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    Girl Power In The Animal Kingdom: Females Can 'Choose' The Sex Of Offspring
    By News Staff | July 10th 2013 06:33 PM | 18 comments | Print | E-mail | Track Comments

    An unknown physiologic mechanism of evolutionary biology has been the ability of mammals to manipulate the sex ratios of their offspring as part of a highly adaptive evolutionary strategy. A new paper analyzing 90 years of breeding records from the San Diego Zoo says that mammalian species can "choose" the sex of their offspring in order to beat the odds and produce extra grandchildren.

    The scientists assembled three-generation pedigrees of more than 2,300 animals and found that grandmothers and grandfathers were able to strategically choose to give birth to sons, if those sons would be high-quality and in turn reward them with more grandchildren. The process is believed to be largely controlled by the females, said Joseph Garner, PhD, associate professor of comparative medicine at Stanford University School of Medicine and senior author of the study. The results applied across 198 different species.

    The paper supports a hypothesis first proposed in a 1973 paper by scientists - who would come to be called evolutionary sociobiologists - Robert Trivers and Dan Willard. They disagreed that sex determination in mammals is random, with parents investing equally in their offspring to generate a 50-50 sex ratio in the population. Instead, they hypothesized that mammals are selfish creatures, manipulating the sex of their offspring in order to maximize their own reproductive success. Thus, parents in good condition, based on health, size, dominance or other traits, would invest more in producing sons, whose inherited strength and bulk could help them better compete in the mating market and give them greater opportunities to produce more offspring. Conversely, mothers in poor condition would likely play it safe, producing more daughters, whose productivity is physiologically limited.

    Other hypotheses make similar predictions — that females who choose mates with particularly "good genes" (e.g. for attractiveness) should produce so called "sexy sons" as a result, Garner said.

    "This is one of the holy grails of modern evolutionary biology — finding the data which definitively show that when females choose the sex of their offspring, they are doing so strategically to produce more grandchildren," said Garner. "You can think of this as being girl power at work in the animal kingdom. We like to think of reproduction as being all about the males competing for females, with females dutifully picking the winner. But in reality females have much more invested than males, and they are making highly strategic decisions about their reproduction based on the environment, their condition and the quality of their mate. Amazingly, the female is somehow picking the sperm that will produce the sex that will serve her interests the most: The sperm are really just pawns in a game that plays out over generations."

    The hypothesis was also supported in 1984 in a Nature paper by T.H. Clutton-Brock at the University of Cambridge, who found that among wild red deer, dominant mothers produced significantly more sons than deer who held a subordinate position within the herd.

    "This paper was a huge leap forward, providing the first suggestion that the idea might work in mammals," Garner said. "But because it relied on data from only two generations, it couldn't show whether females that produced more sons also gained more grandchildren from those sons."

    This key prediction of the hypothesis remained untested, because complete three-generation pedigrees are so hard to obtain in the wild, Garner said.

    So Garner and colleagues reconstructed three-generation pedigrees of multiple species. They turned to the San Diego Zoo, enlisting the help of animal-care supervisor Greg Vicino in combing through decades of records on more than 38,000 animals from 678 species. The project was labor-intensive, requiring years of work to reconstruct the pedigrees and breeding histories of the animals.

    The researchers ended up with a pool of 1,627 granddams (female grandparents) and 703 grandsires (male grandparents) for whom they had a complete record of three generations. Major mammal groups were represented, including primates; carnivores, such as lions, bears and wolves; cloven-hoofed animals, such as cows, buffalo and deer; and odd-toed grazing animals, such as horses and rhinos.

    They found that when females produced mostly sons, those sons had 2.7 times more children per capita than those whose mothers bore equal numbers of male and female offspring.


    Grandparents who bias the sex of the offspring, have more successful offspring, gaining more grandchildren. A) Granddams and B) grandsires who biased birth SR towards males had greater total success measured as total grandchildren produced (P<0.0001; P = 0.0108, respectively). Birth SR is shown as a Z-score, to control for number of F1 offspring (the X-axes also give examples of male biases for a given Z-score). C) Granddams, and D) grandsires, who biased birth SR towards males had greater success specifically via F1 males (for both, P<0.0001). E) Granddams who biased birth SR towards females had greater success specifically via F1 females (P = 0.0272), but no effects were found for female-biasing grandsires (P = 0.9426), (nor did they have more total grandchildren overall; see text). For clearer data visualization, the data were split into 10th percentiles by Z-score, and plotted values are least-squares means and standard errors within those percentiles. The solid line indicates the least-squares regression line partialled for the controlling variables. In A and B, the Y-axes shows F0 success as total grandchildren born. In C–F, granddam and grandsire success is shown as the grandchildren (F2) born per each of their F1offspring born of a given sex (i.e. the mean reproductive output of the F1 children of each sex). doi:10.1371/journal.pone.0067867

    "The question is, within each species, among females who had more sons, did those sons do better in terms of producing more grandchildren per capita? And the answer is yes," Garner said. "Females are choosing and being very Machiavellian about it. They're doing it for their own benefit."

