Heritable epigenetic changes at single genes: challenges and opportunities in Caenorhabditis elegans

Chey, Mary; Jose, Antony M.

doi:10.1016/j.tig.2021.08.011

Cited by 15 publications

(10 citation statements)

References 15 publications

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“…Genes expressed within the germline are likely regulated by positive feedback loops required to continually produce factors for maintaining germline immortality and for preserving form and function across generations 85–86 Thus, germline genes could be particularly vulnerable to heritable epigenetic changes, where deviations in the expression levels of a gene that is regulated by or is part of such feedback loops has the potential to become permanent in descendants. Our analysis of sdg-1 expression suggests that it is part of a regulatory architecture that is susceptible to heritable epigenetic changes through the perturbation of RNA regulation (Figures 4, 5 and 6).…”

Section: Discussionmentioning

confidence: 99%

Intergenerational transport of double-stranded RNA limits heritable epigenetic changes

Shugarts

Chan

et al. 2021

Preprint

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RNAs in circulation carry sequence-specific regulatory information between cells in animal, plant, and host-pathogen systems. Double-stranded RNA (dsRNA) delivered into the extracellular space of the nematode C. elegans accumulates within the germline and reaches progeny. Here we provide evidence for spatial, temporal, and substrate specificity in the transport of dsRNA from parental circulation to progeny. Temporary loss of dsRNA transport resulted in the persistent accumulation of mRNA from a germline gene. The expression of this gene varied among siblings and even between gonad arms within one animal. Perturbing RNA regulation of the gene created new epigenetic states that lasted for many generations. Thus, one role for the transport of dsRNA into the germline in every generation is to limit heritable changes in gene expression.One Sentence SummaryRNA from parental circulation reduces heritable changes in gene expression.

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Section: Discussionmentioning

confidence: 99%

Intergenerational transport of double-stranded RNA limits heritable epigenetic changes

Shugarts

Chan

et al. 2021

Preprint

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“…In addition, epigenetic changes may also contribute to the evolutionary responses observed here (Cavalli & Heard, 2019). Our common garden experimental design accounts for possible plastic and parentally (single‐generation) heritable epigenetic changes, but the design does not account for any epigenetic changes that are stably inherited across multiple generations (Cavalli & Heard, 2019; Chey & Jose, 2022) and we can thus not exclude their role in driving fitness evolution. Both epistasis and epigenetic inheritance could buffer fitness evolution against reduced genetic diversity in small populations.…”

Section: Discussionmentioning

confidence: 99%

Population bottleneck has only marginal effect on fitness evolution and its repeatability in dioecious Caenorhabditis elegans

et al. 2022

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The predictability of evolution is expected to depend on the relative contribution of deterministic and stochastic processes. This ratio is modulated by effective population size. Smaller effective populations harbor less genetic diversity and stochastic processes are generally expected to play a larger role, leading to less repeatable evolutionary trajectories. Empirical insight into the relationship between effective population size and repeatability is limited and focused mostly on asexual organisms. Here, we tested whether fitness evolution was less repeatable after a population bottleneck in obligately outcrossing populations of Caenorhabditis elegans. Replicated populations founded by 500, 50, or five individuals (no/moderate/strong bottleneck) were exposed to a novel environment with a different bacterial prey. As a proxy for fitness, population size was measured after one week of growth before and after 15 weeks of evolution. Surprisingly, we found no significant differences among treatments in their fitness evolution. Even though the strong bottleneck reduced the relative contribution of selection to fitness variation, this did not translate to a significant reduction in the repeatability of fitness evolution. Thus, although a bottleneck reduced the contribution of deterministic processes, we conclude that the predictability of evolution may not universally depend on effective population size, especially in sexual organisms.

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“…In addition, epigenetic changes may also contribute to the evolutionary responses observed here (Cavalli and Heard, 2019). Our common garden experimental design accounts for possible plastic and parentally (single-generation) heritable epigenetic changes, but the design does not account for any epigenetic changes that are stably inherited across multiple generations (Cavalli and Heard, 2019; Chey and Jose, 2022) and we can thus not exclude their role in driving fitness evolution. Both epistasis and epigenetic inheritance could buffer fitness evolution against reduced genetic diversity in small populations.…”

Section: Discussionmentioning

confidence: 99%

Population bottleneck has only marginal effect on fitness evolution and its repeatability in dioecious C. elegans

Bisschop

Blankers

Mariën

et al. 2021

Preprint

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Evolution is a key process by which populations can adapt to novel conditions, but it is not well understood how predictable this process is. Predictability is expected to depend on the ratio of deterministic and stochastic processes that contribute to evolutionary change and this ratio is modulated by the effective population size. Smaller effective populations harbor less genetic diversity and stochastic processes are generally expected to play a larger role, leading to less repeatable evolutionary trajectories. Empirical insight into the relationship between effective population size and repeatability is limited and biased towards asexual unicellular organisms. Here, we used populations of obligately outcrossing Caenorhabditis elegans to test whether fitness increase and selection response were more heterogeneous after a moderate or strong population bottleneck compared to a scenario without bottleneck. Nematodes were exposed to a novel bacterial prey and lower temperature. Population sizes after one week of growth (as a proxy of fitness) were measured before and after 15 generations of evolution. We found that replicates across all (no/moderate/strong bottleneck) treatments evolved higher fitness and no significant difference in average or maximum fitness was found among treatments. Partitioning fitness variance among effects from selection and effects from chance showed that a strong (but not a moderate) bottleneck reduced the relative contribution of selection effects to fitness variation. However, the reduced contribution from selection did not translate to a significant reduction in the repeatability of fitness evolution. Thus, although a strong bottleneck reduced the contribution of deterministic evolutionary change, we found only marginal effects on quantitative measurements of repeatability in evolution. We conclude that the extent to which evolution is predictable may not universally depend on effective population size.

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Heritable epigenetic changes at single genes: challenges and opportunities in Caenorhabditis elegans

Cited by 15 publications

References 15 publications

Intergenerational transport of double-stranded RNA limits heritable epigenetic changes

Intergenerational transport of double-stranded RNA limits heritable epigenetic changes

Population bottleneck has only marginal effect on fitness evolution and its repeatability in dioecious Caenorhabditis elegans

Population bottleneck has only marginal effect on fitness evolution and its repeatability in dioecious C. elegans

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