Females having multiple sexual partners may be more fertile

Researchers have discovered that females that have multiple sexual partners can be more fertile than those that are monogamous and, very surprisingly, that this is the result of an "overproduction" of sons. The study - still only published as a provisional article but already one of the most accessed in BCM Evolutionary Biology - helps to explain a puzzle that has been haunting evolutionary biologist for decades: why during a mating season so many females chase multiple sexual partners when one is enough to fertilize all her eggs and to do it is costly and dangerous. The finding that multiple mating allows females to have more descendants (and to manipulate offspring gender to their advantage) could be why. After all, in evolution, success is about passing one's genes to future generations.

The study is a collaboration between the University of Aveiro in Portugal, the University of St Andrews, Scotland and James Cook University in Australia

In the last decades scientists have discovered that multiple mating is everywhere, even among those species once seen as the epitome of monogamy, like swans and penguins. And also that both males and females are out there chasing multiple partners. While this makes sense to males - since the more they mate the more descendants they have to carry their genes - with females the situation is different. Not only they have a limited number of eggs per breeding cycle (so a limited number of babies) that one partner usually is capable of fertilizing, but the practice is also particularly dangerous to females. Still, more and more cases of species where females actively pursue polyandry (female multiple mating) are being discovered. So why is this?

Since everything in nature is about costs and advantages, a behaviour, such as polyandry, will only be pursued by females if its benefits outweigh its costs. Ultimately, this means that it has to improve the female's fitness (capability to pass its genes to future generations). There are two types of possible benefits that can do this: direct (when the female is directly benefited, for example with increased fecundity or longevity) or indirect (when is the next generation that gets the advantages by becoming for example more attractive or stronger, all characteristics that improve their chances to reproduce). If one or both types are enough to compensate the costs of polyandry to females, then it could be explained why the practice persists.

And in fact, several cases of female-initiated polyandry with indirect benefits (so leading to "improved" offsprings) have already been discovered, and even suggested that they could be enough to offset polyandry costs. But so far this remains to be proved.

In order to test this Miguel Barbosa from University of Aveiro, Anne E Magurran and Maria Dornelas from University of St Andrews and Sean Connolly and Mizue Hisano from James Cook University developed an approach that tracked the fate of the offspring across to two generations (since the number of "grand-offspring" to achieve maturity is a good measure of fitness), which, importantly, allowed to distinguish between direct and indirect benefits (a problem in previous works) to help clarify which ones are relevant to the females.

The study was done in Trinidadian guppies, a small and colourful freshwater fish where multiple mating is common among both sexes, and females often initiate polyandry despite the males bringing nothing (no help) but sperm to reproduction. They are also easy and fast to breed what helps.

Barbosa and colleagues started by mating females with either one or multiple males, and following the results for two generations looking at both their first offspring (their "children") and their second (the "grandchildren"). They discovered that polyandrous (multiple mating) females had about 1.5 more "grand-children" than monogamous ones. And more, that this was due to them having many more viable "sons" (first offspring), actually an extraordinary 83% more, than single mating females. Evolutionary theory predicts that when conditions are good females should invest more in the sex with greater variability, which in this case are males. After all males are not limited in number of children they can have (contrary to females), so more sons will mean extra number of descendants.

These two benefits - more descendants and an ability to change the sex ratio of the offspring - would be important "weapons" for the evolutionary success of females, helping to explain why they spend so much time and energy, risking infection or even predators' attacks, to pursue multiple sexual partners.  

Interestingly, Barbosa and colleagues found no differences between monogamous and polyandrous mothers, on those offspring characteristics linked to indirect benefits, such as size at birth, growth rate, time to sexual maturation and survival, contrary to previous studies. This, however, could be due to different environmental conditions- when not under of stress, animals tend to increase their overall numbers instead of changing their characteristics.

"Our results have broad implications for evolutionary studies and in particular for the evolution of female mating choice", says Miguel Barbosa, the first author of the work, "there is still the intrinsic idea that female reproductive success is independent of number of mates, but rather on the number of eggs fertilized. This idea follows the suggestion that females are the passive sex with a limited ability to change the course of the mating process. Our results together with previous studies, refute this idea, by showing that females are on the driving seat of the reproductive process and obtain direct fecundity benefits from mating multiply. "