    The same was true of grandsires, with the researchers showing that when grandfathers produced mostly sons, those sons on average had 2.4 times more children per capita.

    "A grandfather producing more male offspring also has more success. But that could be entirely determined by the female," as she may be deciding the sex ratio to produce based on the quality of the male, Garner said.

    He compared the mating gambit to a kind of gambling game. "I'm gambling on how many grandchildren I'm going to produce. If I'm producing nothing but daughters, I'm making a safe bet — I'm going to make the average."

    Sons, on the other hand, are a "high-risk, high-reward bet." If an animal produces a fertile, high-quality son, in effect it has hit the jackpot in terms of reproductive potential.

    "Think about lions," Garner said. "Most male lions don't reproduce. There may be 10 or 15 females but only one male that fathers everybody. The same is true with baboons. There is one alpha male. If you are the parent of that harem-holding male, then you have hit the genetic jackpot because he might produce tens or hundreds of offspring. If you have a bachelor male, who never produces offspring, he produces zero. So males are a high-risk, high-payoff bet. Who would take the bet unless they knew they could rig it?"

    But how, in fact, do parents manipulate the sex of their offspring? Garner said the mechanism isn't really known, though one theory holds that females can control the "male" and "female" sperm, which have different shapes, as they move through the mucous in the reproductive tract, selectively slowing down or speeding up the sperm they want to select. There are some notable examples of sex-ratio manipulation in the insect world; for instance, yellow dung flies, who engage in an elaborate mating game, collect sperm from different mates and then selectively choose the "best" sperm for the environmental conditions (dung) of each clutch of eggs laid, he said.

    Garner said there may be some parallels among humans, with some studies suggesting that they may be able to adjust their sex-ratios in response to social cues. For instance, in polygamous societies, the top-ranking wife is much more likely to have a son than the lower-ranking wife (the son holds the economic power in the family). And a study of 400 U.S. billionaires, published in 2013, found that they were more likely to have sons than daughters — presumably, the scientists hypothesized, because sons tend to retain the family's wealth.

    Garner's personal favorite is a study published in 1988. It found that mothers with an inherited speech disorder had three times as many sons as daughters, in theory because a son with a speech impediment would have an easier time finding a mate than a speech-impaired daughter, whose success is more dependent on speech and social skills, Garner said.

    Garner said their study emphasizes the huge research potential of zoo data. "The temptation might be to assume that data from captive animals in the zoo has inherent problems," he said. For instance, zoo animals are subject to managed breeding, with less opportunity to select mates. Moreover, females in the wild rely on environmental cues to tell them to produce sons or daughters, but these cues may be misleading among animals in captivity, he said.

    "You would think that all of these conditions would hide the result, so the fact that females can still manipulate their sex ratio to produce an advantage despite the zoo environment makes the data even more convincing," Garner said. In fact, the study raises a concern that captive populations may be under threat, as the disproportionate success of certain individuals means that genetic variability is lost from the population faster than expected, the researchers note.

    Lack of genetic diversity can promote inbreeding-related health problems and a population's overall vulnerability to diseases and parasites. A better understanding of sex-ratio manipulation in captive animals could help lead to interventions that would help preserve the species, they conclude.

    Citation: Collette M. Thogerson, Colleen M. Brady, Richard D. Howard, Georgia J. Mason, Edmond A. Pajor, Greg A. Vicino, Joseph P. Garner, 'Winning the Genetic Lottery: Biasing Birth Sex Ratio Results in More Grandchildren', PLoS ONE 8(7): e67867. doi:10.1371/journal.pone.0067867


    Comments

    Gerhard Adam
    Why does this sound like gibberish?
    They found that when females produced mostly sons, those sons had 2.7 times more children per capita than those whose mothers bore equal numbers of male and female offspring.
    ?????
    "A grandfather producing more male offspring also has more success. But that could be entirely determined by the female," as she may be deciding the sex ratio to produce based on the quality of the male, Garner said.
    ?????
    Mundus vult decipi
    Hfarmer
    The thing that doesn't make total sense to me is the sexy son hypothesis.  It only makes sense if a woman chooses one kind of man to have sons with and another to have daughters with.  

