All Eggs Are Not Equal: The Maternal Environment Affects Progeny Reproduction and Developmental Fate in Caenorhabditis elegans

Harvey, Simon C.; Orbidans, Helen E.

doi:10.1371/journal.pone.0025840

Cited by 36 publications

(33 citation statements)

References 30 publications

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“…It is, of course, possible that parallel maternal and offspring-specific developmental and physiological mechanisms determined adaptation, besides glycogen provisioning and possibly consumption, which could have increased embryo survival under anoxia [50,74,79,80]. We can conclude, however, that oocyte-size-related traits were not involved, as might have been expected from classical life-history theory predicting a fitness tradeoff between offspring size and number under resourcelimited situations (S7 Fig; but see [81,82]). …”

Section: Discussionmentioning

confidence: 58%

Adaptation to temporally fluctuating environments by the evolution of maternal effects

Dey

Proulx

Teotónio

2015

Preprint

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All organisms live in temporally fluctuating environments. Theory predicts that the evolution of deterministic maternal effects (i.e., anticipatory maternal effects or transgenerational phenotypic plasticity) underlies adaptation to environments that fluctuate in a predictably alternating fashion over maternal-offspring generations. In contrast, randomizing maternal effects (i.e., diversifying and conservative bet-hedging), are expected to evolve in response to unpredictably fluctuating environments. Although maternal effects are common, evidence for their adaptive significance is equivocal since they can easily evolve as a correlated response to maternal selection and may or may not increase the future fitness of offspring. Using the hermaphroditic nematode Caenorhabditis elegans, we here show that the experimental evolution of maternal glycogen provisioning underlies adaptation to a fluctuating normoxia-anoxia hatching environment by increasing embryo survival under anoxia. In strictly alternating environments, we found that hermaphrodites evolved the ability to increase embryo glycogen provisioning when they experienced normoxia and to decrease embryo glycogen provisioning when they experienced anoxia. At odds with existing theory, however, populations facing irregularly fluctuating normoxia-anoxia hatching environments failed to evolve randomizing maternal effects. Instead, adaptation in these populations may have occurred through the evolution of fitness effects that percolate over multiple generations, as they maintained considerably high expected growth rates during experimental evolution despite evolving reduced fecundity and reduced embryo survival under one or two generations of anoxia. We develop theoretical models that explain why adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that such deterministic maternal effects are more likely to contribute to adaptation than randomizing maternal effects. Competing Interests: The authors have declared that no competing interests exist. Author SummaryMothers can influence the phenotype of their offspring, independently of the genes that they transmit to them; such phenomena are known as "maternal effects." Theory suggests that maternal effects can be advantageous when the environment changes between generations, but a direct demonstration of this has been missing. Using the hermaphroditic nematode Caenorhabditis elegans, we show that the experimental evolution of maternal glycogen provisioning underlies the adaptation to a fluctuating normoxia-anoxia environment by increasing the survival of embryos under anoxic conditions. Evolution of this maternal effect only occurred in populations facing oxygen deprivation during embryogenesis every other generation (i.e., where fluctuation was regular or predictable). Unexpectedly, populations facing irregularly fluctuating oxygen levels did not evolve "bethedging" strategies, but instead adapted by the evolution of long-term tran...

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Section: Discussionmentioning

confidence: 58%

Adaptation to temporally fluctuating environments by the evolution of maternal effects

Dey

Proulx

Teotónio

2015

Preprint

View full text Add to dashboard Cite

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“…This effect of social behaviour on dauer larvae formation is a clear example of an indirect effect on dauer larvae development, particularly given that it has previously been shown that there is no effect of bordering on dauer larvae development in standard dauer assays (Viney et al, 2003). As lower numbers of dauer larvae are observed in the npr-1 mutants, the opposite result to what one might predict if clumping behaviour produces high local pheromone concentrations and low local food levels, the reduction of dauer larvae development may be similar to the effects on dauer larvae development seen as a consequence of reduced maternal food availability (Harvey and Orbidans, 2011), that is, a harsher maternal environment resulting in the production of progeny that are less likely to develop as dauer larvae. The reduced numbers of dauer larvae formed in the npr-1 mutants also suggests that there is significant genetic variation which would act to increase dauer larvae development in many wild isolates (Figure 1), as the majority of these lines display the clumping phenotype.…”

