One Weird Trick Female Animals Use to Control Who Gets Them Pregnant

By Kaitlyn Tierney | February 19, 2015 | 7:10pm

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Much like the United States Congress, the history of science is overwhelmingly white and male, and unsurprisingly, this has led to a pretty significant lag time in scientific understanding of things that relate to women. When it comes to animal sexual selection, we know a lot about how and why males compete for female attention, as well as about how sperm compete against each other for implantation, and about the adaptations male animals have involved to ensure their reproductive success (never forget: corkscrew duck penis).

But we know much less about the many ways that female animals protect their reproductive interests throughout the entire courtship, mating, and reproductive process. And so it may surprise you to know that one of the greatest examples of gendered political bias—former U.S. representative Todd Akin’s infamous “legitimate rape” comment—actually points to a grain of scientific truth.

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In other words, we can’t “shut that whole thing down” with our bodies, but some female animals can, and do.

This is a much under-discussed phenomenon: Some female animals can control their reproductive process after mating, even after sex with multiple partners. No matter the circumstances—whether their sexual act occurred after being chased down by a pack of male animals, or after choosing the male with the flyest mating dance—they can influence paternity clandestinely, all the while concealing their decisions from competing males.

This process is called cryptic female choice. (The term was first used in a 1983 paper by Randy Thornhill, and it’s decent tagline for Plan B, even.) It’s called “cryptic” because the influence exerted by the female is internal: the males don’t know they’re being shut down or rejected when she discards (or digests, or redirects, or blocks) his sperm.

For example, in the case of ducks, complex counter-clockwise vaginal structure (i.e., morphology) protects females from insemination during frequent, violent forced copulations. Without the repeated contractions and relaxation of her cloacal muscles—reserved for preferred males and consensual matings—males can’t achieve full penetration. (For more details on this phenomenon, check out this article, which is rife with the unintentional hilarity of researchers inverting duck penises into glass tubes lubed up with mineral oil.)

But morphology is just one of many internal mechanisms for cryptic female choice. These mechanisms vary widely, and are, in many cases, poorly understood. Historically, scientists have generally assumed that males who mated more with a given female sired more of her offspring. This assumption has remained unchallenged until somewhat recently—in part because researchers were limited to observing behavior. Zoological researchers, including notable awesome women Jane Goodall and Dian Fossey, would observe wild animal populations and take detailed notes. They’d try to track which animals mated with others and painstakingly record social interactions, but their explanations included as much assumption and guesswork as anything. Previously, if researchers observed a female mating with several different males, there was no way for them to know who “won,” in an evolutionary sense.

Thanks to modern innovations in population genetics and molecular biology, we’re now able to see that behavioral observations don’t tell the full story. In a recent study of bison at Fort Niobrara National Wildlife Refuge, researchers collected behavioral observations of breeding behavior among the herd and compared their observations with genetic paternity data from tissue samples. They found that, while some behavioral characteristics—things like dominance, overall copulation frequency, and age—were significant factors contributing to paternity, that observed matings had “no predictive power regarding likelihood of paternity.” None. Zero.

The way that scientists have been studying breeding success for 100+ years completely discounts any female post-copulatory role in reproduction, and the model is deeply flawed as a result. Beyond that, a recently published literature review indicates that male bias in evolutionary biology studies of animal genitalia has actually worsened since 2000, which seems to be a discriminatory practice in the field reflecting “enduring assumptions about the dominant role of males in sex.”

In his book Female Control: Sexual Selection by Cryptic Female Choice, William G. Eberhard provides a concise description of this bias: “Females are often assumed to be passive, and there is an overemphasis on male rather than female perspectives in many evolutionary interpretations.” Over the next 300+ pages, Eberhard describes the myriad aspects of reproductive biology that can be influenced by cryptic female choice—more than 20 specific mechanisms are described in detail, with numerous examples for each. And although it’s possible that male adaptations have evolved or will evolve to circumvent some of these mechanisms, Eberhard suggests that “the multiplicity of female mechanisms reduces the likelihood that males will be able to evolve overall control of female reproductive processes.”

In other words, evolutionary biology is still somewhat of an old-fashioned Cold War–style arms race, gender against gender.

Take the example of nature’s most vilified antagonists: bedbugs. As if they weren’t already horrifying enough, male bedbugs developed hypodermic insemination, i.e., the ability to inject sperm into the bodies of female bedbugs with syringe-like genitalia, in order to bypass the intermediate female sperm-handling structures. This proved to be effective, until females evolved a new set of structures with the ability to actually kill sperm.

This is another example of morphology, which isn’t designed to actively reject sperm or male advances, but rather to selectively accept them. When that selective ability is eliminated, as in the case of ducks or bedbugs, females evolve ways to regain a measure of control. As the following examples show, the possibilities for female control are sometimes bizarre, frequently fascinating, and found in all corners of the animal kingdom—including humans.

Sperm dumping

Sperm dumping is probably the least cryptic example of female choice, but most familiar to anyone who’s found themselves reaching for a cum rag after sex. “Flow-back” is the technical term for all the ejaculate that dribbles out after copulation, and how much control females have over the volume of flow-back is still up for debate, but some studies have found evidence of reduced flow-back when ejaculation immediately preceded female orgasm. Or, in Eberhard’s colorful words, “it appears that the male’s behavior during copulation and perhaps his morphology influences how much of his ejaculate is discarded in the flow-back soon after copulation ends.”

