www.quantamagazine.org /why-sex-biologists-find-new-explanations-20200423/

Why Sex? Biologists Find New Explanations

By Christie WilcoxApril 23, 2020
17-22 minutes


Why did sex evolve? Theories usually focus on the diversity of future generations, but some researchers find compelling explanations in the immediate benefits to individuals.

Sex might be biology’s most difficult enigma. The downsides of relying on sex to reproduce are undeniable: It takes two individuals, each of whom gets to pass on only part of their genome. Because these individuals generally have to get fairly intimate, they make themselves vulnerable to physical harm or infections from their partner. Asexual reproduction, or self-cloning, has none of these disadvantages. Clones can be made anywhere and anytime, and they receive the full complement of an individual’s genes.

Yet despite all its benefits, asexual reproduction is the exception, not the norm, among organisms that have compartmentalized cells (eukaryotes). In plants, for example — which are somewhat known for their genetic flexibility — less than 1% of species are thought to reproduce asexually often. Among animals, only one out of every thousand known species is exclusively asexual. For centuries, biologists have pondered this apparent paradox.

In 1932, the geneticist Hermann Muller, whose work on radiation-induced mutations would eventually garner a Nobel Prize, believed he had the answer. “Genetics has finally solved the age-old problem of the reason for the existence (i.e., the function) of sexuality and sex,” he boasted in The American Naturalist. He went on to explain, “Sexuality, through recombination, is a means for making the fullest use of the possibilities of gene mutations.”

In other words, the purpose of sex is simple: It increases genetic diversity in the pool of offspring. That diversity could then raise the fitness of future generations by making them stronger, faster, more resistant to parasites or otherwise more adaptable. Muller wasn’t the first biologist to suggest this, but his influence was so great that his name has been forever tied to the idea, which remains prevalent today.

But perhaps it shouldn’t be. After all, the diversity justification doesn’t explain how or why single-celled organisms evolved an essential component of sex: meiosis, the process of halving the genome that enables the production of egg and sperm cells.

“The focus of sexual selection and sexual hypotheses tend to really focus on the future generations,” said Caitlin McDonough, who studies the evolution of reproductive systems at Syracuse University. McDonough’s work on the evolution of sexual behaviors has found evidence that theories centering exclusively on ideas about what’s good for offspring or the species as a whole are incomplete. “Research has often overlooked the potential for direct benefits to the individual” from having sex, they said.

McDonough and other researchers are now reexamining how sex and its associated cellular and physiological processes affect individuals. Their results suggest that the reason biologists have struggled to find a truly unifying explanation for sex is that there isn’t one. Instead, there’s a veritable smorgasbord of potential benefits from sex, and organisms may engage in it for whichever ones help them the most.

Everybody Does It

In some ways, sex is universal — almost every eukaryotic organism has sex. But it is also a unique experience for each species. What sex looks like is different if you’re talking about a plant, a single-celled protozoan, a fruit fly or a human being.

Even the idea that sex is for reproduction doesn’t hold across the entire swath of eukaryotes. For the algae studied by Aurora Nedelcu, a biologist at the University of New Brunswick in Canada, sex isn’t about making more offspring. “They reproduce better asexually,” she said. The Volvox species she works with are facultatively sexual, meaning that they choose whether to clone themselves or have sex. When they opt for sex, it’s to improve their odds of survival.

For most of their lives, these algae live with what would be considered half a genome by human standards: They have only one copy of each chromosome, and so are haploid. In this state, they can undergo mitosis, the process of cloning themselves that all cells perform. First they make a copy of each of their chromosomes, then those copies line up down the centerline of the cell and are pulled apart into two new daughter cells identical to their parent.

Side-by-side photographs of Volvox colonies in two different life stages. Both are green spherical balls of cells, but with differences in the appearance of their germ cells.

The multicellular Volvox algae studied by Aurora Nedelcu of the University of New Brunswick are sexual only when it suits their purposes. Usually, the algae live as an asexual colony (left) that contains a dozen or more germ cells (green spheres inside). Under stressful conditions, the colony becomes sexual (right) and its germ cells fuse to become resistant spores (red spheres).

Aurora Nedelcu

Sometimes, though, when their environment gets too hot or lacks needed nitrogen, the algae reproduce differently. The haploid algae fuse with one another to make cells with two copies of each chromosome. In effect, the algae “have sex” and become diploid like us.

The algae go the sexual route only when life gets rough, however. Nedelcu and her colleagues found that if you alleviate their physiological stress — by providing them with a boost of antioxidants — they don’t have sex. The researchers concluded that the primary purpose of sex in these algae isn’t to produce offspring but to make the algae hardier and better able to cope with those stresses.

The immediate benefit of sex for the algae is that they form resistant diploid spores that can outlast a bad environment. When better conditions return, the algal cells return to their haploid state through meiosis. But as Nedelcu and her colleagues point out, the process of meiosis also offers unique opportunities for genomic improvement that go beyond diversity.

