise that it was simply by chance the ureters in metatheria are centrally located, and this placement may or may not have had direct ramifications on the length of gestation and the degree of development of the young before they are expelled from the internal body of the mother. The resulting altricial young, however, would have direct influence upon the length of lactation and parental care given. The fact that metatherian termination of investment in the current young is relatively easy in comparison to eutherians may be coincidental to these other complications; however, it may also have favoured the metatherian mode of reproduction, facilitating its persistence.
Selective pressures possibly favouring the metatherian reproductive method
Unpredictable conditions
It may be thought that the metatherian mode of reproduction is favoured under conditions where the environment is uncertain: where termination is profitable at regular intervals, and a flexible, perhaps opportunistic strategy was encouraged (Low 1978). Consideration must be given, however, to the fact that during the early Cretaceous, when metatherians and eutherians were beginning to diverge, the Australian climate was not as uncertain and unpredictable as the climate we are familiar with today. Instead of vast expanses of desert, tropical rainforests dominated the countryside. These humid, perhaps warm, temperate rainforests persisted within central Australia at least until 15 mya (Archer & Clayton 1984).
Given this, it may be that the metatherians had no strong advantage over the eutherians in Australia, had eutherians been present upon the continent during this time. The origin of Australian marsupials is largely debateable, but suffice to say that metatherians within Australia have supposedly been entirely free of eutherians until relatively recently. Fossil evidence will never be able to show a complete lack of eutherian presence, but we must speculate and assume in the absence of information.
Due to the largely predictable nature of the climate during the early radiation of the metatherians, it is my supposition that the metatherian urinogenital system persisted simply because there were no selective pressures against it. The family Dasyuridae, whom are characterised by having large litter sizes, a high degree of investment in their litters, and leaving their young in a nest (Russell 1982), may represent metatherians who were dominant during the majority of the early Cretaceous.
As the climate began to change, gradually becoming warmer and drier, species whom were able to reproduce rapidly in an environment that still had an extended period of favourable conditions prevalent (Russell 1982) may have been selected for. The family Peramelidae, whom have litters consisting of more than one young, and low levels of investment (Russell 1982), may be representative of the type of animals becoming more widespread during this era of change.
With grasslands extending over the country, species “with small litter size, lower total investment, but investment in individual young is not too low, and investment in carrying young to an advanced stage of development is high” (Russell 1982) may have become more common. The family Diprotodonta displays these characteristics, and Macropodidae is seen as an ‘extreme’ of these features, with one joey in the pouch at a time, diapause and the ability to produce two types of milk simultaneously to nourish successive offspring.
This slow change in the environmental conditions may be why there is what Russell (1982) describes as being three main lines of “patterns of parental care and investment” within the metatheria. I have not yet tested this hypothesis against any current phylogenetic trees, as “there are almost many phylogenies as there are phylogeneticists” (P.C. Withers 2003), all having altered priorities on different characteristics, and novel methods for distinguishing the species and families from each other. Examination of this possible correlation would indeed be interesting.
I hypothesise that there were no harsh selective pressures against the metatherian mode of reproduction until the environment began to change. With the arrival of a more arid climate, there was an opportunity for the very ‘extreme’ Macropodidae to develop and proliferate. Recognition must be given, however, to the fact that the species to which I refer to as prevailing in a climate far different from the arid conditions of today, still thrive to this day. If my hypothesis bears any semblance to what truly happened, then it can only demonstrate the robust nature of the methatherians and their inherent flexibility in the face of change.
Termination of investment
It has been stated by Low (1978) that the cost to terminate the investment in offspring not only includes the costs that have been already invested in the offspring, but also incorporates the cost of the act of termination. Low (1978) concluded that for many eutherians, the act of abortion during gestation and before birth might be energetically expensive, and risky to the mother. This is opposed to metatherians, who have lower parental investment in their young at birth compared to the eutherians (Hayssen et al. 1985).
Hayssen et al. (1985) elaborated upon Low’s (1978) thoughts on termination, claiming that abandonment of young (whether by desertion or abortion) is likely to be favoured when it will increase the probability of success in another investment, either in the present or future. Thus the act of termination “protects the female’s ability to reproduce in the future” (Hayssen et al. 1985), and this will be enhanced in an unpredictable environment. Hence, the marsupial reproductive method, characterised by the short gestation time and lengthy period of lactation possesses a relatively lower cost to terminate than a eutherian (Hayssen et al. 1985).
Hayssen et al. (1985) proposed that it is likely that although is it possible for a eutherian to terminate her investment in her young by aborting in utero development, it is not without cost. Low (1978) stated that the act of abortion may carry with it high risks to the mother, that increase with the progression of the pregnancy, due to the size of the foetus. An early termination in eutherians is better in terms of costs and risks, however metatherians seem capable of terminating their commitment to their offspring at a relatively low cost during all stages of development.
Basal metabolic rate
Morton et al. (1982) proposed that metatherians display a characteristics such as slow rates of growth and development because of their low metabolic rates, which are seen to be an adaptation to living in environments with variable or limited resources. Hayssen et al. (1985) blatantly dispute this claim, stating that the metabolic rates may change when animals become reproductive. I am in agreement with their statement that “if marsupials do have lower metabolic rates during reproduction than do eutherians of similar weight, their mode of reproduction must be more efficient energetically than that of eutherians” (Hayssen et al. 1985 p. 624).
