Evidence for the non-quasispecies evolution of RNA viruses [corrected

The quasispecies model of RNA virus evolution differs from those formulated in conventional population genetics in that neutral mutations do not lead to genetic drift of the population, and natural selection acts on the mutant distribution as a whole rather than on individual variants. By computer simulation, we show that this model could be inappropriate for many RNA viruses because the neutral sequence space may be too large to allow the formation of a quasispecies distribution. This view is supported by our analysis of gene sequences from vesicular stomatitis virus, which is considered a prototype RNA virus quasispecies. Our results are relevant to the evolution of RNA systems in general.     

Selection and demographic history shape the molecular evolution of the gamete compatibility protein bindin in Pisaster sea stars

Reproductive compatibility proteins have been shown to evolve rapidly under positive selection leading to reproductive isolation, despite the potential homogenizing effects of gene flow. This process has been implicated in both primary divergence among conspecific populations and reinforcement during secondary contact; however, these two selective regimes can be difficult to discriminate from each other. Here, we describe the gene that encodes the gamete compatibility protein bindin for three sea star species in the genus Pisaster. First, we compare the full‐length bindin‐coding sequence among all three species and analyze the evolutionary relationships between the repetitive domains of the variable second bindin exon. The comparison suggests that concerted evolution of repetitive domains has an effect on bindin divergence among species and bindin variation within species. Second, we characterize population variation in the second bindin exon of two species: We show that positive selection acts on bindin variation in Pisaster ochraceus but not in Pisaster brevispinus, which is consistent with higher polyspermy risk in P. ochraceus. Third, we show that there is no significant genetic differentiation among populations and no apparent effect of sympatry with congeners that would suggest selection based on reinforcement. Fourth, we combine bindin and cytochrome c oxidase 1 data in isolation‐with‐migration models to estimate gene flow parameter values and explore the historical demographic context of our positive selection results. Our findings suggest that positive selection on bindin divergence among P. ochraceus alleles can be accounted for in part by relatively recent northward population expansions that may be coupled with the potential homogenizing effects of concerted evolution.     

Maintaining heritable variation via sex-limited temporally fluctuating selection: a phenotypic model accommodating non-Mendelian epigenetic effects

Using a phenotypic model, we show that significant heritable variation can be maintained in a population subjected to temporally fluctuating selection if only one sex is subject to selection. In fact, more variation is maintained with sex-limited selection at a given selection intensity than if both sexes are subject to half that selection intensity. This result is commensurate with existing population genetic models. However, genetic models may be inappropriate for sexually selected traits because many of them may be of non-genetic origin, such as maternal effects or – more likely –epigenetic effects. Phenotypic models obviate this problem by accommodating both genetic and epigenetic effects, as well as maternaleffects. Our phenotypic model of sex-limited temporally fluctuating selection shows that substantial heritable variation can be maintained and therebyprovides impetus to develop population epigenetic models.     

Phenotypic evolution in stochastic environments: The contribution of frequency- and density-dependent selection

Understanding how environmental variation affects phenotypic evolution requires models based on ecologically realistic assumptions that include variation in population size and specific mechanisms by which environmental fluctuations affect selection. Here we generalize quantitative genetic theory for environmentally induced stochastic selection to include general forms of frequency- and density-dependent selection. We show how the relevant fitness measure under stochastic selection relates to Fisher's fundamental theorem of natural selection, and present a general class of models in which density regulation acts through total use of resources rather than just population size. In this model, there is a constant adaptive topography for expected evolution, and the function maximized in the long run is the expected factor restricting population growth. This allows us to generalize several previous results and to explain why apparently “-selected” species with slow life histories often have low carrying capacities. Our joint analysis of density- and frequency-dependent selection reveals more clearly the relationship between population dynamics and phenotypic evolution, enabling a broader range of eco-evolutionary analyses of some of the most interesting problems in evolution in the face of environmental variation.     

Some population consequences of variation in preference among individual predators

A number of foraging studies have demonstrated that populations of predators rarely consist of individuals with identical preferences for particular types of prey. Variation among predators can lead to frequency-dependent changes in population preference, because those predators mat prefer the rarer type of prey generally have the greatest influence on population preference. In this study we develop a series of theoretical models which demonstrate how anti-apostatic selection (i.e. selection against the rare form) can arise out of (a) bimodal and (b) normal variation in preference among individuals of the same species. We show that population level anti-apostatic selection can occur even when individual predators show pro-apostatic selection (i.e. selection against the common form). Furthermore, patterns of population prey selection that arise out of variation in preference can potentially be pro-apostatic over one range of relative densities and anti-apostatic over another range of relative densities. Finally, we examine a case study involving predation by female waterboatmen Notonecta glauca and show that the variation in preference in this species is large enough to generate higher anti-apostatic selection than would be expected from the diet selected by the average individual.     

