Michael Travisano

Adaptive radiation in a heterogeneous environment.

Successive adaptive radiations have played a pivotal role in the evolution of biological diversity. The effects of adaptive radiation are often seen, but the underlying causes are difficult to disentangle and remain unclear. Here we examine directly therole of ecological opportunity and competition in driving genetic diversification. We use the common aerobic bacterium Pseudomonas fluorescens, which evolves rapidly under novel environmental conditions to generate a large repertoire of mutants. When provided with ecological opportunity (afforded by spatial structure), identical populations diversify morphologically, but when ecological opportunity is restricted there is no such divergence. In spatially structured environments, the evolution of variant morphs follows a predictable sequence and we show that competition among the newly evolved niche-specialists maintains this variation. These results demonstrate that the elementary processes of mutation and selection alone are suifficient to promote rapid proliferation of new designs and support the theory that trade-offs in competitive ability drive adaptive radiation,.

Methyl donor supplementation prevents transgenerational amplification of obesity

Background:The obesity epidemic, recognized in developed nations for decades, is now a worldwide phenomenon. All age groups are affected, including women of childbearing age, fueling concern that maternal obesity before and during pregnancy and lactation impairs developmental establishment of body weight regulatory mechanisms in the fetus or infant, causing transgenerational amplification of obesity prevalence and severity. The biological mechanisms underlying such processes remain unknown.Methods:We used agouti viable yellow (Avy) mice to test the hypothesis that maternal obesity induces transgenerational amplification of obesity. We passed the Avy allele through three generations of Avy/a females and assessed cumulative effects on coat color and body weight. By studying two separate but contemporaneous populations of mice, one provided a standard diet and the other a methyl-supplemented diet that induces DNA hypermethylation during development, we tested whether potential transgenerational effects on body weight might be mediated by alterations in epigenetic mechanisms including DNA methylation.Results:The genetic tendency for obesity in Avy mice was progressively exacerbated when the Avy allele was passed through successive generations of obese Avy females. This transgenerational amplification of body weight was prevented by a promethylation dietary supplement. Importantly, the effect of methyl supplementation on body weight was independent of epigenetic changes at the Avy locus, indicating this model may have direct relevance to human transgenerational obesity.Conclusion:Our results show that in a population with a genetic tendency for obesity, effects of maternal obesity accumulate over successive generations to shift the population distribution toward increased adult body weight, and suggest that epigenetic mechanisms are involved in this process.

Season of Conception in Rural Gambia Affects DNA Methylation at Putative Human Metastable Epialleles

Throughout most of the mammalian genome, genetically regulated developmental programming establishes diverse yet predictable epigenetic states across differentiated cells and tissues. At metastable epialleles (MEs), conversely, epigenotype is established stochastically in the early embryo then maintained in differentiated lineages, resulting in dramatic and systemic interindividual variation in epigenetic regulation. In the mouse, maternal nutrition affects this process, with permanent phenotypic consequences for the offspring. MEs have not previously been identified in humans. Here, using an innovative 2-tissue parallel epigenomic screen, we identified putative MEs in the human genome. In autopsy samples, we showed that DNA methylation at these loci is highly correlated across tissues representing all 3 embryonic germ layer lineages. Monozygotic twin pairs exhibited substantial discordance in DNA methylation at these loci, suggesting that their epigenetic state is established stochastically. We then tested for persistent epigenetic effects of periconceptional nutrition in rural Gambians, who experience dramatic seasonal fluctuations in nutritional status. DNA methylation at MEs was elevated in individuals conceived during the nutritionally challenged rainy season, providing the first evidence of a permanent, systemic effect of periconceptional environment on human epigenotype. At MEs, epigenetic regulation in internal organs and tissues varies among individuals and can be deduced from peripheral blood DNA. MEs should therefore facilitate an improved understanding of the role of interindividual epigenetic variation in human disease.

The Prisoner's Dilemma and polymorphism in yeast SUC genes.

