Warring sexes


Both Twisty and Amanda seem a bit weirded out by this news that the fetus can be viewed as a kind of parasite. This story has been around long enough that a lot of us just take it for granted—I wrote about the example of preeclampsia a while back.

There are worse feminist-troubling theories out there, though. In particular, there is the idea of intersexual evolutionary conflict and male-induced harm. In species where there is some level of promiscuity, it can be to the male’s evolutionary advantage to compel his mate to a) invest more effort in his immediate progeny, b) increase her short-term reproduction rate, and c) suppress her ability to mate with other males. After all, his optimal strategy is to flit from female to female, copulate, and put her to work producing his offspring. The female’s preferred strategy, on the other hand, is to take her time, maximize her lifetime reproduction rate, and select the best genetic endowment for her children.

i-329f38f05caa891197fa415a12401b11-adapt_counteradapt.gif

This sets up a cycle of counter-adaptations in the population. If a male acquires a mutation that increases his fitness at the expense of his mate’s—for instance, if some component of his semen works on her brain to suppress her interest in remating—it will spread through the population due to its positive effect on male fitness, even though it reduces female fitness. Subsequently, a female who acquired a counter-adaptive resistance to the male’s hormonal sabotage would have an advantage, and that gene would spread through the population, reducing male fitness by making them less capable of controlling female reproduction. Then, of course, males could evolve some other sneaky way of maximizing their reproduction rate—vaginal plugs, secretions that make the mated female unattractive to other males, proteins that put her ovaries into overdrive to produce more eggs now at the expense of the female’s long term survival.

It all sounds improbable and dystopian, but all of these mechanisms and more have been observed in that exceptionally promiscuous species, Drosophila. Drosophila seminal fluid has the property of reducing the female’s interest in remating, increasing her rate of egg-laying, and is also mildly toxic. Artificial selection in the lab can produce females that are resistant to the effects, and males that produce more and more potent semen to overcome their resistance, to the point where the line of “super potent” males, when crossed to unselected females, kill their partners with their ejaculations. There is literally a battle of the sexes in these species.

To speak up in my defense, though, not all males are evil exploitive pigs. The logic of this pattern of sexual competitiveness vanishes as species exhibit greater and greater monogamy—if you have only one mate, it is to your advantage to take good care of him or her, because a loss diminishes your reproductive fitness.


Rice WR (2000) Dangerous Liaisons. Proc. Nat. Acad. Sci. USA 97(24):12953-12955.

Rice WR (1996) Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381(6579):189-90.

Comments

  1. says

    …to the point where the line of “super potent” males, when crossed to unselected females, kill their partners with their ejaculations.

    Death by snoo-snoo! @.@

  2. says

    My favorite example is offspring size in viviparous animals, where it clearly benefits the male to have larger infants, even should they spring fully-formed from the womb like Athena and kill the mother, while the latter will obviously prefer moderation; result, a battle of the sexes where males pass on genes that increase size of offspring and females imprint the fuck out of them so they won’t be expressed.

  3. Mccavity says

    Or, as we at my lab love to say, she has a well differentiated germ cell tumor.

  4. says

    …to the point where the line of “super potent” males, when crossed to unselected females, kill their partners with their ejaculations.

    Sounds like Larry Niven’s “Man of Steel, Woman of Kleenex.”

  5. idlemind says

    Sounds like Larry Niven’s “Man of Steel, Woman of Kleenex.”

    I think the mechanism is more analogous to the development of pesticide resistance. Females better able to detoxify the semen are selected for, males secrete more toxin, lather, rinse, repeat. Nice demonstration of evolution in action. A question: if such a thing were to occur in nature, wouldn’t speciation result? I wonder how many new species have developed solely on the basis of such male/female competitive reproductive strategies?

  6. says

    … if you have only one mate, it is to your advantage to take good care of him or her, because a loss diminishes your reproductive fitness

    nevertheless, there have been recent assays of genetic composition in humans showing that large chunks of the population descended from one father. (there has also been at least one study i know which showed a sizeable portion descending from one mother, someplace in eastern Europe.) so, it matters what is being optimized here. sheer genetic survival implies one strategy, other criteria imply others.

