Evolution of polygenic traits under global vs local adaptation

Observations about the number, frequency, effect size, and genomic distribution of alleles associated with complex traits must be interpreted in light of evolutionary process. These characteristics, which constitute a trait’s genetic architecture, can dramatically affect evolutionary outcomes in applications from agriculture to medicine, and can provide a window into how evolution works. Here, I review theoretical predictions about the evolution of genetic architecture under spatially homogeneous, global adaptation as compared with spatially heterogeneous, local adaptation. Due to the tension between divergent selection and migration, local adaptation can favor “concentrated” genetic architectures that are enriched for alleles of larger effect, clustered in a smaller number of genomic regions, relative to expectations under global adaptation. However, the evolution of such architectures may be limited by many factors, including the genotypic redundancy of the trait, mutation rate, and temporal variability of environment. I review the circumstances in which predictions differ for global vs local adaptation and discuss where progress can be made in testing hypotheses using data from natural populations and lab experiments. As the field of comparative population genomics expands in scope, differences in architecture among traits and species will provide insights into how evolution works, and such differences must be interpreted in light of which kind of selection has been operating.     

Evolution of physiological tolerance and performance during freshwater invasions

Invasive species that penetrate habitat boundaries are likelyto experience strong selection and rapid evolution. This studydocuments evolutionary shifts in tolerance and performance followingthe invasion of fresh water by the predominantly estuarine andsalt marsh copepod Eurytemora affinis. Common-garden experimentswere performed on freshwater-invading (Lake Michigan) and ancestralsaline (St. Lawrence marsh) populations to measure shifts inadult survival (at 0, 5, and 25 PSU), and survival during developmentand development time (both using full-sib clutches split across0, 5, 15, and 25 PSU). Results showed clear evidence of heritableshifts in tolerance and performance associated with freshwaterinvasions. The freshwater population exhibited a gain in low-salinitytolerance and a reduction in high-salinity tolerance relativeto the saline population, suggesting tradeoffs. These tradeoffswere supported by negative genetic correlations between survivalat fresh (0 PSU) versus higher salinities. Mortality in responseto salinity occurred primarily before metamorphosis, suggestingthat selection in response to salinity had acted primarily onthe early life-history stages. The freshwater population exhibitedcurious patterns of life-history evolution across salinities,relative to the saline population, of retarded development tometamorphosis but accelerated development from metamorphosisto adulthood. This pattern might reflect tradeoffs between developmentrate and survival in fresh water at the early life-history stages,but some other selective force acting on later life-historystages. Significant effects of clutch (genotype) and clutch-by-salinityinteraction (G x E) on survival and development time in bothpopulations indicated ample genetic variation as substrate fornatural selection. Variation for high-salinity tolerance waspresent in the freshwater population despite negative geneticcorrelations between high- and low-salinity tolerance. Resultsimplicate the importance of natural selection and document theevolution of reaction norms during freshwater invasions.     

Studying Patterns of Recent Evolution at Synonymous Sites and Intronic Sites in Drosophila melanogaster

Most previous studies of the evolution of codon usage bias (CUB) and intronic GC content (iGC) in Drosophila melanogaster were based on between-species comparisons, reflecting long-term evolutionary events. However, a complete picture of the evolution of CUB and iGC cannot be drawn without knowledge of their more recent evolutionary history. Here, we used a polymorphism dataset collected from Zimbabwe to study patterns of the recent evolution of CUB and iGC. Analyzing coding and intronic data jointly with a model which can simultaneously estimate selection, mutational, and demographic parameters, we have found that: (1) natural selection is probably acting on synonymous codons; (2) a constant population size model seems to be sufficient to explain most of the observed synonymous polymorphism patterns; (3) GC is favored over AT in introns. In agreement with the long-term evolutionary patterns, ongoing selection acting on X-linked synonymous codons is stronger than that acting on autosomal codons. The selective differences between preferred and unpreferred codons tend to be greater than the differences between GC and AT in introns, suggesting that natural selection, not just biased gene conversion, may have influenced the evolution of CUB. Interestingly, evidence for non-equilibrium evolution comes exclusively from the intronic data. However, three different models, an equilibrium model with two classes of selected sites and two non-equilibrium models with changes in either population size or mutational parameters, fit the intronic data equally well. These results show that using inadequate selection (or demographic) models can result in incorrect estimates of demographic (or selection) parameters.     

