Frequent nonrandom shifts in the temporal sequence of developmental landmark events during teleost evolutionary diversification.

Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony-based methods-event-pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event-dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.

Distinguishing Among Evolutionary Forces Acting on Genome-Wide Base Composition: Computer Simulation Analysis of Approximate Methods for Inferring Site Frequency Spectra of Derived Mutations.

Inferred ancestral nucleotide states are increasingly employed in analyses of within- and between -species genome variation. Although numerous studies have focused on ancestral inference among distantly related lineages, approaches to infer ancestral states in polymorphism data have received less attention. Recently developed approaches that employ complex transition matrices allow us to infer ancestral nucleotide sequence in various evolutionary scenarios of base composition. However, the requirement of a single gene tree to calculate a likelihood is an important limitation for conducting ancestral inference using within-species variation in recombining genomes. To resolve this problem, and to extend the applicability of ancestral inference in studies of base composition evolution, we first evaluate three previously proposed methods to infer ancestral nucleotide sequences among within- and between-species sequence variation data. The methods employ a single allele, bifurcating tree, or a star tree for within-species variation data. Using simulated nucleotide sequences, we employ ancestral inference to infer fixations and polymorphisms. We find that all three methods show biased inference. We modify the bifurcating tree method to include weights to adjust for an expected site frequency spectrum, "bifurcating tree with weighting" (BTW). Our simulation analysis show that the BTW method can substantially improve the reliability and robustness of ancestral inference in a range of scenarios that include non-neutral and/or non-stationary base composition evolution.

Contribution of gene flow to the evolution of recombination suppression in sex chromosomes.

Polymorphism of alleles that benefit one sex but harm the other (sexually antagonistic alleles) generates selective pressures for reduced recombination between themselves and sex-determination loci. Such polymorphism can be maintained within a population when selection coefficients are sufficiently balanced between males and females. However, if regulatory mutations restrict gene expression only to one sex, these alleles become neutral in the other sex and easily fixed within a population, removing the selective pressures for recombination suppression in sex chromosomes. When there is spatial variation in selection regimes, however, alleles that are deleterious in one sex and neutral in the other can be maintained in other neighboring populations and gene flow may continuously supply deleterious alleles. We hypothesized that this maintenance of genetic variation may promote the establishment of recombination suppression in sex chromosomes even in cases where selection is limited to one sex. Using individual-based simulations, we show that spatial variation in male-limited selection and gene flow can promote the establishment of Y-autosome fusions, a special case of recombination suppression in sex chromosomes. This can be explained by the fact that fused Y-chromosomes that capture alleles that are beneficial for local males have a higher mean fitness compared to unfused Y chromosomes in the presence of deleterious gene flow. We also simulated the case of sex-concordant selection and found that gene flow of alleles that are deleterious in both sexes did not substantially increase the establishment rates of Y-autosome fusions across the parameter space examined. This can be accounted for by the fact that foreign alleles that are deleterious in both sexes can be efficiently removed from the population compared to alleles that are neutral in females. These results indicate that how gene flow affects the establishment rates of Y-autosome fusions depends largely on selection regimes. Spatial variation in sex-specific selection and gene flow should be appreciated as a factor affecting sex chromosome evolution.

The intricate relationship between sexually antagonistic selection and the evolution of sex chromosome fusions.

Sex chromosomes are among the most evolutionarily labile features in some groups of animals. One of the mechanisms causing structural changes of sex chromosomes is fusion with an autosome. A recent study showed that the establishment rates of Y chromosome-autosome fusions are much higher than those of other fusions (i.e., X-autosome, W-autosome, and Z-autosome fusions) in fishes and reptiles. Although sexually antagonistic selection may be one of the most important driving forces of sex chromosome-autosome fusions, a previous theoretical analysis showed that sexually antagonistic selection alone cannot explain the excess of Y-autosome fusions in these taxa. This previous analysis, however, is based on the assumption that sexually antagonistic selection is symmetric, sexually antagonistic alleles are maintained only by selection-drift balance (i.e., no supply of mutation), and only one type of fusion arises within a population. Here, we removed these assumptions and made an individual-based model to simulate the establishment of sex chromosome-autosome fusions. Our simulations showed that the highest establishment rate of Y-autosome fusion can be achieved when the fusion captures a rare male-beneficial allele, if the recurrent mutation rates are high enough to maintain the polymorphism of alleles with asymmetric, sexually antagonistic effects. Our results demonstrate that sexually antagonistic selection can influence the dynamics of sex chromosome structural changes, but the type of fusion that becomes the most common depends on fusion rates, recurrent mutation rates, and selection regimes. Because the evolutionary fate of sex chromosome-autosome fusions is highly parameter-sensitive, further attempts to empirically measure these parameters in natural populations are essential for a better understanding of the roles of sexually antagonistic selection in sex chromosome evolution.

