Mothers in Waiting
An odd assortment of animals can delay their pregnancies; how they do so remains a mystery
Rodney Mead of the University of Idaho has spent much of the last 30 years of his life in the company of pregnant skunks. Western spotted skunks, to be precise. His interest is not in the creatures' distinctive markings, nor in their well-known ability to defend themselves by releasing unpleasant odors. Though Mead is fond of pointing out that his charges are "very docile, for a carnivore," temperament also has nothing to do with the animals' appeal to the scientist. No, his interest lies with the secret workings of the spotted skunks' wombs, where--in one of nature's great unsolved mysteries--fertilized eggs can essentially go on hold for periods of time before starting to grow and develop.
Called delayed implantation, or embryonic diapause, the phenomenon has long puzzled reproductive experts. Scientists have known for decades that in more than 100 species of mammals, like the western spotted skunk, healthy embryos sometimes temporarily cease developing and do not immediately attach to the uterine wall. Existing instead as microscopic balls of cells called blastocysts, they free-float in the uterus until the female is physiologically "convinced" she is ready for them to develop. Now increased understanding of that process promises to help wildlife managers preserve animal populations in the field--and could eventually help researchers understand the workings of cancer in humans.
Mammals with varying cycles of delayed pregnancies--some by a few days and others by more than a year--include weasels, seals, otters, bats, armadillos, kangaroos, nutrias and red pandas. "It's an adaptive advantage," says Mead, one of the country's leading specialists on the subject. There's no mystery to the kinds of competitive edge implantation can give: For example, if a marten pregnant in the fall can wait to give birth until spring, she gives her offspring a long summer to learn survival skills before the harsh tests of the next winter. But the advantages of some of the timing remain a mystery to us.
"The fisher is one of the real puzzles," says William Krohn of the Maine Cooperative Fish and Wildlife Research Unit. In Maine, fishers give birth in late February through early April, with most births occurring in mid-March. Within ten days or so of delivery, the female mates again, yet delays implantation for 9 to 10 months. Why would a female fisher, already stressed with nursing young, mate in early spring if the embryos are not going to implant until the next winter? "I can't answer that," says Krohn.
Though researchers don't completely understand the phenomenon of delayed implantation, they've learned enough to be able to induce it in certain species by varying environmental conditions such as amounts of simulated daylight. "It's a handy technique if you want, for instance, to get a room full of mice pregnant at the same time," says Allen Enders, professor of human anatomy and cell biology at the University of California at Davis. But that trick gets old fast, and researchers attracted to the subject often find themselves in a sort of failed romance. The field "is something that is often picked up and put down" by scientists, says Enders.
Why the disenchantment with such a promising field? The answer lies in the few frustrating twists and turns of the phenomenon's maze that science has explored. First, there are two types of delayed implantation. Facultative delay, which appears largely in rodents, shrews and some marsupials, is triggered by suckling of the female's teats. A nursing female rat, for instance, even though she may mate soon after giving birth, will not implant new embryos until her litter has stopped nursing or is removed by other natural means such as predation.
Then there is obligate delay, which occurs in a wide variety of carnivores, lasts for various lengths of time and seems to be seasonal. One puzzle of this kind of delay is that it may not occur in closely related species that appear to share the same habitat and food sources.
Critical to the process is the hormone progesterone, which stimulates changes in the wall of the uterus, preparing it for implantation. But what about creatures like the armadillo, which will implant after delaying even if its ovaries have been removed (ovaries being the source of progesterone)?
These sorts of questions cause reproductive biologists to scratch their heads and eventually move on to other fields. The exceptions are a handful of scientists worldwide, including Mead, who have consistently studied the physiology and biology of seasonal delayed implantation. Mead has been studying it ever since he discovered evidence of delayed-implanting blastocysts in skunks as a student in the 1960s. He calls the skunks "the ideal species" for such studies. His colleagues in Canada, France and Australia have conducted similar research on the mink, European badger and tammar wallaby, respectively.
The earliest research on the subject was conducted by German scientists in the late 1800s. They believed back then, just as many scientists do now, that the effects of pregnancy on the female's ability to gather food are important to the phenomenon.
