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The Hidden Side of Sex

Sexual selection doesn’t end when females choose a mate. Females and males of many animal species employ an array of tactics to stack the deck in their reproductive favor.

By | July 1, 2014

© DONBANTUMPHOTOGRAPHY.COM

A female mallard duck feeds in a pond, her mate following closely. The pair has spent the winter together and is now searching for a nest site. Other drakes also feed and swim nearby, seemingly uninterested in the couple. Suddenly, an unknown male rushes the female, bobbing his head up and down. Her mate chases him, and she flees to the edge of the pond. Other males are drawn to the activity, and before long, the hen is mobbed by the group, despite her quacks and attempts to escape. The males grab her by the neck and forcibly mate with her, one after the other, while her partner watches helplessly from afar. (See photograph above.) He may have lost this battle, but, luckily for both him and his mate, the rogue males almost never win the long-term war to pass on their genes.

PENIS VERSUS VAGINA: The mallard duck penis (right) is a coun­terclockwise corkscrew-shape organ that can force itself into the female reproductive tract (shown dissected at left), which has blind pockets and clockwise spirals to block full penetration.PATRICIA L.R. BRENNAN As many as 35 percent of all copulations with a mallard female are forced by unwanted males, yet these males sire only 3 percent to 5 percent of her offspring.1 In mallards, reproductive success is not a simple function of mating frequency. Rather, female mallards have a say in which sperm fertilize their eggs. A convoluted vaginal anatomy can prevent a penis—which in mallards and other ducks is a long, counterclockwise corkscrew-shape organ that can explosively inseminate a female in less than a third of a second (see photograph at right)—from fully everting inside her oviduct. Specifically, blind pockets and clockwise spirals in the vagina can physically block a penis, causing the sperm channel that runs along the outside of the male organ to ejaculate to the side, rather than at the tip, far away from where the female reproductive tract stores sperm for fertilization. (See illustration.) Thus, drakes may be able to force female mallards into unwanted copulations, but females, it seems, have the final say. If the female is receptive to a male’s advances, contractions in the oviduct likely open up the lumen to allow the penis to bypass the barriers.

The ducks that I study are not the only animals to have evolved such elaborate genitalia in the name of reproductive control. In bed bugs, the male’s penis is a piercing needle used to stab the female and deposit sperm into her coelomic cavity. This reduces female control of where the sperm end up and gives males a reproductive advantage, often at the expense of female fitness. More recently, researchers described a genus of cave-dwelling barklice in which females have evolved a spiny, penis-like organ that is inserted into a vagina-like male receptacle in order to grab sperm packages known as spermatophores that provide not only sperm but also nutrients.2 (See “Geni-Tales.”)

TWISTED SEX: In mallard ducks, forced mating is common, with unwanted suitors forcing as many as 35 percent of a female’s copulations. But the battle for paternity of her offspring doesn’t end there. The female’s convoluted, corkscrew-shape vagina, which has numerous blind pockets, can prevent successful penetration by unwanted suitors, such that 95 percent or more of her chicks are fathered by her partnered male.
See full infographic: JPG | PDF
© CATHERINE DELPHIA
These and other amazing genital adaptations illustrate an evolutionary war that plays out during and after copulation. More often than not, female animals mate with—and collect sperm from—more than one male per reproductive cycle. As a result, competition for fertilizations is intense. Males try to fertilize more eggs by releasing more or faster-swimming sperm into the female, and/or by plugging her reproductive tract when they’re through. Meanwhile, females have evolved ways to use sperm from preferred males to fertilize their eggs by managing where and how sperm are stored, used, or disposed of. These tactical strategies—known as sperm competition and cryptic female choice, respectively—are at the root of a perpetual battle of the sexes.

Females in charge

When Charles Darwin developed his theory of sexual selection, he was unaware of these hidden reproductive battles. He envisioned a straight line connecting mating and reproductive success, with males competing and posturing to secure a reproductive encounter with a monogamous female. But in the last four decades scientists have discovered that, in most species, females mate with multiple males, and that paternity of offspring in a single brood is often mixed.

Although the trauma of mallard mating illustrates that promiscuity can sometimes be forced upon females, most examples of multiple mating by females are entirely volitional. A promiscuous female stands to gain direct benefits—such as extra paternal care, food in the form of nuptial gifts and access to a territory, or protection from other males—as well as indirect benefits for her offspring, such as better genes or greater genetic diversity to fortify her brood against unpredictable environmental challenges.

Females have often evolved sophisticated behaviors and morphologies to maximize the benefits they receive from multiple mates. For example, female chimpanzees often mate with both low- and high-ranking males to confuse paternity and reduce the chances that any male will kill her offspring. However, females mate more often with high-ranking males closer to estrus, increasing the chances that their offspring will inherit better genes.