Section: Discussionmentioning

confidence: 88%

“…QTLs defined only by sequential IL mapping are shown in bold. Butcher et al, 2007;Pungaliya et al, 2009;Park et al, 2012), on food availability and temperature (Golden and Riddle, 1984) and potentially on an assessment of individual quality (Harvey and Orbidans, 2011). Within growing populations, variation between genotypes in the number of dauer larvae could therefore be a consequence of variation in traits that affect the likelihood of dauer larvae development, the perception of the environment, or the way in which the population grows.…”

Section: Discussionmentioning

confidence: 99%

Genetic mapping of variation in dauer larvae development in growing populations of Caenorhabditis elegans

et al. 2013

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In the nematode Caenorhabditis elegans, the appropriate induction of dauer larvae development within growing populations is likely to be a primary determinant of genotypic fitness. The underlying genetic architecture of natural genetic variation in dauer formation has, however, not been thoroughly investigated. Here, we report extensive natural genetic variation in dauer larvae development within growing populations across multiple wild isolates. Moreover, bin mapping of introgression lines (ILs) derived from the genetically divergent isolates N2 and CB4856 reveals 10 quantitative trait loci (QTLs) affecting dauer formation. Comparison of individual ILs to N2 identifies an additional eight QTLs, and sequential IL analysis reveals six more QTLs. Our results also show that a behavioural, laboratory-derived, mutation controlled by the neuropeptide Y receptor homolog npr-1 can affect dauer larvae development in growing populations. These findings illustrate the complex genetic architecture of variation in dauer larvae formation in C. elegans and may help to understand how the control of variation in dauer larvae development has evolved.

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“…Early experience also modulates adult behaviors in the nematode Caenorhabditis elegans, and recent studies suggest that a subset of these effects can be transmitted to descendants (Rose et al 2005;Ebrahimi and Rankin 2007;Hall et al 2010;Remy 2010;Harvey and Orbidans 2011). Environmental cues experienced during early larval stages regulate a particularly critical developmental decision in C. elegans.…”

Section: Introductionmentioning

confidence: 99%

RNAi pathways contribute to developmental history-dependent phenotypic plasticity in C. elegans

Hall

Chirn

Lau

et al. 2013

RNA

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Early environmental experiences profoundly influence adult phenotypes through complex mechanisms that are poorly understood. We previously showed that adult Caenorhabditis elegans that transiently passed through the stress-induced dauer larval stage (post-dauer adults) exhibit significant changes in gene expression profiles, chromatin states, and life history traits when compared with adults that bypassed the dauer stage (control adults). These wild-type, isogenic animals of equivalent developmental stages exhibit different signatures of molecular marks that reflect their distinct developmental trajectories. To gain insight into the mechanisms that contribute to these developmental history-dependent phenotypes, we profiled small RNAs from post-dauer and control adults by deep sequencing. RNA interference (RNAi) pathways are known to regulate genome-wide gene expression both at the chromatin and post-transcriptional level. By quantifying changes in endogenous small interfering RNA (endo-siRNA) levels in post-dauer as compared with control animals, our analyses identified a subset of genes that are likely targets of developmental history-dependent reprogramming through a complex RNAi-mediated mechanism. Mutations in specific endo-siRNA pathways affect expected gene expression and chromatin state changes for a subset of genes in post-dauer animals, as well as disrupt their increased brood size phenotype. We also find that both chromatin state and endo-siRNA distribution in dauers are unique, and suggest that remodeling in dauers provides a template for the subsequent establishment of adult post-dauer profiles. Our results indicate a role for endo-siRNA pathways as a contributing mechanism to early experience-dependent phenotypic plasticity in adults, and describe how developmental history can program adult physiology and behavior via epigenetic mechanisms.

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All Eggs Are Not Equal: The Maternal Environment Affects Progeny Reproduction and Developmental Fate in Caenorhabditis elegans

Cited by 36 publications

References 30 publications

Adaptation to temporally fluctuating environments by the evolution of maternal effects

Adaptation to temporally fluctuating environments by the evolution of maternal effects

Genetic mapping of variation in dauer larvae development in growing populations of Caenorhabditis elegans

RNAi pathways contribute to developmental history-dependent phenotypic plasticity in C. elegans

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