Genetic linkage and natural selection

The prevalence of recombination in eukaryotes poses one of the most puzzling questions in biology. The most compelling general explanation is that recombination facilitates selection by breaking down the negative associations generated by random drift (i.e. Hill–Robertson interference, HRI). I classify the effects of HRI owing to: deleterious mutation, balancing selection and selective sweeps on: neutral diversity, rates of adaptation and the mutation load. These effects are mediated primarily by the density of deleterious mutations and of selective sweeps. Sequence polymorphism and divergence suggest that these rates may be high enough to cause significant interference even in genomic regions of high recombination. However, neither seems able to generate enough variance in fitness to select strongly for high rates of recombination. It is plausible that spatial and temporal fluctuations in selection generate much more fitness variance, and hence selection for recombination, than can be explained by uniformly deleterious mutations or species-wide selective sweeps.     

The strength of phenotypic selection in natural populations

How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |beta| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |beta| for selection on morphological and on life-history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |beta| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |gamma| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of gamma values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.     

Genetic and phenotypic correlations in a natural population of song sparrows

We estimated heritabilities, and genetic and phenotypic correlations between beak and body traits in the song sparrow ( Melospiza melodia ). We compared these estimates to values for the same traits in the Galápagos finches, Geospiza (Boag, 1983; Grant, 1983). Morphological variance is low in the song sparrow, and our results show that genetic and phenotypic correlations are considerably lower than correlations in the morphologically more variable Geospiza. Comparison using a larger sample of Galapagos populations confirms the existence of an association between variance and correlation for phenotypic values. We suggest two possible explanations for this association. First, most traits studied are functionally related, and the joint evolution of variance and correlation may have resulted from stabilizing selection about a line of optimal allometry between traits. Alternatively, introgression between populations and species could have caused correlation and variance to evolve jointly. Both selection and introgression were probably influential in producing the observed pattern, but it is not possible to estimate their relative importance with current data. Genetic and phenotypic correlations were correlated in the song sparrow, but heritabilities of traits varied greatly. As a result, the genetic variance-covariance matrix for traits is not simply a constant multiple of the phenotypic matrix. Evolutionary response to natural selection cannot, therefore, be predicted from the measurement of phenotypic characteristics alone.     

Genetic biodiversity impacts of silvicultural practices and phenotypic selection in white spruce

Forest-management practices relying on natural and/or artificial regeneration and domestication can significantly affect genetic diversity. The aim of the present study was to determine and compare the genetic diversity of the pristine old-growth, naturally and artificially regenerated and phenotypically selected white spruce, and to determine the genetic-diversity impacts of silvicultural practices. Genetic diversity was determined and compared for 51 random amplified polymorphic DNA (RAPD) loci for the adjacent natural old-growth, naturally regenerated and planted white spruce stands at each of four sites, one oldest plantation and open-pollinated progeny of 30 phenotypic tree-improvement selections of white spruce from Saskatchewan. Each of the 420 white spruce individuals sampled was genetically unique. The old-growth stands had the highest, and the phenotypic selections the lowest, genetic diversity. The genetic diversity of the natural regeneration was comparable to that of the old-growth, whereas the genetic diversity of the plantations was comparable to that of the selections. On average, the genetic diversity of the old-growth and natural regeneration was significantly higher than that of the plantations and selections. The mean percent of loci polymorphic, the number of alleles per locus, the effective number of alleles per locus, heterozygosity, and Shannon’s index was 88.7, 83.8, 72.2 and 66.7; 1.89, 1.84, 1.72 and 1.67; 1.69, 1.62, 1.53 and 1.46; 0.381, 0.349, 0.297 and 0.259; and 0.548, 0.506, 0.431 and 0.381 for the old-growth stands; natural regeneration; plantations; and open-pollinated progeny of selections; respectively. Reduced genetic diversity in the plantations and selections suggest that their genetic base is relatively narrow, and should therefore be broadened in order to maintain genetic diversity, and sustainably manage and conserve white spruce genetic resources. Received: 12 March 1999 / Accepted: 17 March 1999     

Community assembly,natural selection and maximum entropy models

The papers in this Forum discussion debate various aspects of my maximum entropy model of community assembly. The questions raised centre around (1) the possible mechanisms generating the patterns predicted by my maxent model of community assembly, and (2) the appropriate statistical methods for testing the patterns. Here I briefly explain the proposed mechanistic basis of the model: natural selection occurring between individuals of different species. If trait differences are linked to differential demographic probabilities (i.e. fitness differences) then natural selection will constrain the average trait values found in the community and such average (‘community‐aggregated’) traits will then possess information that is translated into the maximum entropy probabilities. If community assembly is strictly neutral then the maxent model will have no predictive ability. This also justifies the null model, and the permutation test, proposed by Roxburgh and Mokany.     

Speciation by natural and sexual selection: models and experiments

A large number of mathematical models have been developed that show how natural and sexual selection can cause prezygotic isolation to evolve. This article attempts to unify this literature by identifying five major elements that determine the outcome of speciation caused by selection: a form of disruptive selection, a form of isolating mechanism (assortment or a mating preference), a way to transmit the force of disruptive selection to the isolating mechanism (direct selection or indirect selection), a genetic basis for increased isolation (a one- or two-allele mechanism), and an initial condition (high or low initial divergence). We show that the geographical context of speciation (allopatry vs. sympatry) can be viewed as a form of assortative mating. These five elements appear to operate largely independently of each other and can be used to make generalizations about when speciation is most likely to happen. This provides a framework for interpreting results from laboratory experiments, which are found to agree generally with theoretical predictions about conditions that are favorable to the evolution of prezygotic isolation.     