    Other hypotheses make similar predictions — that females who choose mates with particularly "good genes" (e.g. for attractiveness) should produce so called "sexy sons" as a result, Garner said.


    What if you have daughters anyway?  What makes a son sexy tends to make a daughter homely. 
    Science advances as much by mistakes as by plans.
    Hank
    The children of Angelina Jolie and Brad Pitt are doomed to look like Quasimodo.
    Hfarmer
    Or to come out with Brads face and Angelina's body or vice versa.   I have seen some "beautiful" couples have really homely kids.   I won't name names that wouldn't be good manners.  
    Science advances as much by mistakes as by plans.
    rholley
    Talking of “naming names” suggests that your are referring to persons in the public eye, such as are called celebrities.
     
    One celebrity mag showed 30 female celebrities without their make-up, compared with their usual glossy presentation.  They looked like quite coarse.

    But then I don’t find them attractive anyway, however glossed up.
    Robert H. Olley / Quondam Physics Department / University of Reading / England
    Gerhard Adam
    Bear in mind that the "sexy son" hypothesis is supposed to be generally applicable to all sexually reproducing animals where mate selection is a factor.  Given that we are quite ignorant about what females might find attractive, this seems to be quite a stretch.

    In humans it is largely irrelevant.  Despite many claims to the contrary, males are not nearly as prolific reproductively, so it would be hard to argue or quantify what would constitute a fitness advantage.  At best, most such considerations have only covered a few generations, which hardly qualifies as being biologically significant.  In addition, I'm not clear on why this is often expressed as a competition when it clearly is not.  After all, if one considers that any animal that is 100% successful [i.e. out-competing all others regarding fitness] will have few opportunities for survival, since all the available mates will be related, resulting in inbreeding.

    Mundus vult decipi
    'sex-ratio manipulation' - sounds like an extraordinary claim...Is this generally accepted in biology? Or this is still controversial?

    Hank
    It's not accepted, that is why they think they have something with this examination, but proponents say the original paper is one of the most important in 20th century evolutionary biology. Maybe one day it will be.

    Sentences like "Amazingly, the female is somehow picking the sperm that will produce the sex that will serve her interests the most: The sperm are really just pawns in a game that plays out over generations" are a yellow flag.  They looked at historical records from a zoo and drew a circumstantial conclusion.



    is not rewriting any textbooks but it's interesting data. Their claim that their paper proves "sex ratio manipulation is a widespread and highly adaptive evolutionary strategy in mammals" doesn't hold up. Yet.
    Gerhard Adam
    How they can claim to know who sired who?  They only looked at records, and if the animals were allowed to breed at will, then there's no way to establish history.  If the breeding was controlled, then the entire set of numbers is bogus [and it largely was].

    In addition, we now have additional "scientific" support that the rich are decreed to be so by natural selection.
    Humans in the highest economic bracket leave more grandchildren through sons than through daughters. Therefore, adaptive variation in sex ratios is expected, and human mothers in the highest economic bracket do give birth to more sons, suggesting similar sex ratio manipulation as seen in other mammals.
    http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0004195
    So, apparently natural selection and sex ratios can be influenced by your bank account. 

    Interestingly it appears that biology is sexist, by presuming that wealth can only be inherited by male offspring. 
    Mundus vult decipi
    Hank
     it appears that biology is sexist, by presuming that wealth can only be inherited by male offspring. 
    BOOMSTICK!


    Gerhard Adam
    Perhaps I should have specifically linked to this article "Chromosomes Are So 20th Century - Male Genes Really Determine Baby Gender, Says Study"
    The family tree study showed that whether you're likely to have a boy or a girl is inherited.
    Mundus vult decipi
    Hank
    I have a lot of articles in drafts that never got written because you do some work and nothing real ever comes of it. And one of them was a mailbag question about that paper, asking basically if anything more had come of it. So I decided to find out and wrote the author, etc., because I kind of want there to be something to it, like I am cautiously optimistic something may come of this one, but, nope, still nothing on the male genes determining gender thing.

