Population genetics of polymorphism and divergence in rapidly evolving populations

In rapidly evolving populations, numerous beneficial and deleterious mutations can arise and segregate within a population at the same time. In this regime, evolutionary dynamics cannot be analyzed using traditional population genetic approaches that assume that sites evolve independently. Instead, the dynamics of many loci must be analyzed simultaneously. Recent work has made progress by first analyzing the fitness variation within a population, and then studying how individual lineages interact with this traveling fitness wave. However, these "traveling wave" models have previously been restricted to extreme cases where selection on individual mutations is either much faster or much slower than the typical coalescent timescale T_c. In this work, we show how the traveling wave framework can be extended to intermediate regimes in which the scaled fitness effects of mutations (T_c s) are neither large nor small compared to one. This enables us to describe the dynamics of populations subject to a wide range of fitness effects, and in particular, in cases where it is not immediately clear which mutations are most important in shaping the dynamics and statistics of genetic diversity. We use this approach to derive new expressions for the fixation probabilities and site frequency spectra of mutations as a function of their scaled fitness effects, along with related results for the coalescent timescale T_c and the rate of adaptation or Muller's ratchet. We find that competition between linked mutations can have a dramatic impact on the proportions of neutral and selected polymorphisms, which is not simply summarized by the scaled selection coefficient T_c s. We conclude by discussing the implications of these results for population genetic inferences.

The adaptive potential of non-heritable somatic mutations

Non-heritable somatic mutations are typically associated with deleterious effects such as in cancer and senescence, so their role in adaptive evolution has received little attention. However, most somatic mutations are harmless and some even confer a fitness advantage to the organism carrying them. We hypothesized that heritable, germline genotypes that are likely to express an advantageous phenotype via non-heritable somatic mutation will have a selective advantage over other germline genotypes, and this advantage will channel evolving populations toward more fit germline genotypes, thus promoting adaptation. We tested this hypothesis by simulating evolving populations of developing organisms with an impermeable germline-soma separation navigating a minimal fitness landscape. The simulations revealed the conditions under which non-heritable somatic mutations promote adaptation. Specifically, this can occur when the somatic mutation supply is high, when only very few cells with the advantageous somatic mutation are required to increase organismal fitness, and when the somatic mutation also confers a selective advantage to cells with that mutation. We therefore provide proof-of-principle that non-heritable somatic mutations can promote adaptive evolution via a process we call somatic genotypic exploration. We discuss the biological plausibility of this phenomenon, as well as its evolutionary implications.

GroEL/S helps purge deleterious mutations and reduce genetic diversity during adaptive protein evolution

Chaperones are proteins that help other proteins fold. They also affect the adaptive evolution of their client proteins by buffering deleterious mutations and increasing the genetic diversity of evolving proteins. We study how the bacterial chaperone GroE (GroEL + GroES) affects the evolution of green fluorescent protein (GFP). To this end we subjected GFP to multiple rounds of mutation and selection for its color phenotype in four replicate E. coli populations, and studied its evolutionary dynamics through high-throughput sequencing and mutant engineering. We evolved GFP both under stabilizing selection for its ancestral (green) phenotype, and to directional selection for a new (cyan) phenotype,. We did so both under low and high expression of the chaperone GroE. In contrast to prevailing wisdom, we observe that GroE does not just buffer but also helps purge deleterious mutations from evolving populations. In doing so, GroE helps reduce the genetic diversity of evolving populations. In addition, it causes phenotypic heterogeneity in mutants with the same genotype, potentiating their effect in some cells, and buffering it in others. Our observations show that chaperones can affect adaptive evolution through more than one mechanism.HighlightsGroE reduces genetic diversityGroE potentiates the effect of deleterious mutationsGroE intensifies purifying selection and leads to higher activity of client proteins

Identification and characterization of base-substitution mutations in the macronuclear genome of the ciliate Tetrahymena thermophila

Polyploidy can provide adaptive advantages and drive evolution. Amitotic division of the polyploid macronucleus (MAC) in ciliates acts as a non-sexual genetic mechanism to enhance adaptation to stress conditions and thus provides a unique model to investigate the evolutionary role of polyploidy. Mutation is the primary source of the variation responsible for evolution and adaptation; however, to date, de novo mutations that occur in ciliate MAC genomes during these processes have not been characterized and their biological impacts are undefined. Here, we carried out long-term evolution experiments to directly explore de novo MAC mutations and their molecular features in the model ciliate, Tetrahymena thermophila. A simple but effective method was established to detect base-substitution mutations in evolving populations while filtering out most of the false positive base-substitutions caused by repetitive sequences and the programmed genome rearrangements. The detected mutations were rigorously validated using the MassARRAY system. Validated mutations showed a strong G/C→A/T bias, consistent with observations in other species. Moreover, a progressive increase in growth rate of the evolving populations suggested that some of these mutations might be responsible for cell fitness. The established mutation identification and validation methods will be an invaluable resource to make ciliates an important model system to study the role of polyploidy in evolution.

