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Decades ago, behavioral neurobiologist David Crews read a strange report about the desert grassland whiptail, a small, slender lizard that lives in the sagebrush of the American Southwest. The paper claimed that the species was entirely female, and reproduced by cloning. It tested the limits of what Crews felt to be biologically plausible in higher vertebrates. “I didn’t believe that such a thing existed,” he says. But he was curious, and a friend who was going to New Mexico offered to collect some from the wild. Crews, who at the time was at the Harvard Museum of Comparative Zoology, installed a half-dozen whiptail lizards in glass tanks in his animal room. One day, he noticed a lizard biting at her cagemate’s rear legs and tail, and soon after that, riding atop her. Crews instantly recognized that they were doing what lizards do when they have sex. But why would two females simulate the act of mating?
“I literally fell out of my chair trying to get to my camera,” Crews says. “In those days, you’d keep the film in the freezer, and I’m trying to cram it into the camera so I could document it, because at that time I thought it was rare—just weird.” He snapped photos as the two adopted the “donut” pose—a contorted mating posture in which the top lizard twists around and bites the belly of the other.
Crews, now a professor of zoology and psychology at the University of Texas at Austin, looked beyond the possibility that the whiptails were just having fun. What he saw that day was crucial to his decades-long exploration of the neural basis of sexual behavior in these lizards. For him, that day in the animal room opened up a whole new world of biological understanding. He and other researchers have since shown that parthenogenesis—the ability to reproduce without sex—turns out to be more relevant to our understanding of the relationship between reproduction and evolution than anyone would have believed.
Sex is far from a perfect way to reproduce. It imposes a huge cost on a species, and that cost is called “males.” If roughly 50 percent of a species is made up of males who are incapable of producing babies, it is at a serious reproductive disadvantage relative to another species made up mostly of females capable of reproducing on their own.
And an animal that reproduces by herself has a big advantage when moving into new territory, because she doesn’t need a partner to be fruitful and multiply. Every single one of her babies will also produce its own offspring. Sexual reproduction “seems like a simple thing, but from an evolutionary perspective, it’s so inefficient,” says Rob Denton, who studies unisexual salamanders at Ohio State University. “It’d be so much easier if everyone were female.”
Brains don’t come pre-wired to act male or female, but are organized by sex chromosomes, hormones, environment, and experience.
Despite its drawbacks, sex does seem to offer a species an incontrovertible advantage. It recombines individuals’ genes so that the species as a whole can maintain the diversity of traits it needs to survive whatever challenges—faster predators, changing climate, giant comet impacts—the future may throw at it. That way the species as a whole can benefit from any useful mutations that randomly pop up in one individual. Sex also protects any one individual from inbreeding—being burdened by too many recessive genes, which often are dangerous. “Genetic diversity has always been seen as the way to adapt to changing conditions,” says Warren Booth, an evolutionary biologist and geneticist at the University of Tulsa.
By this logic, parthenogenesis is an evolutionary cul-de-sac. A population of unisexuals with essentially a single genome between them should be catastrophically unprepared for the challenges of survival. And yet the desert grassland whiptail lizard thrives. It’s also not alone. Since DNA testing has become cheap, parthenogenic reproduction has begun to reveal itself like some dark secret that certain species have been hiding from biologists since before Darwin’s voyage on the HMS Beagle. And some researchers have begun to suspect that it might not be such a bad way to survive.
In the early 2000s, Peter Baumann, a Howard Hughes investigator and molecular biologist at the Stowers Institute for Medical Research in Kansas City, started poking around inside the cells of whiptails for a better understanding of how some members of the whiptails’ genus reproduce sexually while others are parthenogenic—and whether unisexuality really is an evolutionary dead end. Back in the 1960s, researchers had discovered that individual unisexual whiptails are more genetically diverse than would be expected for a species that reproduces by cloning. In work that he hasn’t yet published, Baumann has found just as much genetic diversity in unisexual whiptails at some points in the genome as in closely related sexual species—in other parts, there’s far less.
Earlier this year, a team from the American Museum of Natural History compared easily measurable traits such as scales along the belly, or pores on the right leg, from seven generations of one line of parthenogenic whiptails with a sexually reproducing species. The parthenogens showed just as much physical variability as sexually reproducing whiptails, even though the parthenogens all had identical DNA.
