Digest: Male and female beetle genitalia are under stabilizing selection*

The effect of selection on female genitalia is poorly studied, but such selection could affect mating success. House et al. (2020) studied the form and strength of selection acting on male and female Tribolium castaneum. They found that the sex organs of both male and female T. castaneum are under multivariate stabilizing selection and that both male and female genitalia interact to influence mating success.     

Mistranslation Reduces Mutation Load in Evolving Proteins through Negative Epistasis with DNA Mutations

Translational errors during protein synthesis cause phenotypic mutations that are several orders of magnitude more frequent than DNA mutations. Such phenotypic mutations may affect adaptive evolution through their interactions with DNA mutations. To study how mistranslation may affect the adaptive evolution of evolving proteins, we evolved populations of green fluorescent protein (GFP) in either high-mistranslation or low-mistranslation Escherichia coli hosts. In both hosts, we first evolved GFP under purifying selection for the ancestral phenotype green fluorescence, and then under directional selection toward the new phenotype yellow fluorescence. High-mistranslation populations evolved modestly higher yellow fluorescence during each generation of evolution than low-mistranslation populations. We demonstrate by high-throughput sequencing that elevated mistranslation reduced the accumulation of deleterious DNA mutations under both purifying and directional selection. It did so by amplifying the fitness effects of deleterious DNA mutations through negative epistasis with phenotypic mutations. In contrast, mistranslation did not affect the incidence of beneficial mutations. Our findings show that phenotypic mutations interact epistatically with DNA mutations. By reducing a population’s mutation load, mistranslation can affect an important determinant of evolvability.     

Perturbation expansions of multilocus fixation probabilities for frequency-dependent selection with applications to the Hill-Robertson effect and to the joint evolution of helping and punishment

Natural populations are of finite size and organisms carry multilocus genotypes. There are, nevertheless, few results on multilocus models when both random genetic drift and natural selection affect the evolutionary dynamics. In this paper we describe a formalism to calculate systematic perturbation expansions of moments of allelic states around neutrality in populations of constant size. This allows us to evaluate multilocus fixation probabilities (long-term limits of the moments) under arbitrary strength of selection and gene action. We show that such fixation probabilities can be expressed in terms of selection coefficients weighted by mean first passages times of ancestral gene lineages within a single ancestor. These passage times extend the coalescence times that weight selection coefficients in one-locus perturbation formulas for fixation probabilities. We then apply these results to investigate the Hill-Robertson effect and the coevolution of helping and punishment. Finally, we discuss limitations and strengths of the perturbation approach. In particular, it provides accurate approximations for fixation probabilities for weak selection regimes only (Ns?1), but it provides generally good prediction for the direction of selection under frequency-dependent selection.     

Effects of intrinsic environmental predictability on intra-individual and intra-population variability of plant reproductive traits and eco-evolutionary consequences

Background and AimsIt is widely accepted that changes in the environment affect mean trait expression, but little is known about how the environment shapes intra-individual and intra-population variance. Theory suggests that intra-individual variance might be plastic and under natural selection, rather than reflecting developmental noise, but evidence for this hypothesis is scarce. Here, we experimentally tested whether differences in intrinsic environmental predictability affect intra-individual and intra-population variability of different reproductive traits, and whether intra-individual variability is under selection.MethodsUnder field conditions, we subjected Onobrychis viciifolia to more and less predictable precipitation over 4 generations and 4 years. We analysed effects on the coefficient of intra-individual variation (CV_i-i) and the coefficient of intra-population variation (CV_i-p), assessed whether the coefficients of intra-individual variation (CsV_i-i) are under natural selection and tested for transgenerational responses (ancestor environmental effects on offspring).Key ResultsLess predictable precipitation led to higher CsV_i-i and CsV_i-p, consistent with plastic responses. The CsV_i-i of all studied traits were under consistent stabilizing selection, and precipitation predictability affected the strength of selection and the location of the optimal CV_i-i of a single trait. All CsV_i-i differed from the optimal CV_i-i and the maternal and offspring CsV_i-i were positively correlated, showing that there was scope for change. Nevertheless, no consistent transgenerational effects were found in any of the three descendant generations, which contrasts with recent studies that detected rapid transgenerational responses in the trait means of different plant species. This suggests that changes in intra-individual variability take longer to evolve than changes in trait means, which may explain why high intra-individual variability is maintained, despite the stabilizing selection.ConclusionsThe results indicate that plastic changes of intra-individual variability are an important determinant of whether plants will be able to cope with changes in environmental predictability induced by the currently observed climatic change.     

