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

Abstract

In many animals, the germline differentiates early in embryogenesis, so only mutations that accumulate in germ cells are inherited by offspring. Exceptions to this developmental process may indicate that other mechanisms have evolved to limit the effects of deleterious mutation accumulation. Stony corals are animals that can live for hundreds of years and have long been thought to produce gametes from somatic tissue. To clarify conflicting evidence about germline-soma distinction in corals, we sequenced high coverage, full genomes with technical replicates for parent coral branches and their sperm pools. We identified single nucleotide variants (SNVs) unique to each parent branch, then checked if each SNV was shared by the respective sperm pool: 26% of post-embryonic SNVs were shared by the sperm and 74% were not. We also identified germline SNVs, those that present in the sperm but not in the parent. These data suggest that self-renewing stem cells in corals differentiate into germ and soma throughout the adult life of the colony, with SNV rates and patterns differing markedly in stem, soma, and germ lineages. In addition to informing germline evolution, these insights inform how corals may generate adaptive diversity necessary in the face of global climate change.

Inheritance of somatic mutations by animal offspring

“…These alleles could have arisen from other sources such as germline mutations, postembryonic mutations, or technical artifacts. While the exact source of these mutations is unknown, germline mutations found exclusively in coral sperm from Acropora hyacinthus made up 8.5% of all identified mutations ( 19 ), in line with our findings here. Future work is required to confirm somatic mutation inheritance by biparental offspring as estimated in our analysis.…”

“…Mutations may have originated in the soma, dedifferentiated into stem cells, and then redifferentiated into germ cells, or somatic cells may have transdifferentiated directly into germ cells ( 39 ). Stem cells have not yet been identified in corals; however, the regenerative properties of anthozoans ( 40 , 41 ) and the identification of progenitor/undifferentiated cells with stem cell characteristics in a sea anemone ( 42 ) and in coral cell lines ( 43 ) both point to their existence ( 19 , 35 ). In any case, the mutations identified and tracked in this study must have occurred after embryogenesis of the primary polyp that founded the genet was complete because the mutations were not shared among all polyps of the adult parent genet or all ramets of the genet.…”

“…Beneficial (or neutral) mutations that survive developmental selection can therefore be disproportionately represented in the cells of a genet (50) For example, at locus AX-212300259, one offspring had an unexpected mutant AA genotype, while the parent from Florida did not have an A allele to contribute. These unexpected alleles in the offspring may have resulted from technical errors (26) or represent de novo (germline) mutations (19,35). n/a, no mutant allele detected.…”

“…While parental somatic mutations were previously observed in coral gametes ( 19 , 20 ), the technical difficulty of tracking somatic mutations from parents, into gametes, through sexual reproduction, and into offspring has prevented researchers from determining whether somatic mutations can be passed to viable offspring and thus play a role in coral evolution ( 21 , 22 ). Here, we discover a class of uniparental, coral offspring and we leverage this phenomenon to show that parental somatic mutations are inherited by healthy coral offspring.…”

Evolution via somatic genetic variation in modular species

“…As predicted from theory, (e.g. [7,22], substantial somatic genetic variation has now been identified in clonal plants [3,16], fungi [19], algae [20] and basal invertebrates such as corals [17,18,23]. Some species of fungi and of plants feature much less somatic genetic variation than anticipated, suggesting dedicated mechanisms of keeping somatic mutation rates low and hence, maintaining genome integrity [24,25].…”