BioEd Online

Female redback spiders are not the most sympathetic of lovers: they routinely begin to eat their suitors before they've had a chance to finish mating. And now research shows that their internal anatomy also helps them get one over males, by influencing which mates get to fertilize their eggs.

The female redback (Latrodectus hasselti) has two organs for storing sperm, called spermathecae, explain Lindsay Snow and Maydianne Andrade, of the University of Toronto in Canada. Although biologists already knew about these twin sperm sacs, they had not investigated how they affect the issue of paternity when a spider mates with more than one male.

The two sperm sacs help to prevent a male from stealing a mating advantage simply by being the first to court a female, Snow and Andrade suggest. A male has two sperm-depositing organs, called palps, that correspond to the female's two sperm sacs, although he can use only one palp in a mating session.

A male tends to break off the end of his mating palp inside the female's sperm sac, partly blocking its entrance, the researchers say. "This functions as a plug, a kind of chastity belt," explains Paul Hillyard, curator of arachnids at the Natural History Museum in London.

Having two sperm sacs may therefore give females extra choice over who fathers her young, Snow and Andrade say. If one of the sacs is blocked by a mate, a subsequent partner can still be given the opportunity to deposit his sperm in the other.

Choice chop

The researchers tested this idea by manipulating which spermatheca a male inseminates. For each male, they cut off one mating palp, giving the spider no choice over which sac to inject with sperm. When two rival males had palps removed from the same side, forcing them to deposit in the same spermatheca, the one who went first fertilized an average of 80% of the eggs. This shows that going first has an advantage regardless of mate quality.

But, as the researchers report in Proceedings of the Royal Society B¹, when males filled opposite sperm sacs, this advantage was removed, giving them an equal start in the race to fatherhood.

Andrade suspects that females cannot select which sperm to use when her eggs are fertilized, but rather that the contents of both spermathecae are released together. The lion's share of the offspring would then be sired by the male who had deposited the most, or best-quality, sperm.

Eating on the job

The female redback's penchant for mid-coital cannibalism may also help her to select a good father for her offspring, the researchers suggest. During copulation, the position adopted by the male leaves him dangling invitingly in front of the much larger female's fangs. "Females seem to hold all the cards in this species," says Andrade.

A larger male, however, is more likely to survive the first mating and be granted a second, Snow and Andrade report. "Despite being partially digested, the male is able to get off and recopulate," Andrade says.

This gives larger, higher-quality males the opportunity to fertilize 100% of a female's eggs. By mating twice over, once with each of his two sperm-depositing palps, he can ensure that the female is filled with his, and only his, sperm. That's assuming, of course, that she lets him.

The phenomenon may also operate in other spiders, Andrade adds. "There is currently no evidence that females of other species use their internal genitalia in the same way," she says. "But in spiders, dual organs are the norm, so the potential is there for this to be occurring."