Does operational sex ratio influence relative strength of purging selection in males versus females?

According to theory, sexual selection in males may efficiently purge mutation load of sexual populations, reducing or fully compensating ‘the cost of males’. For this to occur, mutations not only need to be deleterious to both sexes, they also must affect males more than females. A frequently overlooked problem is that relative strength of selection on males versus females may vary between environments, with social conditions being particularly likely to affect selection in males and females differently. Here, we induced mutations in red flour beetles (Tribolium castaneum) and tested their effect in both sexes under three different operational sex ratios (1:2, 1:1 and 2:1). Induced mutations decreased fitness of both males and females, but their effect was not stronger in males. Surprisingly, operational sex ratio did not affect selection against deleterious mutations nor its relative strength in the sexes. Thus, our results show no support for the role of sexual selection in the evolutionary maintenance of sex.     

A Combination of Structural and Cis-Regulatory Factors Drives Biochemical Differences in Drosophila melanogaster Malic Enzyme

The evolutionary significance of molecular variation is still contentious, with much current interest focusing on the relative contribution of structural changes in proteins versus regulatory variation in gene expression. We present a population genetic and biochemical study of molecular variation at the malic enzyme locus (Men) in Drosophila melanogaster. Two amino acid polymorphisms appear to affect substrate-binding kinetics, while only one appears to affect thermal stability. Interestingly, we find that enzyme activity differences previously assigned to one of the polymorphisms may, instead, be a function of linked regulatory differences. These results suggest that both regulatory and structural changes contribute to differences in protein function. Our examination of the Men coding sequences reveals no evidence for selection acting on the polymorphisms, but earlier work on this enzyme indicates that the biochemical variation observed has physiological repercussions and therefore could potentially be under natural selection.     

Correlated response in plasticity to selection for early flowering in Arabidopsis thaliana

Phenotypic plasticity is an important strategy for coping with changing environments. However, environmental change usually results in strong directional selection, and little is known empirically about how this affects plasticity. If genes affecting a trait value also affect its plasticity, selection on the trait should influence plasticity. Synthetic outbred populations of Arabidopsis thaliana were selected for earlier flowering under simulated spring- and winter-annual conditions to investigate the correlated response of flowering time plasticity and its effect on family-by-environment variance (Vg×e) within each selected line. We found that selection affected plasticity in an environmentally dependent manner: under simulated spring-annual conditions, selection increased the magnitude of plastic response but decreased Vg×e; selection under simulated winter-annual conditions reduced the magnitude of plastic response but did not alter Vg×e significantly. As selection may constrain future response to environmental change, the environment for crop breeding and ex situ conservation programmes should be carefully chosen. Models of species persistence under environmental change should also consider the interaction between selection and plasticity.     

Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution

The selective pressure at the protein level is usually measured by the nonsynonymous/synonymous rate ratio (omega = dN/dS), with omega < 1, omega = 1, and omega > 1 indicating purifying (or negative) selection, neutral evolution, and diversifying (or positive) selection, respectively. The omega ratio is commonly calculated as an average over sites. As every functional protein has some amino acid sites under selective constraints, averaging rates across sites leads to low power to detect positive selection. Recently developed models of codon substitution allow the omega ratio to vary among sites and appear to be powerful in detecting positive selection in empirical data analysis. In this study, we used computer simulation to investigate the accuracy and power of the likelihood ratio test (LRT) in detecting positive selection at amino acid sites. The test compares two nested models: one that allows for sites under positive selection (with omega > 1), and another that does not, with the chi2 distribution used for significance testing. We found that use of the chi(2) distribution makes the test conservative, especially when the data contain very short and highly similar sequences. Nevertheless, the LRT is powerful. Although the power can be low with only 5 or 6 sequences in the data, it was nearly 100% in data sets of 17 sequences. Sequence length, sequence divergence, and the strength of positive selection also were found to affect the power of the LRT. The exact distribution assumed for the omega ratio over sites was found not to affect the effectiveness of the LRT.     

