Juvenile corals inherit mutations acquired during the parent’s lifespan

Abstract

128 years ago, August Weismann proposed that the only source of inherited genetic variation in animals is the germline¹. Julian Huxley reasoned that if this were true, it would falsify Jean-Baptiste Lamarck’s theory that acquired characteristics are heritable². Since then, scientists have discovered that not all animals segregate germline cells from somatic cells permanently and early in development³. In fact, throughout their lives, Cnidaria^4–6 and Porifera⁷ 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^8–10—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 mutations¹⁰. This mechanism challenges our understanding of animal adaptation and prompts a deeper examination of both the process of germline determination in Cnidaria and the role of post-embryonic genetic mutations in adaptation and epigenetics of modular animals. Understanding the role of post-embryonic mutations in animal adaptation will be crucial as ecological change accelerates in the Anthropocene.