Inheritance of somatic mutations by animal offspring

Kuntz, Kate L. Vasquez; Kitchen, Sheila A.; Conn, Trinity; Vohsen, Samuel A.; Chan, Andrea N.; Vermeij, Mark J. A.; Page, Christopher A.; Marhaver, Kristen L.; Baums, Iliana B.

doi:10.1126/sciadv.abn0707

Cited by 20 publications

(14 citation statements)

References 81 publications

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“…R. Soc. B 290: 20221766 also in the sperm, or that there was a strong correlation between the parent VAF and the sperm VAF for P + S SNVs, we would have concluded that Acropora corals developed gametes directly from those tissues [15,16]. By contrast, the occurrence of both types of patterns suggests that germ cell differentiation in corals occurs in a different manner than posited by Weismann's Germ Plasm Theory.…”

Section: Discussionmentioning

confidence: 93%

“…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, or that there was a strong correlation between the parent VAF and the sperm VAF for P + S SNVs, we would have concluded that Acropora corals developed gametes directly from those tissues [ 15 , 16 ]. By contrast, the occurrence of both types of patterns suggests that germ cell differentiation in corals occurs in a different manner than posited by Weismann's Germ Plasm Theory.…”

Section: Discussionmentioning

confidence: 99%

“…If these mutations are inherited by the coral's gametes, they may 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 ]. These studies tracked few mutations, ranging from 9 to 170, and none detected germline mutations in gametes or offspring.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2023

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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 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 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 post-embryonic single nucleotide variants (SNVs) unique to each parent branch, then checked if each SNV was shared by the respective sperm pool. Twenty-six per cent of post-embryonic SNVs were shared by the sperm and 74% were not. We also identified germline SNVs, those that were present in the sperm but not in the parent. These data suggest that self-renewing stem cells 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 the evolution of germlines in metazoans, these insights inform how corals may generate adaptive diversity necessary in the face of global climate change.

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Section: Discussionmentioning

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2023

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“…Animal colonies consisting of many modules may remain coherent entities where colony traits have the evolutionary potential to respond to natural selection (Simpson et al., 2020). Remarkably, variants may arise locally, and single modules may have some evolutionary potential (Vasquez Kuntz et al., 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Animal colonies consisting of many modules may remain coherent entities where colony traits have the evolutionary potential to respond to natural selection(Simpson et al, 2020). Remarkably, variants may arise locally, and single modules may have some evolutionary potential(Vasquez Kuntz et al, 2022).Local modular plasticity was accompanied by significant methylome and transcriptome modifications. Our data showed a significant light-mediated change in coral morphology, a phenotypic adjustment reflected in molecular signatures of changes in growth, including soft tissue growth and biomineralization.…”

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confidence: 99%

Phenotypic plasticity for improved light harvesting, in tandem with methylome repatterning in reef‐building corals

Gomez‐Campo,

Sanchez,

Martinez‐Rugerio

et al. 2023

Molecular Ecology

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Acclimatization through phenotypic plasticity represents a more rapid response to environmental change than adaptation and is vital to optimize organisms' performance in different conditions. Generally, animals are less phenotypically plastic than plants, but reef‐building corals exhibit plant‐like properties. They are light dependent with a sessile and modular construction that facilitates rapid morphological changes within their lifetime. We induced phenotypic changes by altering light exposure in a reciprocal transplant experiment and found that coral plasticity is a colony trait emerging from comprehensive morphological and physiological changes within the colony. Plasticity in skeletal features optimized coral light harvesting and utilization and paralleled significant methylome and transcriptome modifications. Network‐associated responses resulted in the identification of hub genes and clusters associated to the change in phenotype: inter‐partner recognition and phagocytosis, soft tissue growth and biomineralization. Furthermore, we identified hub genes putatively involved in animal photoreception–phototransduction. These findings fundamentally advance our understanding of how reef‐building corals repattern the methylome and adjust a phenotype, revealing an important role of light sensing by the coral animal to optimize photosynthetic performance of the symbionts.

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On the distribution and diversity of tissue-specific somatic mutations in honey bee (Apis mellifera) drones

Shultz,

Carey,

Ragheb

et al. 2024

Insect. Soc.

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Somatic mutations originate from both exogenous (e.g. UV radiation, chemical agents) and endogenous (e.g., DNA replication, defective DNA repair) sources and can have significant impacts on an animal’s reproductive success. This may be especially true for haploid organisms that are susceptible to any deleterious alleles inherited from their parent and any that arise over their lifetime. Unfortunately, little is known about the rate of somatic mutation accumulation across individuals and tissues of haplodiploid animal populations, the functional processes through which they arise, and their distribution across tissues and the genome. Here, we generated short-read whole-genome sequencing data for four tissues of haploid honey bee males. We paired this with estimates of telomere length and tissue-specific DNA content to address three major questions: is there variance in somatic mutational load across haploid individuals and specific tissues therein, does increased DNA content in a tissue contribute to somatic mutational load, and does telomere length correlate with mutational load? Our results suggest that variance in somatic mutational load is better captured across individuals than across tissues, that tissue-specific DNA content is not associated with somatic mutation load, and that variance in telomere length does not correlate with somatic mutation loads across tissues. To our knowledge, this is the first observational study on somatic mutational load in Apoidea and likely Hymenoptera. It serves as a useful advent for additional studies understanding the processes through which haploids tolerate or repair somatic mutations.

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Inheritance of somatic mutations by animal offspring

Cited by 20 publications

References 81 publications

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

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

Phenotypic plasticity for improved light harvesting, in tandem with methylome repatterning in reef‐building corals

On the distribution and diversity of tissue-specific somatic mutations in honey bee (Apis mellifera) drones

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