Codon Usage Selection Can Bias Estimation of the Fraction of Adaptive Amino Acid Fixations.

A growing number of molecular evolutionary studies are estimating the proportion of adaptive amino acid substitutions (α) from comparisons of ratios of polymorphic and fixed DNA mutations. Here, we examine how violations of two of the model assumptions, neutral evolution of synonymous mutations and stationary base composition, affect α estimation. We simulated the evolution of coding sequences assuming weak selection on synonymous codon usage bias and neutral protein evolution, α = 0. We show that weak selection on synonymous mutations can give polymorphism/divergence ratios that yield α-hat (estimated α) considerably larger than its true value. Nonstationary evolution (changes in population size, selection, or mutation) can exacerbate such biases or, in some scenarios, give biases in the opposite direction, α-hat < α. These results demonstrate that two factors that appear to be prevalent among taxa, weak selection on synonymous mutations and non-steady-state nucleotide composition, should be considered when estimating α. Estimates of the proportion of adaptive amino acid fixations from large-scale analyses of Drosophila melanogaster polymorphism and divergence data are positively correlated with codon usage bias. Such patterns are consistent with α-hat inflation from weak selection on synonymous mutations and/or mutational changes within the examined gene trees.

An Individual-Based Diploid Model Predicts Limited Conditions Under Which Stochastic Gene Expression Becomes Advantageous.

Recent studies suggest the existence of a stochasticity in gene expression (SGE) in many organisms, and its non-negligible effect on their phenotype and fitness. To date, however, how SGE affects the key parameters of population genetics are not well understood. SGE can increase the phenotypic variation and act as a load for individuals, if they are at the adaptive optimum in a stable environment. On the other hand, part of the phenotypic variation caused by SGE might become advantageous if individuals at the adaptive optimum become genetically less-adaptive, for example due to an environmental change. Furthermore, SGE of unimportant genes might have little or no fitness consequences. Thus, SGE can be advantageous, disadvantageous, or selectively neutral depending on its context. In addition, there might be a genetic basis that regulates magnitude of SGE, which is often referred to as "modifier genes," but little is known about the conditions under which such an SGE-modifier gene evolves. In the present study, we conducted individual-based computer simulations to examine these conditions in a diploid model. In the simulations, we considered a single locus that determines organismal fitness for simplicity, and that SGE on the locus creates fitness variation in a stochastic manner. We also considered another locus that modifies the magnitude of SGE. Our results suggested that SGE was always deleterious in stable environments and increased the fixation probability of deleterious mutations in this model. Even under frequently changing environmental conditions, only very strong natural selection made SGE adaptive. These results suggest that the evolution of SGE-modifier genes requires strict balance among the strength of natural selection, magnitude of SGE, and frequency of environmental changes. However, the degree of dominance affected the condition under which SGE becomes advantageous, indicating a better opportunity for the evolution of SGE in different genetic models.

Evaluation of Ancestral Sequence Reconstruction Methods to Infer Nonstationary Patterns of Nucleotide Substitution.

Inference of gene sequences in ancestral species has been widely used to test hypotheses concerning the process of molecular sequence evolution. However, the approach may produce spurious results, mainly because using the single best reconstruction while ignoring the suboptimal ones creates systematic biases. Here we implement methods to correct for such biases and use computer simulation to evaluate their performance when the substitution process is nonstationary. The methods we evaluated include parsimony and likelihood using the single best reconstruction (SBR), averaging over reconstructions weighted by the posterior probabilities (AWP), and a new method called expected Markov counting (EMC) that produces maximum-likelihood estimates of substitution counts for any branch under a nonstationary Markov model. We simulated base composition evolution on a phylogeny for six species, with different selective pressures on G+C content among lineages, and compared the counts of nucleotide substitutions recorded during simulation with the inference by different methods. We found that large systematic biases resulted from (i) the use of parsimony or likelihood with SBR, (ii) the use of a stationary model when the substitution process is nonstationary, and (iii) the use of the Hasegawa-Kishino-Yano (HKY) model, which is too simple to adequately describe the substitution process. The nonstationary general time reversible (GTR) model, used with AWP or EMC, accurately recovered the substitution counts, even in cases of complex parameter fluctuations. We discuss model complexity and the compromise between bias and variance and suggest that the new methods may be useful for studying complex patterns of nucleotide substitution in large genomic data sets.