    BTW, i don’t know if the explanation of pre-eclampsia in the NYT article, one based upon nutrients, is the whole story. there’s the observation from Steven Vogel in his Comparative Biomechanics that metabolic rates for fetuses differ in utero and outside. metabolic rates for small fry are nearly always higher than for big fry. Vogel sees the change from in utero to outside as following the change from being a part of the mom to not.

    but, hey, the magic of pregnancy is, too, why shouldn’t the fetuses be rejected by the mom’s immunse system? or is that well understood?

  7. Steviepinhead says

    ekzept:

    nevertheless, there have been recent assays of genetic composition in humans showing that large chunks of the population descended from one father. (there has also been at least one study i know which showed a sizeable portion descending from one mother, someplace in eastern Europe.)

    This doesn’t necessarily signify that the one father or one mother was gloriously promiscuous during his or her own lifetime. Given a few thousand years, virtually all human beings will be descended from the same set of remote ancestors, which is pretty much everybody alive several thousand years ago who has living descendants at all. The one-father, one-mother examples tend to be cases of direct descent in the male line or direct descent in the female line (because they are assaying gender-linked genes). If you remove that constraint, and if you go back enough generations (but probably no more than a couple-three thousand years), we all turn out to be descended from, not just these past notable figures, but also from almost everybody else who was alive at the same time! http://www.slate.com/id/2138060/?nav=tap3.
    If it didn’t work like that, the fitter alleles wouldn’t be able to spread throughout the population so effectively.
    This isn’t to say that a given “reproductive strategy” isn’t a major assist toward having any descendants a few generations down the line…

  8. says

    I mostly think it’s nifty, truth told. I’m fascinated by the way that humans can’t help but put motivations to these things when they evolve brainlessly for no ulterior reasons.

  9. Ken C. says

    I would be grateful for any explanation or pointers for something I’ve wondered about: why are there large males? Male lions may kill hyenas, but wouldn’t there be more food for females and cubs if the males were smaller? Although larger males are able to shove aside smaller males, does that help species survival? Aside from acting as genetic reservoirs for sexual reproduction, how do males aid fitness, generally? Why don’t more species have large females and tiny males, to the point that males are basically something females keep in their metaphorical back pocket?

  10. Steviepinhead says

    Yeah, it’s kinda cool how even brains can brainlessly evolve, consciousness can non-consciouslessly evolve, coolness can un-coolly evolve, and like all that there.

  11. says

    thanks for the explanation, Steviepinhead.

    regarding your flurry on how stuff “brainlessly evolves”, i’m increasingly coming to understand that there’s basic physics behind a bunch of it, like why you’ll never see intelligent, self-aware amoebae. or mice.

    that doesn’t make us superior. we’re just bigger.

    although, if we as a species ever do get beyond our parchocial interest in bashing each other’s heads in, there’s something to be said for being able to deal with threats to survival that no other species on the planet can hope to challenge, like incoming asteroids or comets.

  12. Steviepinhead says

    Well, it doesn’t hurt to be fast either. If ya see the comet looming, head for the horizon, pronto–the one over which lies the non-incoming side of the whole planet. And then hunker down, but not too close to a coastline, a cliff, or an incipient rift…

  13. fwiffo says

    A couple of the reasons that bearing children is so dangerous in humans has to do directly with a few of our particularly human adaptations, specifically, upright walking and our grossly inflated monkey heads.

    Another good example of this sort of thing occurs in lions. Males have some sort of imprinting that causes larger cubs, and females have a similar mechanism to counteract that. Tigers, having a totally different social structure, don’t have this particular arms race. Hybrids between the two species where the lion is the father (a liger) produce giant cats. If the tiger is the father (a tigon), the hybrid cubs are dwarfs.

  14. RyanG says

    Ken C, you re forgetting that all men are bastards.

