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The Myth of Monogamy
Fidelity and Infidelity in Animals and People
David Barash and Judith Lipton
In 1960's US successfully eradicated screw-worm by sterilizing millions of males, dropping them over mating grounds. But this was the sole success for the tactic. Screw-worms almost only insect species which is monogamous. All others mate with several males, so even with overwhelming numbers of steriles, takes just a few successful matings to keep the cycle going. This was a landmark insight - already knew that males liked multiple mates, but now it turned out that females did too.
Biologists traditionally assumed that because species appears socially monogamous, that means that they are sexually monogamous as well. But not the case. In fact EPC Extra Pair Coupling overwhelmingly the rule. When migrating birds trapped and tested, found that 25% of females already carrying sperm even before reached breeding grounds and selected a mate.
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Of the 4000 species of mammals, no more than a few dozen form pair-bonds.
Standard behaviour seems to be maintain a pair bond with a female, and help her raise offspring, but be ready and available for additional copulations as opportunity arises.
There are some species with reversed sex roles - where the female is colorful, aggressive and/or promiscuous, and the male is drab, coy and sexually choosy. In some insects the male produces a huge high protein jelly which the female devours after sex. She actually gains more calories than she expends producing eggs. So, not surprisingly, it is the male of this species who says "No".
Most men understand other men wanting sexual variety, even with the best wife at home. But few females understand why a happily married man would want to stray.
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NZ stitchbirds unique in that copulate face-to-face - the only bird known to do that. Very localised population on Titiri Matangi bird sanctuary in Hauraki Gulf, so able to get DNA sample from every bird. Form pair bonds, but males heavily over-represented (by about 3:1 in one year of the study) so lots of 'floaters'. Turned out 80% of nests had eggs fathered by a floater.
Dungfly females lay their eggs in fresh cowpats. Male dungflies hang around the cowpats waiting for females. She arrives having already copulated and having enough sperm to fertilize her eggs. Yet she copulates again, apparently because the male will guard her (for a whole 20 minutes) while she lays her eggs, sparing her harassment from other males.
Some extreme mate guarding tactics in nature - beetles where male dies and leaves half his abdomen stuck over the female tract, or insects which remain locked in coitus for weeks. Irony is that mate guarding only needed if the males go round looking for extra sex. If a male is out gallivanting for strays, that means his mate is unguarded. Rather cruel field biologists capture males and isolate them from their mates, then watch to see whether the unguarded females are taken advantage of. Sure enough, if removed when female fertile, intrusions shot up. But if removed when incubating, and no longer fertile, none. But the intruders rebuffed by female unless they were in better body shape than the removed mate, which suggests that the female has a lot of say in whether EPC's take place.
Two groups of gibbons met - alpha male of group 1 distracted by a scrap with a sub-adult from group 2. While that was going on, the alpha male from group 2 rushed in and copulated with the female in group 1 harem who was in heat. Perhaps that is why the sub-adults are tolerated - for their team work diversionary skills.
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Type of swallow called purple martin, older birds monopolized early mating opportunities. But once their mates were incubating eggs, the dominant martins encouraged younger birds to set up house in nest-boxes nearby, where before they'd been fighting them off. But once the younger males had set up shop with mates, the older birds muscled in with so many EPCs that they fathered 70% of chicks in new nests.
Male birds that are cuckolded lose twice. They are rated as lower quality, so their mates available if a higher quality male appears. And because they are lower quality, other females are not interested in them for EPC's. (And their much more assiduous mate-guarding is also obvious).
Males have strategies to counter EPCs. Many species, including most mammals, part of the sperm coagulates into a rubbery plug. Possibly stops sperm leaking out, but more likely to stop other males. Such devices would not be necessary if females were not inclined to mate with multiple males.
Grevy's zebras females will mate with multiple males, except when they have a foal and a male controls a reliable waterhole, in which case they will become monogamous.
Galapagos hawk unusual in that up to 5 males will bond socially and sexually, with one female. As soon as one male copulates with her, the others quickly line up to do the same.
Penis not just for inserting sperm - also, in some like black-winged damselfly, it has so many lateral horns and spines that it looks like a scrubbing brush, and the male scrapes out most of competitors sperm before depositing his own.
Rape clearly apparent in many species, including mammals and other primates. Bird studies show that younger, less desirable birds are likely to be cuckolded by older, more desirable birds, but because of their lower rank, don't get chances for ECPs themselves. So they force sex, often in gang rapes.
For reasons that are not clearly understood, it seems that there needs to be millions of sperm available for fertilization to be likely. If a man produces "only" 10 million sperm per ejaculation, he is considered sterile.
Socially monogamous female animals have same 'supermarket' problem that human females have. The best female gets the top male, and all the rest have to 'settle' for less desirable mates. She will get a nesting territory and fertilized eggs, but her offspring not optimum. So she has an incentive to stray. But she rarely chooses a bachelor, because logically he is less desirable: she chooses someone else's mate. This is why makes sense for females to congregate together in one mating area - they can assess competition even after chosen a mate.
So what bird studies showed was that females mated to alpha male never strayed, and those who did, had EPC's with older more desirable birds. In other words, ring for better genes rather than just a random bit on the side.
In species where female tends to have multiple partners the males have longer penises. But in species which have internal fertilization, the penis is never long enough to directly reach the eggs. To get there, sperm must undertake a long difficult journey in a hostile environment - cilia beating in opposite direction, acidic vaginas, elaborate upstream routes, and even when get there, an egg which is difficult to penetrate.
If a female was always mated with just one partner, it makes little sense to put the sperm through such a rigorous stress test. o payoff in making life difficult. But if she has multiple mates, makes evo sense to try to 'choose' the fittest sperm .
External fertilization poses its own challenges: how to get sperm to the eggs before gets washed or blown away. A species of catfish, Corydorus aenus, practices a unique form of oral sex. Female drinks the male's sperm, which then passes rapidly through digestive system and is excreted at same time as she lays her eggs, into a protective space she creates with her fins.
Species which are polygamous all have females maturing before males, presumably because males need to delay until bigger, stronger and smarter (the ones who started looking for sex too early presumably killed off by older competitors). Another clue is male violence, which only appears when mate-guarding necessary, which itself only when females stray unless guarded.
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