Weak selection and protein evolution

The "nearly neutral" theory of molecular evolution proposes that many features of genomes arise from the interaction of three weak evolutionary forces: mutation, genetic drift, and natural selection acting at its limit of efficacy. Such forces generally have little impact on allele frequencies within populations from generation to generation but can have substantial effects on long-term evolution. The evolutionary dynamics of weakly selected mutations are highly sensitive to population size, and near neutrality was initially proposed as an adjustment to the neutral theory to account for general patterns in available protein and DNA variation data. Here, we review the motivation for the nearly neutral theory, discuss the structure of the model and its predictions, and evaluate current empirical support for interactions among weak evolutionary forces in protein evolution. Near neutrality may be a prevalent mode of evolution across a range of functional categories of mutations and taxa. However, multiple evolutionary mechanisms (including adaptive evolution, linked selection, changes in fitness-effect distributions, and weak selection) can often explain the same patterns of genome variation. Strong parameter sensitivity remains a limitation of the nearly neutral model, and we discuss concave fitness functions as a plausible underlying basis for weak selection.     

Experimental evidence that selection favors character displacement in the ivyleaf morning glory

While there is abundant evidence to suggest that pollinators influence the evolution of plant floral traits, there is little direct evidence that interactions between plant species shape the evolution of such characteristics. The purpose of this study was to determine whether the presence of the morning glory Ipomoea purpurea alters patterns of selection on floral traits of its congener, Ipomoea hederacea. We show that while selection on I. hederacea floral traits is effectively neutral when I. purpurea flowers are absent, selection acts to increase clustering of anthers about the stigma when I. purpurea flowers are present. Our results provide direct experimental evidence that the presence of flowers of a co-occurring congener can influence patterns of natural selection on floral traits that influence the mating system and contribute to prezygotic isolation. To the extent that this result is general, it also lends support to the claim that distributional patterns interpreted as ecological and reproductive character displacement in other plant species have been caused by natural selection generated by interactions among plant species.     

Natural Selection Constrains Neutral Diversity across A Wide Range of Species

The neutral theory of molecular evolution predicts that the amount of neutral polymorphisms within a species will increase proportionally with the census population size (Nc). However, this prediction has not been borne out in practice: while the range of Nc spans many orders of magnitude, levels of genetic diversity within species fall in a comparatively narrow range. Although theoretical arguments have invoked the increased efficacy of natural selection in larger populations to explain this discrepancy, few direct empirical tests of this hypothesis have been conducted. In this work, we provide a direct test of this hypothesis using population genomic data from a wide range of taxonomically diverse species. To do this, we relied on the fact that the impact of natural selection on linked neutral diversity depends on the local recombinational environment. In regions of relatively low recombination, selected variants affect more neutral sites through linkage, and the resulting correlation between recombination and polymorphism allows a quantitative assessment of the magnitude of the impact of selection on linked neutral diversity. By comparing whole genome polymorphism data and genetic maps using a coalescent modeling framework, we estimate the degree to which natural selection reduces linked neutral diversity for 40 species of obligately sexual eukaryotes. We then show that the magnitude of the impact of natural selection is positively correlated with Nc, based on body size and species range as proxies for census population size. These results demonstrate that natural selection removes more variation at linked neutral sites in species with large Nc than those with small Nc and provides direct empirical evidence that natural selection constrains levels of neutral genetic diversity across many species. This implies that natural selection may provide an explanation for this longstanding paradox of population genetics.     

