Marsupials are notorious reproductive record breakers. They have the largest sperm and the shortest pregnancies among all mammals. They also have the longest periods of embryonic diapause, that is they can put embryo development on hold during unfavourable conditions like times of scarce food or poor weather.
Kangaroos and wallabies also regularly support their young at three different stages of development – an embryo in the uterus, an early stage pouch young, and a semi-dependent young at foot, still sucking milk.
Our latest study has now shown that one species, the swamp wallaby (Wallabia bicolor), has accomplished another reproductive feat – it is the only mammal known to be permanently pregnant throughout its life.
For the research, published in Proceedings of the National Academy of Sciences USA, we used high resolution ultrasound to track pregnancy and mating in 10 female swamp wallabies.
What we found amazed us – the females come into oestrus, their fertile period, mate and form a new embryo one to two days before the end of their existing pregnancy.
So how is this possible?
Unlike humans, kangaroos and wallabies have two uteri. The new embryo formed at the end of pregnancy develops in the second, ‘unused’ uterus.
Then, once the newborn from the first pregnancy begins to suck milk, the new embryo enters a long period of developmental arrest that may last up to 11 months or more.
When the sucking stimulus from the young in the pouch declines, the dormant embryo starts growing again and the cycle starts anew, with females returning to oestrus in late pregnancy, mating, and forming another embryo.
This cycle means that female swamp wallabies are permanently pregnant their whole adult lives.
As far as we know, this is unique among mammals. Most mammals require a break between pregnancies either to support new young with milk, which is energetically demanding, or during periods of low seasonal resources, like harsh winters.
And there are many other reasons why mating during an established pregnancy might be ill-advised. Male seminal fluid may contain foreign material like microbes that could contaminate the sterile environment of the womb, affecting the existing pregnancy.
Mammalian pregnancy is generally a lengthy affair (up to 22 months in elephants), with several stages that require different combinations of hormones. This balance may be disrupted by the differing hormonal environment required for ovulation.
Space in the common uterus may also be an issue with the late-stage fetus taking up most of the space in the uterus for a new embryo to develop and implant.
The swamp wallaby may be able to navigate the hazards of a new conception during pregnancy for a number of reasons.
For one, their extraordinary reproductive tracts include three vaginas, two completely separate ovaries, oviducts and uteri, which they use alternatively through successive pregnancies, with the third vagina only becoming active during birth.
This means that the local hormonal environment of each set of ovaries and uteri may allow it to operate in isolation from the one with the incumbent young.
Pre-birth ovulation and conception also occurs only in the final six percent of the initial pregnancy, so any mating or contamination of the existing pregnancy may not disrupt or antagonise successful delivery of the late-stage fetus.
The final component of swamp wallaby reproduction that allows this remarkable double pregnancy is embryonic diapause. Embryonic diapause refers to the arrested development of embryos, usually at the blastocyst stage of development (whe it is just 80-100 cells).
Many animals do this to pause reproduction until it is desirable. For wallabies this would be when the pouch becomes free again, but it can also be triggered by season, climate or food availability in other species.
In the swamp wallaby, embryonic diapause occurs as soon as the mature fetus is born and attaches to one of the four teats in the pouch. The sucking action causes the hormone prolactin to be released from the pituitary gland, and this hormone inhibits development of an ovarian gland called the corpus luteum.
The corpus luteum produces the hormone progesterone, which is necessary for embryo development. The embryo therefore stops developing after only a few days.
If this didn’t happen, the swamp wallaby would birth new young every 30 days, which it couldn’t support in the pouch.
There is currently only one other species of mammal known to go into oestrus while still pregnant – the European Brown Hare (Lepus europaeus). This species also returns to oestrous in late pregnancy and conceives additional embryos before giving birth.
This feat may be all the more remarkable in the hare because the embryos are conceived within common uterine horns already supporting late-stage fetuses.
The European Brown Hare has restricted breeding seasons each year of about six months between January and August, and the pre-birth oestrus and conception in this species allows them to produce about one-third more offspring each year. However, they are not pregnant through the cold seasons.
The difference between this strategy and the swamp wallaby is that embryonic diapause allows the swamp wallaby to maintain either an embryo in diapause or a developing fetus in one of two uteri at all times of its life, continuously.
Indeed, for two days of each pregnancy it is likely to have a conception in each of its two uteri.
Furthermore, this species also exhibits a phenomenon called asynchronous concurrent lactation, where it may support one young in the pouch and a semi-independent young at foot with milks of entirely different volume and composition.
So not only is it continuously pregnant, it is also likely to be continuously lactating throughout life.
Other kangaroos and wallabies mate after giving birth, and we are yet to fully understand why the swamp wallaby has broken from this convention. Presumably, given this is the only marsupial to do so, and that relatively few mammals in general do this, there are barriers or constraints to achieving this outcome.
Whatever the reason, this reproductive strategy means the swamp wallaby is an incredibly successful and ubiquitous species in Australia, occupying a range that stretches from the Western Victoria/South Australian border all the way up the eastern seaboard and to Cape York in far north Queensland.
Our future research will help understand the biology behind permanent pregnancy in the swamp wallaby.
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