    Having small males would benefit the species, but the biggest males often have the reproductive advantage. As you pointed out, the small males get pushed aside. What you forgot is that this means genes for large size are passed on, while the species-benefiting smallness genes disappear.

  15. Phoenician in a time of Romans says

    Then, of course, males could evolve some other sneaky way of maximizing their reproduction rate […] secretions that make the mated female unattractive to other males

    Around here, we call those “engagement rings”.

    Having spent some time yesterday with an infatuatee who was, herself, gushing over her current boyfriend, I can state that human pair-bonding mechanisms really suck when you’re stuck with them only half working.

  16. the amazing kim says

    That doesn’t make us superior. we’re just bigger.

    Wow, elephants must be really smart then. :)

  17. moioci says

    Not to get all nitpicky and stuff, but isn’t Drosophila a genus, and D. melanogaster the often-seen species? Not that biology professors should be held to a higher standard or anything…

  18. A says

    > To speak up in my defense, though, not all males are evil exploitive pigs.

    The phrase “evil exploitive pigs” implies some sort of motivation. But this post was purely about biological evolution that males and females have no control over. Further, there are examples of organisms where females have reduced the survivability of males – could we call female peacocks exploitative of males by forcing them to have large plumes of feathers, making them easy prey?

    On the other hand, I know some married men who have become shells of their former selves. (Might as well point that some women have exploited the monogamy situation.)

    > I would be grateful for any explanation or pointers for something I’ve wondered about: why are there large males?

    There are lots of cases of sexual dimorphism. Sometimes the males are very small (as in spiders), and sometimes very large (male gorillas are twice the weight of females). It can usually be traced back to social structure and competition between males.

  19. says

    Artificial selection in the lab can produce females that are resistant to the effects, and males that produce more and more potent semen to overcome their resistance, to the point where the line of “super potent” males, when crossed to unselected females, kill their partners with their ejaculations.

    I blame the Petri-archy.

  20. jayackroyd says

    It’s concealed ovulation in humans that makes me wonder about the male/female arms race.

  21. ceibatree says

    Two great books about this subject are:
    “Promiscuity : An Evolutionary History of Sperm Competition”
    by Tim Birkhead

    “The Red Queen: Sex and the Evolution of Human Nature”
    by Matt Ridley

  22. says

    Evolution before our eyes.

    Evolution in the males of India has produced a most curious behavior. When courting an attractive female, if the female spurns the sexual advances of the male or rejected his proposal of marriage, then male hurls acid into the females face. This instantly reduces this previously attractive female to a disfigured female with little chance of mating or reproducing. Thereby attractive females are not passing on their attractive genes, whereby the “acid throwers” are free to pass on their “acid throwing” genes. I’m surprised none of you scientist have observed this. Perhaps too many hours staring into the microscope?

    Shalom,
    Bro. Bartleby

  23. Bruce says

    I have a quick question about labwork: how do you get seminal fluid from Drosophila? I’m thinking tweezers won’t do it, but when I read PZ’s posts I’m often stumped by the mechanics.
    Western males use diamonds as vaginal plugs, right?

  24. says

    Doesn’t the child have an interest in the survival of the mother? For its own survival and the possibility of survival of shared genes in future siblings?

    Bruce, to answer your question, if you can get the old book, To Know A Fly, by Vincent Gaston Dethier, I strongly recommend it.

  25. Ken C. says

    RyanG:
    “Having small males would benefit the species, but the biggest males often have the reproductive advantage. As you pointed out, the small males get pushed aside. What you forgot is that this means genes for large size are passed on, while the species-benefiting smallness genes disappear.”

    I didn’t forget. Yes, the genes for large males would be passed on, but this would seem to be to the detriment of the species: if male lions were small and ate little, there would be more for females and cubs, and so such a kind of lion would propagate and spread faster and farther, wouldn’t it? Such males would provide the same genetic mixing mixing service as large males, of course. So the claim is: the selection pressure for large males overwhelms the selection pressure on the species as a whole? This seems a bit surprising.

