Single Nucleotide Mapping of the Locally Accessible Trait Space in Yeast Reveals Pareto Fronts that Constrain Initial Adaptation, bioRxiv, 2019-03-30
AbstractTradeoffs constrain the improvement of performance of multiple traits simultaneously. Such tradeoffs define Pareto fronts, which represent a set of optimal individuals that cannot be improved in any one trait without reducing performance in another. Surprisingly, experimental evolution often yields genotypes with improved performance in all measured traits, perhaps indicating an absence of tradeoffs at least in the short-term. Here we densely sample adaptive mutations in S. cerevisiae to ask whether first-step adaptive mutations result in tradeoffs during the growth cycle. We isolated thousands of adaptive clones evolved under carefully chosen conditions and quantified their performances in each part of the growth cycle. We too find that some first-step adaptive mutations can improve all traits to a modest extent. However, our dense sampling allowed us to identify tradeoffs and establish the existence of Pareto fronts between fermentation and respiration, and between respiration and stationary phases. Moreover, we establish that no single mutation in the ancestral genome can circumvent the detected tradeoffs. Finally, we sequenced hundreds of these adaptive clones, revealing novel targets of adaptation and defining the genetic basis of the identified tradeoffs.
biorxiv evolutionary-biology 100-200-users 2019Bacterial biodiversity drives the evolution of CRISPR-based phage resistance in Pseudomonas aeruginosa, bioRxiv, 2019-03-25
Approximately half of all bacterial species encode CRISPR-Cas adaptive immune systems1, which provide immunological memory by inserting short DNA sequences from phage and other parasitic DNA elements into CRISPR loci on the host genome2. Whereas CRISPR loci evolve rapidly in natural environments3, bacterial species typically evolve phage resistance by the mutation or loss of phage receptors under laboratory conditions4,5. Here, we report how this discrepancy may in part be explained by differences in the biotic complexity of in vitro and natural environments6,7. Specifically, using the opportunistic pathogen Pseudomonas aeruginosa and its phage DMS3vir, we show that coexistence with other human pathogens amplifies the fitness trade-offs associated with phage receptor mutation, and therefore tips the balance in favour of CRISPR-based resistance evolution. We also demonstrate that this has important knock-on effects for P. aeruginosa virulence, which became attenuated only if the bacteria evolved surface-based resistance. Our data reveal that the biotic complexity of microbial communities in natural environments is an important driver of the evolution of CRISPR-Cas adaptive immunity, with key implications for bacterial fitness and virulence.
biorxiv evolutionary-biology 0-100-users 2019Structural color in Junonia butterflies evolves by tuning scale lamina thickness, bioRxiv, 2019-03-22
AbstractStructural color is a pervasive natural phenomenon, caused by photonic nanostructures that refract light. Diverse organisms employ structural color to mediate ecological interactions and create specific optical effects such as iridescence. Despite its importance for living systems, the developmental, genetic, and evolutionary processes that generate structural color largely remain mysterious. Here, we focus on simple photonic structures, thin film reflectors, in the lower lamina of Junonia butterfly scales. We present multiple lines of evidence that the thickness of the lamina quantitatively controls lamina color, which is an important determinant of overall wing color, even when pigments are also present. First, in a lineage of buckeye butterflies artificially selected for blue wing color for 12 generations, a thicker lamina resulted in a color shift from brown to blue. A similar lamina thickness increase explains the appearance of blue scales in butterflies with mutations in the optix wing patterning gene. Finally, lamina thickness variation underlies the color diversity that distinguishes seasonal variants, sexes, and species throughout the genus Junonia. Thus, quantitatively tuning a single dimension of the existing scale architecture allows butterflies to evolve a broad spectrum of hues over both microevolutionary and macroevolutionary time frames. Because the lower lamina is an intrinsic component of typical butterfly scales, our findings imply that lamina structural color influences wing color in most butterflies.Significance StatementStructural colors, which result from photonic nanostructures that refract light and can create iridescence, are an important tool for many organisms. We use thin films, which are morphologically simple nanostructures that generate structural color in the lower lamina of butterfly scales, to dissect how photonic structures evolve. By combining interspecies comparisons with two different experimental approaches—artificial selection on wing color, and genetically engineered mutation of the optix wing patterning gene—we demonstrate that lamina thickness controls the wavelength (hue) of the structural color. These lamina structural colors are ubiquitous in the genus Junonia, and determine wing color along with pigments. Our results suggest that lamina structural colors probably exist in most butterflies, and that tuning lamina thickness facilitates wing color evolution.