    Statistics can do funny things, and even make for fun titles, but all alone they aren't where the Cadillacs are, scientifically speaking.
    Gerhard Adam
    Comments like this just raise eyebrows:
    If offspring sex can be manipulated, and a grandparent can predict the likely success of their offspring, then a grandparent can obtain a fitness advantage...
    It's questionable whether animals have the cognitive ability to perceive a future and yet, here we have the researchers assigning future predictive capabilities to grandparents.  Then after that, they presume that it is a conscious choice based on external cues, which then allows the egg to make the decision about which sperm is going to fertilize it?

    How exactly does that information get to the egg if a female's eggs are already established by the time she is born?

    Mundus vult decipi
    Hfarmer
    ....and the guy with the Boomstick got the hottest chick in that movie, at least for a while. 
    There is certainly something to this idea of sons leading to more grandchildren than daughters.  

    Historically Pocahontas had one known son by John Rolfe  (Perhaps one by her Patawomeck husband Kocoum)  Her son had two daughters by two different women  (Jane and Anne).  Their mother Jane may have selected for girls, by this theory, since colonial women were in short supply in the 1600's.  A man either found a Indian woman or, at that time before slavery as we think of it, convinced a black woman to be his consort, or bought a woman mail order with 100lbs or so of Tobacco.    Those daughters then had many sons... Pocahontas now has a number of descendants on the order of 100,000's.  

    We can also look at a human culture where, for better or worse, fathers sticking to one woman is now the exception instead of the rule*.  Among black people since desegregation and the great society it has become the case that the state can provide the bread.  So, unless a man keeps a woman very happy, she can just kick him to the curb.  Likewise many men don't even try to keep a woman long term.  This is spreading to other subcultures in the US and becoming normalized.  Who has the most grandchildren?  A woman who had a number of sons, or a woman who had a number of daughters?   That would be the study to do.  

    it would not surprise me if those women who have many sons do better in the long run genes wise.  It is then up to the women to choose what kind of men will exist in the future.  If we select for thugs for enough generations we can't be surprised if that's what we get.   

    Perhaps we will see a reversal of the millions of years long trend of women sexually selecting the mate who was most clever, usually taller and more upright standing?  Probably not. A population bottle neck, of some kind, will sort it out. 


    *Before then and quite ironically as older black people have pointed out adversity strengthened the family.  A man had to be around to stand up to marauding bands of hooded white men and provide sustenance for the family. http://www.youtube.com/watch?v=izy6BiCV3Nw  Now men are disposable, even the hot, smart ones are sometimes just used to provide sperm then chased off like a male Black widow fleeing before he gets eaten.
    Science advances as much by mistakes as by plans.
    Gerhard Adam
    Pocahontas now has a number of descendants on the order of 100,000's.
    But what does that supposedly mean?  To listen to many of these discussions one would presume that there must be some "Pocahontas gene" that is so important that it must be preserved.  Yet, I suspect that if one could take DNA samples of Pocahontas and compare it to all her descendants there would be few similarities. 

    The problem is that the argument is invariably based on the notion that genes are different enough that they somehow "strive" to be represented in the future, yet at it's absolute best, this could only apply to a few genes that are highly heritable.  It is no coincidence that the majority of our genes are shared between all manner of animals and therefore represent nothing unique with respect to heritage.

    So unless someone can identify why a particular gene is important enough to worry about passing it on, it's a specious argument.  In my view, the entire process is much simpler.  A greater number of offspring simply increases the probability that someone will survive into the future.  It's purely a population numbers game.  Obviously if there are important traits involved then they will become integrated into the population and can convey an advantage.  However, in most of these cases there is no fitness trait involved that could be claimed to provide some survival advantage.
    Mundus vult decipi
    Hfarmer
    But what does that supposedly mean?  To listen to many of these discussions one would presume that there must be some "Pocahontas gene" that is so important that it must be preserved.  Yet, I suspect that if one could take DNA samples of Pocahontas and compare it to all her descendants there would be few similarities.  
    Just using her as an example of a grandmother with a 12+ generation family tree that is well known and accepted (http://pocahontas.morenus.org/).  Queen Victoria's descendant tree would be just as instructive but as I am a American, and it's close to the 4th of July I went with what was close to home. :)   


    As for how much genetic influence Pocahontas, or any other grandmothers DNA could maintain over generations lets look at the evidence.  Take a look at this person.  Matoaka Whittle-Sims.  
    http://www.geni.com/people/Matoaka-Sims/6000000007445847485







    Looks pretty darn Indian for someone who's about 8 to 10 generations away from Pocahontas. That person was a descendant of Pocahontas on both sides of her family and was born in 1844. 

    http://www.victorianvilla.com/sims-mitchell/history/whittle_james.htm


    There is no ready data about Pocahontas's DNA.  However her people do have one trait which is heritable.  Consider that American Indians and Hispanics.  Both  are groups where there is a non-negligible amount of Amerindian heritage have very low rates of lung cancer compared to the general population.  (CDC statistics) Any genetic reason for this would probably confer resistance to other cancers as well, but not Smallpox. 