Multilevel Selection in Models of Prebiotic Evolution II: A Direct Comparison of Compartmentalization and Spatial Self-Organization

Multilevel selection has been indicated as an essential factor for the evolution of complexity in interacting RNA-like replicator systems. There are two types of multilevel selection mechanisms: implicit and explicit. For implicit multilevel selection, spatial self-organization of replicator populations has been suggested, which leads to higher level selection among emergent mesoscopic spatial patterns (traveling waves). For explicit multilevel selection, compartmentalization of replicators by vesicles has been suggested, which leads to higher level evolutionary dynamics among explicitly imposed mesoscopic entities (protocells). Historically, these mechanisms have been given separate consideration for the interests on its own. Here, we make a direct comparison between spatial self-organization and compartmentalization in simulated RNA-like replicator systems. Firstly, we show that both mechanisms achieve the macroscopic stability of a replicator system through the evolutionary dynamics on mesoscopic entities that counteract that of microscopic entities. Secondly, we show that a striking difference exists between the two mechanisms regarding their possible influence on the long-term evolutionary dynamics, which happens under an emergent trade-off situation arising from the multilevel selection. The difference is explained in terms of the difference in the stability between self-organized mesoscopic entities and externally imposed mesoscopic entities. Thirdly, we show that a sharp transition happens in the long-term evolutionary dynamics of the compartmentalized system as a function of replicator mutation rate. Fourthly, the results imply that spatial self-organization can allow the evolution of stable folding in parasitic replicators without any specific functionality in the folding itself. Finally, the results are discussed in relation to the experimental synthesis of chemical Darwinian systems and to the multilevel selection theory of evolutionary biology in general. To conclude, novel evolutionary directions can emerge through interactions between the evolutionary dynamics on multiple levels of organization. Different multilevel selection mechanisms can produce a difference in the long-term evolutionary trend of identical microscopic entities.     

Evolution of dispersal in spatially and temporally variable environments: The importance of life cycles

Spatiotemporal variability of the environment is bound to affect the evolution of dispersal, and yet model predictions strongly differ on this particular effect. Recent studies on the evolution of local adaptation have shown that the life cycle chosen to model the selective effects of spatiotemporal variability of the environment is a critical factor determining evolutionary outcomes. Here, we investigate the effect of the order of events in the life cycle on the evolution of unconditional dispersal in a spatially heterogeneous, temporally varying landscape. Our results show that the occurrence of intermediate singular strategies and disruptive selection are conditioned by the temporal autocorrelation of the environment and by the life cycle. Life cycles with dispersal of adults versus dispersal of juveniles, local versus global density regulation, give radically different evolutionary outcomes that include selection for total philopatry, evolutionary bistability, selection for intermediate stable states, and evolutionary branching points. Our results highlight the importance of accounting for life‐cycle specifics when predicting the effects of the environment on evolutionarily selected trait values, such as dispersal, as well as the need to check the robustness of model conclusions against modifications of the life cycle.     

Evolution of protein-coding genes in Drosophila

Several contributing factors have been implicated in evolutionary rate heterogeneity among proteins, but their evolutionary mechanisms remain poorly characterized. The recently sequenced 12 Drosophila genomes provide a unique opportunity to shed light on these unresolved issues. Here, we focus on the role of natural selection in shaping evolutionary rates. We use the Drosophila genomic data to distinguish between factors that increase the strength of purifying selection on proteins and factors that affect the amount of positive selection experienced by proteins. We confirm the importance of translational selection in shaping protein evolution in Drosophila and show that factors such as tissue bias in expression, gene essentiality, intron number, and recombination rate also contribute to evolutionary rate variation among proteins.     

Role of Utility and Inference in the Evolution of Functional Information

Functional information means an encoded network of functions in living organisms from molecular signaling pathways to an organism’s behavior. It is represented by two components: code and an interpretation system, which together form a self-sustaining semantic closure. Semantic closure allows some freedom between components because small variations of the code are still interpretable. The interpretation system consists of inference rules that control the correspondence between the code and the function (phenotype) and determines the shape of the fitness landscape. The utility factor operates at multiple time scales: short-term selection drives evolution towards higher survival and reproduction rate within a given fitness landscape, and long-term selection favors those fitness landscapes that support adaptability and lead to evolutionary expansion of certain lineages. Inference rules make short-term selection possible by shaping the fitness landscape and defining possible directions of evolution, but they are under control of the long-term selection of lineages. Communication normally occurs within a set of agents with compatible interpretation systems, which I call communication system. Functional information cannot be directly transferred between communication systems with incompatible inference rules. Each biological species is a genetic communication system that carries unique functional information together with inference rules that determine evolutionary directions and constraints. This view of the relation between utility and inference can resolve the conflict between realism/positivism and pragmatism. Realism overemphasizes the role of inference in evolution of human knowledge because it assumes that logic is embedded in reality. Pragmatism substitutes usefulness for truth and therefore ignores the advantage of inference. The proposed concept of evolutionary pragmatism rejects the idea that logic is embedded in reality; instead, inference rules are constructed within each communication system to represent reality, and they evolve towards higher adaptability on a long time scale.     