  26. Chris Doyle says

    Ryan, evolutions works to the benefit of the individual, not the species – species benefit is incidental. Male Gorillas I believe when they gain dominance over another male, will do their best to kill any baby gorillas as they will be carrying the genes of the the previous dominant, and if they wait around till the females are receptive again they themselves may have been displaced. For the species (especially an endangered one) this is very detrimental, but that is the way evolution works.

  27. Torbjorn Larsson says

    “Doesn’t the child have an interest in the survival of the mother?”

    PZ’s link to preeclampsia discusses how a balance is maintained by a fitting level of maternal cooperation.

    “whereby the “acid throwers” are free to pass on their “acid throwing” genes”

    I don’t think anyone has seen such a simple connection between social behavior and genes. With one exception; it is generally known that web trolls with nationalistic and/or racistic expressions doesn’t mate well, since they obviously aren’t social and must spend their time caressing a keyboard instead. So their genes are junk(ed).

    “you re forgetting that all men are bastards.”

    Heh! But AFAIK, technically it’s the reverse. Women has to choose which X-cromosome genes to switch off IIRC, so they are all mosaics, ie mongrels, ie bastards. :-)

    OTOH in the intended sense, that makes men pure bastards. :-~

  28. says

    The problem, Tobjorn, is that these equilibrium points need to be predicted, not just observed, otherwise, it becomes a “just-so” story. What do we know about preeclampsia in other species? How does it square with e.g., bears
    http://www.mountainnature.com/Wildlife/Bears/BearReproduction.htm

    If the sow is not in peak condition at the onset of hibernation, her body will reabsorb the embryo and not give birth that year.

    ?

    Do bears suffer from preeclampsia?

  29. Niamh says

    Does this mean that the presence or absence of the father during pregnancy might affect the nature of the gene war (as presumably it says something about the nature of the relationship?)? And is there any way the maternal or fetal genes could detect that and respond accordingly– or is that a really stupid question?

  30. Chadwick says

    Niamh-

    A lot of the psychological work recently has focused on oxytocin as the “pair bonding” hormone. It doesn’t seem so far fetched that oxytocin could have a primary or secondary effect on the fetus (through less stress, etc.)

  31. says

    Are the following two made-up stories ruled out on theoretical grounds? Note that I’m not a biologist and cannot put in the right terminology, so please don’t quibble on those grounds.

    1. In mammals, fetal cells linger in the mother’s bloodstream after birth and help heal her wounds more rapidly that without them. Survival of the mother improves the chances of the survival of the offspring.

    2. In fly species X, the male insemination turns on production of a neurotransmitter so that the female fly is for a period of time, in a state of heightened sensory acuity. This state is not detrimental, merely energetically expensive, which is why the fly has not evolved to be normally in this state. This period of time of heightened acuity is roughly coincident with the average time between insemination and egg-deposition. Presumably the female is better able to evade predators during this crucial period.

  32. Torbjorn Larsson says

    “The problem, Tobjorn, is that these equilibrium points need to be predicted, not just observed, otherwise, it becomes a “just-so” story.”

    I can’t tell if that’s bothering professional biologists, or if they already have a theory that satisfies you. You have to ask them.

    Meanwhile, I will point out that it seems to me it’s most probable the mothers cooperation is controlled, since the immune system otherwise is controlled.

  33. Torbjorn Larsson says

    Oh, I forgot. Arun, that was an acute observation. I didn’t think of it concretely before you formulated the question.

  34. Ken C. says

    “Ryan, evolutions works to the benefit of the individual, not the species – species benefit is incidental. Male Gorillas I believe when they gain dominance over another male, will do their best to kill any baby gorillas as they will be carrying the genes of the the previous dominant, and if they wait around till the females are receptive again they themselves may have been displaced. For the species (especially an endangered one) this is very detrimental, but that is the way evolution works.”