Outside of behavioral adaptations that play out through copulation, the females of some species have evolved intricate sperm-storage organs that keep sperm alive. In many ants and other social insects, for example, the queen mates only once before going underground to start a colony where she will lay eggs for the rest of her life. Queens have specialized paired spermathecae that allow them to store viable sperm for decades. In other animals, such as bats, sperm can remain viable for several months, swimming in place along the walls of the female’s uterus.

SEX BOTH WAYS: Hermaphroditic flatworms engage in what’s known as reciprocal mating, in which two individuals will both inseminate and be inseminated simultaneously via the penetration of the stylet (flatworm penis) into the antrum (flatworm vagina). The worms are capable of sucking out the sperm following copulation, but some worms have evolved filamentous structures on the sperm heads help protect against such manipulation by anchoring the sperm inside the antrum.
See full infographic: JPG | PDF
© CATHERINE DELPHIA
Females can also eject unwanted ejaculates from their reproductive tract. In hermaphroditic flatworms, for example, a single worm will both inseminate and be inseminated by its partner, a phenomenon known as reciprocal mating. However, inseminated worms will often suction the sperm out of their female genital opening using their mouth when copulation is over.3 Some worms have also evolved countermeasures against such rejection: filamentous structures on the side of the sperm heads that anchor the genetic packages into the body cavity.4 (See illustration.)

Interactions between the two sexes and between competing males commonly occur after the pageantry of courtship and mating subsides, and the battles reach all the way down to the level of genitalia and gametes.

And even if females do end up using sperm from less-than-ideal males to fertilize their eggs, they sometimes seem able to cut their losses by investing less in those offspring, as seen in some birds. Mallard females, for example, lay smaller eggs when mated to less-preferred males, while female canaries deposit less testosterone in their eggs when exposed to less-attractive male songs. Females are not just the arenas where fertilization occurs, they are active participants with seemingly unlimited potential to influence the outcome of sex in different ways, and at different points during the reproductive saga.

The art of penetration

Females may actively seek out multiple mates, then pick and choose among them, but that doesn’t mean males don’t have a say in paternity, during and after copulation. In some taxa, males have elaborate copulatory displays to woo females. Genital structures of male tsetse flies, for example, rhythmically stroke the female while mating; experimentally altering those structures to prevent males from stroking results in reduced reproductive success.5 Even more intimate are the stimulations provided to the ridges of a sow’s cervix by the corkscrew filament at the end of the pig penis. Such stimulation helps a male secure paternity, and the artificial insemination industry has taken note, designing inseminating needles of a similar corkscrew shape.

Other features of male genitalia can also bring greater reproductive success. For example, male mice with a wider penis bone, or baculum, appear to father more offspring, while in many insects the length of penises, called aedeagi, is correlated with reproductive success.

PENETRATION TOOL: An everted and inflated rattlesnake hemipenis (yellow), its base covered in spines, laid on top of the female vagina and oviducts (white)PATRICIA L.R. BRENNAN Armored penises and detachable members work too. Like many snakes (see photograph here), male garter snakes have two spiky hemipenises that look a bit like medieval weapons and hook into the internal surface of the female’s vagina. This affords males a foothold to deposit a copulatory plug full of sperm, as well as proteins that make females unreceptive to further copulation for a few hours. Sever the big spines at the base of a male’s hemipenises, and copulation duration and plug size decrease significantly.6 In some spiders the male genitalia simply break off inside the female to plug her up, to the frustration of her subsequent suitors. This bizarre genital self-mutilation results from the very low probability that a male will ever be lucky enough to mate again.

But females do not take kindly to such manipulation, and have evolved countermeasures. Adaptations include thickened epithelia within the reproductive tract that minimize the damage penile spines can inflict; flaps and genital coverings that make penis intromission more difficult; and, in the case of the stabbing bed bugs, a whole new paragenital system that guides the penis to stab females in places where the damage will be limited. Some female strategies for thwarting sexual manipulation by the males are more subtle, such as the vaginal contractions of female garter snakes, which shorten copulation duration and may limit the damage inflicted by the male’s hemipenises. Further studies of variation in female physiology and morphology that can impact fitness will help us better understand postcopulatory selection, but for now this area of research remains in its infancy. (See “Size Matters.”)

Prodigious sperm

Even after coitus, the struggle for paternity continues. In species that practice internal fertilization, anywhere from hundreds to billions of sperm are cast into a novel molecular environment in search of ova. Each sperm vies for a coveted fertilization among a sea of its brethren in a chemical soup that can be downright lethal to the gametes, perhaps as part of the female’s plot to allow only the fittest sperm to reach her eggs.