The lack of influence metabolic rate has over reproductive adaptations is further enhanced by the lack of any data supporting the claim made by Morton et al. (1982). Hayssen et al. (1985) gave an example of a study on the North American opossum, Didelphis virginiana, where the energetics devoted to reproduction was examined. Fleming et al. (1981) discovered that “the resting metabolic rate of lactating females is 92% higher than that of nonlactating females” (Hayssen et al. 1985). They also found the rate of energy transferred from mother to her offspring is no different between the didelphid metatheria compared to eutherians (Hayssen et al. 1985). There is little correlation between the basal metabolic rate and the gestation and lactation length within the eutherians even (Hayssen et al. 1985).
Morton et al.’s (1982) claim that the metatherians cannot reproduce large numbers of young quickly may still hold true, but for a reason different than the basal metabolic rate. When Macropodia were evolving, there were few higher-order carnivores present, and vast plains of grassland. Macropodia may be unable to produce many young rapidly, as doing so would be an incredible strain on the population due to the resulting competition within the groups for resources. To mediate this, lowering their rate of reproduction may have been favoured (S.D Bradshaw 2003b). I doubt, however, that the basal metabolic rate had any influence on sustaining the metatherian mode of reproduction.
Lactation
A long period of lactation has been thought to be energetically more costly than simply maintaining the foetus within the uterus, and transferring nutrients via a placenta (Low 1978). Low (1978) stated that would seem this early shift to lactation might result in a “higher caloric cost per unit weight of offspring” when compared to eutherians. This higher cost may be minimised by those females whom are capable of simultaneously producing two types of milk to sustain joeys of differing ages (Low 1978). The milk produced for the younger joey may be cheaper to manufacture, but as the amounts of fats and proteins increase to support an older joey, the cost is likely to also increase (Low 1978). Low (1978) suspected that this production of two milks, with one being incredibly cheap to create, would be less costly than the cost a eutherian would bear when producing milk to sustain its young after giving birth.
Low’s suspicion was supported by Hayssen et al. (1985), who stated that people tended to overlook the fact that eutherians suffer a cost when producing a placenta, and the maintenance that incurs with a female enduring a long gestation. Ergo, the overall cost of early lactation may be energetically less costly or similar to the overall costs of the long gestation of the eutherians. Thus, an early shift to lactation may facilitate or compensate for the incredibly short gestation period, and would inadvertently aid in the selection for small, altricial young.
Conclusions
The metatherian urinogenital organs are fundamentally different from that possessed by the eutherians, however these differences arise because of a simple alteration in the positioning of the ureters. This slight adjustment, I hypothesise, was completely by chance, and as there were no strict selection pressures against the different modes, the metatherian method persisted within the Australian continent. Early shifts toward lactation would compensate for the short gestation period of the metatherians, and in turn select for altricial young who displayed accelerated development of necessary characteristics. The relative ease of termination of investment in metatherian offspring also favoured the metatherian reproductive mode and permitted its persistance.
When the climate began to change from tropical to semi-arid and arid, with grasslands becoming predominant over much of Australia, the macropods became extreme in their method of reproduction, taking advantage of diapause, and carrying their young for extended periods of time within their pouch. The fact that the gestation period of metatherians is short enough to not interrupt the oestrus cycle is something I consider to be purely coincidental, but is exploited by the metatherians nonetheless.
The metatherian reproductive structure, and the resulting consequences and implications, does not seem to inhibit the proliferation of the metatherians. Instead of being inferior to the eutherian methods, and doomed to submit to evolutionary stagnation, the metatherians seem to be incredibly evolutionarily flexible (Hayssen et al. 1985).
References
Archer, M. & Clayton, G. (eds) (1984) Vertebrate Zoogeography and Evolution in Australasia. Hespeian Press, NSW, Australia.
Bradshaw, S.D., 2003: Anatomical considerations. September 11 lecture, Marsupial Biology 313, University of Western Australia.
Bradshaw, S.D., 2003: Gestation and hormonal profiles. September 18 lecture, Marsupial Biology 313, University of Western Australia.
Fleming, M. W, Harder, J.D. & Wukie, J.J. 1981. “Reproductive energetics of the Virginia opossum compared with some eutherians” Comparative Biochemistry and Physiology. B, Comparative Biochemistry 70: 645-648.
Hayssen, V., Lacy, R.C. & Parker, P.J. 1985. “Metatherian reproduction: transitional or transcending?” The American Naturalist 126(5): 617-632.
Low, B.S. 1978. “Environmental uncertainty and the parental strategies of marsupials and placentals” The American Naturalist 112: 197-213.
Russell, E.M. “Parental care and parental investment in marsupials” Biological Reviews 57: 423-486.
Withers, P.C., 2003: Taxonomy and phylogeny of marsupials. July 31 lecture, Marsupial Biology 313, University of Western Australia.
Comments:
The field metabolic rate is the critical parameter, not the BMR.
Interesting approach! Well argued and thought out. 8/10.
Marked by S.D. Bradshaw.