Birds do it. Bees do it. And over 541 million years ago, weird organisms that looked like armored carpets did it. Exactly how they did so, though, was a bit different from the ways we’re familiar with.
University of Cambridge paleontologist Emily Mitchell and colleagues were the ones to reconstruct how these puzzling species reproduced. They focused on a species from the Ediacaran period called Fractofusus. The fossil is a strange, branching frond preserved as flat impressions in the ancient sediment, but it’s so unlike anything alive today that scientists are still unsure whether it was an animal, a plant, or what. Nevertheless, by studying the geographic pattern of how these fossils are preserved across the rocks of Newfoundland, Canada, Mitchell and coauthors have been able to reconstruct how Fractofusus made more Fractofusus.
It wasn’t as simple as catching Fractofusus in The Act. This was still tens of millions before the earliest days of internal fertilization, after all. Rather, Mitchell and colleagues write, the clusters of Fractofusus are patterned in such a way that suggests they’re organized by reproductive factors rather than by currents or other environmental details.
The largest, and therefore oldest, Fractofusus seem to be arranged randomly in respect to each other. This may indicate that these were the first to colonize the habitat, initially carried as tiny “waterborne propagules” that then settled and grew. But from there, Mitchell and coauthors wrote, Fractofusus started doing something different.
The smallest Fractofusus, the researchers found, grouped around the medium-sized ones, which in turn clustered around the largest individuals. With no evidence of little buds or fragments coming off any of the fossils, Mitchell and colleagues suggest that this pattern belies reproduction and connection by a way of a stolon – a wispy “runner” that connects individuals into a kind of communal group. Marine invertebrates, such as some bryozoans, do this today, and, in the prehistoric case, the large Fractofusus would have sent out runners to produce a garden of little Ediacaran clones.
So tell me: Of all the males on our planet—and I’m talking all, scale be damned, from the littlest insects to the biggest of whales—who’s got the most impressive appendage? Who (you should pardon the expression) is our Biggest Daddy?
And I don’t mean just sex organs, impressive as they sometimes are. I’m talking about any outstanding male appendage—whatever guys have that thrills the ladies, the obvious non-penile example being the peacock tail, which as we all know when fully displayed makes peahens dream of George Clooney.
Impressive? Yes. The problem being that between trysts, a superheavy tail must be a drag to lug around. It costs energy to maintain and more energy to get up and unfurled. But the drive to reproduce is a powerful thing, and sexual selection, as Darwin taught us, just keeps pushing the limits of bigness.
Obviously, there is such a thing as too big. I imagine it gets awkward to be a walrus with tusks curling dangerously close to your chest.
And the weight of these things? Not the absolute weight, but the proportional weight—that’s another limitation. How much can a guy carry? According to Douglas Emlen in his wonderful book Animal Weapons: The Evolution of Battle, while the rack of bone that sits atop a male caribou is hugely impressive (those antlers can weigh 20 pounds and stretch five feet across) …
… as big as they are, they account for only 8 percent of the male’s total body weight. Moose and elk have even larger antlers, but even the biggest elk antlers equal only 12 percent of its body weight. So that’s doable. Once upon a time, 11,000 years ago, there was a deer (called Megaloceros giganteus, or the Irish elk) that wandered Europe and Asia, and those guys had boney tops so insanely branched, so crazily big, that our prehistoric humans painted them worshipfully onto the cave walls at Lascaux.
But even these antlers, 12 feet across and wildly branched, weighed less than 20 percent of the total animal.
Go Small to Get Big
You have to drop down to the insect family, to a group of horned beetles, to find a big appendage that approaches a third of the animal’s body weight. There are several beetles that have fighting, clamping horns almost the size of their bodies, and a thing like that growing out of your skull, writes Emlen, “is a little like having your leg sticking up out of your forehead.” You feel it.
But if you’re looking for the male who wears the crown, whose appendage is so big, so startling, so colorful, so attractive, so monstrous, and therefore unequaled in the animal kingdom—if you’re looking for the champ? Well …
He’s not in the African savannah. He doesn’t have a tusk. He’s not especially large. You have to look down to see him, down near your feet when you’re at the beach. This is him:
He’s a fiddler crab. And that appendage is his claw. And while sizes vary from crab to crab, the biggest fiddler crab claws weigh roughly half the body weight of the animal. Half! That’s nature’s biggest appendage, says Emlen. And what is it for? Not for feeding. The claw is useless at mealtime. Males eat with their other, smaller claw only. But, says Cornell biologist John Christy, the claw’s bright colors definitely attract female attention. It can also snap down and inflict real harm, so they’re potential weapons. But mostly, he discovered, males use them—I kid you not—to wave.
“Up and down, up and down, again and again,” writes Emlen, “they raise their claws high and drop them. Dozens of times each minute, thousands of times per hour, hour after hour … ” They look a little silly doing this, like a lonely fan trying to start a stadium wave. Check out this fellow:
Why are they waving? It’s a warning. “Look what I’ve got!” the male is saying to any male who would trespass into his burrow. “This thing is going to pound you if you come near, so stay away!” In effect, Emlen writes, “fiddlers are employing their claws as warnings rather than instruments of battle.” And it works. “An overwhelming majority of contests end before they ever begin, without anything even resembling a fight. A mere glance at a big claw is sufficient to deter smaller males.”
The male has built a tunnel, which leads to a nesting burrow. His claw has attracted a lady, and she’s down below raising his family. His job is to stay on top, waving till she’s done or he drops. It’s a tough life, lifting that gigantic appendage over and over, using up energy, constantly getting bothered by would-be challengers. The male can’t eat. Not while he’s guarding. His food is at the water’s edge, which is down lower on the beach. So he stands there, day after day, getting hungrier, until eventually, Emlen says, “Even the best males run out of steam and are forced to abandon their burrows to go feed and refuel. The instant they leave, others will claim their burrows.” And then they become challengers and have to start all over again.
So while it may be glamorous to top the list of Biggest Appendage Ever, what with the lifting, the waving, the straining, the not eating, the worrying about how long you’ll last, it might be better to have a medium-size claw and not have to be always worrying about the biggest bullies at the beach. Yes, the big claw does dramatically increase your chances of producing babies, which, as Darwin will tell you, is the whole point. But if I were a fiddler crab lucky enough to have the biggest appendage in the world, I think I’d get myself a nail file (claw file?), erase my genetic advantage, and spend lazy afternoons sipping pond scum by the ocean’s edge. I like a gentler life.
Douglas J. Emlen’s book, Animal Weapons: The Evolution of Battle, is a fascinating account of how animal weaponry, both offensive (claws, horns, teeth) and defensive (armor, shelter, thorns, claws again) parallel human weaponry, both offensive (arrows, lances, swords, missiles, A-bombs) and defensive (armor, castles, spying). It’s a compelling, fun, often scary analysis. And David Tuss’ drawings, especially his animals, made me jealous.
At room temperature, a bearded dragon’s sex depends on two chromosomes. If they have two Z chromosomes, these lizards develop as males. Those with a Z and a W become females. But raise the thermostat up a few notches, and something different happens. If a clutch of dragon eggs are incubated at 34 degrees Celsius, their bodies ignore the usual instructions from their sex chromosomes. Even if half of them are genetically male (ZZ), all of them will hatch as females.
Clare Holleley from the University of Canberra found some of these “sex-reversed” ZZ females in the wild, and bred them with the usual ZZ males. All the offspring from these crosses should have two Z chromosomes, so you might guess that all of them would turn out male.
You’d be wrong. In fact, their chromosomes didn’t matter at all. Instead, their sex depended entirely on the temperature at which they are incubated. Warm clutches produced females; cooler ones produced males. In a single generation, these lizards had evolved a radically different way of determining their sex—one in which their genes completely cede control to the heat of the world.
No one knew that these flips could happen so quickly, but they must surely happen. After all, animals are incredibly varied in their ways of determining sex. In humans, other mammals, and some insects, females usually have two of the same chromosomes (XX), while males tend to have different ones (XY). In birds and some reptiles, including the bearded dragons, the female is the one with different chromosomes (ZW), while the male has identical ones (ZZ). Other reptiles ignore chromosomes altogether and rely on temperature. Turtle eggs are more likely to hatch as males at cooler temperatures, and as females in warmer ones. In crocodiles, this pattern is reversed.