The effects of deleterious mutations on evolution at linked sites

The process of evolution at a given site in the genome can be influenced by the action of selection at other sites, especially when these are closely linked to it. Such selection reduces the effective population size experienced by the site in question (the Hill-Robertson effect), reducing the level of variability and the efficacy of selection. In particular, deleterious variants are continually being produced by mutation and then eliminated by selection at sites throughout the genome. The resulting reduction in variability at linked neutral or nearly neutral sites can be predicted from the theory of background selection, which assumes that deleterious mutations have such large effects that their behavior in the population is effectively deterministic. More weakly selected mutations can accumulate by Muller's ratchet after a shutdown of recombination, as in an evolving Y chromosome. Many functionally significant sites are probably so weakly selected that Hill-Robertson interference undermines the effective strength of selection upon them, when recombination is rare or absent. This leads to large departures from deterministic equilibrium and smaller effects on linked neutral sites than under background selection or Muller's ratchet. Evidence is discussed that is consistent with the action of these processes in shaping genome-wide patterns of variation and evolution.     

Levels of genetic polymorphism: marker loci versus quantitative traits.

Species are the units used to measure ecological diversity and alleles are the units of genetic diversity. Genetic variation within and among species has been documented most extensively using allozyme electrophoresis. This reveals wide differences in genetic variability within, and genetic distances among, species, demonstrating that species are not equivalent units of diversity. The extent to which the pattern observed for allozymes can be used to infer patterns of genetic variation in quantitative traits depends on the forces generating and maintaining variability. Allozyme variation is probably not strictly neutral but, nevertheless, heterozygosity is expected to be influenced by population size and genetic distance will be affected by time since divergence. The same is true for quantitative traits influenced by many genes and under weak stabilizing selection. However, the limited data available suggest that allozyme variability is a poor predictor of genetic variation in quantitative traits within populations. It is a better predictor of general phenotypic divergence and of postzygotic isolation between populations or species, but is only weakly correlated with prezygotic isolation. Studies of grasshopper and planthopper mating signal variation and assortative mating illustrate how these characters evolve independently of general genetic and morphological variation. The role of such traits in prezygotic isolation, and hence speciation, means that they will contribute significantly to the diversity of levels of genetic variation within and among species.     

Sexual selection and population divergence II. Divergence in different sexual traits and signal modalities in field crickets (Teleogryllus oceanicus)

Sexual selection can target many different types of traits. However, the relative influence of different sexually selected traits during evolutionary divergence is poorly understood. We used the field cricket Teleogryllus oceanicus to quantify and compare how five traits from each of three sexual signal modalities and components diverge among allopatric populations: male advertisement song, cuticular hydrocarbon (CHC) profiles and forewing morphology. Population divergence was unexpectedly consistent: we estimated the among‐population (genetic) variance‐covariance matrix, D , for all 15 traits, and D_max explained nearly two‐thirds of its variation. CHC and wing traits were most tightly integrated, whereas song varied more independently. We modeled the dependence of among‐population trait divergence on genetic distance estimated from neutral markers to test for signatures of selection versus neutral divergence. For all three sexual trait types, phenotypic variation among populations was largely explained by a neutral model of divergence. Our findings illustrate how phenotypic integration across different types of sexual traits might impose constraints on the evolution of mating isolation and divergence via sexual selection.     

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within‐population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.     

CONSUMER–RESOURCE INTERACTIONS AND THE EVOLUTION OF MIGRATION

Theoretical studies have demonstrated that selection will favor increased migration when fitnesses vary both temporally and spatially, but it is far from clear how pervasive those theoretical conditions are in nature. Although consumer–resource interactions are omnipresent in nature and can generate spatial and temporal variation, it is unknown even in theory whether these dynamics favor the evolution of migration. We develop a mathematical model to address whether and how migration evolves when variability in fitness is determined at least in part by consumer–resource coevolutionary interactions. Our analyses show that such interactions can drive the evolution of migration in the resource, consumer, or both species and thus supplies a general explanation for the pervasiveness of migration. Over short time scales, we show the direction of change in migration rate is determined primarily by the state of local adaptation of the species involved: rates increase when a species is locally maladapted and decrease when locally adapted. Our results reveal that long‐term evolutionary trends in migration rates can differ dramatically depending on the strength or weakness of interspecific interactions and suggest an explanation for the evolutionary divergence of migration rates among interacting species.     

DNA Barcoding Works in Practice but Not in (Neutral) Theory

Background

DNA barcode differences within animal species are usually much less than differences among species, making it generally straightforward to match unknowns to a reference library. Here we aim to better understand the evolutionary mechanisms underlying this usual “barcode gap” pattern. We employ avian barcode libraries to test a central prediction of neutral theory, namely, intraspecific variation equals 2 Nµ, where N is population size and µ is mutations per site per generation. Birds are uniquely suited for this task: they have the best-known species limits, are well represented in barcode libraries, and, most critically, are the only large group with documented census population sizes. In addition, we ask if mitochondrial molecular clock measurements conform to neutral theory prediction of clock rate equals µ.

