The Balance of Parental Effects and Within Generation Plasticity: The Role of Parent and Offspring DNA Methylation on Response to Cues of Neighbor Presence

Abstract

While phenotypic plasticity has been widely documented, the relative contribution of parent versus offspring environment to determining progeny phenotypes and the persistence of parental effects throughout progeny development under different environments remain unknown. In predictable and/or seasonal environments, parental effects are predicted to be favored during early life stages of offspring, while offspring environment is predicted to increase in relative importance as the accuracy of offspring perception increases over the course of development. Furthermore, as plastic responses to the environment are both transmissible across generations and dynamic across development, epigenetic mechanisms are likely involved in the regulation of parental effects and phenotypic plasticity. The neighboring community is an important environmental factor for plants since sessile plants cannot escape competition within their current generation. Whether interactions with neighbors are positive or negative likely depends on the environment, as competition is hypothesized to increase in favorable environments and the neighboring community of plants may change over a seasonal progression. For these reasons, neighbor environment is an interesting and ecologically important environmental variable that can be used to investigate how parental and progeny environment regulate progeny phenotypes throughout development. To test these predictions, this dissertation evaluated how progeny phenotypes responded to the combination of parental and offspring environments, quantified how parental and progeny methylation regulate offspring phenotypes, and examined their effects on plasticity. To address which generation’s environment and DNA methylation affect phenotypes in offspring, I manipulated simulated and real neighbor environments and DNA methylation within and across generations in Arabidopsis thaliana, a winter annual native to Eurasia widely introduced across North America. In Chapter 1, using chemical demethylation, I tested whether parental and progeny DNA methylation influences germination, and whether parental DNA regulates germination response to past and present simulated canopy. I found that germination of offspring is regulated by parental DNA methylation and is responsive to parent, not seed, environment for most genotypes. Furthermore, I confirmed using mutant lines that all contexts of DNA methylation were involved in the transmission of parental effects, but they may operate through different pathways controlling germination. In Chapter 2, I quantified how parental versus progeny methylation regulate progeny phenotypic responses to parental and progeny canopy shade. I found that both parent and offspring canopy affect offspring traits across development, but parental environment had stronger effects at the seedling stage. Both parent and offspring DNA methylation affected offspring response to canopy, but parental DNA methylation only affected traits at the seedling stage. Trait correlations were significantly altered by chemical demethylation of parents and offspring, indicating that DNA methylation of both generations are important in regulating development and integrating phenotypic response to canopy. Finally, in Chapter 3, I tested whether parent or offspring DNA methylation affected response to the heterospecific neighbor, Stellaria media, under simulated seasonal conditions. I found that growing with competitors decreased fitness for all genotypes, but genotypes varied in the effect of neighbors on morphology and fitness. Both parent and offspring DNA methylation had direct effects on growth and fitness in all genotypes, but genotypes varied in how DNA methylation influenced response to neighbors. In one genotype, plastic response to neighbors was unaffected by chemical demethylation treatments, indicating that neighbor-induced plasticity is not always mediated via DNA methylation. Together, these results indicated that offspring phenotypes are shaped by both parent and offspring environment, and that parental environment and parental DNA methylation are especially important in regulating offspring traits early in life. The genetic variation observed in the expression of phenotypic plasticity via parental and progeny DNA methylation suggests that the epigenetic regulation of progeny phenotypes has a genetic basis and may evolve.