Scientists used to think that these two strategies—genetic sex determination (GSD) or temperature sex determination (TSD)—were mutually exclusive. Animals could use one mode or the other, but never both. That idea was put to rest in 2007, when a team led by Jennifer Marshall Gravesexperimentally switched bearded dragons from GSD to TSD by raising them at high temperatures. “But we didn’t know if this was something that happens naturally or if the sex-reversed females are fertile,” says Holleley.
Her team solved both mysteries by capturing 131 wild bearded dragons from eastern Australia, and identifying 11 ZZ females among them. They do exist in the wild, they can mate with males, and they can themselves be mothers of dragons. When Holleley incubated their eggs at 30C or under, they all hatched as males. At 36C, they were all female. At intermediate temperatures, she got a mix. In just one lab-bred generation, the W chromosome had completely disappeared, and the dragons had switched completely to TSD.
“It is often thought that once a species veers down the path of chromosomal sex determination, there’s no going back,” explains Melissa Wilson-Sayres from Arizona State University. That’s because the two chromosomes develop sex-specific versions of important genes, and one of them—such as the Y in humans—loses so many genes that it becomes small and stunted. This supposedly creates an inescapable rut. “But this paper suggests that not only is it possible for a population jump out of the chromosomal sex determination rut, but that it actually occurs in the wild,” says Wilson-Sayres. “It’s fantastic because it shows how much variation can exist right below our noses.”
“This makes me think of the statements I’ve seen about trans individuals not being “truly male” or “truly female”, because of their (presumed) set of sex chromosomes,” she adds. “This research tells us that even with chromosomal sex determination, exceptions occur all the time. In the bearded dragon, the exception may even be a benefit, as ZZ females lay more eggs that ZW females. This tells us that we’re thinking much too simply if we say with confidence that only XX is female and XY is male.”
Holleley doesn’t understand exactly how the lizards flip from GSD to TSD because the genetics of sex determination are still a mystery in reptiles. In mammals, the Y chromosome has a gene called SRY that acts as a master sex-determining gene—if individuals have it, they’re usually male, and if not, they’re usually female. In birds, the equivalent gene is called DMRT1. But the reptilian counterpart is still a mystery. “We’ll have to figure out what the gene is, and how it’s regulated by temperature,” says Holleley.
The consequences of her discovery are also unclear. In the wild, the switch from GSD to TSD would be more gradual than what Holleley saw in the lab. Still, “there are many reasons why we think that if you get an extreme climatic event, and sex reversal starts happening, it’ll snowball,” she says.
First, as Wilson-Sayres noted, the sex-reversed ZZ females produce twice as many eggs as the usual ZW ones. Second, the offspring of the ZZ females are more likely to reverse sexes themselves—that is, males will hatch as females at lower temperatures than their mothers did. The third reason is more complicated. In a warmer world, ZW individuals all still become females but so do some ZZ individuals. This means that males become rarer. It also means that mothers become more successful if they have more sons, since those sons face less competition and can find mates more easily. So evolution should push mothers to have more ZZ male offspring.
These three effects all spell trouble for the W chromosome and—provided the climate stays very hot—should eventually eradicate it. In the end, all the dragons should be ZZ and all of them should rely on TSD.
What happens next? It all depends on the threshold temperature at which all-male broods give way to all-female ones. If the threshold is a sensible one, and keeps in step with environmental changes, then the dragons will be fine. They’ll just stick with TSD as many other reptiles do. But if the threshold is too low, and the world keeps getting hotter, then trouble looms. “They could potentially get more and more female-biased, and if you end up with all females, you’ll go extinct,” says Holleley.
Reptiles have obviously lived through many extreme fluctuations in climate, and they’re still around. Indeed, Holleley’s discovery does suggest that “reptiles may have greater capacity to cope and compensate for climate change than previously appreciated.” Then again, the current rate of warming is far steeper than what they would have encountered in the past. It’s a brave new world; how reptiles will fare in it is anyone’s guess.
Reference: Holleley, O’Meally, Sarre, Graves, Ezaz, Matsubara, Azad, Zhang & Georges. 2015. Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature http://dx.doi.org:10.1038/nature14574
It starts with a light, soft touch, one tentacle gently reaching out, hesitant, hopeful, hanging lightly in the air. There’s a pause. Skin touches skin. One softly strokes the other and slides closer, and then, carefully, they wrap themselves together, stroking, probing, entwining. They glisten as they move, and because they are snails, everything happens very slowly. The rubbing, the rapture, the intensity of it all—snail sex is extraordinarily lovely to look at. (If you aren’t at your office desk or on a train where people can see your screen, I’ve got one about a garden snail named Chip who’s trying to lose his virginity, or take a quick peek—30 seconds will do—of this coupling in a garden.)
Lovely but So Dangerous
Garden snails make love in the open—on garden patios, in clearings on the forest floor—and they do it luxuriantly for one, two, three hours at a time, under the sky, where they can be seen by jays, orioles, frogs, snakes, shrews, mice, beetles, and other animals that might want to eat them. Snails can’t make quick getaways, so exposing themselves like this is dangerous, crazily dangerous. What’s going on? What’s making them so impervious, so deeply preoccupied with each other? Here’s one answer: Snail sex is very complicated. Snails have a lot to think about when they make love—because they’re hermaphrodites.
Unlike you, garden snails can produce sperm like males and carry eggs like females at the same time.
Which is both an advantage and a problem. Professor David George Haskell, a Tennessee biologist, once squatted down on a patch of forest floor and watched what you just saw in that video—a snail couple going at it—except with a magnifying glass and only a few feet from the action. What he noticed was their mood. Hot as it was, he writes in his book The Forest Unseen, “Their extended courtship and copulation is choreographed like cautious diplomacy.” Snails don’t pounce, they circle. They “slowly edge into position, always ready to pull back or realign.” Their sex is tense, charged, on, off, then on again, “a prenuptial conference over the terms of the union.” What are they negotiating about?
In most animals, snails included, sperm is plentiful, cheap to produce, and fun to unload. So one presumes that both copulating snails are eager to get that part done.
Eggs, on the other hand, are limited and hard to produce—and therefore precious. You don’t let just anybody fertilize your egg sack. So, in Haskell’s imagination, if one of these snails picks up “a whiff of disease” on the other, it may be happy to poke but is not at all interested in being poked. No one wants its precious eggs fertilized by a sick dad, so the receiving snail might lock its partner out of its opening while also trying to penetrate it. This could produce feelings of frustration, confusion, and even unfairness in the other.
“In hermaphrodites,” writes Haskell, “mating becomes fraught, with each individual being cautious about receiving sperm while simultaneously trying to inseminate its partner.” Sexually speaking, two snails with four minds—a foursome in a twosome—makes for complex fornication. That’s why snails are always on tiptoe, Haskell thought as he watched them on the forest floor: They have so much to figure out.
So why be a hermaphrodite? Are there a lot of them? Well, here’s a surprise: They’re everywhere.
Eighty percent of the plant kingdom produces both seeds (pollen) and eggs (ovules) and can give or receive, making them hermaphroditic. They’ve learned that when the weather gets wet or cold, bees can’t be depended upon to buzz by and pollinate, so they have a we-can-do-this-ourselves backup plan.
Animals, generally speaking, are sexual, divided into male and female. But, writes Stanford biology professor Joan Roughgarden in her book The Genial Gene, if you subtract insects, which make up more than 75 percent of the animal kingdom and are not hermaphrodites, we are left, she calculates, “ … with a figure of 1/3 hermaphrodite species among all animal species.” That’s a hunk of hermaphrodites.
So Who’s a Hermaphrodite?
They’re not animals we pay much attention to (flukes, flatworms, killifish, parrot fish, moray eels, barnacles, slugs, earthworms, and tapeworms, among many others), but they are switch-hitters: They can either give or receive or switch sides during their lifetime. “All in all,” writes Roughgarden, “across all the plants and animals combined, the number of species that are hermaphroditic is more-or-less tied with the number who has separate males and females, and neither arrangement of sexual packaging can be viewed as the ‘norm.’”
Anyone who thinks that male/female is nature’s preference isn’t looking at nature, says Roughgarden. And she goes further.
Adam and Eve or AdamEve?
She wonders, Which came first, the hermaphrodite or the male/female? We have lived so long with the Adam and Eve story—Adam first, Adam alone, Adam seeking a mate, God providing Eve—that the question seems almost silly: Of course complex animals started with males and females.