    Surely evolution operates on many levels at once, hence altruism and sexual reproduction; it’s a question of which kind of selection pressure dominates. Suppose a breed of lions is created with tiny males. Such a breed would likely reproduce faster than current breeds, and so eventually wipe them out. On the other hand, among those tiny males, the larger ones might well be more successful in reproduction, and so males would evolve to be larger. So the idea seems to be that the selective pressure for large males is greater, in some sense, than for the pressure for overall species success. This seems to hold even for species, like lions, where the male contribution to care of offspring is minimal, or even negative. Do males of these species do *nothing* for the females and children, or otherwise contribute to species survival? I mean, besides kill the occasional hyena?

  35. says

    “Ryan, evolutions works to the benefit of the individual, not the species – species benefit is incidental.”

    The Redback spider willingly offering himself up as a living meal for additional mating chances and improved nourishment for the female is certainly not to the benefit of the individual.

    I’d say evolution works to the individual’s breeding success, and in that, there are multiple successful paths.

  36. chris doyle says

    Left wing fox,
    You are quite correct that was a sloppy way to say it I should have said to the indvidual’s genetic success….

  37. says

    Describing the balancing of resources in fetal development as a battle or conflict is awfully teleological. I’m surprised to find it in a serious biological discussion. What happened to all those evolutionary biologists who pounce on “X evolved Y” and point out that X did not evolve Y, but rather those X with attribute Y were more likely to contribute genetically to the next generation of X?

    After all, one could describe the workings of a bimetallic thermostat as a continuation of the age old war between the metals, with copper and tin and their different feelings about elemental fire.

  38. Torbjorn Larsson says

    “Describing the balancing of resources in fetal development as a battle or conflict is awfully teleological.”

    Huh? I don’t see the connection to a religious principle about purpose. Also, evolution are conflicts en masse (predation, sexual selection, …).

    And I don’t think it’s as simple as a conflict only. PZ’s link on preeclampsia discusses mother’s cooperation.

  39. Torbjorn Larsson says

    Oops, apparently I meant ”evolution are conflicts at large’. Idioms are not for idiots. :-/

  40. says

    Do bears suffer from preeclampsia?

    A PubMed search on:

    “Ursidae”[MeSH] AND (eclampsia OR preeclampsia OR pre-eclampsia)

    yielded exactly zero hits. Certainly for the species I am working on (Helarctos malayanus, the sun bear), I know of no reported cases, yet not enough is known about their reproductive biology to say they definitely do not. I’d be surprised if, even for the more-studied species (such as American black bear), there was enough information to definitively rule it out.

    There is precedent for it occurring in small carnivores (dog and cat), and rat models of the disease have been developed, so I’d be hesitant to say it can’t occur in bears, just that there are no reported cases.

  41. RyanG says

    Ken, male lions do hunt, so it’s not like they don’t contribute anything.

    I think natural selection probably works on the gene level, since it adequately explains individual, family, and species level selection that can be observed.

  42. Ken C. says

    RyanG:

    “Ken, male lions do hunt, so it’s not like they don’t contribute anything.”

    OK, that’s interesting. I assume you mean the ones that are with a pride, not the solitary ones. Factoring those in, is the contribution of males still positive?

    “I think natural selection probably works on the gene level, since it adequately explains individual, family, and species level selection that can be observed.”

    This is a fine point of terminology that I’ll keep in mind: you don’t say “selection working at the species level”, you “species level selection.” OK.

    One could also say that computers function at the transistor level, and that’s how a compiler works, or congress works at the subatomic level, and that’s how a bill becomes law. These things are true, as far as they go, but say everything and nothing.

  43. Caledonian says

    Factoring those in, is the contribution of males still positive?

    If it wasn’t, natural selection would tend to produce defense mechanisms for female lions. If the drain on the species became sufficiently great, they’d go extinct.

  44. Ken C. says

    If it wasn’t, natural selection would tend to produce defense mechanisms for female lions. If the drain on the species became sufficiently great, they’d go extinct.

    Well, yes, but natural selection also tends to produce offense mechanism for male lions, and evidently the drain on the species has *not* been *sufficiently* great. So these considerations don’t seem to say very much.