Why Female Promiscuity Makes Sense – And Yeah Even Swans And Penguins Do It
    By Catarina Amorim | December 2nd 2010 03:42 AM | 13 comments | Print | E-mail | Track Comments
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    After many years as a scientist (immunology) at Oxford University I moved into scientific journalism and public understanding of science. I am...

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    Contrary to what many of us would predict most female animals are not monogamous. Not even swans or penguins, those (supposedly) hallmarks of monogamy. Also surprising is the evidence that in most cases the female deliberately looks for the multiple sexual partners since female multiple mating (known as polyandry) is costly, risky and seems to bring no benefits to the females involved.

    But two elegant studies in guppies by Miguel Barbosa and colleagues from the Gatty Marine Laboratory, at the University of St Andrews, Scotland are finally shedding light on the mystery by showing that the progenies of polyandrous mothers are “better” adapted, with higher reproductive success than those from monogamous females. Since mothers and offspring share many of their genes this implies that the mother’s genes will also have a higher chance of passing to future generations – the sign of success in evolution – what can start to explain why so many females practice polyandry.

    The findings have implications in the way scientists see and study evolutionary processes; polyandry emerges as a potential mechanism for species evolution or even the creation of new ones, while females, no longer passive recipients of sperm, determine their own evolutionary success. The two studies, published in Environmental Biology of Fishes (1) and Journal of Evolutionary Biology (2) were done in collaboration with scientists at the James Cook University in Australia and the Universidade de Aveiro in Portugal.

    The reason why female species routinely mate with several partners and, apparently, are often the ones initiating the behaviour has been under debate for years. To males multiple mating makes sense because the more descendants they have higher are the chances that their genes will survive in the future. The same does not apply to females that have a limited number of descendants in each breeding cycle. More, multiple mating spends time and energy, which are always in short supply, carries risks from predators’ attacks, disease or even sexual violence and except for the sporadic case - like when the male is eaten during copulation providing nutrients to the future mother (…) - seems to bring no direct advantages to females. In conclusion, the reason why females would pursue polyandry has been a mystery.

    It is in the context that Barbosa and Magurran decided to look at polyandry in Trinidadian guppy. Male guppy (Poecilia reticulata)This small colourful freshwater fish is an ideal model to investigate the reasons and consequences of polyandry as it lives in a promiscuous mating system where multiple mating is common - 95% of all progeny produced in a population have more than one father. Also, despite intense sexual harassment - females receive on average one sexual attempt per minute (…) - female’s guppies are known to control paternity what have led scientists to suspect that they could also control polyandry.

    In their first study, now online in the journal Environmental Biology of Fishes, Barbosa started by testing if polyandry in guppies resulted simply from sexual harassment or if it could also be a female’s choice. This was done by releasing females into an environment where they had to choose between joining a single male or a group, which could be either composed of males or of females. This allowed researchers to distinguish if joining involved social or sexual reasons. And although females start by going for the isolated male, probably to assure fecundation, after a while they prefer the group of males what meant - since sexual harassment by males was inevitable - that they were courting multiple mating. With this very simple experiment Barbosa and Magurran were able to conclude that - despite no direct benefits and sexual harassment - female guppies actively chose multiple sexual partners showing that polyandry in guppies is, at least in part, the result of female’s choice.

    The next step was to understand why this occurred. Polyandry clearly gives evolutionary advantages to females or they would not pursue it, and since no direct benefits are seen then the alternative are indirect/genetic benefits. Indirect benefits occur if a female produces an offspring with high reproductive success because – since mother and descendants share genes – this increases the mother’s chance to see her genes in future generations (the mark of success in evolution).

    So in the second study, out in the November edition of the Journal of Evolutionary Biology, Barbosa and Magurran, together with colleagues in Portugal and Australia, compared the offspring from polyandrous (multi-mating) and monogamous females. And with the help of a novel statistical approach they were able to find that sons from polyandrous mothers were not only more colourful (a sign of attractiveness among guppies) but, more importantly, had higher variability of looks than the offspring of monogamous mothers, While more colourful/attractive males should copulate more, high variability is linked to of one of the oldest strategies in evolution called “bet-hedging” (better know as “don’t put all your eggs in the one basket”). “The advantages of a progeny with high variability - explains Barbosa – is to permit adaptation to different conditions but also to reduce competition between brothers improving their chances to survive and reproduce”. And the production of descendants with better odds of procreating and surviving, carrying the mother’s genes to future generations, can, at last, start to explain why female guppies chose the risky and costly business of multiple mating.

    Also important is the fact that Barbosa’ work introduces polyandry as a new mechanism for species to evolve, or even to create new ones, because, with polyandry as widespread as it is, this means a new look towards the evolution of many, many species. Finally and not less important – also because too often social movements root their arguments in what is supposed to be the “natural” behaviour – the work challenges the idea that females are passive recipients in a world of sexually aggressive males. As Barbosa puts: ”these results destroy the myth of the submissive female, no longer passive vessels these females are crucial to its own mating success and need to be considered as a relevant force when studying evolutionary processes”.

