Nongenetic individuality, changeability, and inheritance in bacterial behavior

Isogenic populations often display remarkable levels of phenotypic diversity even in constant, homogeneous environments. Such diversity results from differences between individuals (“nongenetic individuality”) as well as changes during individuals’ lifetimes (“changeability”). Yet, studies that capture and quantify both sources of diversity are scarce. Here we measure the swimming behavior of hundreds of Escherichia coli bacteria continuously over two generations and use a model-independent method for quantifying behavior to show that the behavioral space of E. coli is low-dimensional, with variations occurring mainly along two independent and interpretable behavioral traits. By statistically decomposing the diversity in these two traits, we find that individuality is the main source of diversity, while changeability makes a smaller but significant contribution. Finally, we show that even though traits of closely related individuals can be remarkably different, they exhibit positive correlations across generations that imply nongenetic inheritance. The model-independent experimental and theoretical framework developed here paves the way for more general studies of microbial behavioral diversity.

Indirect parental effects on offspring viability by egg-derived fluids in an external fertilizer

The capacity for parents to influence offspring phenotypes via nongenetic inheritance is currently a major area of focus in evolutionary biology. Intriguing recent evidence suggests that sexual interactions among males and females, both before and during mating, are important mediators of such effects. Sexual interactions typically extend beyond gamete release, involving both sperm and eggs, and their associated fluids. However, the potential for gamete-level interactions to induce nongenetic parental effects remains under-investigated. Here, we test for such effects using an emerging model system for studying gamete interactions, the external fertilizer Mytilus galloprovincialis . We employed a split-ejaculate design to test whether exposing sperm to egg-derived chemicals (ECs) from a female would affect fertilization rate and offspring viability when those sperm were used to fertilize a different female's eggs. We found separate, significant effects of ECs from non-fertilizing females on both fertilization rate and offspring viability. The offspring viability effect indicates that EC-driven interactions can have nongenetic implications for offspring fitness independent of the genotypes inherited by those offspring. These findings provide a rare test of indirect parental effects driven exclusively by gamete-level interactions, and to our knowledge the first evidence that such effects occur via the gametic fluids of females.

Nongenetic inheritance and multigenerational plasticity in the nematode C. elegans

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.

DNA Methylation Profiles Suggest Intergenerational Transfer of Maternal Effects

The view of maternal effects (nongenetic maternal environmental influence on offspring phenotype) has changed from one of distracting complications in evolutionary genetics to an important evolutionary mechanism for improving offspring fitness. Recent studies have shown that maternal effects act as an adaptive mechanism to prepare offspring for stressful environments. Although research into the magnitude of maternal effects is abundant, the molecular mechanisms of maternal influences on offspring phenotypic variation are not fully understood. Despite recent work identifying DNA methylation as a potential mechanism of nongenetic inheritance, currently proposed links between DNA methylation and parental effects are indirect and primarily involve genomic imprinting. We combined a factorial breeding design and gene-targeted sequencing methods to assess inheritance of methylation during early life stages at 14 genes involved in growth, development, metabolism, stress response, and immune function of Chinook salmon (Oncorhynchus tshawytscha). We found little evidence for additive or nonadditive genetic effects acting on methylation levels during early development; however, we detected significant maternal effects. Consistent with conventional maternal effect data, maternal effects on methylation declined through development and were replaced with nonadditive effects when offspring began exogenous feeding. We mapped methylation at individual CpG sites across the selected candidate genes to test for variation in site-specific methylation profiles and found significant maternal effects at selected CpG sites that also declined with development stage. While intergenerational inheritance of methylated DNA is controversial, we show that CpG-specific methylation may function as an underlying molecular mechanism for maternal effects, with important implications for offspring fitness.