The surprising negative correlation of gene length and optimal codon use - disentangling translational selection from GC-biased gene conversion in yeast

Background  

Surprisingly, in several multi-cellular eukaryotes optimal codon use correlates negatively with gene length. This contrasts with the expectation under selection for translational accuracy. While suggested explanations focus on variation in strength and efficiency of translational selection, it has rarely been noticed that the negative correlation is reported only in organisms whose optimal codons are biased towards codons that end with G or C (-GC). This raises the question whether forces that affect base composition - such as GC-biased gene conversion - contribute to the negative correlation between optimal codon use and gene length.     

Evaluating outlier loci and their effect on the identification of pedigree errors

Homozygosity outlier loci, which show patterns of variation that are extremely divergent from the rest of the genome, can be evaluated by comparison of the homozygosity under Hardy-Weinberg proportions (the sum of the squares of allele frequencies) with the expected homozygosity under neutrality. Such outlier loci are potentially under selection (balancing selection or directional selection) when genome-wide effects (such as bottleneck and rapid population growth) are excluded. Outlier loci show skewed allele frequencies with respect to neutrality and may therefore affect the identification of pedigree errors. However, choosing neutral markers (excluding outlier loci) for the identification of pedigree errors has been neglected thus far. Our results showed that 4.1%, 5.5%, and 1.5% of the microsatellite markers, Illumina single-nucleotide polymorphisms (SNPs), and Affymetrix SNPs, respectively, on the autosomes appear to be under balancing selection (p or=40%) appear to be under balancing selection. Pedigree structure errors in 15 of 143 pedigrees were detected using microsatellite markers from the autosomes and/or selected SNPs from chromosomes 1 to 18 of the Illumina and/or selected SNPs from chromosomes 1 to 16 of the Affymetrix. Outlier loci did not make a major difference to the identification of pedigree errors. The Collaborative Study on the Genetics of Alcoholism data has pedigree errors and some of them may be due to sample mix up.     

Substrate selection by Carabus clatratus (Coleoptera, Carabidae) and its consequences for offspring development

In insects, habitat selection should be most distinctly effected by females during oviposition, and this choice should directly affect the performance of the less mobile offspring stages. To date, this behaviour has been poorly investigated in carabid beetles. This study examines sexual differences in microhabitat selection as well as egg-laying behaviour and its consequences for offspring in the stenoecious beetle Carabus clatratus. Laboratory experiments with adults and different offspring stages were undertaken to test the impact of soil moisture and substrate type on microhabitat selection and immature fitness. Only females changed their substrate selection behaviour after copulation, revealing a distinct preference for wet peat for oviposition. Egg mortality was less than 7% under both wet and dry soil conditions. In contrast to other investigations, egg mortality in C. clatratus was therefore of minor importance. Larval mortality was also low, but mortality of third-instar larvae and the pupal stage increased strongly under dry conditions. Furthermore, beetles that developed under dry conditions showed a significantly higher proportion of exoskeleton deformations, and immature adults were smaller when reared under low moisture conditions. The importance of a strong oviposition site selection for wet peat to ensure sufficient moisture conditions for offspring in the stenoecious species C. clatratus is discussed. Received: 14 December 1998 / Accepted: 15 July 1999     

Learning Natural Selection from the Site Frequency Spectrum

Genetic adaptation to external stimuli occurs through the combined action of mutation and selection. A central problem in genetics is to identify loci responsive to specific selective constraints. Many tests have been proposed to identify the genomic signatures of natural selection by quantifying the skew in the site frequency spectrum (SFS) under selection relative to neutrality. We build upon recent work that connects many of these tests under a common framework, by describing how selective sweeps affect the scaled SFS. We show that the specific skew depends on many attributes of the sweep, including the selection coefficient and the time under selection. Using supervised learning on extensive simulated data, we characterize the features of the scaled SFS that best separate different types of selective sweeps from neutrality. We develop a test, SFselect, that consistently outperforms many existing tests over a wide range of selective sweeps. We apply SFselect to polymorphism data from a laboratory evolution experiment of Drosophila melanogaster adapted to hypoxia and identify loci that strengthen the role of the Notch pathway in hypoxia tolerance, but were missed by previous approaches. We further apply our test to human data and identify regions that are in agreement with earlier studies, as well as many novel regions.     