Like all multicellular organisms, these algae have ways of healing small breaks or errors in their DNA. But if the damage is bad enough, those mechanisms struggle to accurately repair it. In those cases, having a second copy of that strand of DNA to use as a template for the repairs can be a lifesaver. “That’s basically what most organisms have by being diploid,” Nedelcu explained.

In a haploid cell, there’s usually no easy way to copy and paste to heal a wounded region of DNA because only one chromosome is present. The exception, however, is during meiosis, when the freshly made pairs of chromosomes line up with the versions from the other parent before being pulled into separate cells. “We think that that is an opportunity for the DNA damage to be repaired,” said Nedelcu.

During meiosis, the chromosomes from each haploid parent line up and may swap sections with each other, a phenomenon known as recombination. This step greatly increases genetic diversity, but it also gives chromosomes the ability to essentially copy and paste sections from the other haploid genome to repair any damage that may have befallen their own.

Scientists have known about the DNA-repair benefit of meiosis for decades, and some earlier work has also suggested that it might explain why harmful mutations are less common than might be expected. But Nedelcu’s research calls attention to why it might have been significant in the initial evolution of sex. The fact that these algae belong to some of the oldest lineages of eukaryotes, Nedelcu said, might suggest that “the ancestral role of sex was not for reproduction.” Instead, “sex appears to have evolved as a means to respond  adaptively to stress.”

Of Plants, Protists and People

The idea that sex evolved to help organisms weather hard times isn’t entirely new. Harris and Carol Bernstein, both professors of cell biology and anatomy at the University of Arizona, proposed it back in the early 1980s. But it’s been somewhat overlooked by mainstream evolutionary biology, according to the evolutionary biologist Francesco Catania of the University of Münster. “I don’t understand why [their hypothesis] may not have been given much more credit and importance than it has,” he said.

Catania stumbled on the idea while working with the protozoa called paramecia. These single-celled organisms are covered in tiny, mobile, hairlike projections that allow them to swim about in fresh water. They, too, sexually reproduce when stressed. As Catania came to realize, when paramecia do have sex, they often do it with themselves.

“There is some anecdotal evidence that suggests self-fertilization [among paramecia] is quite widespread,” he said. That’s probably part of the reason why, overall, paramecium species have very little genetic diversity, a fact that didn’t line up with the prevailing theory that the benefit of sex is diverse offspring. So Catania decided to look a little closer.

When he did, he discovered that like Nedelcu’s algae, paramecia seem to directly and individually benefit from undergoing the process of sex. The ones that self-fertilized survived stressful conditions better than those that didn’t. Paramecia that had recently become capable of sex were similarly hardy. These findings led Catania and his colleagues to believe not only that stress induces sex, but that activating the processes necessary for sex may help paramecia handle stress. Sex, as a process, isn’t just genetic — it’s cellular, and it involves turning on or off a whole suite of genes that have other cellular functions.

Though further experiments are necessary to fully examine this idea, Catania believes that the cellular machineries for sex and for stress response are intrinsically linked. In addition to the survival benefit of self-fertilization and sexual maturity, he and his colleagues found that heat stress also activates several of the genes steering paramecia to reproductive maturity. The mere act of preparing for the merging of genomes — even if that event doesn’t actually happen — simultaneously primes the paramecium to respond well to stressful events.

A figure that shows how the stage of sexual reproduction called meiosis allows repairs to damaged DNA.

Lucy Reading-Ikkanda/Quanta Magazine

Paramecia and algae aren’t animals, of course, so their experience of sex is not guaranteed to teach us about the benefits of sex for other lineages of life. Nedelcu is careful not to extrapolate too much: Even if meiosis first evolved to repair DNA damage, she noted, “the origin of sex might be different from the adaptive role of sex in current species.”

Still, it’s possible that benefits of sex not directly tied to reproduction, such as DNA repair, occur in fungi, plants or animals, too. And even if sex is an animal’s or plant’s only means of reproducing, these indirect benefits of sex may influence why, how, when and how often that happens.

Such indirect benefits may extend far beyond meiosis. “Sex also refers to copulation and sexual behaviors,” McDonough said. Researchers studying everything from crickets to mice are starting to see that having sex can have all sorts of unexpected upsides.

Unexpected, that is, because it’s generally assumed not only that sex is inefficient compared to asexual reproduction, but that it imposes an energy burden on the individuals involved. Producing eggs or sperm, finding a mate, the act of mating — all of it takes energy and resources. Consequently, there’s a trade-off between reproduction and other things an organism might do to survive longer, such as growing bigger or bolstering its immune system.

But a lot of our understanding of the costs and benefits of sex in animals comes from model organisms such as Drosophila fruit flies, and the results in lab animals can be deceiving, said Teri Markow, a professor emeritus of cell and developmental biology at the University of California, San Diego. “The picture that you might get in nature could be very different from what you might see in the lab because the conditions are so different,” she said.

