Behavioural traits propagate across generations via segregated iterative-somatic and gametic epigenetic mechanisms

Emma Mitchell, Shifra L. Klein, Kimon V. Argyropoulos, Ali Sharma, Robin B. Chan, Judit Gal Toth, Luendreo Barboza, Charlotte Bavley, Analia Bortolozzi, Qiuying Chen, Bingfang Liu, Joanne Ingenito, Willie Mark, Jarrod Dudakov, Steven Gross, Gilbert Di Paolo, Francesc Artigas, Marcel van den Brink and Miklos Toth ()
Additional contact information
Emma Mitchell: Weill Cornell Medical College
Shifra L. Klein: Weill Cornell Medical College
Kimon V. Argyropoulos: Memorial Sloan Kettering Cancer Center
Ali Sharma: Weill Cornell Medical College
Robin B. Chan: Columbia University Medical Center
Judit Gal Toth: Weill Cornell Medical College
Luendreo Barboza: Weill Cornell Medical College
Charlotte Bavley: Weill Cornell Medical College
Analia Bortolozzi: Institut d’Investigacions Biomèdiques de Barcelona (IIBB-CSIC)
Qiuying Chen: Weill Cornell Medical College
Bingfang Liu: Weill Cornell Medical College
Joanne Ingenito: Mouse Genetics Core Facility, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
Willie Mark: Mouse Genetics Core Facility, Sloan Kettering Institute, Memorial Sloan Kettering Cancer Center
Jarrod Dudakov: Memorial Sloan Kettering Cancer Center
Steven Gross: Weill Cornell Medical College
Gilbert Di Paolo: Columbia University Medical Center
Francesc Artigas: Institut d’Investigacions Biomèdiques de Barcelona (IIBB-CSIC)
Marcel van den Brink: Memorial Sloan Kettering Cancer Center
Miklos Toth: Weill Cornell Medical College

Nature Communications, 2016, vol. 7, issue 1, 1-16

Abstract: Abstract Parental behavioural traits can be transmitted by non-genetic mechanisms to the offspring. Although trait transmission via sperm has been extensively researched, epidemiological studies indicate the exclusive/prominent maternal transmission of many non-genetic traits. Since maternal conditions impact the offspring during gametogenesis and through fetal/early-postnatal life, the resultant phenotype is likely the aggregate of consecutive germline and somatic effects; a concept that has not been previously studied. Here, we dissected a complex maternally transmitted phenotype, reminiscent of comorbid generalized anxiety/depression, to elementary behaviours/domains and their transmission mechanisms in mice. We show that four anxiety/stress-reactive traits are transmitted via independent iterative-somatic and gametic epigenetic mechanisms across multiple generations. Somatic/gametic transmission alters DNA methylation at enhancers within synaptic genes whose functions can be linked to the behavioural traits. Traits have generation-dependent penetrance and sex specificity resulting in pleiotropy. A transmission-pathway-based concept can refine current inheritance models of psychiatric diseases and facilitate the development of better animal models and new therapeutic approaches.

Date: 2016
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DOI: 10.1038/ncomms11492

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