Horizontal gene transfer becomes disadvantageous in rapidly fluctuating environments

Horizontal gene transfer (HGT) allows organisms to share genetic material with non-offspring, and is typically considered beneficial for evolving populations. Recent unexplained observations suggest that HGT rates in nature are linked with environmental dynamics, being high in static environments but surprisingly low in fluctuating environments. Here, using a geometric model of adaptation, we show that this trend might arise from evolutionary constraints. During adaptation in our model, a population of phenotype vectors aligns with a potentially fluctuating environmental vector while experiencing mutation, selection, drift and HGT. Simulations and theory reveal that HGT shapes a trade-off between the adaptation speed of populations and their fitness. This trade-off gives rise to an optimal HGT rate which decreases sharply with the rate of environmental fluctuations. Our results are consistent with data from natural populations, and strikingly suggest that HGT may sometimes carry a significant disadvantage for populations.

How old are (Pet) Dog Breeds?

Dogs are our Pets. Everybody knows dog breeds. A dog is often understood only as a specimen of a breed or a mongrel of several breeds. Some scholars argue, that dog breeds would be created as an artificial product starting 150 years ago in the Victorian era. The original dog would be an uniform dog type called “village dog”, hanging around human settlements while scavenging human waste and faeces. Astonishingly we only find very little research on evolution and history of dog breeds and dog breeding. In our article we will search for evidence. We found many records in history, archaeology and genetics pointing out that dog breeds have a long history likely starting in prehistoric times or at least in antiquity. Dog breeds shape no static monuments over thousands of years. We should understand dog breeds as steadily evolving populations in changing ecologies - like each species. Dogs’ ecological niches were made primarily by human. We are able to identify and clearly differ dogs in breeds, each breed fitting to its special niches. We are using dogs’ different traits since thousands of years. Dogs always had and have their jobs as hunting-, herding-, sledding-partners or as pets. Thus, dogs have been shaped to fit optimally to each job. Eventually, they evolved with their changing jobs in continually evolving human societies. Breeds have not been simply invented. Breeds did not derive artificially during some decades in the Victorian era. Victorian dog breeding culture only switched the focus from the behaviour to the appearance and that mainly with regard to fashion dogs. Even standardized modern purebred dogs on the official shows are continuously changing their traits and appearance following human fashions. Dog breeds may be understood as a reflection of human culture. Understanding the history of dog breeds is helpful for a better understanding of our dogs, the human-dog bonding and ourselves.

Adaptation Through Lifestyle Switching Sculpts the Fitness Landscape of Evolving Populations: Implications for the Selection of Drug-Resistant Bacteria at Low Drug Pressures

Novel genotypes evolve under selection through mutations in pre-existing genes. However, mutations have pleiotropic phenotypic effects that influence the fitness of emerging genotypes in complex ways. The evolution of antimicrobial resistance is mediated by selection of mutations in genes coding for antibiotic-target proteins. Drug-resistance is commonly associated with a fitness cost due to the impact of resistance-conferring mutations on protein function and/or stability. These costs are expected to prohibit the selection of drug-resistant mutations at low drug pressures. Using laboratory evolution of rifampicin resistance in Escherichia coli, we show that when exposed intermittently to low concentration (0.1 × minimal inhibitory concentration) of rifampicin, the evolution of canonical drug resistance was indeed unfavorable. Instead, these bacterial populations adapted by evolving into small-colony variants that displayed enhanced pellicle-forming ability. This shift in lifestyle from planktonic to pellicle-like was necessary for enhanced fitness at low drug pressures, and was mediated by the genetic activation of the fim operon promoter, which allowed expression of type I fimbriae. Upon continued low drug exposure, these bacteria evolved exclusively into high-level drug-resistant strains through mutations at a limited set of loci within the rifampicin-resistance determining region of the rpoB gene. We show that our results are explained by mutation-specific epistasis, resulting in differential impact of lifestyle switching on the competitive fitness of different rpoB mutations. Thus, lifestyle-alterations that are selected at low selection pressures have the potential to modify the fitness effects of mutations, change the genetic structure, and affect the ultimate fate of evolving populations.

Rapid adaptive evolution in novel environments acts as an architect of population range expansion

Colonization and expansion into novel landscapes determine the distribution and abundance of species in our rapidly changing ecosystems worldwide. Colonization events are crucibles for rapid evolution, but it is not known whether evolutionary changes arise mainly after successful colonization has occurred, or if evolution plays an immediate role, governing the growth and expansion speed of colonizing populations. There is evidence that spatial evolutionary processes can speed range expansion within a few generations because dispersal tendencies may evolve upwards at range edges. Additionally, rapid adaptation to a novel environment can increase population growth rates, which also promotes spread. However, the role of adaptive evolution and the relative contributions of spatial evolution and adaptation to expansion are unclear. Using a model system, red flour beetles (Tribolium castaneum), we either allowed or constrained evolution of populations colonizing a novel environment and measured population growth and spread. At the end of the experiment we assessed the fitness and dispersal tendency of individuals originating either from the core or edge of evolving populations or from nonevolving populations in a common garden. Within six generations, evolving populations grew three times larger and spread 46% faster than populations in which evolution was constrained. Increased size and expansion speed were strongly driven by adaptation, whereas spatial evolutionary processes acting on edge subpopulations contributed less. This experimental evidence demonstrates that rapid evolution drives both population growth and expansion speed and is thus crucial to consider for managing biological invasions and successfully introducing or reintroducing species for management and conservation.