The SUC multigene family of the single–celled yeast Saccharomyces cerevisiae is polymorphic, with genes varying both in number and activity. All of the genes encode invertase, an enzyme that is secreted to digest sucrose outside of the cell. This communal endeavour creates the potential for individual cells to defect (cheat) by stealing the sugar digested by their neighbours without contributing the enzyme themselves. We measured the fitness of a defector, with a deleted suc2 gene, relative to an otherwise isogenic cooperator, with a functional SUC2 gene. We manipulated the level of social interaction within the community by varying the population density and found that the defector is less fit than the cooperator at low levels of sociality but more fit in dense communities. We propose that selection for antisocial cheating causes SUC polymorphism in nature. The infamous Prisoners Dilemma game shows that social behaviour is generally unstable, and the success of both cooperation and defection can vary continuously in time and space. The variation in SUC genes reflects constant adaptation to an ever–changing biotic environment that is a consequence of the instability of cooperation. It is interesting that social interactions can have a direct effect on molecular evolution, even in an organism as simple as yeast.

Experimental evolution of multicellularity

Multicellularity was one of the most significant innovations in the history of life, but its initial evolution remains poorly understood. Using experimental evolution, we show that key steps in this transition could have occurred quickly. We subjected the unicellular yeast Saccharomyces cerevisiae to an environment in which we expected multicellularity to be adaptive. We observed the rapid evolution of clustering genotypes that display a novel multicellular life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. The multicellular clusters are uniclonal, minimizing within-cluster genetic conflicts of interest. Simple among-cell division of labor rapidly evolved. Early multicellular strains were composed of physiologically similar cells, but these subsequently evolved higher rates of programmed cell death (apoptosis), an adaptation that increases propagule production. These results show that key aspects of multicellular complexity, a subject of central importance to biology, can readily evolve from unicellular eukaryotes.

Long-term experimental evolution in Escherichia coli. II.Changes in life-history traits during adaptation to a seasonal environment

Twelve populations of the bacterium Escherichia coli were propagated for 2,000 generations in a seasonal environment, which consisted of alternating periods of feast and famine. The mean fitness of the derived genotypes increased by ∼35% relative to their common ancestor, based on competition experiments in the same environment. The bacteria could have adapted, in principle, by decreasing their lag prior to growth upon transfer to fresh medium (L), increasing their maximum growth rate (Vm), reducing the concentration of resource required to support growth at half the maximum rate (Ks), and reducing their death rate after the limiting resource was exhausted (D). We estimated these parameters for the ancestor and then calculated the opportunity for selection on each parameter. The inferred selection gradients for Vm and L were much steeper than for Ks and D. The derived genotypes showed significant improvement in Vm and L but not in Ks or D. Also, the numerical yield in pure culture of the derived genotypes was significantly lower than the yield of the common ancestor, but the average cell size was much larger. The independently derived genotypes are somewhat more variable in these life-history traits than in their relative fitnesses, which indicates that they acquired different genetic adaptations to the seasonal environment. Nonetheless, the evolutionary changes in life-history traits exhibit substantial parallelism among the replicate populations.

Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female

The effects of nonmutagenic environmental exposures can sometimes be transmitted for several generations, suggesting transgenerational inheritance of induced epigenetic variation. Methyl donor supplementation of female mice during pregnancy induces CpG hypermethylation at the agouti viable yellow (Avy) allele in Avy/a offspring. Epigenetic inheritance occurs at Avy; when passed through the female germ line, Avy epigenotype is not completely “reset.” We therefore tested whether diet‐induced epigenetic alterations at Avy are inherited transgenerationally. Female Avy/a mice were weaned onto either control (n=6) or a methyl‐supplemented diet (n=5). These F0 dams were mated with a/a males. All F1 and F2 Avy/a females were weaned onto the same diet as their mothers, then mated with a/a males. F1, F2, and F3 Avy/a offspring were classified for coat color, an indicator of Avy methylation. In total, 62 F1, 98 F2, and 209 F3 Avy/a mice were studied. As expected, average Avy/a coat color was darker in the supplemented group (P<0.01). However, there was no cumulative effect of supplementation across successive generations. These results suggest that, in the female germ line, diet‐induced Avy hypermethylation occurs in the absence of additional epigenetic modifications that normally confer transgen‐erational epigenetic inheritance at the locus.—Waterland R. A., Travisano, M., Tahiliani K. G. Diet‐induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J. 21, 3380–3385 (2007)