    1- Environmental Biology of Fishes, DOI: 10.1007/s10641-010-9721-y
    “Evidence of female-promoted polyandry in Trinidadian guppies “

    2- Journal of Evolutionary Biology, November 2010, 23 (11), 2442–2452
    “Effects of polyandry on male phenotypic diversity


    Gerhard Adam
    OK, I have to ask... what's the scientific basis for the following statement?
    Finally and not less important – also because too often social movements root their arguments in what is supposed to be the “natural” behaviour – the work challenges the idea that females are passive recipients in a world of sexually aggressive males.
    This sounds suspiciously like taking the polyandry examples and trying to extrapolate them into human social interpretations. 
    Mundus vult decipi
    The intention was exactly the opposite Gerhard and that was why also my natural is between "", the most bizarre arguments on monogamy (I remember the huge discussions on it when the march of the penguins was on our screens and how the church still uses it as an argument of the natural law of god), the role of women as passive partners etc keeps being justified by nature laws, my point was to counter-argue this idiocy in their own territory a kind of "so what now, hum?"
    1) Why put "promiscuity" into the title if it is about polyandry?
    2) "surprising is the evidence that ... are finally shedding light on the mystery ..." It is long known that such occurs e.g. among chimps for instance in order to stop males from killing offspring (keeps them unsure of who is the father) and other reasons. Not saying that there is no news in the articles, but it wasn't the big counter intuitive mystery you make it out to be.
    Nobody know what is polyandry Sascha and this is not a scientific article , people's intuitive perception of promiscuity is "to sleep around" and that is exactly what these females do and anyway polyandry is a promiscuous system Polyandry initiated by females is actually a big unknown and very difficult to prove so far, just read a few reviews on the subject and you will see. I don't know enough about non-human primates' structures to be able to argue with you properly but from a quick look around it seems that 1- what you refer is an occasional event, only new world monkeys use that as a more general rule and even those not always 2- chimps have a social structure and a level of development that always makes them particular examples within the biological rules. From what I know female-initiated polyandry have only been studied in insects because it's incredibly difficult to understand if polyandry is the result of sexual harassment or female choice. This research is so interesting because it manages to clearly make the distinction. If you read reviews on polyandry you will see that actually everyone disagree on if it's proved or not
    Just to clarify - New world monkeys have polyandry, nothing on if it's started by females or not- which is the important point
    Dear Sascha,

    As you said describing polyandry is far from being a novelty, since it has been more than 150 years since first described by Charles Darwin on Barnacles. Evidence for female promoted polyandry, on the other hand is rare. In particular in species where there are no direct benefits such ours, to my knowledge there have not been any reports of females driving polyandry. In this subject our study is without any doubts a novelty.
    Mating benefits from polyandry have been reported for many species, and it was beyond the scope of our paper to just describe benefits. Our aim was instead, of using a different statistical approach, to answer an intriguing question, do polyandrous females get indirect benefits. By shifting our analysis from the common mean testing to look at differences in variability instead, we were able to find that polyandry promotes phenotypic variability. To my knowledge there has only been another study that used variance to assess female mating benefits (Arnqvist, G. 1998. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393: 784-786). His study however, used only CV comparisons. We were, therefore, the firsts to use variability rather than an average approach to test for potential indirect benefits. Again, I think our study deserves some credit for this.
    Hope these justifications clarify your hesitations regarding our work. Please do not hesitate in contact me on in case you need more information on the two papers
    Best wishes,

    makes sense, the best "provider" isn't neccessarily the best "reproducer"

    a female has to do what a female has to do to get the best offspring and best provider for said offspring
    so, for a female to do this, it has to be sneaky

    Gerhard Adam
    ...makes sense, the best "provider" isn't neccessarily the best "reproducer"...
    Actually that statement makes no sense if you're applying it to biology and genetics.  After all, one would presume that the "provider" and "reproducer" are both heritable traits that would be reflected in the offspring (otherwise they are irrelevant traits and can be treated as random events).  If they are heritable traits, then it would be foolish for a female to mate with a "reproducer" simply to produce offspring that are poor "providers".  It's a genetic Catch-22.

    In fact, I suspect that polyandry will tend to occur when a female has the possibility of multiple eggs being fertilized and/or produces large numbers of offspring.  In both those cases, there would be an implicit benefit to ensure that every possible means were employed to maximize fertilized eggs that result in live birth.  In the case of large numbers of offspring, it may well be nothing more than "playing the odds", since large numbers of eggs are involved, having a diversity of "fathers" distributes the genetic odds of survival a bit more.
    Mundus vult decipi
    Steve Davis
    "...this implies that the mother’s genes will also have a higher chance of passing to future generations – the ultimate goal in evolution..." Catarina, Catarina, how could you? For a moment there I thought it was Richard Dawkins writing the article! Evolution has no goal; I think that possibly you meant "the ultimate goal of life", but that is not correct either. The goal of life is to produce or nurture life. And life does not require genes as a primary factor. God, I'm picky today! But Hey, you know it's my favourite subject!
    I will slap my hand for you Steve, I was thinking that you were very quiet actually
    Steve Davis
    Despite the comment I still enjoyed the article, thanks.
    Thanks Steve, and I did change the comment
    Steve Davis
    You've nailed it now!