Browsing by Subject "Phenotypic plasticity"

As habitat fragmentation and changing climatic conditions continues to pose threats to species persistence, it is important to study the traits that may ensure survival of individual plants and the population-level effects of those traits. Previous studies have highlighted the importance of one such trait, dispersal, for population persistence under changing conditions. Dispersal allows plants to track spatial and seasonal changes in the environment. Plants can disperse through space, i.e., pollen and seed dispersal, and through time, i.e., delaying germination within seasons (seed dormancy) or between years (seed banking). Spatial sorting of good dispersers has been highlighted as a mechanism to facilitate spatial habitat tracking, but few studies have evaluated how interactions between spatial sorting and plasticity of dispersal-related traits may interact to impact dispersal dynamics. In addition, theory predicts that both spatial dispersal as a form of bet-hedging, and seasonal seed dormancy as a form of habitat selection, may stabilize population demography across years, thereby reducing population extinction risk. Few studies have experimentally manipulated spatial and temporal dispersal in the field to test these theoretical predictions. My dissertation quantifies spatial dispersal at a small scale, tests for the genetic basis and plasticity of dispersal-related traits, tests the metapopulation consequences of local spatial dispersal versus spatial isolation, and quantifies the population-level consequences of seasonal seed dormancy. I combined field, greenhouse, and quantitative genetic approaches to assess the demographic effects of spatial and temporal dispersal in the model plant species Arabidopsis thaliana. In my first chapter I show that limited dispersal results in predictable variation in post-dispersal density across space. Further, I show that the traits that enhance dispersal ability in the field have a genetic basis, exhibit plasticity to density and season length, and genetic variation in that plasticity. Plasticity and genotypic differences in plasticity can alter the effects of spatial sorting on dispersal ability across a species range. Specifically, plasticity can augment the effects of spatial sorting of genotypes, by enhancing dispersal at low-post-dispersal density. Genetic differences in plasticity of good versus poor dispersers can mask genetic differences in dispersal ability and thereby slow spatial sorting of genotypes at high density but augment genetic differences and spatial sorting at low density. In my second chapter I show that, compared to isolated populations, populations open to dispersal had smaller between-year population size fluctuations, increased survival of individuals within years, and less between-population differentiation in morphological traits. Those demographic effects of dispersal may have increased the effective population size of populations open to dispersal, facilitating a recovery from the effects of harsh environmental conditions. Finally, my third chapter demonstrates that seasonal seed dormancy may allow populations to better take advantage of favorable conditions by increasing population size and stabilizing population demography over time in more permissive environments. However, contrary to expectations, dormancy did not reduce the effects of environmental variation due to its inability to counter the effects of population bottlenecks induced by harsh environmental conditions. The findings of my dissertation highlight the importance of considering the interaction between spatial sorting, phenotypic plasticity, and genetic variation in plasticity when projecting range expansion dynamics. My dissertation also provides some of the first experimental validation of the theory that predicts that spatial and temporal dispersal can stabilize population demography and facilitate population persistence. Therefore, when predicting how species may respond to anthropogenic changes it is important to not only consider the effects of dispersal on environmental tracking, but also the effects of dispersal on population demography. Finally, given the limited dispersal of Arabidopsis thaliana and many annual species like it, it is important to measure population dynamics at a micro-scale, otherwise researchers risk underestimating regional-level extinction risk.