But Roughgarden wonders if animals started as hermaphrodites …
… and then “hermaphrodite bodies disarticulate[d] into separate male and female bodies?” How would that have happened? Roughgarden cites a paper she did with her colleague Priya Iyer.
They propose that maybe the earliest animals started out as both sperm and egg carriers, and a subgroup got especially good at inserting their penises into enclosures, aiming, and directing the sperm to its target (the authors call it “home delivery”). They did this so effectively that they needed fewer and fewer eggs and essentially became sperm sharpshooters or, as we call them now, “males.”
That development gave others a chance to give up sperm altogether to concentrate on chambering their eggs in nurturing nooks, thereby becoming “females,” and so more and more animals found it advantageous to be gendered.
Ayer and Roughgarden aren’t sure this happened. They say that, on available evidence, the story can go “in either direction.”
The alternate view is almost the story you know. It’s Adam and Eve, with a twist: In the beginning, early animals were gendered—except when it was inconvenient.
If, for example, you imagine a group of, well, let’s make them snails …
… and something awful happens—there’s a terrible disease, an ice age, a new ferocious predator, or maybe a volcanic eruption…..
… so that we’re left looking at a lone individual, all by itself, looking around for a reproductive opportunity, crawling across the landscape, hoping to bump into somebody, anybody, to reproduce with, and after a long, long, anxious period, it finally sees what it’s been looking for. It crawls closer, closer, the excitement building.
But as it gets within wooing range, it suddenly sees that—oh, no—it’s the same gender!
No possibility of babymaking here. And this happens half of the time. (Statistically, that’s the likelihood.) Now instead of being your friend, male/femaleness is your enemy. What wouldn’t you give for a hermaphrodite, a he/she snail that could, in a pinch, be whatever sex you need it to be. With a hermaphrodite, you can (again statistically) always make a baby. What a relief. So maybe that’s what happened. Gender difference disappears when gender no longer helps produce more babies (and when you don’t have to stick around and be a parent).
Which is the true story? We don’t know. Maybe the only story is that nature is flexible. When gender is useful, you get genders. When not, you don’t. What we forget, being humans, is that there are so many ways to flirt, to combine, to make babies—and the world is full of wildly different ways to woo. Tony Hoagland knows this. He’s not a scientist but a poet who lives in New Mexico, and in his poem entitled “Romantic Moment,” he imagines a boy on a date who sits next to his girl imagining … How shall I put this? … how the Other Guys do it.
Romantic Moment by Tony Hoagland
After the nature documentary we walk down,
into the plaza of art galleries and high end clothing stores
where the mock orange is fragrant in the summer night
and the smooth adobe walls glow fleshlike in the dark.
It is just our second date, and we sit down on a rock,
holding hands, not looking at each other,
and if I were a bull penguin right now I would lean over
and vomit softly into the mouth of my beloved
and if I were a peacock I’d flex my gluteal muscles to
erect and spread the quills of my cinemax tail.
If she were a female walkingstick bug she might
insert her hypodermic proboscis delicately into my neck
and inject me with a rich hormonal sedative
before attaching her egg sac to my thoracic undercarriage,
and if I were a young chimpanzee I would break off a nearby tree limb
and smash all the windows in the plaza jewelry stores.
And if she was a Brazilian leopard frog she would wrap her impressive
tongue three times around my right thigh and
pummel me lightly against the surface of our pond
and I would know her feelings were sincere.
Instead we sit awhile in silence, until
she remarks that in the relative context of tortoises and iguanas,
human males seem to be actually rather expressive.
And I say that female crocodiles really don’t receive
enough credit for their gentleness.
Then she suggests that it is time for us to go
to get some ice cream cones and eat them.
Thanks to the poet Thomas Dooley for suggesting Tony Hoagland’s poem, and to Mr. Hoagland for giving us permission to print it here in full. Reading “Romantic Moment” I giggled a little to think of eating ice cream on a sugar cone as a homo sapien mating ritual—but thinking back, I think he’s onto something. The poem can be found in Tony Hoagland’s collectionHard Rain.
There’s not really a good time to bring up amphibian mating habits at the dinner table. I figured that I was probably safe given that I was surrounded by scientists, but, all the same, I tried to make sure that no one was raising a fork to their mouths when I blurted out “You guys! There are frogs that have sex!”
The inspiration for my outburst came from a PLOS One paper published just before I headed out the door for New Year’s Eve dinner. In it, biologists Djoko Iskandar, Ben Evans, and Jimmy McGuire describe a frog that reproduces unlike any other known species.
Most frogs and toads look like they’re having sex when they’re mating, but this is a superficial illusion. It’s a behavior called amplexus in which the male amphibian clasps the female around the torso, shoulders, or head and releases his sperm as she lays her eggs.
The new frog species – named Limnonectes larvaepartus – is one of the rare exceptions. Like a handful of other frogs and toads, this newly-described amphibian from Sulawesi Island is capable of internal fertilization. The way the frogs accomplish this is a mystery – the Limnonectes larvaepartus males appear to lack what science has politely called an “intromittent organ” – but what happens next is a sure sign that the fanged frogs don’t spawn like other species.
All other frogs and toad species that have sex deliver their young in one of two ways. The females either lay their internally-fertilized eggs in typical amphibian fashion or the mothers give birth to well-developed froglets. Limnonectes larvaepartus splits the difference. Females of the new species, Iskandar and colleagues report, gives live birth to tadpoles.
The researchers first discovered this unusual ability while prepping collected frogs. When they dissected some of the females, “the abdominal wall was observed to quiver, and incision resulted in living tadpoles emerging from the opening.” Live frogs later gave birth to squiggly tadpoles at the time of collection and while being held for study.
While there’s a possibility that the fanged frogs may have been capable of retaining those tadpoles until they fully metamorphosed into froglets, Iskandar and coauthors consider this unlikely. All 19 pregnant females collected for the study had tadpoles inside, not froglets, and the researchers also found free-living tadpoles in streamside pools. Once released into the outside world, the developing frogs live off what little yolk they have left before starting to feed for themselves. And given that this news was received positively as dinner concluded, I can heartily recommend that you share the tale of this remarkable frog the next time you meet friends for a meal. I’m sure they’ll find it ribbiting.
In humans, it’s every sperm for itself: sperm cells race to reach an egg and the first one there gets to fertilise it. But in many other animals, sperm can clump together to form cooperative bundles that outswim any solo cells.
Take the deer mouse. The sperm of this common North American rodent have heads that are flattened paddles with small hooks, rather than the usual round teardrops. These heads can stick to each other, forming clusters of up to 35 sperm. Scientists have reasonably assumed that the sperm swim better as a team, but that’s not always the case. Sometimes, the groups are faster; sometimes, they barely move.
Heidi Fisher from Harvard University knows why. Her collaborators Luca Giomi and L Mahadevan created a mathematical model that simulated the swimming sperm. It showed that while groups don’t swim any faster, they do swim straighter because each cell cancels out the wobbling movements of its neighbours. Their speed stays the same but their velocity—their speed in a straight line—goes up. “The aggregate gets to the finish faster,” says Fisher.
But once the clusters get too big, their members start swimming against each another and their velocity falls. The optimal number is seven. A seven-strong sperm swim-team will get to an egg faster than either a smaller or a bigger group.
When Fisher then timed the sperm of actual mice under a microscope, she found that they behaved exactly as the model predicted: groups of seven really do have the highest velocity. And the mice are very good at meeting this ideal number. Fisher compared the sperm of two species—the deer mouse and the oldfield mouse—and found that in both, the average number of sperm per cluster is 6 or 7.
But Fisher also found one critical difference between the two species: the deer mice somehow keep tighter control over the size of their sperm clusters. Look at the graph below. The red diamonds represent the average size of a sperm cluster in different male deer mice; they range from 5 to 7. The blue diamonds represent the average cluster sizes in male oldfield mice; they range from 4 to 9.
Why? Because the two species, though closely related, have very different sex lives. The oldfield mouse is strictly monogamous: females only ever mate with one male at a time. The deer mouse is promiscuous: females mate with many males in quick succession, and often have the sperm of many suitors in their bodies. These cells must then compete to fertilise the female’s eggs.
So, relative to the easy-going oldfield mice, the deer mice are under intense evolutionary pressure to have more competitive sperm. That’s why their sperm are better at gathering in exactly the right numbers for straighter swimming.
They’re also better at recognising each other. In 2010, Fisher showed that the sperm of deer mice prefer to stick with sperm from the same species, and especially to sperm from the same male. Oldfield mouse sperm cells are less fussy; they’ll just stick to whatever’s nearby.