    So unless someone can identify why a particular gene is important enough to worry about passing it on, it's a specious argument. 
    Well, the reason is built really deep into our reptilian brain.  We want our genes to pass on more than anyone else's because back in the primordial oceans, if our fishy ancestors did not lay the biggest possible clutch of eggs all their children were eaten.   


    Most of mating behavior is unconcious.  Consider has a woman lover ever did any of these non obvious things to you.  http://femalebible.com/gospel-according-to-belinda/michael-12-marking-territory
    Science advances as much by mistakes as by plans.
    Gerhard Adam
    The problem with your example of lung cancer is that it isn't a fitness argument.  So, while there may be a trait that is perceived to convey some advantage, it has no biological relevance.  My point about Pocahonta's DNA is that there is clearly nothing special about it.  There is no group of individuals alive today that somehow has a fitness advantage that clearly distinguishes them from others.  It is all rather homogenous, so the notion that there's some special benefit doesn't follow.
    We want our genes to pass on more than anyone else's because back in the primordial oceans, if our fishy ancestors did not lay the biggest possible clutch of eggs all their children were eaten.  
    While that is certainly true for some animals, it isn't a trait that exists much outside of that realm.  This suggests that there was a greater evolutionary benefit to the "higher" animals in restricting their progeny and focusing more on providing resources to ensure survival.

    In addition, while it may be important to ensure the survival of one's offspring, the argument becomes less clear as to why it should be relevant to a great-grandparent [except as an aesthetic value].  Among humans we certainly have many cultural values that point to such a heritage, but it is a much more difficult argument to make biologically.
    Mundus vult decipi
    Hfarmer
    The problem with your example of lung cancer is that it isn't a fitness argument.  So, while there may be a trait that is perceived to convey some advantage, it has no biological relevance.  My point about Pocahonta's DNA is that there is clearly nothing special about it.  There is no group of individuals alive today that somehow has a fitness advantage that clearly distinguishes them from others.  It is all rather homogenous, so the notion that there's some special benefit doesn't follow.
    Your focusing a bit too much on Pocahontas.  She is an example of a specific person for whom a very detailed and generally accepted descendant tree can be found.   Just one American Indian.  



    A study of family trees like her's, or the lines of descent from other notable people like Queen Victoria, or Davy Crokett, could test what the article says in humans without having to perform an unethical experiment or even engage with a live human subject. 




    I also showed you CDC statistics which show the rates of lung cancer in various racial groups.  Hispanics and American Indians, both have lots of Native American ancestry, have significantly lower incidences of lung cancer.  
    It's not for lack of tobacco use, good diet, or access to health care.  (Perhaps Native descended people use Tobacco lightly, not so much chain smoking. That could be part of it.) 

    http://www.lung.org/stop-smoking/about-smoking/facts-figures/american-indians-tobacco.html

    http://minorityhealth.hhs.gov/templates/content.aspx?ID=6457 


    While that is certainly true for some animals, it isn't a trait that exists much outside of that realm.  This suggests that there was a greater evolutionary benefit to the "higher" animals in restricting their progeny and focusing more on providing resources to ensure survival.
    Some animals.... that would be all of the animals descended from an animal that laid large clutches of eggs in a predator filled marine environment...which is all animals now extant.   If an animal wasn't as prolific as possible then it did not survive.   This leads to a strong reproductive drive.  Even gay and lesbian people seek to reproduce, before invitro they did it heterosexually with or without being married etc. It is a drive that is deeper than sex.


    As for why a great grandparent or grandparent cares about having grandchildren it is the same reason they care about having children, to perpetuate themselves.  This is why grandparents invest in grandchildren and great grandchildren. 







    What does seem dubious about the work reported in this article, to me is just how on earth could a body reliably ensure a male vs female ratio of births?  I mean so what the female tenses their ..... muscles down there in a different way or something?  Ultimately wouldn't mens sperm evolve in a way to counter female sex selection by making sperm that are as well formed and similar as possible.  The sperm of males that are most likely to get through would be the ones that are not different in any way based on their having and X or Y chromosome.
    Science advances as much by mistakes as by plans.