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, Cnidaria4-6 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 animals8-10−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 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.

Mutations in coral soma and sperm imply lifelong stem cell renewal and cell lineage selection

“…If we had found only separate parent and sperm SNVs this would have shown that Acropora corals have classical Weismannian germ and somatic cell lineage differentiation at the embryonic stage, which has been suggested previously 17 . Likewise, if we had found that all parent tissue SNVs were also in the sperm, we would have concluded that Acropora corals developed gametes directly from those tissues 15,16 . However, 74% of the SNVs that we identified in parent tissue were also present in the sperm spawned from that branch, and 26% were not.…”

“…If these mutations are inherited by the coral's gametes, they must increase the heritable mutational load of these animals. Some previous studies identified putative somatic mutations in the gametes or juvenile offspring of mutant parents 15,16 , but others have reported absence of somatic mutations in the gametes 17 . Wilcox test (two-tailed, paired) Parent Only, GOH Full: 4.4 x10 -7 ± 0.6 x10 -7 Coding: 9.2 x10 -8 ±3.1 x10 -8 V=28, P= 0.016…”

Extending the natural adaptive capacity of coral holobionts

“…The standing genetic diversity of corals is presumably large [71][72][73][74] , suggesting a capacity to recover from reductions in population size under suitable conditions, at least for some species 73 . Corals could also have the capacity to adapt via heritable somatic mutations 75,76 . The ability to rapidly adapt (years to decades) to changing environments is further supported by the presence and frequency of thermotolerance alleles and the modeling of population trajectories under different climate change scenarios 72,77 .…”