How is that possible? One reason is that the desert grassland whiptail started out as a hybrid. The whole lineage is the product of two closely related whiptail species that apparently had a sexual adventure many thousands of years ago. Hybrids that survive often flourish, presumably because they’re so outbred: They get the benefit of genes from two different species, which reduces the possibility of inheriting two copies of a dangerous recessive gene variant.
Perhaps because of the mismatch between her parents, the desert grassland whiptail is born with three sets of DNA, something Lewis Pennock discovered in 1965. Instead of the usual two copies of the genome in each cell, she has two from her hybrid mother, and one from her father, who was a different species. For any given gene, she might have three slightly different versions, increasing the odds that one of them turns out to be useful. “It’s very clear that having an extra set of genes is an advantage,” says Baumann, although exactly how the lizards’ bodies regulate and control those extra genes to take advantage of their variety is a mystery.
In a 2010 study, Baumann also found that whiptails use a special mechanism to preserve this genetic diversity over many generations. Normally, in animals that reproduce sexually, much of the parental DNA gets tossed out during egg and sperm cell formation: After the genome duplicates itself, the complementary chromosomes line up next to each other and “cross over,” swapping segments of DNA. In a female’s body, for example, as she produces an egg, the copy of chromosome 21 that originally came from her own father recombines with the chromosome 21 that originally came from her mother. This reshuffling of the genetic deck creates a unique combination of her parents’ genomes in each of her own eggs. The same thing happens in sperm. It’s why siblings can be so different from one another—each child gets a different mix of each of its parents’ genetic inheritance.
As this happens, approximately half of that ancestral genetic variation is also lost. That’s not a problem for a sexual species, where an egg cell combines with a genetically distinct sperm. But in a unisexual species, it’s bad news: As the chromosomes recombine and cross over in each generation, more and more variation is lost, and more and more of the genes have multiple copies (alleles) of the same variant. Eventually, later generations would have identical alleles for every gene in the genome, predisposing them to recessive genetic diseases. It’s like an old cassette tape that’s been duplicated over and over again, losing a little bit of information every time.
In that paper, Baumann explained how whiptails have customized the process of egg formation to prevent that loss of genetic variation. When a whiptail egg forms, the genome duplicates itself a second time. The extra DNA allows a tweak to the process, so that only chromosomes that are already identical trade genetic material. Since they’re the same, recombining and crossing over changes nothing: The resulting egg cell, which will soon become a new baby whiptail, has half its DNA from the female lizard’s long-ago female ancestor, and half from her long-ago male ancestor. All the genetic information is retained for the next generation, a form of lossless reproduction. Each generation of unisexual whiptails thus maintains the genetic diversity of the one before it.
What’s more, mathematical models created by evolutionary biologists suggest that good mutations can actually spread almost as fast in a population that is primarily parthenogenic.1 The benefits of sex seem to top out if it happens just once every 10 or 20 generations; as one recent paper put it, sexually reproducing just 5 to 10 percent of the time is enough to get the same genetic advantages as doing it every time. But models aside, for a long time there wasn’t much direct experimental evidence that parthenogenesis can succeed over the longer haul.
That could explain how parthenogenesis is such a successful strategy for whiptails. But why would they have fake sex? What, exactly, was Crews seeing in his lab back in the summer of 1979? The answer has to do with the complexity of gender roles in the species.
Desert grassland whiptails don’t take on a single gender role. Each of them can act either “male” or “female” at different times, and they can switch back and forth. In the majority of sexual species, sexual behavior is shaped by two different sets of chromosomes (XX and XY), different behavior-related hormones that shape brain development, and different hormonal patterns as adults. Somehow, the whiptails reproduce male-like behavior without any of that machinery. Lauren O’Connell, a former graduate student in Crews’ lab who herself is now a Bauer fellow at Harvard, is investigating the gene changes that enabled the desert grassland whiptails’ shift to unisexuality. She found that in these animals, one gene that is normally switched on or off by testosterone and other “male” hormones is now sensitive instead to progesterone, a hormone previously thought to be most important in maintaining pregnancy.
