Sperm competition drives suicidal reproduction in antechinus and other marsupials, according to a new study by Australian researchers.
The research, which was published in the journal Proceedings of the National Academy of Sciences, overturns previous theories that linked the post-mating mass die-off to altruism or to food availability.
Die-off in males occurs in around a fifth of all known species of insectivorous marsupials, including all 12 species of antechinus, three species of phascogale, and kalutas. Some populations of northern quoll and dibbler also experience die-offs to a lesser extent, as do some other South American species.
The study found that extreme stress, and the failure of the corticosteroid mechanism that controls it, cause immune system collapse, infections and internal bleeding, leading to death.
"We wanted to find out why semelparity (suicidal reproduction) evolved in these small insectivorous marsupials and no others," says biologist Diana Fisher from the University of Queensland who led the study.
"Males of semelparous species spend most of their lives as immature animals and mature at 11 months, just before the breeding season," she adds. "They have a few other peculiarities as well: they all shut down their testes before breeding and so rely on sperm stored in the epididymis for mating, which is also lost in their urine."
"This gives them some urgency to mate, so it is no wonder that the breeding season is so frantic. Each mating can take 12 to 14 hours and they do this over and over again. Even if they survived the breeding period, they would be infertile anyway."
Going out with a bang
A previous explanation for the male die-off was that it avoided competition with their offspring because of seasonal availability of food. However, Fisher says the animals' lack of territoriality and promiscuous nature makes this highly unlikely.
"Males have offspring all over the place, and even if food was critically short and dying did help the next generation, this would benefit the young of others, not only their own young," she says.
To test that hypothesis, the researchers looked at life history data for 52 species of insectivorous marsupial from Australia, Papua New Guinea and South America. They found that seasonal availability of food is related to the timing and length of the breeding season, and males of species with shorter breeding seasons have lower survival, but this doesn't explain mass male die off.
"Although insect peaks vary between years — and are likely to do so increasingly in a changing climate females' — synchronised ovulation often occurs on the same day over a number of years and is triggered by rate of change in day length," Fisher says.
"Peaks in prey availability coincide with shorter breeding seasons, with females timing their energy intensive reproductive cycles to coincide with maximum food abundance while they raise their huge litters of offspring."
This is much more of an issue in higher latitudes than in the tropics where food is available year round, Fisher says, and the short breeding season further south places stress on males as they compete for females, however, it doesn't entirely explain suicidal reproduction.
Instead, the researchers found that females of species with the most extreme male strategy of die-off have even shorter breeding seasons than the availability of food dictates, and this time pressure imposes severe competition on males.
In response, semelparous males have large testes relative to body size that allow them to fertilize as many females as possible.
Disintegration of their testes before mating means that males devote as much energy to competitive mating as possible. They aren't spending energy on making sperm by this stage, and use their body tissues to fuel the mating frenzy.
"The males don't engage in physical competition; instead their sperm are left to battle it out in the female's reproductive tract," Fisher says.
"Our previous work showed that females benefit from sperm competition because the best males sire more of their offspring — antechinus males that excel at sperm competition have better offspring survival.
"This means it is actually pressure imposed by females via their reproductive timing and encouragement of sperm competition that has selected for semelparity in males. Using all their energy on the one breeding season gives males an advantage in sperm competition, so it's reproductively worthwhile for them even though they die," she adds.
"The only way for males to avoid die-off is for them to be raised independently of any females so they are never exposed to the hormones that kickstart the mating frenzy."
"But that's not much fun for them either."