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Published October 21, 2020 | Supplemental Material + Submitted
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Juvenile corals inherit mutations acquired during the parents lifespan

Abstract

128 years ago, August Weismann proposed that the only source of inherited genetic variation in animals is the germline. Julian Huxley reasoned that if this were true, it would falsify Jean-Baptiste Lamarck′s theory that acquired characteristics are heritable. Since then, scientists have discovered that not all animals segregate germline cells from somatic cells permanently and early in development. In fact, throughout their lives, Cnidaria and Porifera maintain primordial stem cells that continuously give rise to both germline and somatic cells. The fate of mutations generated in this primordial stem cell line during adulthood remains an open question. It was unknown whether post−embryonic mutations could be heritable in animals−until now. Here we use two independent genetic marker analyses to show that post-embryonic mutations are inherited in the coral Acropora palmata (Cnidaria, Anthozoa). This discovery upends the long-held supposition that post-embryonic genetic mutations acquired over an animal′s lifetime in non-germline tissues are not heritable2. Over the centuries-long lifespan of a coral, the inheritance of post-embryonic mutations may not only change allele frequencies in the local larval pool but may also spread novel alleles across great distances via larval dispersal. Thus, corals may have the potential to adapt to changing environments via heritable somatic mutations. This mechanism challenges our understanding of animal adaptation and prompts a deeper examination of both the process of germline determination in clonal animals and the role of post−embryonic genetic mutations in adaptation and epigenetics. Understanding the role of post−embryonic mutations in animal adaptation will be crucial as ecological change accelerates in the Anthropocene.

Additional Information

The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license. Posted October 20, 2020. We would like to thank Kathryn Stankiewicz for her assistance with R and Drs. Dana Williams and Margaret Miller provided field support for the 2017 experiment. We also thank Meghann Devlin-Durante for her help with the microsatellite analysis, Dr. Mary Hagedorn for overseeing the larval shipment to Mote Marine Laboratory, Daisy Flores, Lucas Tichy, and Valerie Chamberland for dive and lab assistance, and Cornelia Osborne for manuscript edits. Funding was provided by Funding for this project was supported by NOAA Office for Coastal Management NA17NOS4820083, and NSF OCE-1537959 to IBB. Special thanks to the Paul G. Allen Family Foundation for funding spawning operations and larval rearing in Curacao and Florida 2018. Data and code availability: SNP data for the samples in this study can be exported at https://coralsnp.science.psu.edu/galaxy/. Code will be provided on a GitHub repository at the time of publication. Author contributions: K.L.V.K. carried out the 2017 experiment, designed the 2018 experiment, analyzed data, and co-wrote the paper; S.A.K. contributed to the design and execution of the 2017 experiment, carried out part of the SNP analyses and co-wrote the paper; T.L.C. assisted with the parentage analysis and performed the RFLP assays; S.A.V. helped with the SNP analyses and edited the paper; A.N.C. assisted with the 2017 experiment and edited the paper; C.P. reared the recruits used for SNP analyses; K.L.M. and M.J.V. collected spawn and tissue samples, coordinated fieldwork, and edited the paper; I.B.B. oversaw the research, co-designed the 2017 and 2018 experiments, obtained funding, and co-wrote the paper. The authors declare no competing interests.

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Additional details

Created:
August 19, 2023
Modified:
October 20, 2023