Progesterone is the trigger for girl lizards to act like boys.2 Before a desert grassland whiptail ovulates, when her progesterone levels are low and estrogen is high, she plays the female role for sex. Technically, this is “pseudosex”: It may seem fake, but it is entirely real for the lizard, triggering hormonal changes that start her reproductive process. Fake sex stimulates the eggs within the “receptive” partner (the one who was getting bit and mounted) to begin developing by re-synchronizing her hormonal rhythms. After ovulation, as her progesterone rises, she’ll act male. When she mounts and bites another female, she probably already has eggs developing inside her.
Sex is far from a perfect way to reproduce. It imposes a huge cost on a species, and that cost is called “males.”
Lizards that don’t get the chance to fake-mate don’t lay as many eggs, Crews found in several studies in the mid-1980s. He later showed in 2008 that two regions of the brain—the medial preoptic area and the ventromedial nucleus of the hypothalamus—are involved in both behaviors, yin-yang style. During male-like behavior, the medial preoptic area becomes more active, and the hypothalamic nucleus goes quiet. During female-like behavior, it’s the opposite.3, 4
Both male and female possibilities are there in the lizard’s brain, just waiting for the right input. “The brain is inherently bisexual,” Crews believes. But in species with two sexes, “it’s just predisposed in one direction or another.” It’s obvious in whiptails, but to one degree or another, it’s true of animal brains in general, he says. These parthenogens show us the limits of our assumptions about sexuality. Brains don’t come pre-wired to act male or female, says Crews, but are organized by sex chromosomes, hormones, environment, and experience. Fake sex complicates simplistic assumptions about male hormones and female hormones, male genes versus female ones. “All vertebrates have these same genes,” says Crews. “It’s literally an orchestra of the same players, but they play different tunes.”
It’s true for us too, he says. He was the first to demonstrate a biological component to same-sex interactions, and his research was championed by early gay and lesbian activists. In his mind, it’s been clear from early on that sexuality is not binary, but only recently has the broader culture caught up with that reality. “People are animals,” he says. “We’re just an animal, who happens to have a society and culture.”
Actual parthenogenesis, though, would never work for us or any other mammal the way it does for these lizards. In mammalian eggs and sperm, some sets of genes are permanently turned off or on depending on whether they’re inherited from the paternal or maternal side. If this complementary system is disrupted, embryos can’t develop normally. So if we have parthenogens in our ancestry, they would’ve lurked far back in the vertebrate past.
However, in that long history of evolution, hybridizations that create new unisexual species may have been not so rare. Hybrid crosses followed by parthenogenesis might have always been a crucible for generating novel unisexual species like desert grassland whiptails—not slowly and gradually over many generations, but all of a sudden, in one sexual act. If the hybrid they create is unisexual, the new line is reproductively isolated from the get go. Presto: instant speciation.
It’s an argument that Baumann finds compelling. In his lab, his group created their own hybrid parthenogens in 2014, when two species of whiptails: specifically, a little striped whiptail (a sexual species) and a Chihuahuan spotted whiptail (normally a parthenogen) reproduced. Although most of the resulting babies were sterile, they did produce four lineages of new parthenogenic hybrids, each with four copies of the genome—an incipient new species.
Since it happened so naturally in the lab, Baumann and his collaborators have begun looking for that same cross roaming the sage scrub of New Mexico. They suspect that since it looks a lot like its parents—a slender, tawny striped lizard with a long tail washed in sky blue—it’s out there already. It’s just that nobody’s recognized them yet.
Kat McGowan is an independent journalist based in Berkeley, California, and New York City. Find her on Twitter @mcgowankat.
References
1. Servedio, M.R., et al. Just a theory—The utility of mathematical models in evolutionary biology. PLOS Biology 12, e1002017 (2014).
2. Moore, M.C., Whittier, J.M., & Crews, D. Sex steroid hormones during the ovarian cycle of an all-female, parthenogenetic lizard correlation with pseudosexual behavior. General and Comparative Endocrinology 60, 144-153 (1985).
3. Rand, M.S. & Crews, D. The bisexual brain: Sex behavior differences and sex difference in parthenogenetic and sexual lizards. Brain Research 663, 163-167 (1994).
4. Wade, J. & Crews, D. The relationship between reproductive state and “sexually” dimorphic brain areas in sexually reproducing and parthenogenetic whiptail lizards. The Journal of Comparative Neurology 309, 507-514 (1991).
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