The researchers still don’t understand how the deer mouse keeps a tighter rein on the size of its sperm teams. “That’s the next step,” says Hopi Hoekstra, who led the study. They also don’t know how the cells stick together; contrary to what they used to think, the hooks are not involved. “How do they actually clump and recognise each other? We have no idea.”
Similar evolutionary pressures have shaped the sperm of other animals. In the desert ant, Cataglyphis savignyi, females also mate with many males, sperm cells also gather in groups (of 50 to 100 cells!), and the groups also swim faster than individual cells. In diving beetles, hundreds or even thousands of sperm can unite into long worm-like trains that navigate the females’ maze-like reproductive tracts—the more convoluted her anatomy, the more cooperative his sperm. The sperm of the promiscuous wood mouse also forms similarly spectacular trains.
In all these creatures, the sperm hook up after ejaculation, but opossum sperm come pre-paired. The cells form paired clusters within the male’s body and once they are shot into the female, their tails start beating in sync like a pair of frog’s legs. These clusters are far smaller than those of the diving beetle, desert ant, or mice, but they are perhaps the ultimate example of cooperative sperm. Alone, these cells swim in a futile circle. They can only create the next generation of opossums as a team.
With their impressive fins and stunning colours, the poeciliids—a group of small fish that includes guppies, mollies and swordtails—are understandably popular in aquariums. Some have beautiful fan-shaped tails that look like flamenco dresses. Others resemble Kandinsky paintings given life.
But some poeciliids are rare in aquaria, because they are relatively drab—silver-and-black oddities in a family known for extravagance. They also tend to share another weird and less obvious trait: they have placentas.
Unlike most fish, which lay eggs, all poeciliids give birth to live young. Mothers nurture their offspring inside their own bodies. Some produce eggs, but keep them inside their ovaries until the young are ready to enter the world. Others have evolved organs that bring the mother’s tissues so close to her baby’s that she can pass nutrients over—in other words, a placenta. Anatomically, this organ is very different to the placentas that human mothers use to nourish their babies, but it does the same job.
Mammals only evolved placentas once. But the poecilids have evolved these organs on at least eight separate occasions, and in a very short span of time. “The placenta is a very complex organ. Imagine if the eye evolved several times in the hominids. It’s that kind of complexity,” says Bart Pollux from the University of California, Riverside.
Now, Pollux has shown that the rise of the placenta was accompanied by drastic changes in the bodies and lifestyles of the poeciliids. The species with these organs are less ornate. They lack obvious courtship rituals. The males tend to be smaller, but their genitals are bigger. And he thinks that this seemingly unrelated constellation of traits arose because the placenta radically changes the relationship between mothers and their developing young.
Consider an egg-laying species. A female fish loads her eggs with nutritious yolk before they are fertilised. At this point, her investment is set. The most important decision she can now make is to choose a good mate, so her eggs get fertilised by the best possible sperm. In this scenario, the battle of the sexes plays out through discerning females and competitive males. You see bright colours, flashy courtship displays, and perhaps large size differences between the sexes.
In species with placentas, things are different. Mothers continue to provide nutrients to their young long after fertilisation. That opens up a new type of conflict between mother and child. The developing embryo does best if it gets as much nutrition from mum as possible. The mother, however, may do badly at raising future children if she invests too much energy in her current one. So in these species, evolution should drive embryos to want more and mums to hold back.
What about fathers? If the species in question doesn’t form life-long partnerships, a father does best if his mate invests heavily in her current child (which he sired) than in future children (which he won’t). And he can influence her investment because his genes are inside the embryo that’s growing within her. These paternal genes act against her maternal ones in an evolutionary tug-of-war with the baby as the rope.
So, what looks like a conflict between mother and offspring is really still a conflict between male and female. But instead of a showy battle of courtship rituals and bright colours, it’s a covert one that takes place in the womb. It’s a Cold War of the sexes. And that is why the placental species evolve away from showy, flashy traits towards sneaky, understated ones.
Pollux first came across this hypothesis in a paper by David and Jeanne Zeh, published in 2000. “They didn’t know how to test these predictions, but we found a way,” he says. He realised that he needed a large family of animals that have a variety of sexual traits and behaviours, and have evolved placentas over and over again. The poeciliids were perfect.
By studying 110 species, his team showed that the placental ones were less likely to have exaggerated traits like sword tails, wavy fins on their backs, bright colours, or elegant courtship. By contrast, they were more likely to have smaller males and relatively longer genitals. They have moved away from obvious displays that help females to choose mates, and towards traits that make it easier for males to sneak up on females and stealthily mate with them.
The team showed that almost all the poeciliids with placentas have an unusual ability: they can get pregnant while they’re already pregnant. This talent is called superfetation, and it stops any single male from monopolizing an entire litter by fertilising every available egg. Rather than being careful about choosing mates, a female can now mate with many males and let their genes duke it out for investment in the womb.
“It all fit!” says Pollux. All the traits he saw pointed to the same shift from choices and competitions that take place before sex, to subtler battles that are waged after it. Zeh, for one, is pleased to see evidence that supports her hypothesis. “The results of this study fundamentally advance our understanding of sexual selection,” she says.
Of course, this leaves a chicken-and-egg problem. Did the placenta drive the evolution of these other traits, or did the other traits drive the evolution of the placenta? The authors think it’s the former—that’s certainly what the title of the paper implies.
But David Haig from Harvard University, who has studied parent-offspring conflict, thinks it was the other way round. He thinks the first change was a move away from formal courtship and towards forced mating. Now, the males, rather than competing for a female’s attention are competing inside her via their sperm. Haig sees superfetation in the context of this sperm competition, as an adaptation that allows sperm to “get in first” and fertilise eggs before they are fully loaded with yolk. The female continues to add nutritious yolk to what is now an embryo, paving the way for the evolution of a placenta.
Reference: Pollux, Meredith, Springer & Reznick. 2014. The evolution of the placenta drives a shift in sexual selection in livebearing fish. Nature http://dx.doi.org/10.1038/nature13451
In 2009, duck penises took the Internet by storm. Thanks to a newly published study and an eye-opening video, people learned that while most birds lack penises at all, male ducks have huge, corkscrew-shaped ones. During sex, they extrude these into females at high speed. Since then, duck penises have become a short-hand for the “ain’t nature wacky” genre of science writing, and an unexpected focal point for debates about the value of basic science.
And during that time, one important part of the original study was lost. People forgot that the story of duck penises is really the story of duck vaginas.
Duck sex can be fiercely competitive, and several males will often try to force themselves onto a female. Their extreme penises help them to deposit sperm as far inside her as possible. But duck vaginas are also long and twisting. They’re lined with dead-end pockets and they spiral in the opposite direction to the male’s penis. This shape stops the progress of a male’s ballistic organ—something that Patricia Brennan proved by getting drakes to launch their penises into variously shaped glass tubes.
As I wrote in 2009, a duck’s vagina is an “organic chastity belts that evolved to limit the effectiveness of the males’ lengthy genitals.” If she actually wants to mate, she can change her posture and relax the walls of her genital tract to offer a male easy passage. If not, she makes him insert his key into an inconveniently shaped lock. To a casual observer, the male looks like the one with the power, but the female is actually in control, thanks to her convoluted genitals.
And yet, everyone talks about the penises.
This isn’t just relevant to ducks. It’s a problem that runs through all of zoology. Animal genitals are really interesting—they are extraordinarily diverse in their shape and use, and they tell us fascinating things about evolutionary conflicts. Many scientists have realised this. In the early 1990s, only five studies on genital evolution got published every year. In 2012, there were 40 such studies.
But males have benefited from this rising interest more than females. By analysing 364 studies published in the last 25 years, Malin Ah-King, Andrew Barron and Marie Herberstein found that 49 percent only looked at male genitals, 8 percent only looked at female genitals, and 44 percent looked at both. There’s some variation: people who study spiders, snails and slugs are more likely to pay attention to female genitals. But in general, female sex organs—vaginas, bursas, cloacas, spermathecae and more—get a short shrift.
The gender of the scientists themselves isn’t a factor. Ah-King, Barron and Herberstein found that both male and female scientists are just as likely to skew towards studying male genitals.
One possibility is that the bias is justified because female genitals vary less than male ones do. But Ah-King, Barron and Herberstein disagree with this argument. They point to many groups of flies, spiders, ducks and even primates, where female genitals vary a lot between species, or even within them.