biorxiv evolutionary-biology 0-100-users 2019Evolutionary dynamics in structured populations under strong population genetic forces, bioRxiv, 2019-03-16
High rates of migration between subpopulations result in little population differentiation in the long-term neutral equilibrium. However, in the short-term, even very abundant migration may not be enough for subpopulations to equilibrate immediately. In this study, we investigate dynamical patterns of short-term population differentiation in adapting populations via stochastic and analytical modeling through time. We characterize a regime in which selection and migration interact to create non-monotonic patterns of the population differentiation statistic FST when migration is weaker than selection, but stronger than drift. We demonstrate how these patterns can be leveraged to estimate high migration rates that would lead to panmixia in the long term equilibrium using an approximate Bayesian computation approach. We apply this approach to estimate fast migration in a rapidly adapting intra-host Simian-HIV population sampled from different anatomical locations. Notably, we find differences in estimated migration rates between different compartments, all above Nem = 1. This work demonstrates how studying demographic processes on the timescale of selective sweeps illuminates processes too fast to leave signatures on neutral timescales.
biorxiv evolutionary-biology 100-200-users 2019Frequent birth of de novo genes in the compact yeast genome, bioRxiv, 2019-03-13
AbstractEvidence has accumulated that some genes originate directly from previously non-genic sequences, or de novo, rather than by the duplication or fusion of existing genes. However, how de novo genes emerge and eventually become functional is largely unknown. Here we perform the first study on de novo genes that uses transcriptomics data from eleven different yeast species, all grown identically in both rich media and in oxidative stress conditions. The genomes of these species are densely-packed with functional elements, leaving little room for the co-option of genomic sequences into new transcribed loci. Despite this, we find that at least 213 transcripts (~5%) have arisen de novo in the past 20 million years of evolution of baker’s yeast-or approximately 10 new transcripts every million years. Nearly half of the total newly expressed sequences are generated from regions in which both DNA strands are used as templates for transcription, explaining the apparent contradiction between the limited ‘empty’ genomic space and high rate of de novo gene birth. In addition, we find that 40% of these de novo transcripts are actively translated and that at least a fraction of the encoded proteins are likely to be under purifying selection. This study shows that even in very highly compact genomes, de novo transcripts are continuously generated and can give rise to new functional protein-coding genes.
biorxiv evolutionary-biology 0-100-users 2019Frequent birth ofde novogenes in the compact yeast genome, bioRxiv, 2019-03-13
AbstractEvidence has accumulated that some genes originate directly from previously non-genic sequences, orde novo, rather than by the duplication or fusion of existing genes. However, howde novogenes emerge and eventually become functional is largely unknown. Here we perform the first study onde novogenes that uses transcriptomics data from eleven different yeast species, all grown identically in both rich media and in oxidative stress conditions. The genomes of these species are densely-packed with functional elements, leaving little room for the co-option of genomic sequences into new transcribed loci. Despite this, we find that at least 213 transcripts (~5%) have arisende novoin the past 20 million years of evolution of baker’s yeast-or approximately 10 new transcripts every million years. Nearly half of the total newly expressed sequences are generated from regions in which both DNA strands are used as templates for transcription, explaining the apparent contradiction between the limited ‘empty’ genomic space and high rate ofde novogene birth. In addition, we find that 40% of thesede novotranscripts are actively translated and that at least a fraction of the encoded proteins are likely to be under purifying selection. This study shows that even in very highly compact genomes,de novotranscripts are continuously generated and can give rise to new functional protein-coding genes.
biorxiv evolutionary-biology 0-100-users 2019