Cancer Evolution Is Associated with Pervasive Positive Selection on Globally Expressed Genes

Cancer is an evolutionary process in which cells acquire new transformative, proliferative and metastatic capabilities. A full understanding of cancer requires learning the dynamics of the cancer evolutionary process. We present here a large-scale analysis of the dynamics of this evolutionary process within tumors, with a focus on breast cancer. We show that the cancer evolutionary process differs greatly from organismal (germline) evolution. Organismal evolution is dominated by purifying selection (that removes mutations that are harmful to fitness). In contrast, in the cancer evolutionary process the dominance of purifying selection is much reduced, allowing for a much easier detection of the signals of positive selection (adaptation). We further show that, as a group, genes that are globally expressed across human tissues show a very strong signal of positive selection within tumors. Indeed, known cancer genes are enriched for global expression patterns. Yet, positive selection is prevalent even on globally expressed genes that have not yet been associated with cancer, suggesting that globally expressed genes are enriched for yet undiscovered cancer related functions. We find that the increased positive selection on globally expressed genes within tumors is not due to their expression in the tissue relevant to the cancer. Rather, such increased adaptation is likely due to globally expressed genes being enriched in important housekeeping and essential functions. Thus, our results suggest that tumor adaptation is most often mediated through somatic changes to those genes that are important for the most basic cellular functions. Together, our analysis reveals the uniqueness of the cancer evolutionary process and the particular importance of globally expressed genes in driving cancer initiation and progression.     

Genetic Constraints on Protein Evolution

ABSTRACT

Evolution requires the generation and optimization of new traits (“adaptation”) and involves the selection of mutations that improve cellular function. These mutations were assumed to arise by selection of neutral mutations present at all times in the population. Here we review recent evidence that indicates that deleterious mutations are more frequent in the population than previously recognized and that these mutations play a significant role in protein evolution through continuous positive selection. Positively selected mutations include adaptive mutations, i.e. mutations that directly affect enzymatic function, and compensatory mutations, which suppress the pleiotropic effects of adaptive mutations. Compensatory mutations are by far the most frequent of the two and would allow potentially adaptive but deleterious mutations to persist long enough in the population to be positively selected during episodes of adaptation. Compensatory mutations are, by definition, context-dependent and thus constrain the paths available for evolution. This provides a mechanistic basis for the examples of highly constrained evolutionary landscapes and parallel evolution reported in natural and experimental populations. The present review article describes these recent advances in the field of protein evolution and discusses their implications for understanding the genetic basis of disease and for protein engineering in vitro.     

Genome size and GC content evolution of Festuca: ancestral expansion and subsequent reduction

Background and Aims: Plant evolution is well known to be frequently associated withremarkable changes in genome size and composition; however,the knowledge of long-term evolutionary dynamics of these processesstill remains very limited. Here a study is made of the finedynamics of quantitative genome evolution in Festuca (fescue),the largest genus in Poaceae (grasses). Methods: Using flow cytometry (PI, DAPI), measurements were made of DNAcontent (2C-value), monoploid genome size (Cx-value), averagechromosome size (C/n-value) and cytosine + guanine (GC) contentof 101 Festuca taxa and 14 of their close relatives. The resultswere compared with the existing phylogeny based on ITS and trnL-Fsequences. Key Results: The divergence of the fescue lineage from related Poeae waspredated by about a 2-fold monoploid genome and chromosome sizeenlargement, and apparent GC content enrichment. The backwardreduction of these parameters, running parallel in both mainevolutionary lineages of fine-leaved and broad-leaved fescues,appears to diverge among the existing species groups. The mostdramatic reductions are associated with the most recently andrapidly evolving groups which, in combination with recent intraspecificgenome size variability, indicate that the reduction processis probably ongoing and evolutionarily young. This dynamicsmay be a consequence of GC-rich retrotransposon proliferationand removal. Polyploids derived from parents with a large genomesize and high GC content (mostly allopolyploids) had smallerCx- and C/n-values and only slightly deviated from parentalGC content, whereas polyploids derived from parents with smallgenome and low GC content (mostly autopolyploids) generallyhad a markedly increased GC content and slightly higher Cx-and C/n-values. Conclusions: The present study indicates the high potential of general quantitativecharacters of the genome for understanding the long-term processesof genome evolution, testing evolutionary hypotheses and theirusefulness for large-scale genomic projects. Taken together,the results suggest that there is an evolutionary advantagefor small genomes in Festuca.     