A more likely explanation is that a tube is much easier to study than a cavity. Male genitals stick out and they’re often rigid, making them easy to observe, measure and manipulate—there’s an entire genre of penis–shaving studies out there. But female genitals are usually concealed. “They have to be dissected out, which changes their shape,” says Michael Jennions from Australian National University. “This is laborious work [and requires] old-school anatomical skills that are declining in modern biology.” (This may explain why the bias is less pronounced in studies of spiders, whose females often have obvious external genitals.)
Instead, they believe that male genitals still get more attention because of longstanding gender stereotypes that have seeped into evolutionary biology. For a long time, researchers believed that males played a dominant role in sex, while females were more passive—Darwin himself referred to them as “coy”.
These stereotypes are pervasive. In the most cited studies on sexual conflict, authors use active words like ‘intimidation’ and ‘coercion’ to describe males, but passive words like ‘resistance’ and ‘avoidance’ to describe females. More tellingly, males have ‘adaptations’ and females have ‘counter-adaptations’. Males act; females react.
But we know that, as in ducks, females exert a tremendous amount of control during sex. They can store sperm in pouches, expel unwanted sperm, or mate with more males. All of these tricks allow them to reject a male as a father even after having sex with him, and all of them are hard to observe unless you’re actually looking. And perhaps, people don’t look very hard.
Although few modern biologists would see females as passive players in sex, Ah-King, Barron and Herberstein argued that this myth has cast a lingering shadow over the field. It meant that people started studying male-focused topics like sperm competiton—where the sperm of different males compete for fertilisation rights inside a female’s body—long before topics like female choice.
Consider also the notion that males are promiscuous and females are choosy. This concept was stamped into textbook wisdom after a classic 1948 paper from geneticist Angus Bateman, based on experiments with fruit flies. Through breeding experiments, Bateman found that males benefit a lot from mating repeatedly but females do not.
But Bateman’s methods included a serious problem, one that undermined his conclusions and was only uncovered last year. As Eric Michael Johnson writes, “the premiere study on sexual selection—which had been cited by more than 2,000 peer-reviewed papers and textbooks—contained a fatal flaw… The uncomfortable implication is that Bateman’s paradigm was so widely cited because it conformed to assumptions about how female sexuality ought to be.”
Bateman’s principle isn’t universally wrong—in the intervening decades, other scientists found many examples to support it. But in suggesting that sexual success matters more to males, and varies more among them, Ah-King, Barron and Herberstein argue that it guided students towards studying males rather than females. Hence: the explosion of studies on penises and sperm, and the relative dearth of research on vaginas and eggs.
This bias leads to problems. We can seriously misinterpret the sexual lives of animals if we only know about half the partners. For example, the corkscrew penis of a male duck looks like a tool for beating other males in sexual conquests, until you realise that the helical vagina of the female grants her control.
Likewise, the male earwig has a long, brush-tipped organ called a virga, which he supposedly uses to scrape the sperm of previous suitors out of a female. As Ah-King, Barron and Herberstein write, “Too often, the female is assumed to be an invariant container within which all this presumed scooping, hooking, and plunging occurs.” In fact, the female earwig has storage organs for sperm, which lie beyond the reach of the virga. The male can scrape away all he wants; the female decides whether to keep or jettison her sperm.
“Increased emphasis on female genitalia would help in understanding genital evolution,” says William Eberhard, a pioneer in the study of female choice. “The authors aren’t the first to point this out, but it is useful and necessary to repeat the arguments periodically.”
But Diane Kelly from the University of Massachussetts, who has studies a wide range of animal penises, adds, “I think the authors underestimate how difficult it is to study female genitalia.” It’s not just that these organs are hidden. They also work in complicated ways.
Penises are simple. They might have piercing tips or attachments for scraping out a rival’s sperm, but they’re still basically tubes with one basic job: get sperm near eggs. Female genitals, on the other hand, might change shape to interact with male organs. They might contract to improve or reduce the odds of insemination. They might release floods of hormones to control the release of eggs or storage of sperm. They’re much more than just simple cavities.
“Faced with that kind of complexity, is it any wonder that the people studying “lock and key” models opt to study the key end of the system?” says Kelly “It’s a lot easier and faster to shave some spines off a male’s penis and assess whether or not that changes his reproductive success than to work through all the factors that a female could be evaluating before she uses or rejects that male’s sperm. In short, when it comes to female genitals, we still have to figure out what they’re doing during sex.
“That’s probably one reason why half of the animal genitalia studies the authors assessed looked at males and females together. I think that’s a good thing. Studying how female genitalia actually behave during copulation is likely to tell us a lot more about the evolutionary pressures on those tissues than we’d learn from studying them in isolation.”
Sometimes, for science, you have to make fashion accessories for animals. I’ve written about swift backpacks, cheetah collars, and beetle mittens. Now, from Ken Murata from the University of Tokyo, comes the goat cap. It’s a custom-made helmet with a few gas-absorbing balls inside. Its purpose is to collect a dose of ‘eau de goat’, so the team could identify the secret ingredients that allow male goats to turn females on.
If you have a herd of female goats or sheep, you can quickly shunt them into the fertile part of their sexual cycles by introducing a male. Something in his scent triggers hormonal changes in the females, who start to ovulate, or produce egg cells.
This “male effect” was discovered decades ago, but no one knew which molecules were responsible. They seemed to be classic examples of ‘primer pheromones’, which work by triggering long-lasting physical changes in their targets, rather than suddenly changing their behaviour.
To identify these mystery pheromones, Murata’s team analysed the odour samples collected by their gas-absorbing caps. Specifically, they were looking for chemicals that were released by normal males but not by castrated ones that don’t induce the male effect. They ended up with a long list of candidates. Now they had to test them.
They knew that the male pheromones act on a particular group of neurons in the female’s brain, which release a hormone called GnRH. This “GnRH pulse generator” works like clockwork, releasing a fresh burst of GnRH every 27 minutes or so. The size and frequency of these pulses dictates a female’s reproductive cycle. For example, she produces an especially large surge of the hormone just before her most fertile phase.
The neurons produce a volley of coordinated electrical activity whenever they released a hormone pulse, and Murata could detect these bursts by sticking electrodes in the right place. He could then waft different scents past their noses to see how the pulse generator responded.
When he held a cup full of male hair up to the female’s noses, their GnRH neurons produced a volley of activity, no matter where they were in their 27-minute cycle. A cocktail of 18 newly identified compounds from the male goats also worked. And eventually, the team found that a single chemical called 4-ethyloctanal did the trick. It seems to be the key ingredient behind the male effect.
4-ethyoctanal has a citrus tang, but it’s one easy chemical reaction away from a substance responsible for a goat’s distinctive “goaty odour”. This is the first time anyone has found the substance in a natural source, and it just so happens that it’s a primer pheromone.
Peter Brennan from the University of Bristol says the discovery is important. “There are relatively few instances in mammals where an individual compound has been positively identified as having a pheromonal effect,” he says. “There are fewer still in non-rodent species that have commercial importance.”
After more work, farmers may be able to use 4-ethyloctanal to more precisely control the reproduction of their herds. And Murata’s group have assembled an even bigger team to find a similar pheromone in an even more commercially important animal—the cow.
“I would expect that what they find in the goat will be true for other mammals and can be more easily studied in more traditional scientific models such as the mouse,” says Lisa Stowers from the Scripps Research Institute notes. But she says that “this finding is unlikely to translate to human reproduction”, since we don’t seem to have any pheromone-detecting neurons similar to the ones that Murata studied in his goats.
There are still some missing pieces to the puzzle, though. Tristram Wyatt form the University of Oxford adds that “4-ethyloctanal is likely to be one of a number of molecules working synergistically.” After all, Murata’s team showed that their 18-molecule cocktail still partly affected the females even when 4-ethyloctanal was removed.
And other stimuli could potentially block the pheromone’s effects—something we still know little about. “In more natural situations, the male effect in sheep (and likely goats) comes especially from exposure to unfamiliar males,” says Wyatt. “So, there is also memory of individual chemical profiles of previously encountered males which blocks the effect of pheromone.”
Stowers adds that the team haven’t shown how the pheromone actually affects the GnRH neurons or how a brief sniff can lead to long-lasting changes over the course of several days. Yukari Takeuchi, one of the study’s leaders, agrees. He says the acid test for their hypothesis would be to expose females to synthetic 4-ethyloctanal and to watch their reproductive behaviour change in the absence of any actual males. To do that, they need to create a device that will continually release the pheromone, and they are building one right now. Their days of goat accessories aren’t over yet.