The emergence and maintenance of diversity: insights from experimental bacterial populations.

Mechanisms maintaining genetic and phenotypic variation in natural populations are central issues in ecology and evolution. However, the long generation times of most organisms and the complexity of natural environments have made elucidation of ecological and evolutionary mechanisms difficult. Experiments using bacterial populations propagated in controlled environments reduce ecosystem complexity to the point where understanding simple processes in isolation becomes possible. Recent studies reveal the circumstances and mechanisms that promote the emergence of stable polymorphisms.

EXPERIMENTAL EVIDENCE FOR SYMPATRIC ECOLOGICAL DIVERSIFICATION DUE TO FREQUENCY-DEPENDENT COMPETITION IN ESCHERICHIA COLI

Abstract We investigate adaptive diversification in experimental Escherichia coli populations grown in serial batch cultures on a mixture of glucose and acetate. All 12 experimental lines were started from the same genetically uniform ancestral strain but became highly polymorphic for colony size after 1000 generations. Five populations were clearly dimorphic and thus serve as a model for an adaptive lineage split. We analyzed the ecological basis for this dimorphism by studying bacterial growth curves. All strains exhibit diauxie, that is, sequential growth on the two resources. Thus, they exhibit phenotypic plasticity, using mostly glucose when glucose is abundant, then switching to acetate when glucose concentration is low. However, the coexisting strains differ in their diauxie pattern, with one cluster in the dimorphic populations growing better in the glucose phase, and the other cluster having a much shorter lag when switching to the acetate phase. Using invasion experiments, we show that the dimorphism of these two ecological types is maintained by frequency‐dependent selection. Using a mathematical model for the adaptive dynamics of diauxie behavior, we show that evolutionary branching in diauxie behavior is a plausible theoretical scenario. Our results support the hypothesis that, in our experiments, adaptive diversification from a genetically uniform ancestor occurred due to frequency‐dependent ecological interactions. Our results have implications for understanding the evolution of cross‐feeding polymorphism in microorganisms, as well as adaptive speciation due to frequency‐dependent selection on phenotypic plasticity.

Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments

Twelve populations of Escherichia coli were founded from a single clone and propagated for 2000 generations in identical glucose‐limited environments. During this time, the mean fitnesses of the evolving populations relative to their common ancestor improved greatly, but their fitnesses relative to one another diverged only slightly. Although the populations showed similar fitness increases, they may have done so by different underlying adaptations, or they may have diverged in other respects by random genetic drift. Therefore, we examined the relative fitnesses of independently derived genotypes in two other sugars, maltose and lactose, to determine whether they were homogeneous or heterogeneous in these environments. The genetic variation among the derived lines in fitness on maltose and lactose was more than 100‐times greater than their variation in fitness on glucose. Moreover, the glucose‐adapted genotypes, on average, showed significant adaptation to lactose, but not to maltose. That pathways for use of maltose and glucose are virtually identical in E. coli, except for their distinct mechanisms of uptake, suggests that the derived genotypes have adapted primarily by improved glucose transport. From consideration of the number of generations of divergence, the mutation rate in E. coli, and the proportion of its genome required for growth on maltose (but not glucose), we hypothesize that pleiotropy involving the selected alleles, rather than random genetic drift of alleles at other loci, was the major cause of the variation among the derived genotypes in fitness on these other sugars.