Effects of Differential Selection in the Sexes on Cytonuclear Polymorphism and Disequilibria

We develop a series of models that examine the effects of differential selection between the sexes on cytonuclear polymorphism and disequilibria. A detailed analysis is provided for populations under constant fertility or viability selection censused at life stages without frequency differences in the sexes. We show analytically that cytonuclear disequilibria can be generated de novo if the cytoplasmic and nuclear loci each affect female fitness and there is a nonmultiplicative fitness interaction between them. While computer simulations demonstrate that the majority of disequilibria produced by random selection are transient and small in magnitude, measurable permanent disequilibria can result from selective differences both within and between the two sexes. We derive analytic conditions for a protected cytonuclear polymorphism and use numerical simulations to quantitate the likelihood of obtaining permanent nuclear, cytoplasmic, and cytonuclear variation under various patterns of selection. The numerical analysis identifies special selection regimes more likely to generate disequilibria and maintain cytonuclear polymorphism and reveals a direct correlation to the strength of selection. As a byproduct, our models also provide the first decomposition of the different parental contributions to cytonuclear dynamics and the analytic conditions under which selection can cause cytoplasmic frequency changes or a cytonuclear hitchhiking effect.     

Differences in the selection response of serially repeated color pattern characters: Standing variation,development, and evolution

Background  

There is spectacular morphological diversity in nature but lineages typically display a limited range of phenotypes. Because developmental processes generate the phenotypic variation that fuels natural selection, they are a likely source of evolutionary biases, facilitating some changes and limiting others. Although shifts in developmental regulation are associated with morphological differences between taxa, it is unclear how underlying mechanisms affect the rate and direction of evolutionary change within populations under selection.     

Effect of migration and environmental heterogeneity on the maintenance of quantitative genetic variation: a simulation study

The paradox of high genetic variation observed in traits under stabilizing selection is a long‐standing problem in evolutionary theory, as mutation rates appear too low to explain observed levels of standing genetic variation under classic models of mutation–selection balance. Spatially or temporally heterogeneous environments can maintain more standing genetic variation within populations than homogeneous environments, but it is unclear whether such conditions can resolve the above discrepancy between theory and observation. Here, we use individual‐based simulations to explore the effect of various types of environmental heterogeneity on the maintenance of genetic variation (V_A) for a quantitative trait under stabilizing selection. We find that V_A is maximized at intermediate migration rates in spatially heterogeneous environments and that the observed patterns are robust to changes in population size. Spatial environmental heterogeneity increased variation by as much as 10‐fold over mutation–selection balance alone, whereas pure temporal environmental heterogeneity increased variance by only 45% at max. Our results show that some combinations of spatial heterogeneity and migration can maintain considerably more variation than mutation–selection balance, potentially reconciling the discrepancy between theoretical predictions and empirical observations. However, given the narrow regions of parameter space required for this effect, this is unlikely to provide a general explanation for the maintenance of variation. Nonetheless, our results suggest that habitat fragmentation may affect the maintenance of V_A and thereby reduce the adaptive capacity of populations.     

GroEL/S Overexpression Helps to 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 the effect of 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 Escherichia 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 previous work, we observe that GroE does not just buffer but also helps purge deleterious (fluorescence reducing) 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, helping to enhance their fluorescence in some cells, and reducing it in others. Our observations show that chaperones can affect adaptive evolution in more than one way.     

Searching for evidence of positive selection in the human genome using patterns of microsatellite variability

