A new study has revealed a mating conundrum in the animal kingdom: Less fit male seed beetles father more offspring than their high quality competitors when they mate with the same female, says a paper published online today in Science. The findings contradict the widespread belief that females can benefit from taking multiple mates by allowing the best male to father the kids.

Female (right) and male seed beetles in mating position Image: Fleur Champion de Crespigny

Researchers have generally assumed that males with the best genes sire more of offspring, passing on their good genes to a female's sons and daughters, but "in this case, it was exactly the opposite," said evolutionary ecologist Alexei Maklakov of Uppsala University in Sweden, who was not involved in the research.

"This is rather puzzling," evolutionary biologist Tom Tregenza of the University of Exeter in England, who was not involved in the research, said in an email. "If males that are better at sperm competition actually have lower fitness offspring, then females should avoid creating sperm competition by only mating with one male."

Female seed beetles, however, do indeed mate with multiple males, despite the high costs of mating -- male genitalia have frightening spikes that can leave some very nasty lacerations. "One of the common explanations [for female promiscuity] is that the female gets direct benefits" such as gifts of food upon copulation, or parental care, explained Trine Bilde, an evolutionary ecologist at University of Aarhus in Denmark and the lead author of the study. While we can't rule it out entirely, this doesn't seem to be the case in this species, she said, and "in mating systems where such benefits are absent, we have to look for other types of benefits."

Researchers previously thought indirect benefits could be gained in the form of a wide choice of sperm -- somehow, it was believed, females were able to choose which male's sperm fertilized a greater proportion of her eggs, and thus, select the best genes for her offspring. But Bilde's results suggest that's not the case: When female seed beetles were mated with two different males -- one known to produce more offspring than the other -- her eggs tend to be fertilized by the less fit partner, which resulted in up to 17% fewer offspring. Furthermore, the daughters of these crosses had fewer offspring as well.

The genitalia of a male seed beetle Image: Johanna Rönn, Uppsala University Wikimedia commons

If there's no fitness benefit, why do females subject themselves to the pain of mating more than once? Maybe it's not their choice, Bilde suggests. It could be that males "are under high selection to evolve traits that allow them to win in sperm competition, [which has] negative side effects on females." Indeed, females are usually resistant to the attempts of male suitors after they have mated once.

This type of conflict between male and female interests is known as sexual antagonism, and "seems to be relatively common" in the animal kingdom, Bilde said. Male Drosophila, for example, produce proteins in their ejaculate that are harmful to their mates. At the same time, "these proteins are also involved in attacking sperm from other males [and] helping males in gaining a high share of paternity," she said.

To really understand if female promiscuity in seed beetles is indeed a case of sexual antagonism, said Maklakov, will require looking at the fitness of the sons. "The current study demonstrates that successful males produce unsuccessful daughters, but it's also possible that these successful males produce successful sons," he said. "It is very likely that the sons of these males could also be relatively successful in sperm competition." The benefits of producing successful sons could "more or less cancel out" the costs of producing unsuccessful daughters, in which case mating with the "lower quality male" isn't so bad for the female after all.


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