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Marsupial Mating Proves Promiscuity Pays




COURTESY OF DIANA FISHER
Male Antechinus stuartii--a brown, mouse-size, insect-eating marsupial with bigger eyes but the same hairless tail as a rat--have a short and desperate life. Heading into the Australian winter, roughly 10 months after birth, the small creatures stop producing sperm and enter an intense, two-week mating season with a finite store of the means to pass on their own genes. Over the course of that season, the marsupial mice engage in mating sessions of five to 14 hours and, of course, copulate with as many females as possible. By the time they reach the end of the breeding season, stress hormones lead to immune system collapse, internal bleeding, infections and an inevitable death. Before the end of their first year, Antechinus males will die. Now a new study proves that all this effort for most of these lotharios may be in vain--only those with the strongest sperm will sire offspring.

Zoologist Diana Fisher of Australian National University in Canberra and her colleagues studied the manic male marsupial to understand why females of the species would choose to mate with multiple partners given the high cost of egg reproduction and the toll taken by such epic mating. Similar studies in insects have shown that such promiscuity, known more technically as polyandry, or multiple fathers, produces better young--better in this case being a measure of offspring survival. Some have proposed that males with more competitive sperm create more viable offspring, but this hypothesis has yet to be unequivocally demonstrated, largely because it is difficult to distinguish whether such survival is the result of better fathers or more mothering from females.

But because the male Antechinus kills himself in the process of mating--and most females only live for one year--the researchers could study the effects of polyandry both in the lab and in the wild. In 2003 the zoologists divided 36 female brown antechinuses into two groups: 17 mated with multiple males and 19 mated with just one. The proportion of each litter surviving to weaning was three times greater in the multiple maters than in their monogamous peers. "Sperm competition is a way of getting eggs fertilized by the best males," Fisher says. "If some males are just better genetic quality than others, and superior males have better performing sperm, then females can get the best fathers for their babies by mating with lots of males, then letting their sperm fight it out in an internal battle for fertilization."

This mating strategy means each brown antechinus litter contains babies from multiple fathers--typically three or four, according to previous studies in the wild--and, in 2004, the researchers calculated the relationship between the paternity share of a particular male and the success of his offspring. The most prolific males--and those with the best competing sperm--did, in fact, sire the best offspring, according to the paper presenting the result in the November 2 issue of Nature, even when monogamously paired. "This means that mating with one good quality male and mating with lots of males of varying quality have the same effect on a female brown antechinus," Fisher notes. "It means she gets the best quality father or fathers for her litter."

The finding in this particular marsupial may not be broadly applicable, but they do lend weight to the "good sperm" theory to explain multiple matings. And nobody understands how the small brown antechinus can endure such epic matings in the wild. "It must be exhausting and difficult for females to manage their times so they get enough to eat," Fisher observes. "Another good thing to do would be to keep multiple generations of males and look at heritability and mechanisms of sperm competition." Regardless, the life of a low-performing antechinus male is short and sad. "We found that quite a few males were poor at competing for fertilizations," she adds. "So a lot of males wouldn't father any young if the female mated with several other males."

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