Reference: Murata, Tamogami, Itou, Ohkubo, Wakabayashi, Watanabe, Okamura, Takeuchi & Mori. 2014. Identification of an Olfactory Signal Molecule that Activates the Central Regulator of Reproduction in Goats.
If you’re an aficionado of sea slugs, you’re probably used to weird and cringe-worthy sex acts. When two of these hermaphrodite animals penetrate each other at the same time like an R-rated yin-yang symbol, you won’t bat an eyelid. When several of them link up in a long mating chain, you’ll have seen it all before. When one amputates its disposable penis after sex only to uncoil a spare, your only reaction will be, “Meh.”
Still, when two sea slugs penetrate each other in the head while having sex, even the most jaded expert might do a double-take.
Rolanda Lange certainly did. An evolutionary biologist from the University of Tubingen, she is well-versed in sea slugs and their sexual antics. Recently, she found a new species while diving at Lizard Island, Australia. It’s just 2 to 3 millimetres long, and looks like an undersea orchid. Its body is white and surrounded by translucent petal-like flanges, rimmed with vivid reds and yellows. It doesn’t have a formal name yet. For now, Lange simply calls it Siphopteron species 1.
Every individual is a hermaphrodite with both male and female genitals. When they have sex, they can simultaneously penetrate each other, with penises that extend to their whole body length. “They are relatively well-endowed, says Lange.
The penises are also forked. One branch ends in a cone-shaped structure called the penile bulb, which is ringed by small spines. It goes inside the partner’s female genital opening, and delivers sperm. The other branch ends in a fiendish spine called the penile stylet. It stabs straight into the partner’s forehead, and pumps fluid from the prostate gland. So, during sex, each slug gets a dose of sperm in the usual place, and an injection of prostate fluid just above its eyes. This goes on for just over 40 minutes.
“You may imagine I was quite excited and surprised to find out they reciprocally injected into their partners’ head!” says Lange.
Back in her lab, she filmed 16 sexual encounters between these sea slugs, and showed that they always aim for the head with their penile stylets. She even spotted one mating circle, in which three slugs stabbed/inseminated each other at the same time.
This wince-inducing brand of sexual puncturing is called “traumatic insemination”. It’s widespread throughout the animal kingdom. Bed bugs famously do it. At least one species of spider does it. Many worms and snails do it. It’s not new to see traumatic insemination among snails and slugs, says Ronald Chase from McGill University. “What is new is the documentation of species-specific injection sites,” he says.
Lange found that some Siphonopteron sea slugs are flexible, aiming for somewhere on the body or foot. Another new species always goes for just next to the genital opening. But Species 1 is the only member of the group that only and always aims for the head. Lange calls it “cephalo-traumatic secretion transfer”; the colloquial version isn’t printable on a National Geographic site.
The obvious question: Why? The short answer: No one knows.
In many species that practice traumatic insemination, females have ways of storing a male’s sperm so that they can choose between many suitors. The males bypass this choice by injecting their sperm into unusual places.
In some cases, the males traumatically inject other fluids to give their sperm a helping hand. The male common garden snail does this by shooting a female with a love dart, which delivers a hormone that stops her from digesting his sperm. “We think it is plausible to assume something similar may be going on in our species,” says Lange. The injections could compel the female into keeping the male’s sperm around.
But: the head! Siphonopteron penises are so long and flexible that they could inject prostate fluids anywhere on their partners. Why does this one species go for the head, when its close relatives don’t?
Lange thinks that it’s aiming for the brain, either injecting near it or directly into it. Many parasites use chemical injections to control their victims’ control their behaviour. The emerald cockroach wasp, for example, turns cockroaches into docile pets by stinging them in their brains. But there’s no record of an animal using similar injections to control a sexual partner’s behaviour. Perhaps this sea slug is the first?
“[That’s] completely speculative,” says Chase. “The paper presents no evidence of neural manipulation, only the possibility based on the site of injection.”
“After head injection, the slugs do become calmer,” adds Lange. “But they have that in common with [similar species] which do not inject into the head. My educated guess is that it does not manipulate observable behaviour, but rather influences something internal, such as sperm storage.”
Lange now wants to use high-resolution scanners to work out exactly where penile stylets are going, and whether they are hitting any nerve clusters. She also wants to analyse the prostate fluids, and work out whether the slugs behave differently after the injections.
It’s August in Australia, and a small, mouse-like creature called an antechinus is busy killing himself through sex. He was a virgin until now, but for two to three weeks, this little lothario goes at it non-stop. He mates with as many females as he can, in violent, frenetic encounters that can each last up to 14 hours. He does little else.
A month ago, he irreversibly stopped making sperm, so he’s got all that he will ever have. This burst of speed-mating is his one chance to pass his genes on to the next generation, and he will die trying. He exhausts himself so thoroughly that his body starts to fall apart. His blood courses with testosterone and stress hormones. His fur falls off. He bleeds internally. His immune system fails to fight off incoming infections, and he becomes riddled with gangrene.
He’s a complete mess, but he’s still after sex. “By the end of the mating season, physically disintegrating males may run around frantically searching for last mating opportunities,” says Diana Fisher from the University of Queensland. “By that time, females are, not surprisingly, avoiding them.”
Soon, it’s all over. A few weeks shy of his first birthday, he is dead, along with every other male antechinus in the area.
The technical term for this is semelparity, from the Latin words for “to beget once”. For semelparous animals, from salmon to mayflies, sex is a once-in-a-lifetime affair, and usually a fatal one. This practice is common among many animal groups, but rare among mammals. You only see it in the 12 species of antechinuses and a few close relatives, all of which are small, insect-eating marsupials. (Although they look like rodents and are colloquially called marsupial mice, antechinuses are more closely related to kangaroos and koalas than to mice or rats.)
Why? Why do these marsupials practice suicidal reproduction, and why are they the only mammals that do so?
The question has vexed biologists for three decades, and many have offered answers. Some say that females don’t survive very well after breeding, so males are forced to hedge their bets by mating with as many as possible. Other suggest that it’s just a feature of the group, which have become locked into a weird breeding system through some unknown quirk of their evolutionary history. Yet others think the males are being altruistic, sacrificing themselves to leave more resources for the next generation.
But Fisher, who has been studying antechinuses for decades, favours a different idea. Her team gathered data on the lives and environments of a wide variety of 52 insect-eating marsupials, from the fully semelparous antechinuses, to relatives where a small number of males survive past their first sexual liaisons, to species that breed repeatedly.
It’s their diet that matters. These animals feed on insects, and some experience a glut of food once a year but very little at other times. This seasonality increases the further you get from the equator. The species with the most seasonal menus also had shorter breeding seasons, and their males were more likely to die after mating.
Fisher thinks that as the ancestors of antechinuses spread south through Australia and New Guinea, they encountered strong yearly fluctuations in their food supply. The females were better at raising their young if they gave birth just before the annual bonanza, and were well-fed enough to wean their joeys. Their mating seasons shortened and synchronised, collapsing into a tight window of time.
That probably wouldn’t have happened if they were placental mammals like shrews or mice, which could have produced several litters during the peak of food. But they were marsupials: their babies are born at an incredible early stage and rely on their mothers’ milk for a long time. A baby shrew suckles for days or weeks; a baby antechinus does so for four months. The females could only fit in one litter during the annual peak.
This had a huge impact on the males, which were forced to compete intensely with each other in a matter of weeks. They didn’t fight. Rather than using claws or teeth, they competed with sperm. The more they had, the more females they impregnated, and the more likely they were to displace the sperm of earlier suitors. Indeed, Fisher found a clear relationship between suicidal reproduction and testes size. The biggest testes of all, relative to body size, belong to species whose males die en masse, followed by those where a minority survive to mate again, and then by those with several breeding seasons.
The males that put the greatest efforts into sperm competition fathered the most young. It didn’t matter if they burned themselves out in the process, if they metabolised their own muscles to fuel their marathon bouts. These animals are short-lived anyway, so putting all their energy into one frenzied, fatal mating season was the best strategy for them. Living fast and dying young was adaptive.
This idea was first proposed in 1979 but Fisher’s data, although mostly correlative, provides fresh support for it. She certainly finds it more plausible than the idea that the males are selflessly sacrificing themselves for the next generation. After all, the males usually live outside the females’ home ranges, so are unlikely to compete with their own young for resources.
