Rogue mitochondria turn hermaphroditic snails into females: study

Ssome individuals from a population of normally hermaphroditic bladder snails (Physa acuta) effectively lost their masculine function and became women, reports a researcher in an article published on April 27 in Current biology. This phenomenon, they say, is linked to mitochondrial DNA which is very different from that of fully functioning hermaphrodites of the species.

“We were studying the molecular diversity of snail populations for other reasons when we discovered that the mitochondrial DNA of these species was very heterogeneous, so that within the species there were individuals who were very, very different”, co-author Patrice David, who studies the evolution of mating systems at the CNRS in France, tells The scientist. “A fraction of the individuals of the species were completely incapable of being men.”

A bladder snail (Physa acuta)

Jean Pierre Pointier

Cytoplasmic male sterility (CMS) has been explored in plants since its discovery by German botanist Joseph Gottlieb Kölreuter in the 1700s. It is a maternally transmitted trait that inhibits the production of functional pollen in individuals carrying certain mitochondrial genomes, which triggers the death of the male sex organs of plants. Kölreuter’s research paved the way for later use of CMS in plant breeding to easily control crossbreeding. In animals, however, while rogue mitochondrial DNA is suspected sometimes cause cell death, it has never been linked to infertility.

“It’s very cool that this is the first time it’s been documented,” says Maryna Lesoway of the Scripps Institution of Oceanography in California, of the new study, which she was not involved in. “But I would be very surprised if we didn’t find it in other molluscs, as well as other animals,” she adds. “That’s probably something we could find if we started to look for it more closely.”

In the study, David and his colleagues traced the individual genotypes of 34 bladder snails near Lyon using a mitochondrial gene called THIS, which serves as a biomarker to study molecular diversity. They noticed that about 15% of individuals shared a variant of THIS which the researchers called mitotype D for “divergent.” the THIS sequence of these individuals was 26 percent different from that of other members of the population. “Within the same species, mitochondrial DNA is usually different by at most 1%,” explains David. The high percentage of snails in the bladder “means something very strange was going on,” he continues, “so we started checking.”

two brown snails mating just under water surface

Mating of two bladder snails

Benjamin Pelissie

By crossing mitotype D snails with non-divergent snails to see if they could successfully interbreed, the researchers noticed behavioral differences between the two groups. Normally, individual hermaphroditic snails are equally likely to play the male or female role when mating, but “some [mitotype D] individuals seem totally incapable of playing the male role, so the behavior of being male is suppressed,” David explains. “They don’t climb on other snails, although they accept other snails to climb on them. Also, they do not produce sperm or produce less sperm than normal individuals. In other words, snails with divergent mitochondrial genomes have male sterility; they had found the first example of CMS in an animal.

The researchers attribute this CMS in snails to rapid mutations in the mitochondrial lineage, although they do not yet understand the mechanisms. They hypothesize that certain mitochondrial genes of mitotype D snails have evolved to erase male function to leave more energy for female function, which passes mitochondria to the next generation. “Basically, the genes in the mitochondria would prefer reproduction to occur entirely through female function, and in this way they conflict with the genes in the nucleus,” David explains.

He suggests the discovery may point to a previously unknown animal sexual system. “Among animals, we know of species with separate sexes. We know hermaphroditic species. Species are known to change sex during their lifetime. But this is the first example of a species that has two categories of individuals – hermaphrodites and females – within the same species,” he says.

“It’s interesting from a basic biology perspective,” says animal geneticist Alison Van Eenennaam of the University of California, Davis, who was not involved in the work. She suggests that male sterility could become a useful tool in animal husbandry, as it already is with plants.

Lesoway suggests that this discovery will help scientists better understand how species evolve different sexual systems. “If we really look at the diversity that exists in the biological world,” she says, “there are many more different varieties of sexual reproduction than we generally know about.”