Results

Intraspecific COI barcode variation was uniformly low regardless of census population size (n = 142 species in 15 families). Apparent outliers reflected lumping of reproductively isolated populations or hybrid lineages. Re-analysis of a published survey of cytochrome b variation in diverse birds (n = 93 species in 39 families) further confirmed uniformly low intraspecific variation. Hybridization/gene flow among species/populations was the main limitation to DNA barcode identification.

Conclusions/Significance

To our knowledge, this is the first large study of animal mitochondrial diversity using actual census population sizes and the first to test outliers for population structure. Our finding of universally low intraspecific variation contradicts a central prediction of neutral theory and is not readily accounted for by commonly proposed ad hoc modifications. We argue that the weight of evidence–low intraspecific variation and the molecular clock–indicates neutral evolution plays a minor role in mitochondrial sequence evolution. As an alternate paradigm consistent with empirical data, we propose extreme purifying selection, including at synonymous sites, limits variation within species and continuous adaptive selection drives the molecular clock.     

A general population genetic framework for antagonistic selection that accounts for demography and recurrent mutation

Antagonistic selection--where alleles at a locus have opposing effects on male and female fitness ("sexual antagonism") or between components of fitness ("antagonistic pleiotropy")--might play an important role in maintaining population genetic variation and in driving phylogenetic and genomic patterns of sexual dimorphism and life-history evolution. While prior theory has thoroughly characterized the conditions necessary for antagonistic balancing selection to operate, we currently know little about the evolutionary interactions between antagonistic selection, recurrent mutation, and genetic drift, which should collectively shape empirical patterns of genetic variation. To fill this void, we developed and analyzed a series of population genetic models that simultaneously incorporate these processes. Our models identify two general properties of antagonistically selected loci. First, antagonistic selection inflates heterozygosity and fitness variance across a broad parameter range--a result that applies to alleles maintained by balancing selection and by recurrent mutation. Second, effective population size and genetic drift profoundly affect the statistical frequency distributions of antagonistically selected alleles. The "efficacy" of antagonistic selection (i.e., its tendency to dominate over genetic drift) is extremely weak relative to classical models, such as directional selection and overdominance. Alleles meeting traditional criteria for strong selection (N(e)s > 1, where N(e) is the effective population size, and s is a selection coefficient for a given sex or fitness component) may nevertheless evolve as if neutral. The effects of mutation and demography may generate population differences in overall levels of antagonistic fitness variation, as well as molecular population genetic signatures of balancing selection.     

Evolution of adaptive phenotypic variation patterns by direct selection for evolvability

A basic assumption of the Darwinian theory of evolution is that heritable variation arises randomly. In this context, randomness means that mutations arise irrespective of the current adaptive needs imposed by the environment. It is broadly accepted, however, that phenotypic variation is not uniformly distributed among phenotypic traits, some traits tend to covary, while others vary independently, and again others barely vary at all. Furthermore, it is well established that patterns of trait variation differ among species. Specifically, traits that serve different functions tend to be less correlated, as for instance forelimbs and hind limbs in bats and humans, compared with the limbs of quadrupedal mammals. Recently, a novel class of genetic elements has been identified in mouse gene-mapping studies that modify correlations among quantitative traits. These loci are called relationship loci, or relationship Quantitative Trait Loci (rQTL), and affect trait correlations by changing the expression of the existing genetic variation through gene interaction. Here, we present a population genetic model of how natural selection acts on rQTL. Contrary to the usual neo-Darwinian theory, in this model, new heritable phenotypic variation is produced along the selected dimension in response to directional selection. The results predict that selection on rQTL leads to higher correlations among traits that are simultaneously under directional selection. On the other hand, traits that are not simultaneously under directional selection are predicted to evolve lower correlations. These results and the previously demonstrated existence of rQTL variation, show a mechanism by which natural selection can directly enhance the evolvability of complex organisms along lines of adaptive change.     

