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smithsonianmag.com

The Evolution of Sex Could Have

Provided a Defense Against Cancer
Cells
Jon Kelvey
8-11 minutes

Why organisms began having sex, rather than simply reproducing

asexually as life did for billions of years—and still does, in the case
of single-celled organisms and some plants and fungi—is a bit of a
mystery. Sexual reproduction evolved around a billion years ago or
more, despite the additional energy required and the seeming
hinderance of needing to find a suitable mate. Prevailing theories
hold that sex became the dominant form of reproduction due to the
benefits of greater genetic diversity, allowing offspring to adapt to
changing environments and keeping species one step ahead of
parasites that evolved to plague the parents.

But in a new paper in PLOS Biology, a team of scientists led by the

University of Montpellier in France and Deakin University in
Australia suggest another reason life started and kept having sex:
the threat of transmissible, cancerous freeloaders.

“We suggest that sexual reproduction evolves to prevent invasion

by transmissible selfish neoplastic cheater cells, henceforth
referred to as transmissible cancer cells,” Frederic Thomas, an
evolutionary biologist at the University of Montpellier and lead

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author of the study, says in an email. “To our knowledge, this

selective scenario for the initial evolution of sex across the tree of
life is novel.”

Cancer wasn’t a problem for the earliest life forms, prokaryotes, or

single-celled organisms that lack a cell nucleus, such as bacteria
and archaea. These creatures reproduce asexually, making a copy
of their singular chromosome and essentially cloning themselves.

But things changed with the evolution of eukaryotes more than 2.5
billion years ago. These organisms contain central nuclei
encompassing their genomes in a set of chromosomes. Groups of
eukaryotes joined together to form the first multicellular
organisms—the predecessors of all complex life on Earth, from
plants to insects and reptiles to mammals. When these organisms
reproduce, genetic material is contributed from two mates, creating
genetically unique offspring.

“Sex seems to have accompanied, directly predated or actually

marked the transition to eukaryotic life,” says Maurine Neiman, an
associate professor of biology at University of Iowa who studies
sexual reproduction but was not involved in the new study. The big
question in evolutionary biology, she says, is why.

Sex is really complicated and inefficient. Many organisms must

invest biological resources in traits that serve the sole purpose of
attracting a mate, such as peacock feathers. Even the act of
copulation itself carries risk. “Organisms are often literally stuck
together, and that’s not really a great situation be in,” Neiman says.
The idea that a creature successful enough to reach reproductive
maturity would want to mess with the genetic formula is also odd.
“You’re kind of a sure thing if you have grown up and been

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successful. Why would you go and make a baby different from

you?”

By blending genetics, sexual reproduction produces greater genetic

diversity in a population, limiting the transmission of cancer cells across
individuals in the population. (Thomas et al. / PLOS Biology 10.1371)

One leading theory is known as the Red Queen hypothesis. The

idea suggests that as multicellular life evolved, so did the parasites
and pathogens that plagued it. By using sex to create offspring with
unique genetic traits, some of the offspring may acquire resistances

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to the bugs that would otherwise threaten entire species. Sexual

reproduction serves as a way to stay a step ahead the evolutionary
arms race. (The name of the hypothesis comes from a statement
by the Red Queen to Alice in Lewis Carroll's Through the Looking-
Glass: “Now, here, you see, it takes all the running you can do, to
keep in the same place.”)

The new study suggests that cancer cells can be considered

another form of parasite. As early cells banded together to form
single, eukaryotic organisms, these organisms would have needed
to guard against member cells that refused to subordinate
themselves to the whole—“internal cheater cells,” or cancer cells.
Early multicellular organisms would also have needed to develop
defenses against invading malignant cells from other organisms, or
transmissible cancers.

Such early immune systems would have had an easier time

differentiating between healthy cells and malignancies, the study
argues, if sexual reproduction created offspring that were
genetically distinct from surrounding organisms. Targeting
cancerous cells could have created an evolutionary pressure to
embrace sex, similar to the pressure from parasites and other
pathogens.

“Malignant cells—at least in our opinion—have the same

importance in evolutionary biology and ecology as non-self
parasites and therefore should be considered as important as
parasites and microbiota,” Thomas says. “Cancer is not only a
disease, it is an evolutionary force.”

This idea could be a powerful new way of thinking about evolution,

according to Steve Johnson, a biologist studying the evolution of

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sex and host-parasite interactions at the University of New Orleans.

“The more I think about it, I really believe this could be a very
important new approach,” he says in an email. “I especially like
their linking Red Queen modeling with the idea that sexual
reproduction reduces a unique kind of parasite, the transmissible
cancer cells.”

“You can think of cancer as this selfish phenomenon that dies with
the individual,” Neiman adds. “But what if it didn’t? How would that
change the evolutionary landscape?”

In the paper, Thomas and colleagues lay out some of the changes
to the evolutionary landscape they would expect to see if their
hypothesis is correct. Transmissible cancers, for example, would
likely be rare in sexually reproducing species, and this is in fact the
case. Only a handful of examples exist, such as Tasmanian devil
facial lesions and leukemia in some clams.

The team also predicts that most asexually reproducing species

would either be relatively young or els specially adapted to resist
cancer. And, indeed, they found that around half of known asexual
lineages are estimated to be less than 500,000 years old. “The
remaining 50 percent of lineages consist of evolutionarily
scandalous” organisms known to be resistant to mutagens, the new
paper says. Such organisms, Thomas says, could be worth
studying to learn more about their anticancer protections for
medical use.

But there is a reason the origin of sex is considered a tough

problem in evolutionary biology. In Neiman’s estimation, there are
elements of the new theory that don’t quite add up—at least not yet.
The rarity of transmissible cancers among creatures today, for

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example, may not support this new theory.

A “universe in which cancer was explaining sex would require that

those contagious cancers were really quite common,” Neiman says.
She also wonders about one of the central assumptions of the
theory, that the genetic distinctness of parents and offspring would
actually be a factor in successfully fighting off cancerous infection.
“I am not sure it’s been well tested, and it’s a very key assumption.”

Thomas admits his team’s hypothesis needs to be validated

through experimentation, which at this point is lacking. “We propose
in the paper several directions for that, the most elegant one would
be to use animal cloning to evaluate the risk of cancer cell
transmission associated with asexual reproduction,” he says. If the
new theory of sexual reproduction is correct, the likelihood that a
mother passes cancer cells to her offspring should be higher if the
embryo is an implanted clone of the mother, rather than a
genetically distinct embryo.

The team is also working with cloned hydra, marine organisms that
can reproduce both sexually and asexually depending on
environmental conditions. According to Thomas Madsen, a life
scientist at Deakin University and coauthor of the new study, the
goal is to “try to ‘infect’ healthy clonal hydras with cancer cells and
investigate their evolutionary response.” If the new theory of sex is
correct, infected hydras should choose sexual reproduction over
asexual.

But the origin of sex has always been messy, and Neiman believes
it will stay that way. “I think the complexity and just messiness of
biology is often going to demand what we call pluralistic or multiple
explanations,” she says. “I don’t think there is going to be a general,

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elegant, single, simple solution, ever.”

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