Population genetics of non-genetic traits: evolutionary roles of stochasticity in gene expression.

The role of stochasticity in evolutionary genetics has long been debated. To date, however, the potential roles of non-genetic traits in evolutionary processes have been largely neglected. In molecular biology, growing evidence suggests that stochasticity in gene expression (SGE) is common and that SGE has major impacts on phenotypes and fitness. Here, we provide a general overview of the potential effects of SGE on population genetic parameters, arguing that SGE can indeed have a profound effect on evolutionary processes. Our analyses suggest that SGE potentially alters the fate of mutations by influencing effective population size and fixation probability. In addition, a genetic control of SGE magnitude could evolve under certain conditions, if the fitness of the less-fit individual increases due to SGE and environmental fluctuation. Although empirical evidence for our arguments is yet to come, methodological developments for precisely measuring SGE in living organisms will further advance our understanding of SGE-driven evolution.

Difference in flowering time can initiate speciation of nocturnally flowering species.

Isolation mechanisms that prevent gene flow between populations prezygotically play important roles in achieving speciation. In flowering plants, the nighttime flowering system provides a mechanism for isolation from diurnally flowering species. Although this system has long been of interest in evolutionary biology, the evolutionary process leading to this system has yet to be elucidated because of the lack of good model species. However, the genetic mechanisms underlying the differences in flowering times and the traits that attract pollinators between a pair of diurnally and nocturnally flowering species have recently been identified in a few cases. This identification enables us to build a realistic model for theoretically studying the evolution of a nocturnally flowering species. In this study, based on previous experimental data, we assumed a model in which two loci control the flowering time and one locus determines a trait that attracts pollinators. Using this model, we evaluated the possibility of the evolution of a nocturnally flowering species from a diurnally flowering ancestor through simulations. We found that a newly emerging nighttime flowering flower exhibited a sufficiently high fitness, and the evolution of a nocturnally flowering species from a diurnally flowering species could be achieved when hybrid viability was intermediate to low, even in a completely sympatric situation. Our results suggest that the difference in flowering time can act as a magic trait that induces both natural selection and assortative mating and would play an important role in speciation between diurnally and nocturnally flowering species pairs.

Difference in flowering time as an isolating barrier.

Although many theoretical studies have reported strong effects of different flowering times on reproductive isolation, such studies have all focused on the different flowering time within a season, and the subsequently developed models are difficult to apply to the cases of diurnal- and nocturnal-flowering species pairs. The different flowering times within a day differ from those within a season because of the simultaneous opening and closing of the flowers for each species and the carry-over of the pollen from early to later times. In this study, we consider pollinator-mediated, diurnal- and nocturnal-flowering plants and build a new model to study the effects of the different flowering times within a day on reproductive isolation. We assume two loci, each with two alleles, which determine the opening and closing times of flowers, respectively. We numerically calculate the changes in the frequencies of the gametes in a model incorporating the reductions in hybrid viability, flowering costs, recombination rate and degree of dominance at each locus. We found that the early-opening flowers had a much higher fitness than the late-opening flowers and that the maintenance of the two species was difficult even if their flowering times were not overlapping. Therefore, some other mechanisms, such as pollinator preference, may be required to explain the coexistence of closely related diurnal and nocturnal flowers.

Enantioselective arylative cyclization of allenyl aldehydes with arylboronic acids under Pd(II)-diphosphine catalysis.

A Pd(OAc)2-SEGPHOS combination catalyzes the first enantioselective arylative cyclization of allenyl aldehydes with arylboronic acids to provide cis-fused five- and six-membered cyclic homoallylic alcohols. The excellent diastereo- and enantioselectivity and the fact that the reaction proceeds at room temperature in the absence of any additives make the process highly practical.