Cranial evolution in sakis (Pithecia, Platyrrhini). II: Evolutionary processes and morphological integration

Patterns of interspecific differentiation in saki monkeys (Pithecia) are quantitatively described and possible evolutionary processes producing them are examined. The comparison of species correlation matrices to expected patterns of morphological integration reveal significant and similar patterns of development-based cranial integration among species. Aspects of the facial region are more heavily influenced by general size variation than features of the neural region. The comparison of pooled within- and between-groups V/CV matrices suggests that genetic drift might be a sufficient explanation for saki cranial evolution. Differential natural selection gradients are also reconstructed because selection may also have caused population differentiation through evolutionary time. These gradients illustrate the inherent multivariate nature of selection, being a consequence of the interaction between existing morphological integration (correlation) among traits and the action of natural selection. Yet, our attempt to interpret selection gradients in terms of their functional significance did not result in any clear association between selection and function. Perhaps this is also an indication that morphological evolution in sakis was mostly neutral.     

Selection, Generalized Transmission and the Evolution of Modifier Genes. I. the Reduction Principle

Modifier gene models are used to explore the evolution of features of organisms, such as the genetic system, that are not directly involved in the determination of fitness. Recent work has shown that a general "reduction principle" holds in models of selectively neutral modifiers of recombination, mutation, and migration. Here we present a framework for models of modifier genes that shows these reduction results to be part of a more general theory, for which recombination and mutation are special cases. The deterministic forces that affect the genetic composition of a population can be partitioned into two categories: selection and transmission. Selection includes differential viabilities, fertilities, and mating success. Imperfect transmission occurs as a result of such phenomena as recombination, mutation and migration, meiosis, gene conversion, and meiotic drive. Selectively neutral modifier genes affect transmission, and a neutral modifier gene can evolve only by generating association with selected genes whose transmission it affects. We show that, in randomly mating populations at equilibrium, imperfect transmission of selected genes allows a variance in their marginal fitnesses to be maintained. This variance in the marginal fitnesses of selected genes is what drives the evolution of neutral modifier genes. Populations with a variance in marginal fitnesses at equilibrium are always subject to invasion by modifier genes that bring about perfect transmission of the selected genes. It is also found, within certain constraints, that for modifier genes producing what we call "linear variation" in the transmission processes, a new modifier allele can invade a population at equilibrium if it reduces the level of imperfect transmission acting on the selected genes, and will be expelled if it increases the level of imperfect transmission. Moreover, the strength of the induced selection on the modifier gene is shown to range up to the order of the departure of the genetic system from perfect transmission.     

Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species

A central aim of evolutionary genomics is to identify the relative roles that various evolutionary forces have played in generating and shaping genetic variation within and among species. Here we use whole-genome resequencing data to characterize and compare genome-wide patterns of nucleotide polymorphism, site frequency spectrum, and population-scaled recombination rates in three species of Populus: Populus tremula, P. tremuloides, and P. trichocarpa. We find that P. tremuloides has the highest level of genome-wide variation, skewed allele frequencies, and population-scaled recombination rates, whereas P. trichocarpa harbors the lowest. Our findings highlight multiple lines of evidence suggesting that natural selection, due to both purifying and positive selection, has widely shaped patterns of nucleotide polymorphism at linked neutral sites in all three species. Differences in effective population sizes and rates of recombination largely explain the disparate magnitudes and signatures of linked selection that we observe among species. The present work provides the first phylogenetic comparative study on a genome-wide scale in forest trees. This information will also improve our ability to understand how various evolutionary forces have interacted to influence genome evolution among related species.     

History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection

Introduced species often exhibit changes in genetic variation, population structure, selection regime and phenotypic traits as they colonize and expand into new ranges. For these reasons, species invasions are increasingly recognized as promising systems for studying adaptive evolution over contemporary time scales. However, changes in phenotypic traits during invasion occur under non-equilibrium demographic conditions and may reflect the influences of prior evolutionary history and chance events, as well as selection. We briefly review the evidence for phenotypic evolution and the role of selection during invasion. While there is ample evidence for evolutionary change, it is less clear if selection is the primary mechanism. We then discuss the likelihood that stochastic events shift phenotypic distributions during invasion, and argue that hypotheses of adaptation should be tested against appropriate null models. We suggest two experimental frameworks for separating stochastic evolution from adaptation: statistically accounting for phenotypic variation among putative invasion sources identified by using phylogenetic or assignment methods and by comparing estimates of differentiation within and among ranges for both traits and neutral markers ( Q _ST vs. F _ST). Designs that incorporate a null expectation can reveal the role of history and chance in the evolutionary process, and provide greater insights into evolution during species invasions.