Nongenetic inheritance and multigenerational plasticity in the nematode C. elegans

Abstract

A rapidly growing body of literature in several organisms suggests that environmentally-induced adaptive changes in phenotype can be transmitted across multiple generations. Although within-generation plasticity has been well documented, multigenerational plasticity represents a significant departure from conventional evolutionary thought. Studies of C. elegans have been particularly influential because this species exhibits extensive phenotypic plasticity, it is often essentially isogenic, and it has well-documented molecular and cellular mechanisms through which nongenetic inheritance occurs. However, while experimentalists are eager to claim that nongenetic modes of inheritance characterized in this and other model systems enhance fitness, many biologists remain skeptical given the extraordinary nature of this claim. We establish three criteria to evaluate how compelling the evidence for adaptive multigenerational plasticity is, and we use these criteria to critically examine putative cases of it in C. elegans. We conclude by suggesting potentially fruitful avenues for future research.

Influence of environmental temperature on mouth-form plasticity in Pristionchus pacificus acts through daf-11-dependent cGMP signaling

“…All three genes, eud-1, nag-1 and nag-2 are expressed in different sensory neurons. The identification of switch genes that govern intra-generational plasticity is important to confirm that plasticity is indeed consistent with the Modern Synthesis of evolution (Baugh and Day, 2020).…”

Evolution of epigenetic transmission when selection acts on fecundity versus viability

“…Experimental evolution in regimes that favour either fecundity or viability has been previously done in Caenorhabditis nematodes [e.g., 70]. Moreover, there is now accumulating evidence that parental effects can rapidly evolve in Caenorhabditis nematodes [19,71], making this an ideal model system to assess the evolution of parental effects in different life-history contexts [72]. A key caveat is, however, that these experimental evolution studies have been performed on well-mixed populations, whereas our study suggests that a difference between viability and fecundity selection may only arise in spatially structured populations with limited dispersal and relatively small deme sizes.…”

A clonal fresh water plants acquires transgenerational stress resistance under recurring copper excess

“…It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted February 8, 2021. ; https://doi.org/10.1101/2021.02.06.430033 doi: bioRxiv preprint polyrhiza and other plants [46,48,70] generations, an involvement of epigenetic inheritance seems likely. Experiments that assess induction and persistence of epigenetic marks upon copper excess and their relation to plant phenotype and fitness may help to resolve the on-going controversy about the importance of epigenetic inheritance to mediate transgenerational stress resistance [5,8,13,26,57].…”

“…Theoretical work suggests that populations may acquire stress resistance through non-genetic inheritance, particularly when transmission fidelity across generations is high [9][10][11]. Experimental support of these predictions in multicellular organisms is however scarce [6,12,13], as such approaches require large-scale multigenerational studies and the ability to disentangle genetic from non-genetic factors.…”