Biological invasions and phenotypic evolution: a quantitative genetic perspective

Among the many different components of global environmental change, biological invasions represent the one with the most long-term ecological and evolutionary consequences, as effects are irreversible. Although the ecological impact of invasive species has been under great scrutiny, its evolutionary aspects and consequences have remained less explored. Once established, an important part of the success of an invasive species will depend on the presence of genetic variation in populations at the geographic boundaries upon which natural selection can act. This information is integrated in G, the matrix of additive genetic variances and covariances for a suite of traits. The G-matrix shows the restrictions and potentialities of adaptive evolution and, together with natural selection determine the direction and rate of phenotypic evolution. Here I propose that a geographic analysis of G in populations of the introduced and native range becomes essential to understand critical evolutionary issues associated with invasion success.     

Experimental Evolution and Its Role in Evolutionary Physiology

Four general approaches to the study of evolutionary physiology—phylogenetically-basedcomparisons, genetic analyses and manipulations, phenotypicplasticity and manipulation, and selection studies—areoutlined and discussed. We provide an example of the latter,the application of laboratory selection experiments to the studyof a general issue in environmental adaptation, differencesin adaptive patterns of generalists and specialists. A cloneof the bacterium Escherichia coli that had evolved in a constantenvironment of 37°C was replicated into 6 populations andallowed to reproduce for 2,000 generations in a variable thermalenvironment alternating between 32 and 42°C. As predictedby theory, fitness and efficiency of resource use increasedin this new environment, as did stress resistance. Contraryto predictions, however, fitness and efficiency in the constantancestral environment of 37°C did not decrease, nor didthermal niche breadth or phenotypic plasticity increase. Selectionexperiments can thus provide a valuable approach to testinghypotheses and assumptions about the evolution of functionalcharacters.     

How Cancer Shapes Evolution and How Evolution Shapes Cancer

Evolutionary theories are critical for understanding cancer development at the level of species as well as at the level of cells and tissues, and for developing effective therapies. Animals have evolved potent tumor-suppressive mechanisms to prevent cancer development. These mechanisms were initially necessary for the evolution of multi-cellular organisms and became even more important as animals evolved large bodies and long lives. Indeed, the development and architecture of our tissues were evolutionarily constrained by the need to limit cancer. Cancer development within an individual is also an evolutionary process, which in many respects mirrors species evolution. Species evolve by mutation and selection acting on individuals in a population; tumors evolve by mutation and selection acting on cells in a tissue. The processes of mutation and selection are integral to the evolution of cancer at every step of multistage carcinogenesis, from tumor genesis to metastasis. Factors associated with cancer development, such as aging and carcinogens, have been shown to promote cancer evolution by impacting both mutation and selection processes. While there are therapies that can decimate a cancer cell population, unfortunately cancers can also evolve resistance to these therapies, leading to the resurgence of treatment-refractory disease. Understanding cancer from an evolutionary perspective can allow us to appreciate better why cancers predominantly occur in the elderly and why other conditions, from radiation exposure to smoking, are associated with increased cancers. Importantly, the application of evolutionary theory to cancer should engender new treatment strategies that could better control this dreaded disease.     