“Antechinus mating habits have appeared in many documentaries, and the explanation of males selflessly sacrifing themselves to increase food supply for young is the one given in all the ones I have seen,” says Fisher. “I hope that documentaries and textbooks now start to give an evidence-based explanation of sexual selection.”
Reference: Fisher, Dickman, Jones & Blomberg. 2013. Sperm competition drives the evolution of suicidal
Daughters inherit many things from their fathers, but a select few get something unusual—a Y chromosome. Women typically have two X chromosomes while men have an X and a Y, but some XY people are born with female genitals and a uterus. They’re almost always raised as girls from birth, and their hidden Y chromosome only becomes obvious during puberty. That’s because they don’t develop working ovaries, and without these organs providing a flood of hormones, they don’t menstruate, grow body hair, or develop larger breasts on their own. They’re also sterile.
This condition, known as Swyer syndrome, is often caused by changes to SRY, a gene on the Y chromosome that acts as a master switch for maleness. Human embryos develop into females by default, but SRY diverts them from this course. It switches on many genes that transform an embryonic ridge into testes instead of ovaries. But SRY can pick up mutations that interfere with this role, and prevents it from launching its male-making programme. As a result, embryos develop into baby girls despite their Y chromosome.
But sometimes, fathers and daughters carry identical copies of SRY. He develops into a typical fertile male. She grows up as a sterile female. How can this be?
Michael Weiss from Case Western Reserve University has the answer. His team, led by graduate student Yen-Shan Chen, studied several pairs of fathers and daughters with identical Y chromosomes, and showed that SRY just isn’t a very strong switch. It doesn’t cleanly flip between on (male) and off (female). Instead, it does just enough to divert an embryo down the male path, and it’s easily affected by the environment or by other genes. Their results show that becoming a boy is a surprisingly precarious event.
Melissa Wilson-Sayres from the University of Berkeley, who studies sex chromosomes and was not involved in the study, compares SRY to a dimmer switch. At its ‘bright’ setting, it sets embryos down a male path; at lower ones, it fails to activate other genes, leading to female traits. “In humans, the dimmer switch isn’t normally set very ‘brightly’, so that slight variations are sufficient to affect the formation of gonads,” she explains.
This idea isn’t new, says Robin Lovell-Badge from the National Institute for Medical Research, who first discovered SRY. Since the 1990s, studies in mice have shown that SRY is active at just above the right threshold for producing testes. Peter Koopman summed up the idea in 2007: “What is clear is that instead of the robust gene one might expect as the pillar of male sexual development, SRY function hangs by a thin thread.”
“But while there have been clues that the same is true in humans, it has not been possible to prove this because of the difficulty of looking at human early gonads,” says Lovell-Badge. Weiss has now done so, and he says it was a necessary experiment. SRY works very differently in rodents and humans, so “there was no reason to believe that this result was true for humans. We now believe it is.”
SRY creates a protein of the same name, and it’s this protein that activates other male-making genes. Weiss’ team showed that their XY father-daughter pairs carried two SRY mutations that don’t much alter the protein’s abilities. Instead, they change its location.
Like all other proteins, SRY is made in the cytoplasm—the soupy liquid that forms the bulk of a cell. But to activate other genes, it needs to get into the nucleus—the central compartment where DNA resides. To do this, it sticks to other proteins that smuggle it in and out of the nucleus. Mutations in SRY can change the balance of these trips so that, for example, it can’t be efficiently imported into the nucleus. When this happens, it can’t do its job effectively, and the activity of its dependent genes falls by a factor of two.
Under some conditions, this difference doesn’t matter and the dependent genes are still active enough to launch the male-making programme. Under other conditions, they aren’t.
This is why fathers can develop as males and daughters can develop as females, even though they share the same copy of SRY. The whole set-up sits balanced on a knife-edge. Random factors like other genes or environmental conditions could send it in either direction, producing either a fertile male or a sterile female.
That’s very strange. There are many master genes that play pivotal roles in our development, controlling the growth of eyes, limbs and more. If these genes don’t work properly, the results could be catastrophic. So, they ought to be exceptionally stable—enforcing the status quo in the face of all but the most severe mutations or environmental conditions. It should take much more than a 2-fold difference in activity to change what they do. “We’d expect to see factors of 50-fold or more,” says Weiss. “These master switches are meant to be rigorously locked in. They’re not meant to be this tenuous.”
So, why does SRY operate from such a wobbly position? Why have a set-up that could so easily lead to infertility? For the variety, says Weiss. He thinks that the vagaries of SRY leads to a wide variety within developing testes, and a wide variation in the amount of testosterone they produce. This hormone influences our behaviour, including many aspects of our social lives. So, at the risk of the occasional infertile XY female, a precariously-set master switch leads to a broad spectrum of male brains, which may make for a better-functioning society. “You can’t have all alpha-males in a group,” suggests Weiss.
It’s a fairly speculative idea, and Wilson-Sayres isn’t convinced. She says that the far simpler explanation is that the Y-chromsome is especially prone to picking up mutations with weak harmful effects. Other chromosomes come in pairs and can swap parts of their DNA—a process that unites bad mutations in the same place, and allows them to be more easily weeded out by natural selection. The Y chromosome doesn’t get this benefit because it’s alone, and has nothing to swap with. It builds up harmful mutations more quickly, making it a treacherous place for a master switch to exist.
Reference: Chen, Racca, Phillips & Weiss. 2013. Inherited human sex reversal due to impaired nucleocytoplasmic trafficking of SRY defines a male transcriptional threshold. PNAS http://dx.doi.org/10.1073/pnas.1300828110
Guppies are small freshwater fishes that are popular in aquariums around the world. Unlike many fishes, where males and females squirt sperm and eggs into the surrounding water, guppy males fertilise females by delivering sperm into their bodies. They don’t have a penis, as such. Instead, they have modified a fin into a penetrating organ called a gonopodium.
These penis-ish organs are tipped with an unpleasant set of claws, hooks ridges and spines. These features evolve very quickly and they’re sometimes the only way of telling one guppy species from another. What are they for? It’s possible that the claws help males to latch onto females, even those that do not want to mate with them. Alternatively, they might help to hold sperm at the tips of the gonopodia, so they can be more easily implanted into the females.
To test these ideas, Lucia Kwan from the University of Toronto used a scalpel to slice off the claws of several males, leaving the rest of their gonopodia intact. She calls it “phenotypic engineering”. That’s a long way of saying: “a shave”.
She then released individual males into tanks with single females, and watched. It was a straightforward experiment with a clear result. Compared to shaved males, clawed ones transferred three times more sperm into unreceptive females, but the same amount into those that willingly mated.
This strongly suggests that the claws are a “sexually antagonistic trait”—one that benefits one sex over the other. In this case, they help the males to grasp resistant females. If they were simply for anchoring sperm, the de-clawed males should suffer when mating with all females, rather than just the unreceptive ones.
This is the latest in a small but growing line of phenotypic engineering genital-shaving studies, which aim to work out just why animal sex organs are so bizarrely adorned. One group laser-shaved the spikes from a fly’s penis to show that they’re like biological Velcro, allowing males to latch onto females. Another team did the same thing with a seed beetle’s penis to show that its terrifying spikes aren’t anchors—their role seems to be to puncture the female’s genital tract for reasons best known to the seed beetle.
The penises of these insects are just as varied in shape, size and spikiness as those of the guppies, so these experiments suggest that the battle of the sexes has fuelled the evolution of these groups, helping them to diversify into the many species we see today. To understand that process, scientists would need to compare the organs of many different species, but these shaving experiments are certainly a good first step.
If you’ve never seen a duck penis before, have a look at the infamous video above. That long corkscrew belongs to a Muscovy duck, and it’s typical of the group. Some ducks have helical penises that are longer than their entire bodies. But forget the helical shape, the size, and the surprisingly explosive extension—the weirdest thing about a duck’s penis is that it has one.
Most birds don’t. There are almost 10,000 species of birds and only around 3 percent of them have a penis. These include ducks, geese and swans, and large flightless birds like ostriches and emus. But eagles, flamingos, penguins and albatrosses have completely lost their penises. So have wrens, gulls, cranes, owls, pigeons, hummingbirds and woodpeckers. Chickens still have penises, but barely—they’re tiny nubs that are no good for penetrating anything.
