Tel Aviv University researchers use worms to


image: Hermaphrodites of the nematode C. elegans after mating with a male. The male’s sperm is fluorescent (in red), which makes it possible to detect insemination events.
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Credit: Itai Toker.

Tel Aviv University researchers using worms to demonstrate that the epigenetic inheritance of sexual attractiveness can impact the evolutionary process

Researchers at Tel Aviv University have found that epigenetic inheritance (not involving changes in DNA sequence) can affect the genetic makeup of the population for many generations. The study, published today in the journal Development Cell, was led by Prof. Oded Rechavi and Dr. Itai Toker, as well as Dr. Itamar Lev and MD student Dr. Yael Mor, who did their PhDs under Prof. Rechavi at the School of Neurobiology, Biochemistry and Biophysics , George S. Wise School of Life Sciences and Sagol School of Neuroscience. The study was conducted in collaboration with Rockefeller University in New York.

“We grew up C.elegans worms in the laboratory under stressful temperature conditions, i.e. at temperatures slightly above normal,” explains Professor Rechavi. “The result was that the worms became more attractive and mated more with males. That in itself is interesting, but the truly fascinating finding is that even after the worms returned to normal temperatures, their offspring, for several generations, continued to be more attractive to males. We found that inherited small RNA molecules, not DNA modifications, transmitted the increased attractiveness between generations. When hermaphroditic worms mate with males instead of fertilizing each other, they only pass on half of their genome to the next generation. This “dilution” of the genetic contribution of the parents is a heavy price to pay, but the advantage is that it increases genetic diversity. By conducting evolutionary experiments in the laboratory, we have indeed discovered that this can be a useful adaptive strategy.”

females of the worm species C.elegans produce both eggs (or oocytes) and sperm, and can self-reproduce (so they are considered hermaphrodites). Hermaphrodites produce their sperm in limited quantities, only when they are young. At the same time, there are also rare C.elegans population males who can supply more sperm to hermaphrodites through mating. Under normal conditions hermaphrodites secrete pheromones to attract males for mating only when they grow old and lack their own sperm (at this point mating becomes the only way for them to continue and reproduce) . Therefore, when the hermaphrodite is young and still has sperm, he can choose to mix his genes by reproducing sexually with a male or not. In the new study, exposure to high temperatures was found to encourage more hermaphrodites to mate, and this trait was also preserved in offspring for several generations, even if they were raised at temperatures comfortable and have not suffered the stress of increased heat.

“In the life cycle of the hermaphrodite worm, the sperm reservoir becomes depleted as the worm ages,” says Dr Itai Toker. “At that point, to continue reproducing, the worm has no choice but to secrete a pheromone that attracts males. The heat conditions we created disrupted the inheritance of small molecules of RNAs that control gene expression in sperm.The worm’s sperm was unable to fertilize the egg with the efficiency it normally would.The worm sensed that the sperm it was producing was partially damaged and therefore began to secrete the pheromone and attract males at an earlier stage when still young.This led to more worms mating at a young age with male worms.This trait (increased attractiveness) was passed down for many generations to offspring that did not experience the higher temperature conditions.

Small RNAs control gene expression through a mechanism known as RNA interference or gene silencing – they can destroy mRNA molecules and thus prevent specific genes from functioning at any given time in a tissue or given cell. “In the past, we discovered a mechanism that transmitted small RNA molecules to future generations, in parallel and in a different way from the usual DNA-based inheritance mechanism. This allows the transmission of certain traits in a transgenerational way. By specifically inhibiting the mechanism of small RNA inheritance, we demonstrated that the inheritance of increased attractiveness depends on the transmission of small RNAs that control sperm activity. Later, we experimented with evolution: we tracked the offspring of mothers who passed on the attractiveness trait to males using small RNAs, and allowed them to compete for males, for many generations, against normal offspring from a control group. We saw that the inheritance of sexual attractiveness led to more matings under these competitive conditions, and as a result, the attractive offspring were able to spread their genes through the population more successfully.”

In general, living beings react to their environment by modifying the expression of their genes, without modifying the genes themselves. The understanding that some of the epigenetic information, including information about parental responses to environmental challenges, is encoded in small RNA molecules and can be passed from generation to generation has revolutionized our understanding of heredity, challenging the dogma that has dominated evolution for a century or more. However, to date, researchers have not been able to find a way in which epigenetic inheritance can affect the genetic (DNA) sequence itself.

“Epigenetics in general, and the inheritance of small RNA-mediated parental responses in particular, is a new area that is getting a lot of attention,” says Dr. Lev. “We have now proven that the environment can modify not only gene expression, but indirectly also genetic inheritance, and this, for many generations. Generally, the epigenetic inheritance of small RNA molecules is a transient phenomenon: the organism is exposed to an environment, and preserves epigenetic information for 3 to 5 generations. In contrast, evolutionary change occurs over hundreds and thousands of generations. We looked for a link between epigenetics and genetics and found that a change in the environment, which is relevant to global warming, induces transgenerational secretion of a pheromone to attract males, and thus affects worm genome evolution.”

Dr Mor adds: “We think this is a way for the environment to adjust genetic diversity. After all, evolution requires variability and selection. The classic theory is that environment can influence selection, but cannot affect variability, which is randomly created as a result of mutations. We found that the environment can actually effect genetic diversity under certain conditions.

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