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Can high temperature accelerate the rate of evolution?

Researchers from Tel Aviv University demonstrated with the help of worms that epigenetic inheritance of sexual attraction can influence the process of evolution

Prof. Oded Ravavi. Photo: Tel Aviv University spokesperson
Prof. Oded Ravavi. Photo: Tel Aviv University spokesperson

What made the worm prefer sexual reproduction with males, when it can fertilize itself, and how did this affect future generations? Researchers from Tel Aviv University discovered that epigenetic inheritance (outside the DNA sequence) can affect the composition of genes in a population for many generations. The research, which is published today in the important journal Development Cell, was led by Prof. Oded Ravavi and Dr. Itai Toker, and Dr. Itamar Lev and Dr. Yael Mor, who completed their PhDs under his supervision, from the Department of Neurobiology at the Faculty of Life Sciences and the Segol School of Neuroscience at Tel Aviv University. The study was conducted in collaboration with Rockefeller University in New York.

"We raised C. elegans worms in the laboratory under heat stress conditions, that is, at slightly higher temperatures than usual," explains Prof. Ravavi. "The result was that the females became more attractive and mated more with males. It's interesting, but the really fascinating finding is that even after the worms were returned to normal temperatures, in subsequent generations, the offspring of these worms continued to attract more males. When the worms mate with males instead of fertilizing themselves, they pass on only half of their genome to the next generation. "Diluting" the hereditary contribution by half is a heavy price to pay, but the benefit is an increase in genetic diversity, and we really discovered with the help of evolution experiments in the laboratory that this may be a useful, i.e. adaptive, strategy."

The female C. elegans worms produce both their own eggs and sperm and thus fertilize themselves (therefore they are considered hermaphrodite). The worms only produce the sperm at a certain stage in their development, and later on they only produce eggs. At the same time, there are also rare males in the population who can mate with them - so it is the female's choice whether to mix her genes in sexual reproduction with a male. The environmental conditions in the experiment pushed more females to mate, a trait that was also preserved in their offspring who grew up in comfortable environments, and did not experience the heat stress.

From self-fertilization to sexual reproduction

"In the life cycle of the hermaphrodite worm, the self-sperm pool runs out when it ages," says Dr. Itai Toker. "At this stage, in order to continue reproducing, she has no choice but to secrete a pheromone that attracts the males. The heat conditions we created disrupted the inheritance of small RNA molecules that heritably control the expression of genes in the sperm, so that the worm's sperm was unable to fertilize the egg with the usual efficiency. The worm felt that the sperm it produced was partially damaged and therefore began to secrete the pheromone and attract males earlier, while it was still young. It so happened that many worms bred at a young age with male worms. This trait has been inherited for many generations to offspring that have not experienced the heat conditions."

"In the past, we discovered a dedicated mechanism that bequeaths the small RNA molecules to future generations, at the same time and in a different way from the normal mechanism that bequeaths DNA to future generations, and enables the inheritance of certain acquired traits. By inhibiting the small RNA inheritance mechanism, we proved that the inheritance of increased attraction depends on the intergenerational transmission of small RNAs that control sperm activity. Later we conducted an experiment in evolution: we followed the offspring of mothers who bequeath an attraction to males with the help of small RNAs and let them compete for males, for many generations, against normal offspring from a control lineage. We saw that the inheritance of sexual attraction led to more mating under these competitive conditions, and that as a result the attractive offspring were able to spread their genes in the population more successfully."

The environment affects the variety

As a rule, living things react to their environment by changing the expression of their genes - without changing the genes themselves. One of those control mechanisms is small RNA molecules that destroy molecules called messenger RNA (mRNA) that are responsible for transferring the genetic information from DNA to proteins - thereby silencing genes that are not needed in the given environment. The understanding that some of the epigenetic information encoded in small RNA molecules is passed from generation to generation revolutionizes our understanding of heredity, and challenges the dogma that has dominated evolution for over a hundred years. However, to date researchers have not been able to find a way in which epigenetic inheritance can affect the genetic sequence itself (DNA).

"Apigenetics in general, and the inheritance of acquired traits mediated by small RNAs in particular, is a new and sensational field," says Dr. Lev. "We have now proven for the first time that the environment can change not only the expression of genes - but, indirectly, also the genetic inheritance itself, and over generations. For the most part, epigenetic inheritance of small RNA molecules is a transient matter: the organism is exposed to a certain environment, and preserves the epigenetic variation for 3-5 generations. In contrast, evolutionary change takes hundreds and thousands of generations. We looked for a connection between epigenetics and genetics and found that a change in the environment that is relevant to global warming induces the inheritance of pheromone secretion to attract males and thus affects the evolution of the worms' genome.'

Dr. Moore adds: "It's actually a way for the environment to adjust the genetic variation." After all, evolution requires variety and choice. The classic theory is that the environment can influence selection, but cannot influence diversity - which is created randomly as a result of mutations. We have shown that the environment can indeed influence diversity under certain conditions."

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