For males, one way to get a leg up on the competition is to send in a stronger, faster, more resilient gametic army. When competition is high, producing more sperm is likely to be a winning strategy—it gives the male more tickets in the raffle. Accordingly, males of promiscuous species tend to have larger testes (in relation to body size) than monogamous animals. But most males don’t simply transfer as much sperm as they can all at once. Ejaculates are costly, and males must conserve their supply. Mating rate, mated status of the female, female identity, and female body size can all influence how much sperm some males are willing to relinquish during any particular copulation. Male chickens and their wild ancestors, red jungle fowl, will allocate less and less sperm to subsequent matings with the same female, for example, not because they are running out of sperm, but because they have already inseminated that female. Present a sex-weary cock with a new hen, and he ramps up ejaculate volume to high levels once again.7

Some species employ other sperm features to win fertilizations. Sperm are one of the most diverse cell types in nature. In some rodents, sperm have hooked heads that connect individual sperm to form a train. With tails beating in unison, hooked sperm swim faster and more quickly navigate to the site of fertilization.8 Amazingly, when female deer mice from a polygynous species—one in which males mate with several females in one breeding season—are inseminated with sperm from two males, trains form preferentially among sperm from the same male, even when those males were brothers. However, in monogamous deer mice, sperm-train formation is indiscriminate, demonstrating that sperm cooperation evolves only in species where sperm competition threatens a male’s paternity.9

More simply, sperm that live the longest and those that can swim fastest or farthest will generally outcompete other sperm. In both externally fertilizing species such as salmon and internally fertilizing animals such as birds, males with the fastest sperm sire the most young. Several bird species have evolved faster sperm cells that typically have longer midpieces, where the mitochondria are stored; longer flagella; and/or relatively small heads.

In addition to sperm, males transfer seminal fluid or other substances that can aid in fertilization. Not only do these secretions provide nourishment for the sperm cells and thwart the females’ immune defenses, but the ejaculates of males of some species, including salmon and some social insects, also inactivate sperm from other males, bettering their own chances of paternity. (See “Semen Says.”) Accessory proteins have been identified in the ejaculate fluid of many species, including humans. In Drosophila these proteins have been well studied, and researchers have shown some of them to increase females’ egg-laying rate at the expense of her survival. And in an even more dramatic example of chemical manipulation by sexual partners, some hermaphroditic snails shoot their mates in the head with a “love dart” prior to copulation. The dart is filled with mucus that makes it less likely that the shot snail will mate again, thereby increasing paternity for the shooter.10

Females are not just the arenas where fertilization occurs, they are active participants with seemingly unlimited potential to influence the outcome of sex in different ways, and at different points during the reproductive race.

Once again, however, females are not passive observers of sperm’s hustle to fertilize. In many species, females have factors in ovarian fluid that are needed to activate sperm; in others, such factors protect sperm from the murderous attacks of their competitors’ seminal fluid. And female Drosophila can employ damage-control mechanisms that limit the influence of seminal proteins, though the mechanisms are still under investigation. We know that when females evolve under monogamy for many generations, they will die sooner when mated to a male that has evolved under polygyny than when mated to a monogamous male. This is because monogamous females have not coevolved any defenses to protect themselves from male adaptations to competition.

It’s becoming increasingly clear that the evolutionary forces of sexual selection are not limited to male ornaments, courtship displays, and fights, and that females are as active as males in determining the fate of their eggs. Interactions between the two sexes and between competing males commonly occur after the pageantry of courtship and mating subsides, and the battles reach all the way down to the level of genitalia and gametes. Adaptations include anatomical, physiological, and chemical changes that have been found in virtually all taxa that scientists have investigated, and there are no doubt many more surprises waiting to be discovered. These sexual features are likely as ubiquitous as they are bizarre. 

SPERM RACE: Fluorescently tagged sperm swimming inside the lower reproductive tract of a Drosophila simulans female, who mated first with a D. mauritiana male (orange sperm heads), followed by a D. simulans male (blue-green sperm heads). The sperm migrate to the female’s specialized sperm-storage organs: the seminal receptacle (tubule, upper right) and a pair of mushroom-shape spermathecae (at far right). In these organs, sperm can remain viable for weeks or months, or can be displaced by the sperm of a new suitor as the female remates.JOHN BELOTE, MOLLIE MANIER, AND SCOTT PITNICKVISUALIZING SPERM WARS

Though it is difficult to see what goes on inside a female fruit fly after copulation, recent genetic advances have allowed scientists to image sperm competition inside storage organs—the seminal receptacle and spermathecae—of female Drosophila melanogaster. Scott Pitnick, Mollie Manier, and John Belote of Syracuse University and colleagues genetically engineered flies to express red or green fluorescent protein in sperm heads. By mating males of each fluorescent color to a single female, the researchers could visualize how sperm behaved and were displaced inside the female sperm storage organs during sequential copulations.1

The research yielded striking microscopic images and revealed that Drosophila sperm behave in active and complex ways. For example, sperm can form helical aggregations inside the female seminal receptacle that may help them move more efficiently. The researchers have witnessed firsthand how sperm from a mating with one male are displaced by a second male’s ejaculate—and how some ejaculates resist displacement better than others.