Much of the fruit fly literature suggests, for example, that there is a cost to mating. But when Markow and her colleagues looked at fruit flies in the wild, they found the opposite — what they called a “cost of virginity.” Females that had mated lived longer than ones that had not. Although she hasn’t done the detailed experiments to confirm it, Markow suspects that’s because the females benefit in more ways than one from receiving a male’s ejaculate.

Amy Worthington, a biology researcher who studies reproductive physiology and behavioral ecology at Creighton University, has seen something similar in field crickets. A female field cricket might be expected to become more vulnerable to infection after mating, when she’s presumably routing most of her energy to making eggs, but instead she becomes more resilient. “We see across species that there is a trend of mated females having stronger survivorship and stronger immune responses relative to virgins,” though the strength of that trend varies, she said.

Worthington suspects that hormonelike compounds called prostaglandins play a big role in this. They are important in the development of eggs, but they also help regulate the immune system. “We know that prostaglandin is in seminal fluids,” she said. It may be that the females can use the prostaglandin they receive from males to increase both their reproductive success and their odds of survival.

Friends With Benefits

Prostaglandin isn’t unique to crickets, or even to insects. It’s found in all kinds of animals. So receiving ejaculate may boost an individual’s immune system, Worthington said, whether that individual “is an insect or a mammal or a lizard.”

Neuroscientists have found there’s much more to the story by looking at male animals. In 2018, Leah Pyter, a professor of psychiatry and neuroscience at the Wexner Medical Center at Ohio State University, and her colleagues showed that male rats get an immune boost in their brains after having sex. This might mean that sex helps protect them from infection. Sex may also alter how well their brains work. Other scientists found that rats perform better on certain cognitive tests after mating, and that mating regularly can slow the decline in brain function associated with age.

“I think that there are definitely secondary consequences [to sexual activity] that are less explored,” Pyter said, but “it’s a tricky subject.” Not only is research on the benefits of sex often technically difficult to do, she explained, but its conclusions can be readily misinterpreted, which can have cultural or societal consequences. Even Nedelcu noted that reporters have asked if her work on algae means that stress induces sex in people — to which she replied, “Not unless you’re a haploid alga.”

Three photographs of a dragonfly, a pair of toads and a cow.

Three photographs of a dragonfly, a pair of toads and a cow.

Three photographs of a dragonfly, a pair of toads and a cow.

Nonreproductive same-sex sexual behaviors are widespread in the animal kingdom among creatures as diverse as cows, dragonflies and toads. As Caitlin McDonough of Syracuse University and their colleagues argued in a recent paper, this fact suggests that the ancestral state of sexual behaviors might not have been based exclusively on different-sex interactions.

Of course, those consequences go both ways: Cultural beliefs and views on sex influence how we go about studying and interpreting the results from research on other organisms. Our biases regarding sexual activity — like which kinds are or aren’t “normal” or proper — “have essentially affected what it is that we’ve deemed important to study in animals,” Worthington said.

McDonough agrees that our preconceptions of what sex should look like and the reasons why an individual should or shouldn’t have it have biased our understanding of animal behavior. They point to the research on same-sex behaviors in animals as a prime example of this. McDonough and their colleagues noticed that the scientific discourse surrounding same-sex behaviors involves a lot of weak or baseless assumptions — for example, that engaging in sexual acts is inherently costly, so same-sex sexual interactions must provide some overwhelming benefit, such as a large increase in lifetime reproductive output, for the behavior to arise and stick around through natural selection. But “in many situations, it isn’t costly, and it may have some kind of benefit that we don’t understand,” McDonough said.

Instead of asking why same-sex behaviors would evolve, McDonough and their colleagues “flipped the question on its head” and asked why the behaviors wouldn’t. When they did this, they realized it’s possible and maybe even likely that same-sex behaviors have occurred all along; they just aren’t costly enough to be selected against. After all, the separation of truly distinct sexes — distinct individuals that produce different-size gametes — probably came about after the evolution of meiosis and the fusion of gametes. Organisms might then have benefited from hedging their bets and attempting to reproduce with any member of their species, as the team explained in their Nature Ecology & Evolution paper last year.

It may even be that, if the fitness costs of the sexual act are low enough and the benefits are high enough, it’s not always worth searching for a suitable mate of another sex. Individuals might ultimately live longer and pass on more of their genes by having sex early and often with any member of their species they come across, or even by frequently engaging in masturbation. Such hypotheses have likely gone unexplored because our views on sex in other species are shaped by our views on sex in our own.

But as more research is conducted on how sex affects different organisms, scientists are shedding that bias and discovering that sex can have myriad positive effects, any of which might subtly shape how a species does it. “Absolutely anything that has even a modicum of benefit in terms of the number of offspring that can be produced or the quality of offspring that could be produced will be selected for by natural selection,” Worthington said.

It makes sense for the evolution of sex to be guided at least somewhat by these upsides. “Having diverse offspring is not incompatible with there being a direct benefit to going through that [sexual] process,” McDonough said. The pervasiveness of sex would make a lot of sense if the act increases reproduction both directly and indirectly, such as by increasing longevity — a win-win, you could say, in terms of evolution.

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