Components of Selection in the Evolution of the Influenza Virus: Linkage Effects Beat Inherent Selection

The influenza virus is an important human pathogen, with a rapid rate of evolution in the human population. The rate of homologous recombination within genes of influenza is essentially zero. As such, where two alleles within the same gene are in linkage disequilibrium, interference between alleles will occur, whereby selection acting upon one allele has an influence upon the frequency of the other. We here measured the relative importance of selection and interference effects upon the evolution of influenza. We considered time-resolved allele frequency data from the global evolutionary history of the haemagglutinin gene of human influenza A/H3N2, conducting an in-depth analysis of sequences collected since 1996. Using a model that accounts for selection-caused interference between alleles in linkage disequilibrium, we estimated the inherent selective benefit of individual polymorphisms in the viral population. These inherent selection coefficients were in turn used to calculate the total selective effect of interference acting upon each polymorphism, considering the effect of the initial background upon which a mutation arose, and the subsequent effect of interference from other alleles that were under selection. Viewing events in retrospect, we estimated the influence of each of these components in determining whether a mutant allele eventually fixed or died in the global viral population. Our inherent selection coefficients, when combined across different regions of the protein, were consistent with previous measurements of dN/dS for the same system. Alleles going on to fix in the global population tended to be under more positive selection, to arise on more beneficial backgrounds, and to avoid strong negative interference from other alleles under selection. However, on average, the fate of a polymorphism was determined more by the combined influence of interference effects than by its inherent selection coefficient.     

Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.     

Selection analysis on the rapid evolution of a secondary sexual trait

Evolutionary analyses of population translocations (experimental or accidental) have been important in demonstrating speed of evolution because they subject organisms to abrupt environmental changes that create an episode of selection. However, the strength of selection in such studies is rarely measured, limiting our understanding of the evolutionary process. This contrasts with long-term, mark–recapture studies of unmanipulated populations that measure selection directly, yet rarely reveal evolutionary change. Here, we present a study of experimental evolution of male colour in Trinidadian guppies where we tracked both evolutionary change and individual-based measures of selection. Guppies were translocated from a predator-rich to a low-predation environment within the same stream system. We used a combination of common garden experiments and monthly sampling of individuals to measure the phenotypic and genetic divergence of male coloration between ancestral and derived fish. Results show rapid evolutionary increases in orange coloration in both populations (1 year or three generations), replicating the results of previous studies. Unlike previous studies, we linked this evolution to an individual-based analysis of selection. By quantifying individual reproductive success and survival, we show, for the first time, that males with more orange and black pigment have higher reproductive success, but males with more black pigment also have higher risk of mortality. The net effect of selection is thus an advantage of orange but not black coloration, as reflected in the evolutionary response. This highlights the importance of considering all components of fitness when understanding the evolution of sexually selected traits in the wild.     

Asexual Experimental Evolution of Yeast Does Not Curtail Transposable Elements

Compared with asexual reproduction, sex facilitates the transmission of transposable elements (TEs) from one genome to another, but boosts the efficacy of selection against deleterious TEs. Thus, theoretically, it is unclear whether sex has a positive net effect on TE’s proliferation. An empirical study concluded that sex is at the root of TE’s evolutionary success because the yeast TE load was found to decrease rapidly in approximately 1,000 generations of asexual but not sexual experimental evolution. However, this finding contradicts the maintenance of TEs in natural yeast populations where sexual reproduction occurs extremely infrequently. Here, we show that the purported TE load reduction during asexual experimental evolution is likely an artifact of low genomic sequencing coverages. We observe stable TE loads in both sexual and asexual experimental evolution from multiple yeast data sets with sufficient coverages. To understand the evolutionary dynamics of yeast TEs, we turn to asexual mutation accumulation lines that have been under virtually no selection. We find that both TE transposition and excision rates per generation, but not their difference, tend to be higher in environments where yeast grows more slowly. However, the transposition rate is not significantly higher than the excision rate and the variance of the TE number among natural strains is close to its neutral expectation, suggesting that selection against TEs is at best weak in yeast. We conclude that the yeast TE load is maintained largely by a transposition–excision balance and that the influence of sex remains unclear.     

Alternate Routes to Sociality in Jays--With a Theory for the Evolution of Altruism and Communal Breeding

The social systems of New World species of jays are comparedbehaviorally and ecologically. Two lines leading to socialityare identified, one connecting the pair-in-territory systemwith the colonial system and a second connecting the pair-in-territorysystem with the communal system. Ecological factors in the evolution of communal breeding andits associated altruistic behavior are considered mainly inthe genus Aphelocoma, but other birds are treated briefly. Threeprincipal origins of communality and altruism in birds are identified:from colonies, from a surplus of males, and by retention ofyoung in the family, the latter being of greatest importance.The theory proposed for the evolution of communal breeding andaltruism emphasizes three main processes: 1) K-selection, (2)kin selection, and (3) kin-group selection in the same chronologicalorder.