If we could somehow parlay that little biological boost into a full-fledged form of birth control, we could sexually select for men who are morphologically and behaviorally inclined to deliver orgasms to women. (I know that science doesn’t really work that way, but that won’t stop me from wishing for it.)

Not all mammals exhibit sperm dumping behaviors, and this can even differ between very similar species. While female Grevy’s zebras (Equus grevyi)—who sometimes mate with multiple males during estrous periods—seem to dump large volumes of sperm immediately after copulating, their monogamous sister species Equus burchelli do not. For other animals, with internal sperm storage areas, sperm dumping can happen at later points following copulation. It’s even possible for females of some species to dump stored sperm from previous mates after copulating with subsequent males.

Mating plugs

Males of many species place “plugs” after mating, blocking the entrance to the female’s genitalic opening—possibly to limit sperm dumping, or to prevent competing males from mating with her. These plugs vary in type from species to species, but generally contain some combination of ejaculate, mucus, seminal fluid and enzymes that promote coagulation. Whether or not the female animal removes those plugs (as well as when she removes them) are examples of cryptic female choice.

For example, female Sciurus squirrels use their teeth to selectively remove the plugs of some males immediately after copulation, while leaving others in place for several hours. Plugs in female paca Agouti paca are slowly expelled over many hours, and she just bends over and eats the material as it emerges.

(Plug play, so to speak, isn’t just limited to females: some male spiders evolved the ability to remove plugs of previous males; whether or not the female allows him to proceed with that is yet another choice she can make.)

Preventing ejaculation, sperm storage, or sperm transfer

Research around sperm competition typically emphasizes the male roles, looking at how subsequent males can displace or eliminate stored sperm from previous males. But it’s likely that female morphology, internal chemical signals from her storage organs, and behavioral characteristics (like contractions of muscles in her reproductive ducts) can all be contributing factors in sperm competition. Even the processes that lead to egg and sperm fusion in mammals are largely performed by the egg, with opportunities for female choice to be exerted at many points during the process.

Take insects, for example. Some males make sperm packets, called spermatophores, which they attach to her. Females then must transfer the sperm into their reproductive tracts, various storage organs, or fertilization sites. But sometimes, they fail to transfer a male’s sperm, or remove the spermatophore before sperm transfer is complete. (Sometimes, they eat it, which I guess might be the insect equivalent of a blow job.)

In order for male honey bees (Apis mellifera) to ejaculate into a female’s open sting chamber, she must open her internal valves, and it’s possible she may be responsible for triggering his ejaculation. Sperm transfer in rosechafer beetles is also dependent on the female to permit deeper penetration by males. And Caribbean fruit flies (Anastrepha suspensa) males produce a specific song during mating to woo the female into extending her ovipositor and permit penetration. Without her cooperation, he can’t navigate the tightly coiled S-curve of her vagina, so his courtship singing had better be impressive.

Failing to ovulate, mature eggs, or prepare the uterus

These cryptic female choice mechanisms are mostly unseen, but nonethelessremarkable. Females of several species of rodents can’t get pregnant by pump-and-dump: the female rodents must produce luteal hormones in order for the uterus to be ready for implantation—but first, males must perform a sufficient number of copulatory intromissions (thrusts, basically).

Essentially, he has to show her a good time before he can even think about getting her pregnant, while still trying to ejaculate before another male tries to interrupt.

Another example: female lions need roughly 25 months to raise a litter of cubs, from the time of conception—and in times of political strife, cryptic female choice can ensure they can have sex without ovulating.

This is how they do it. When a pride of female lions is taken over by a new male or group of males, the females will continue to copulate with the incoming males, but her body delays ovulation until the lion is confident that the new males can retain control long enough for her offspring to survive. By waiting until the dust settles and male dominance is established after a pride takeover, she can reduce the likelihood that her cubs will be killed by another incoming group of males before they reach adulthood.

Abortions

And here’s the last and most dramatic aspect of cryptic female choice: the spontaneous abortion. As a survival mechanism during lean times, or when resources are limited (droughts, limited food supply), some female mammals can abort zygotes rather than try to care for offspring when conditions would make their survival impossible. (The human analogy: irregular periods or temporary cessation of menstruation is a frequent side effect of anorexia, probably for similar reasons.)

Other animals can reduce the rate of births or number of offspring in response to threats, such as infanticidal males. In many rodent species, impregnated females abort their entire litters if they’re exposed to any unfamiliar males. Just the mere odor of a strange male’s soiled bedding is enough to block pregnancy in woodland voles Microtus pinetorum. Lemmings are famously equated with mass suicide, but even they know it’s better to safely abort than to watch one’s babies get eaten by a jealous male. In other cases, female animals have and use the choice to reproduce wisely, saving her resources and strength for potentially more viable babies at a later time.

Cryptic female choice is remarkable, and even a cursory exploration of it will show you that the only thing that’s cut-and-dry about female roles in reproduction is how little we know—and how much still remains to be discovered.

Additional sources:

• Ah-King M, Barron AB, Herberstein ME. 2014. Genital Evolution: Why Are Females Still Understudied? PLoS Biol 12(5): e1001851.

• Eberhard, WG. 1996. Female Control. Princeton University Press, p. 43.

• Baker RR, Bellis MA. 1993. Human sperm competition: ejaculate adjustment by males and the function of masturbation. Animal Behavior 46:861-885.

Kaitlyn Tierney (@krtierney) is a writer and editor, and former librarian for the San Diego Zoo. She’s overeducated and underemployed, and suffers from strident feminism and insatiable wanderlust.

Photo via Shutterstock.