Researchers have discovered that females with multiple sexual partners can be more fertile than those that are monogamous, and this because of an “overproduction” of sons.  The study,  published as a provisional article but already one of the most accessed in BCM Evolutionary Biology, helps to explain a puzzle haunting evolutionary biologist for decades: why so many females chase multiple sexual partners in a mating season, when this is costly and dangerous, and one is enough to fertilize all her eggs.

The discovery that the behavior increases their fertility (and allows them to change the offspring gender) can now explain why. After all, in evolution, success is all about passing one’s genes to future generations, and the more descendants you have higher are the chances of that to happen. 

 In the last decades scientists have discovered that multiple mating is widespread, even among those species once seen as the epitome of monogamy, like swans and penguins. And also that males and females both chase 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 case is very different. Not only they produce a limited number of eggs per breeding cycle 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?  Everything in nature is about costs and advantages, so a behavior, such as polyandry, is only be pursued if its benefits outweigh its costs. Ultimately, this means that it has to improve the individual (in this case the female’s) fitness (ability to pass its genes to future generations). And for polyandry there are two types of benefits possible: 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). The idea being that if one or both types compensate the costs of polyandry to females, then its persistence in nature can be explained. 

 And in fact several cases of female-initiated polyandry with indirect benefits (so leading to “improved” offsprings) have already been discovered, and some even believe that they are enough to offset polyandry costs. That , however, remains to proved. 

 And this is where 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 enter. They developed an approach to track the fate of the offspring across to two generations (since the number of “grand-offspring” to achieve maturity is an efficient measure of fitness), and which, crucially, distinguished between direct and indirect benefits (an issue not clear in previous works) to help clarify which ones are relevant to female polyandry. And used Trinidadian guppies, a small and colorful 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. 

Guppy male (Poeciliidae- Poecilia reticulata). Credit: Ciência Viva - Agência Nacional para a Cultura Científica e Tecnológica

 The researchers started by mating the females with either one or multiple males, and followed the results for two generations, looking at both their first offspring (their “children”) and their second (the “grandchildren”). And found that polyandrous (multiple mating) females were much more fertile than monogamous ones with about 1.5 more “grand-children”. And more, that this was due to them having much more, an extraordinary 83% more, viable “sons” than females with only one sexual partner. This agrees with evolutionary theory’s prediction that when conditions are good, females invest more in the sex with greater variability, which in this case are males. After all males are not limited in number of children (contrary to females), so more sons mean extra descendants. 

 These two discovered “paybacks” of polyandry – more descendants and an ability to manipulate the sex ratio of the offspring for their advantage – are be no doubt important “weapons” for the evolutionary success of a female and help to explain why they risk so much to chase even those apparently worthless guppy males. 

 But contrary to previous studies 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. This is probably due to different environmental conditions though, as when not under of stress, animals tend to increase their overall numbers instead of changing their characteristics.

 “These results have broad implications for evolutionary studies”, says Miguel Barbosa, the first author of the work, “there is still an intrinsic idea that female reproductive success is independent of number of mates,. This 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, and show the females on the driving seat of the reproductive process. “ 

Citation: Miguel Barbosa, Sean R Connolly, Mizue Hisano, Maria Dornelas and Anne E Magurran, 'Fitness consequences of female multiple mating: A direct test of indirect benefits', BMC Evolutionary Biology 2012, 12:185 doi:10.1186/1471-2148-12-185