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Developmental Biology - Inherited Intelligence
Learned Behaviors Can Be Inherited
After only four generations learned behaviors can be inherited via adaptations carried within eggs and sperm...
Princeton University researchers recently discovered learned behaviors can be inherited for multiple generations in the worm C. elegans, transmitted from parent to children via eggs and sperm cells. The paper by Rebecca Moore, Rachel Kaletsky and Coleen Murphy detailing this finding, appears in the June 13 issue of the journal Cell.
These inherited traits are determined exclusively by whether an individual receives the dominant or recessive form of an particular gene from each parent. Other heritable traits are influenced both by genetic makeup and by factors such as nutrition, temperature, or environmental stresses which can affect the expression levels of related genes. Features whose inheritance isn't driven exclusively by DNA sequence are determined to be "epigenetic" ("epi" meaning "on top of" or external to the gene DNA).
An organism's phenotype can change during its lifetime due to epigenetic changes.
For example, in the microscopic roundworm Caenorhabditis elegans, starvation or heat stress prompts them to adapt to these conditions by changing the expression (meaning 'function') of multiple genes. At the DNA level, these changes can be made permanent by altering how tightly packed DNA affects the encoding of that gene, literally regulating its access to RNA transcription. Alternatively, cells can engage mechanisms to destroy or isolate protein-coding RNA transcripts. When these modifications are made in germ cells, they can be passed down to future generations in a phenomenon known as transgenerational epigenetic inheritance.
Studies have shown that C. elegans adaptations to starvation and heat stress can be inherited for several generations. Might more complex phenotypes, such as behavioral changes, also be passed down in this way?
"In their natural environment, worms come into contact with many different bacterial species. Some of these are nutritious food sources, while others will infect and kill them. Worms initially attracted to the pathogen Pseudomonas Aeruginosa, after infection, learn to avoid it. Otherwise they will die within a few days."
Coleen T. Murphy PhD, Professor, Department of Molecular Biology & The Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey, USA.
Moore and her colleagues investigated whether C. elegans can convey this learned avoidance behavior to their offspring. They found that when mother worms learned to avoid pathogenic Pseudomonas aeruginosa, their offspring also knew to avoid the bacteria. The natural attraction of offspring to Pseudomonas was overridden even though they had never previously encountered the pathogen. Remarkably, this inherited aversion behavior lasted for four generations, but in the fifth generation the worms once again were attracted to Pseudomonas. In another surprise, researchers observed that inheritance of learned avoidance was not universal for all pathogenic bacteria.
Although mother worms could learn to avoid the pathogenic bacterium Serratia marcescens, which is less abundant than Pseudomonas in C. elegans' environment, this aversion was not passed down to offspring. Intrigued, the researchers set out to explore what controls transmission of P. aeruginosa avoidance behavior across generations.
The authors showed that C. elegans mothers must actually become ill from ingesting Pseudomonas aeruginosa in order to transmit avoidance to future generations. Simple exposure to odors emitted by the pathogen wasn't enough to provoke avoidance.
Nonetheless, neuronal sensory pathways are important for inherited avoidance, because avoidance behavior in both mothers and their offspring was associated with increased expression of several neuronally associated genes. Among these, elevated expression of the TGF-beta ligand daf-7 in mothers was needed for offspring to inherit pathogen aversion.
Moore and her colleagues found that daf-7 expression in ASI neurons correlated strongly with inherited avoidance behavior.
"The process of inheriting this learned avoidance [also] requires the activity of small RNAs called piRNA," added Murphy. piRNAs have been implicated in other transgenerational epigenetic inheritance pathways in C. elegans, where they are thought to silence gene expression and indirectly regulate DNA packaging. Researchers found that piRNA-associated protein PRG-1, while not necessary for C. elegans mothers to learn avoidance of Pseudomonas aeruginosa, is required for increased daf-7 expression in their offspring — and for any inherited avoidance behavior.
Whether piRNAs and PRG-1 operate primarily in the mother, her children, or both to promote inheritance of avoidance behavior isn't yet known.
Importantly, expression of daf-7 remains elevated in ASI neurons of offspring for four generations, then returns to basal levels in the fifth generation, when the inherited avoidance behavior also disappears. As Murphy points out, although inheritance of avoidance behavior provides a survival advantage, it's necessary for this avoidance behavior to eventually go away because Pseudomonas aeruginosa is only pathogenic at high temperatures. At lower temperatures, it's increasingly safe to eat, as are other Pseudomonas species.
The pathogenic threat being temporary, allows future C. elegans' generations to return to feasting on nutritious Pseudomonas.
Highlights
• C. elegans transmit learned avoidance of P. aeruginosa for four generations
• ASI and the TGF-ß ligand daf-7 are required for transgenerational PA14 avoidance
• Piwi/PRG-1 is required for transgenerational inheritance of P. aeruginosa avoidance
• Transgenerational avoidance of P. aeruginosa provides fitness benefits to offspring
Summary
The ability to inherit learned information from parents could be evolutionarily beneficial, enabling offspring to better survive dangerous conditions. We discovered that, after C. elegans have learned to avoid the pathogenic bacteria Pseudomonas aeruginosa (PA14), they pass this learned behavior on to their offspring, through either the male or female germline, persisting through the fourth generation. Expression of the TGF-ß ligand DAF-7 in the ASI sensory neurons correlates with and is required for this transgenerational avoidance behavior. Additionally, the Piwi Argonaute homolog PRG-1 and its downstream molecular components are required for transgenerational inheritance of both avoidance behavior and ASI daf-7 expression. Animals whose parents have learned to avoid PA14 display a PA14 avoidance-based survival advantage that is also prg-1 dependent, suggesting an adaptive response. Transgenerational epigenetic inheritance of pathogenic learning may optimize offspring decisions to increase survival in fluctuating environmental conditions.
Authors
Rebecca S. Moore, Rachel Kaletsky and Coleen T. Murphy.
Acknowledgements
The authors thank all the nurses and all the parents and babies who participated in this study; and the Division of ENT, the Plateforme de Recherche de Pediatrie, and the Centre for Biomedical Imaging of the University Hospital of Geneva for their support. The authors declare no competing interests. This study was supported by grants from the Swiss National Science Foundation (32473B_135817/1), the foundation Prim’enfance, and European Union’s Horizon 2020 research and innovation programme under Grant Agreement 666992.
This study is financed by the Swiss National Science Foundation as well as, among others, by the Prim'Enfance Foundation.
About MUSC
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Jun 17 2019 Fetal Timeline Maternal Timeline News
 Passing learned behavior on to offspring, through either male or female sex cells, persists through four generations — before reverting back to eating Pseudomonas aeruginosa for its nutritional value.
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