In many species, early life experiences have striking effects on health, reproduction, and survival in adulthood. Thus, early life conditions shape a range of evolutionarily relevant traits, and in doing so alter the genotype-phenotype relationship and the phenotypic distribution on which selection acts. Because of the key role early life effects play in generating variation in fitness-related traits, understanding their evolution and mechanistic basis is crucial. To gain traction on these topics, my dissertation draws on ecological, demographic, and genomic data from a long-term study population of wild baboons in Amboseli, Kenya to address three major themes: (i) the adaptive significance of early life effects, (ii) the molecular mechanisms that connect early life experiences with later life traits, and (iii) the development of laboratory tools for understanding the role of one particular mechanism—DNA methylation—in translating environmental inputs into phenotypic variation. In chapter one, I empirically test two competing explanations for how early life effects evolve, providing novel insight into the evolution of developmental plasticity in long-lived species. In chapter two, I address the degree to which ecological effects on fitness-related traits are potentially mediated by changes in DNA methylation. Finally, in chapter three, I develop a high-throughput assay to improve our knowledge of the phenotypic relevance of changes in the epigenome. Together, this work provides some of the first empirical data on the genes and mechanisms involved in sensing and responding to environmental variation in wild mammals, and more generally addresses several critical gaps in our understanding of how early experiences affect evolutionarily relevant traits.

Seasonal polyphenism in insects is the phenomenon whereby multiple phenotypes can arise from a single genotype depending on environmental conditions during development. Many butterflies have multiple generations per year, and environmentally induced variation in wing color pattern phenotype allows them to develop adaptations to the specific season in which the adults live. Elements of butterfly color patterns are developmentally semi-autonomous allowing for detailed developmental and evolutionary changes in the overall color pattern. This developmental flexibility of the color pattern can result in extremely diverse seasonal phenotypes in a single species. In this study, we asked the following questions: a) How do wing phenotype elements such as shape and pattern vary between seasonal forms? b) Can this variation be explained phylogenetically? c) If so, what are the various pattern development strategies used to achieve crypsis in the dry season form? To answer these questions, we used high resolution images to analyze pattern element variation of 34 seasonally polyphenic butterfly species belonging to the tribe Junoniini (Lepidoptera: Nymphalidae). We show that forewing shape and eyespot size both vary seasonally, and that the methods by which phenotype elements change in the dry seasonal forms is different in different clades and may therefore have independent and diverse evolutionary origins.

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.

Theoretical and empirical studies have consistently shown that the optimal timing of seed germination reduces exposure to physical stress and minimizes competitive interactions with neighbors. However, this research has not accounted for facilitative (positive) interactions among plants, which become more pronounced as environmental stress increases. Facilitation is more likely to occur early in a plant's life when it is more susceptible to stress. In seasonal environments, the stress a given individual experiences can change throughout the year, and some years are more stressful than others. These sources of temporal variation in stress will dictate the facilitation-competition balance that individuals experience. However, it remains unclear how this balance affects the optimal timing of germination. My dissertation research asks how the timing of germination responds to neighbors, how those responses affect the facilitation-competition balance individuals experience, and how that balance in turn affects fitness and demography. More generally, it asks how the timing of germination and other types of emergence affect the facilitation and competition that individuals experience throughout their lives.

I used laboratory, greenhouse, and field experiments to examine how the timing of germination in the winter annual Arabidopsis thaliana (Brassicaceae) responds to cues of neighbors and how those responses affect interactions with neighbors. I then developed a mathematical model of population growth in an annual plant to examine how intraspecific facilitation and competition over ontogeny affect the optimal degree of investment in dormancy (i.e., delayed germination) in variable environments.

My experiments revealed that seeds of A. thaliana typically delay germination in response to neighbors and that these responses can promote facilitative interactions and reduce competitive ones with neighbors. Selection against delayed germination, which occurs because of stress later in the season, can be mitigated by facilitation. Further, delaying germination can be beneficial by increasing the difference in sizes between seedlings and their neighbors, which may promote resource partitioning. In the theoretical study, I found that increasing the degree of investment in the fraction of dormant seeds (i.e., delaying germination) can promote the persistence of populations that experience both facilitation and competition in variable environments. This occurs because increased dormancy prevents high juvenile densities that promote facilitation and consequently limit reproduction in large populations. The findings of this research indicate that plant-plant interactions depend strongly on temporal context, and they reveal that the facilitation-competition balance determined by temporal variation in stress plays a key role in how germination and dormancy traits will evolve in variable environments.