Lurking males lead to hard-to-fertilize mouse eggs

How much male company a female mouse sniffs and sees as she grows up affects how easy her eggs will be for sperm to fertilize.

Female house mice reared amid plenty of male mice in a lab mature to produce eggs that are relatively challenging to fertilize, says Renée Firman of the University of Western Australia in Crawley. Meanwhile, eggs from mice raised in all-female groups accept sperm for fertilization almost twice as readily, Firman and Western Australia colleague Leigh W. Simmons report October 16 in Proceedings of the Royal Society B.

In a sperm-rich locale, tougher-to-fertilize eggs could offer evolutionary advantages for a female mouse. Perhaps an egg more resistant to fertilization is also less likely to end up penetrated by two sperm, a catastrophe that would kill the embryo. Or with resistant eggs, Firman hypothesizes, “only the best-quality males gain fertilization.”

In sperm deserts, evolution should favor more-receptive eggs.

The new study is the first case Firman knows of where scarcity or abundance of future mating partners prompt differences in fertilization-friendliness in eggs. “We’re starting to understand that females can kind of control what’s happening at the gametic level,” Firman says.

She discovered this flexibility in house mice, Mus domesticus, from two wild populations, one high and one low in the chances that females would experience multiple males’ sperm competing to fertilize their eggs. Firman raised descendants of these wild mice from weaning until adulthood with either no signs of males or abundant cues. To create the impression of many future mating options, the researchers arranged periodic sniff-and-see visits with caged males and also enriched the young females’ bedding with redolent used bedding material from male cages. “House mice have a very distinct odor,” Firman says. “It can be a little off-putting at times when you’ve got heaps of animals in a room, especially sexually mature males scent-marking continually.”

When the females reached sexual maturity, Firman mixed the mice’s eggs with sperm in arrays similar to human in vitro fertilization setups. In mice from both wild populations, more eggs from the female-only groups ended up fertilized (73 percent overall) than from male-rich circumstances (38 percent).

What would be interesting next is to reverse the male abundance for the now-adult female mice and see if they switch the kind of eggs they produce, says Eduardo Roldan of the National Museum of Natural Sciences in Madrid.

Whatever females do, male mice are also adjusting their gametes, Firman’s earlier work shows. With lots of other young males around, mice tend to develop more aggressive, ready-to-fertilize sperm, and more of it. In responding to each other’s physiological ploys, mouse sperm and eggs may have their own evolutionary arms race.