In all of these species, males still fertilise a female’s eggs by sending sperm into her body, but without any penetration. Instead, males and females just mush their genital openings together and he transfers sperm into her in a manoeuvre called the “cloacal kiss”. Two dunnocks demonstrate the move in the video below. If you blink at 00:36, you will miss it.
“There are lots of examples of animal groups that evolved penises, but I can think of only a bare handful that subsequently lost them,” says Diane Kelly from the University of Massachusetts in Amherst. “Ornithologists have tied themselves in knots trying to explain why an organ that gives males an obvious selective advantage in so many different animal species disappeared in most birds. But it’s hard to address a question on why something happens when you don’t know much about how it happens.”
That’s where Martin Cohn came in. He wanted to know the how. His team at the University of Florida studies how limbs and genitals develop across the animal kingdom, from the loss of legs in pythons to genital deformities in humans. “In a lab that thinks about genital development, one takes notice when a species that reproduces by internal fertilization lacks a penis,” says graduate student Ana Herrera.
Waves of death
By comparing the embryos of a Pekin duck and a domestic chicken, Herrera and other team members showed that their genitals start developing in the same way. A couple of small swellings fuse together into a stub called the genital tubercle, which gradually gets bigger over the first week or so. (The same process produces a mammal’s penis.)
In ducks, the genital tubercle keeps on growing into a long coiled penis, but in the chicken, it stops around day 9, while it’s still small. Why? Cohn expected to find that chickens are missing some critical molecule. Instead, his team found that all the right penis-growing genes are switched on in the chicken’s tubercle, and its cells are certainly capable of growing.
It never develops a full-blown penis because, at a certain point, its cells start committing mass suicide. This type of ‘programmed cell death’ occurs throughout the living world and helps to carve away unwanted body parts—for example, our hands have fingers because the cells between them die when we’re embryos. For the chicken, it means no penis. “It was surprising to learn that outgrowth fails not due to absence of a critical growth factor, but due to presence of a cell death factor,” says Cohn.
His team confirmed this pattern in other species, including an alligator (crocodilians are the closest living relatives of birds). In the greylag goose, emu and alligator, the tubercle continues growing into a penis, with very little cell death. In the quail, a member of the same order as chickens, the tubercle’s cells also experience a wave of death before the organ can get big.
This wave is driven by a protein called Bmp4, which is produced along the entire length of the chicken’s tubercle, but over much less of the duck’s. When Cohn’s team soaked up this protein, the tubercle’s cells stopped dying and carried on growing. So, it’s entirely possible for a chicken to grow a penis; it’s just that Bmp4 stops this from happening. Conversely, adding extra Bmp protein to a duck tubercle could stop it from growing into its full spiralling glory, forever fixing it as a chicken-esque stub.
Bmp proteins help to control the shape and size of many body parts. They’re behind the loss of wings in soldier ants and teeth of birds. Meanwhile, bats blocked these proteins to expand the membranes between their fingers and evolve wings.
They also affect the genitals of many animals. In ducks and geese, they create the urethra, a groove in the penis that sperm travels down (“If you think about it, that’s like having your urethra melt your penis,” says Kelly.) In mice, getting rid of the proteins that keep Bmp in check leads to tiny penises. Conversely, getting rid of the Bmp proteins leads to a grossly enlarged (and almost tumour-like) penis.
To lose a penis once might be regarded as misfortune…
Penises have been lost several times in the evolution of birds. Cohn’s team have only compared two groups—the penis-less galliforms (chickens, quails and pheasants) and the penis-equipped anseriforms (swans, ducks and geese). What about the oldest group of birds—the ratites, like ostriches or emus? All of them have penises except for the kiwis, which lost theirs. And what about the largest bird group, the neoaves, which includes the vast majority of bird species? All of them are penis-less.
Maybe, all of these groups lost their penis in different ways. To find out, Herrera is now looking at how genitals develop in the neoaves. Other teams will no doubt follow suit. “The study will now allow us to more deeply explore other instances of penis loss and reduction in birds, to see whether there is more than one way to lose a penis,” says Patricia Brennan from the University of Massachussetts in Amherst, the woman behind the duck penis video at the top.
And in at least one case, what was lost might have been regained. The cracids—an group of obscure South American galliforms—have penises unlike their chicken relatives. It might have been easy for them to re-evolve these body parts, since the galliforms still have all the genetic machinery for making a penis.
We now know how chickens lost their penises, but we don’t know why a male animal that needs to put sperm inside a female would lose the organ that makes this possible. Cohn’s study hints at one possibility—it could just be a side effect of other bodily changes. Bmp4 and other related proteins are involved in the evolution of many bird body parts, including the transition from scales to feathers, the loss of teeth, and variations in beak size. Perhaps one of these transformations changed the way Bmp4 is used in the genitals and led to shrinking penises.
There are many other possible explanations. Maybe a penis-less bird finds it easier to fly, runs a smaller risk of passing on sexually-transmitted infections, or is better at avoiding predators because he mates more quickly (remember the dunnocks?).
Females might even be responsible. Male ducks often force themselves upon their females but birds without an obvious phallus can’t do that. They need the female’s cooperation in order to mate. So perhaps females started preferring males with smaller penises, so that they could exert more choice over whom fathered their chicks. (Indeed, the now-infamous story about the duck’s corkscrew penis is really a story about the duck’s corkscrew vagina.) Combinations of these explanations may be right, and different answers may apply to different groups.
And why study the why? Why would scientists care about how penises evolve (and why do I write about them so much)? Cohn makes a good argument. “Genitalia are one of the fastest-evolving organs in animals,” he explains. Even in the groups with backbones, “one sees a remarkable degree of variation”.
A female strawberry poison frog faces an abundance of choice when it comes time to breed. The forest floor is full of bright red males trying to attract her with their songs, and wrestling with other males to defend their territories. She could pick a suitor based on his size or health. She could weigh up the quality of his territory. She could judge him on the depth, volume or length of his croaking, any of which could indicate how strong he is.
Or she could just mate with the first male she finds.
That, rather anticlimactically, is exactly what happens. For all the effort that males put into attracting a partner, the only factor that seems to matter to the females is who’s nearest. And according to Ivonne Meuche from the University of Veterinary Medicine in Hanover, this strategy makes perfect sense for these frogs.
The strawberry poison frog (Oophaga pumilio) has become something of a celebrity among scientists studying frog behaviour. It’s easy to find because of its bright colours and tendency to hop about in the day. And it has lots of sex. On average, a female will only go for 4 to 5 days between partners.
The frogs practice ‘lekking’—a style of mating where many males call at the same time, allowing females to choose between them. Each male defend a small territory, and each female wanders across many of these. When she chooses a mate, the two partners face in opposite directions while she lays eggs and he fertilises them.
Meuche’s team followed 20 female frogs in the rainforests of Costa Rica to see which males they mated with. They compared the qualities of these victors to those of every other male within the females’ home ranges. They also compared the two males that were closest to the females on the morning of their egg-laying days.
In an earlier study, one of the team, Hieke Prohl, suggested that males mated with more females if they called more often and at a lower pitch. But this time, they found that females were completely oblivious to the males’ territory size, weight, length, health or calls. Instead, they just went straight for the nearest one who was calling.
You could argue that females are making pickier choices the night before, so that they’re waking up near their favoured partners on egg-laying days. But in other studies, the team showed that the females’ whereabouts don’t depend on the males but on the availability of food.
They also checked their results by using two speakers to play recordings of males with different call rates and pitches. Forty-five females heard these calls and none of them seem to care about the calls themselves. They just went for the closest speaker.
This is unusual. Lekking is almost synonymous with female choosiness, although some other frogs also use a “closest-male-wins” strategy. It presumably means that they sometimes mate with dud partners while there are prime specimens calling a bit further away.
But Meuche thinks that the females aren’t fussy because there are big costs to shopping around. In this corner of Costa Rica, female strawberry poison frogs outnumber the males. Males are in short supply, and if they’re with another female, they stay silent and cannot be found. If a female rejects a male, she might not be able to find another partner, much less a better one. If this happens, she’ll lose an entire clutch. On her egg-laying days, she has to find a mate within a certain time or she’ll just lay unfertilised eggs that never develop.
The team also found that the males are all much of a muchness. They compete so intensely for territories that those with good ones, which put them closest to as many females as possible, will probably also have good genes. Females have a good chance of getting a high-quality mate even if they grab the closest one.