"Predators like the fisher have to be swift," says Bill Berg, a Minnesota Department of Natural Resources wildlife biologist who studies the habits of fishers, martens and other carnivores that delay. "Carrying blastocysts around instead of developing fetuses makes them lighter in weight and able to perform more survival tasks."
"Delayed implantation allows animals to tailor their reproductive cycle to their yearly food and weather cycles," says wildlife biologist Ken Elowe, who has been studying the occurrence of delays in black bears in Maine. Bears mate in summer but delay implantation until the beginning of winter, after females have had a chance to feed on the summer and fall bounty. "Breeding takes an awful lot out of a bear physiologically and physically. The female needs to take in enough food to get her through the denning period." So the bear must reach what Elowe calls "a nutritional threshold" before the blastocyst will implant. Bears even may self-abort their fetuses if their bodies tell them they are not prepared to sustain a litter.
An advantage to delaying implantation from the fall until the spring is that newborns will have more time to develop hunting skills before facing a harsh winter. Swedish wildlife ecologist Mikael Sandell suggests that some mammals that exhibit seasonal delayed implantation--such as the marten, the western spotted skunk or the South American fur seal--mate in the fall because that's when males are in prime condition. Another creative hypothesis: Some animals may delay implantation in order to prolong the separation of the sexes--decreasing the time that males and females spend together--to reduce competition for food in one specific location.
Perhaps the most intriguing question for scientists is why delayed implantation happens in some animals but not in closely related members of the same species. "Take the long-tailed weasel and the least weasel," says John Gittleman, a zoologist at the University of Tennessee at Knoxville. "They look the same, they eat the same, but the least weasel has no delay while the long-tailed weasel delays for months." This strange dichotomy appears again and again, in various skunks, minks, otters and other creatures. To add to the confusion, some animals, such as Australia's tammar wallaby, even display both facultative and obligate delay.
Part of the answer probably lies in evolution. "There must be some ecological factor we don't know about, some historical component, that took place hundreds of thousands of years ago, which may explain why delayed implantation developed in some species and not in others," says Gittleman. But the question of how delayed implantation came to be "probably has no single answer," says Mead. "We don't have enough information to explain the scenarios in all the species." And since the process has what Mead calls a "spotty distribution" among orders of mammals, it may have evolved independently at different times.
One observation Mead does feel certain of is the importance of the hormone prolactin in delayed implantation for at least three well-studied species: mink, western spotted skunk and tammar wallaby. Prolactin, which is secreted by the pituitary gland, stimulates milk production. It is also critical for controlling the ovaries' production of the all-important hormone progesterone. Mead has concluded that prolactin production increases in the spring and decreases in the fall--apparently influenced, at least in part, by changes in the amount of daylight. But, as in much of this field, even the role of prolactin has its mysteries: In the tammar wallaby, the hormone inhibits progesterone production rather than encouraging it. And no one knows why.
As elusive and baffling as the field of delayed implantation is, the few zoologists who stick with it do so because of its promise. The University of Tennessee's Gittleman asserts that its clues to reproductive potential could save some species from endangerment. Researchers think species that delay are more flexible, says Gittleman, "so the females could handle harsh environmental changes if they had to be reintroduced into another area."
Offers Mead, "You can induce implantation by introducing prolactin or by changing photoperiod [daylight]," he says. "We could speed up the breeding process of endangered species in captive breeding programs to increase populations." He points out, however, that such programs are costly and it is unlikely that less popular species like the spotted skunk, which has been in decline for 20 years, would be able to drum up the kind of attention and concern devoted to more appealing animals like the Florida panther.
There are even speculations on the potential benefits for people of unlocking the phenomenon's secrets. "In delayed implantation, something naturally shuts off the mitotic process, cell division," Mead explains. "Well, cancer cells are characterized by rapid cell division. Understanding the mechanisms that retard cell division could be of great importance." That sort of research is a long way off. Sounding the theme of delayed implantation research, Mead says, "We still don't have a full understanding of the biological process."
As for the application of the process itself to people--what are the chances of learning methods to shut down and then start up our own developing embryos? "I don't even want to think about it," says Gittleman, proving that, for one scientist at least, the mystery of delayed implantation in its original host creatures is quite compelling enough.
Thomas Verde is a Boston-based writer who can be heard on the American Public Radio program "Marketplace." While Verde was researching bizarre animal pregnancies, he and his wife had a standard human pregnancy and son.