Furthermore, females are able to eject sperm from their reproductive tracts and selectively draw sperm from the spermathecae and the seminal receptacle for fertilization. More recently, the team showed that females discriminate against sperm from different species,2 and that sperm from males of the same species outcompete heterospecific sperm, suggesting that sperm selection can be involved in speciation.3

Other model systems are emerging that use the same sperm fluorescence technique, such as in a flour beetle, Tribolium (also at Syracuse University), and in the transparent hermaphroditic flatworm Macrostomum lignano (at the University of Basel). Many novel insights are sure to be gained from comparative observation of sperm behavior inside the female reproductive tract.

  1. J.M. Belote et al., “Opening a window onto sperm competition,” Mol Reprod Dev, 80:79, 2013.
  2. S. Lüpold et al., “Female mediation of competitive fertilization success in Drosophila melanogaster,” PNAS, 110:10693-98, 2013.
  3. M.K. Manier et al., “Postcopulatory sexual selection generates speciation phenotypes in Drosophila,” Curr Biol, 23:1853-62, 2013.



Patricia L.R. Brennan is a research assistant professor at the University of Massachusetts Amherst who studies sexual selection and sexual conflict in vertebrates.

References

  1. P.L.R. Brennan, R. Prum, “Sexual conflict in the narrow sense: New insights from waterfowl biology,” Phil Trans R Soc B, 367:2324-38, 2012.
  2. K. Yoshizawa et al., “Female penis, male vagina, and their correlated evolution in a cave insect,” Curr Biol, 24:1006-10, 2014.
  3. L. Schärer et al., “Mating behaviour of the marine turbellarian Macrostomum sp.: These worms suck,” Mar Biol, 145:373-80, 2004.
  4. L. Schärer et al., “Mating behaviour and the evolution of sperm design,” PNAS, 108:1490-95, 2011.
  5. R.D. Briceño, W.G. Eberhard, “Experimental modifications imply a stimulatory function for male tsetse fly genitalia, supporting cryptic female choice theory,” J Evol Biol, 22:1516-25, 2009.
  6. C.R. Friesen et al., “Sexual conflict over mating in red-sided garter snakes (Thamnophis sirtalis) as indicated by experimental manipulation of genitalia,” Proc R Soc B, 281:20132694, 2014.
  7. T. Pizarri et al., “Sophisticated sperm allocation in male fowl,” Nature, 426:70-74, 2003.
  8. H. Moore et al., “Exceptional sperm cooperation in the wood mouse,” Nature, 418:174-77, 2002.
  9. H.S. Fisher, H.E. Hoekstra, “Competition drives cooperation among closely related sperm of deer mice,” Nature, 463:801-03, 2010.
  10. K. Kimura et al., “The mucus of a land snail love-dart suppresses subsequent matings in darted individuals,” Anim Behav, 85:631-35, 2013.
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Avatar of: James V. Kohl

James V. Kohl

Posts: 173

July 1, 2014

Re: "These and other amazing genital adaptations illustrate an evolutionary war that plays out during and after copulation."

Framing ecological adaptations manifested in morphological and behavioral phenotypes of species from microbes to man in the context of evolution should be detered by experimental evidence of ecological speciation that is nutrient-dependent and pheromone-controlled. For example, see: Ecological selection as the cause and sexual differentiation as the consequence of species divergence?

"Differentiation in the mandibles and male genitalia (figure 2) is quantified and used as a proxy for the presence of divergent selection 7. Studies on the functional morphology of insect mandibles have identified their ecological relevance 20, including in Orthoptera more generally, where their chewing ability appears to be under selection 21. Likewise, genitalia are a good proxy for sexual selection 13; genitalic characters not only show species-level divergence in Amphiacusta but have also been shown to mediate reproductive success in other taxa 13,14."

Avatar of: N K Mishra

N K Mishra

Posts: 21

July 3, 2014

The evolutionary forces of sexual selection work at each level ranging from male ornaments, courtship displays, and association of females in determining the fate of their eggs. It does not end there but continues all the way down to the level of anatomy and physiology of genitalia and gametes.Survival of sperms in the female reproductive tract may range from a few hours to a few decades( in bees). The molecular mileau of the seminal fluid of one participant and its dynamic interaction with those of others and with the female reproductive environment to the point where a sperm makes entry into the egg constitute a gamut of spheres where competition is possible leading ultimately to survival and speciation.

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