Both natural selection and nonequilibrium population-level processes can lead to a skew in the frequency distribution of polymorphisms. Population-level processes are expected to affect all loci in a roughly equal fashion, whereas selection will affect only some regions of the genome. We conducted a sliding-window analysis of the frequency distribution of microsatellite polymorphisms across the human genome to identify regions that may be under positive selection. The analysis was based on a published data set of 5,257 mapped microsatellites in individuals of European ancestry. Observed and expected numbers of alleles were compared under a stepwise mutation model (SMM) using analytical formulae. Observed and expected heterozygosities were compared under a SMM using coalescent simulations. The two sets of analyses gave similar results. Approximately one-fourth of all loci showed a significant deficit of heterozygosity, consistent with a recent population expansion. Forty-three windows were identified with extreme skews in the frequency distribution of polymorphisms (in the direction of a deficit of heterozygosity, given the number of alleles). If these extreme windows are tracking selection at linked sites, theory predicts that they should be more common in regions of the genome with less recombination. We tested this prediction by comparing recombination rates in these extreme windows and in other regions of the genome and found that extreme windows had a significantly lower recombination rate than the genomic average. The proportion of extreme windows was significantly higher on the X chromosome than on the autosomes. Moreover, all the windows with extreme skews on the X chromosome were found in two clusters near the centromere; both these clusters exhibit markedly reduced recombination rates. These analyses point to regions of the genome that may recently have been subject to positive selection. These results also suggest that the effects of positive selection may be more pronounced on the X chromosome than on the autosomes in humans.     

Natural selection on quantitative immune defence traits: a comparison between theory and data

Parasites present a threat for free‐living species and affect several ecological and evolutionary processes. Immune defence is the main physiological barrier against infections, and understanding its evolution is central for predicting disease dynamics. I review theoretical predictions and empirical data on natural selection on quantitative immune defence traits in the wild. Evolutionary theory predicts immune traits to be under stabilizing selection owing to trade‐offs between immune function and life‐history traits. Empirical data, however, support mainly positive directional selection, but also show variation in the form of selection among study systems, immune traits and fitness components. I argue that the differences between theory and empirical data may at least partly arise from methodological difficulties in testing stabilizing selection as well as measuring fitness. I also argue that the commonness of positive directional selection and the variation in selection may be caused by several biological factors. First, selection on immune function may show spatial and temporal variation as epidemics are often local/seasonal. Second, factors affecting the range of phenotypic variation in immune traits could alter potential for selection. Third, different parasites may impose different selective pressures depending on their characteristics. Fourth, condition dependence of immune defence can obscure trade‐offs related to it, thus possibly modifying observed selection gradients. Fifth, nonimmunological defences could affect the form of selection by reducing the benefits of strong immune function. To comprehensively understand the evolution of immune defence, the role of above factors should be considered in future studies.     

Sexual selection affects lifespan and aging in the seed beetle

Sexual selection in general, and sexual conflict in particular, should affect the evolution of lifespan and aging. Using experimental evolution, we tested whether removal of sexual selection leads to the evolution of accelerated or decelerated senescence. We subjected replicated populations of the seed beetle Callosobruchus maculatus to either of two selection regimes for 35 generations. These regimes either allowed (polygamy) or removed the potential (monogamy) for sexual selection to operate. To test for the evolution of intrinsic differences between the two selection regimes, we assayed longevity in replicate cohorts of virgin females and males. Virgin females from populations evolving under sexual selection had reduced lifespan as predicted by the sexual conflict theory of aging. However, this reduction was due to increased baseline mortality rather than an increase in age-specific mortality rates with age. We discuss these findings in light of other data from this model system and suggest that system-specific idiosyncrasies may often modulate the general effects of male–female coevolution on the evolution of aging.     

Resource Elasticity of Offspring Survival and the Optimal Evolution of Sex Ratios

The fitness of any organisms includes the survival and reproductive rate of adults and the survival of their offspring. Environmental selection pressures might not affect these two aspects of an organism equally. Assuming that an organism first allocates its limited resources to maintain its survival under environmental selection pressure, our model, based on the evolutionarily stable strategy theory, surprisingly shows that the sex ratio is greatly affected by the environmental pressure intensity and by the reproductive resource elasticity of offspring survival. Moreover, the concept of the resource elasticity of offspring survival intrinsically integrates the ecological concepts of K selection and r selection. The model shows that in a species with reproductive strategy K, increased environmental selection pressure will reduce resource allocation to the male function. By contrast, in a species with reproductive strategy r, harsher environmental selection pressure will increase allocation to the male function. The elasticity of offspring survival might vary not only across species, but also across many other factors affecting the same species (e.g., age structure, spatial heterogeneity), which explains sex ratio differences across species or age structures and spatial heterogeneity in the same species.