Imbalance of predator and prey armament: geographic clines in phenotypic interface and natural selection

The escalation of defensive/offensive arms is ubiquitous in prey-predator evolutionary interactions. However, there may be a geographically varying imbalance in the armaments of participating species that affects the outcome of local interactions. In a system involving the Japanese camellia (Camellia japonica) and its obligate seed predator, the camellia weevil (Curculio camelliae), we investigated the geographic variation in physical defensive/offensive traits and that in natural selection on the plant's defense among 17 populations over a 700-km-wide area in Japan. The sizes of the plant defensive apparatus (pericarp thickness) and the weevil offensive apparatus (rostrum length) clearly correlated with each other across populations. Nevertheless, the balance in armaments between the two species was geographically structured. In the populations for which the balance was relatively advantageous for the plant's defense, natural selection on the trait was stronger because in the other populations, most plant individuals were too vulnerable to resist the attacks of the weevil, and their seeds were infested independent of pericarp thickness. We also found that the imbalance between the defensive/offensive armaments and the intensity of natural selection showed clear latitudinal clines. Overall, our results suggest that the imbalance of armament between sympatric prey and predator could determine the strength of local selection and that climatic conditions could affect the local and overall trajectory of coevolutionary arms races.     

Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow

Divergent natural selection, adaptive divergence and gene flow may interact in a number of ways. Recent studies have focused on the balance between selection and gene flow in natural populations, and empirical work has shown that gene flow can constrain adaptive divergence, and that divergent selection can constrain gene flow. A caveat is that phenotypic diversification may be under the direct influence of environmental factors (i.e. it may be due to phenotypic plasticity), in addition to partial genetic influence. In this case, phenotypic divergence may occur between populations despite high gene flow that imposes a constraint on genetic divergence. Plasticity may dampen the effects of natural selection by allowing individuals to rapidly adapt phenotypically to new conditions, thus slowing adaptive genetic divergence. On the other hand, plasticity may promote future adaptive divergence by allowing populations to persist in novel environments. Plasticity may promote gene flow between selective regimes by allowing dispersers to adapt to alternate conditions, or high gene flow may result in the selection for increased plasticity. Here I expand frameworks for understanding relationships among selection, adaptation and gene flow to include the effects of phenotypic plasticity in natural populations, and highlight its importance in evolutionary diversification.     

Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions

There are now thousands of estimates of phenotypic selection in natural populations, resulting in multiple synthetic reviews of these data. Here we consider several major lessons and limitations emerging from these syntheses, and how they may guide future studies of selection in the wild. First, we review past analyses of the patterns of directional selection. We present new meta-analyses that confirm differences in the direction and magnitude of selection for different types of traits and fitness components. Second, we describe patterns of temporal and spatial variation in directional selection, and their implications for cumulative selection and directional evolution. Meta-analyses suggest that sampling error contributes importantly to observed temporal variation in selection, and indicate that evidence for frequent temporal changes in the direction of selection in natural populations is limited. Third, we review the apparent lack of evidence for widespread stabilizing selection, and discuss biological and methodological explanations for this pattern. Finally, we describe how sampling error, statistical biases, choice of traits, fitness measures and selection metrics, environmental covariance and other factors may limit the inferences we can draw from analyses of selection coefficients. Current standardized selection metrics based on simple parametric statistical models may be inadequate for understanding patterns of non-linear selection and complex fitness surfaces. We highlight three promising areas for expanding our understanding of selection in the wild: (1) field studies of stabilizing selection, selection on physiological and behavioral traits, and the ecological causes of selection; (2) new statistical models and methods that connect phenotypic variation to population demography and selection; and (3) availability of the underlying individual-level data sets from past and future selection studies, which will allow comprehensive modeling of selection and fitness variation within and across systems, rather than meta-analyses of standardized selection metrics.     

Testing for environmentally induced bias in phenotypic estimates of natural selection: theory and practice

Measuring natural selection has been a fundamental goal of evolutionary biology for more than a century, and techniques developed in the last 20 yr have provided relatively simple means for biologists to do so. Many of these techniques, however, share a common limitation: when applied to phenotypic data, environmentally induced covariances between traits and fitness can lead to biased estimates of selection and misleading predictions about evolutionary change. Utilizing estimates of breeding values instead of phenotypic data with these methods can eliminate environmentally induced bias, although this approach is more difficult to implement. Despite this potential limitation to phenotypic methods and the availability of a potential solution, little empirical evidence exists on the extent of environmentally induced bias in phenotypic estimates of selection. In this article, we present a method for detecting bias in phenotypic estimates of selection and demonstrate its use with three independent data sets. Nearly 25% of the phenotypic selection gradients estimated from our data are biased by environmental covariances. We find that bias caused by environmental covariances appears mainly to affect quantitative estimates of the strength of selection based on phenotypic data and that the magnitude of these biases is large. As our estimates of selection are based on data from spatially replicated field experiments, we suggest that our findings on the prevalence of bias caused by environmental covariances are likely to be conservative.     

Optimal restricted phenotypic selection

Phenotypic selection is modified by introducing upper limits on the portion (P ₁) of individuals selected from a family as well as on the portion (P ₂) of family number that are allowed to contribute. At a preset selection proportion, P and P ₁, the maximum genetic gain is obtained by finding an optimum restriction on family number (P ₂ ^* ). A numerical procedure for solving the problem of optimization is developed for infinite populations. In small populations, maximum gain and P ₂ ^* can be found by simply comparing all possible P₂. Numerical examples are demonstrated for infinite breeding populations, assuming a normally-distributed family mean and within-family deviation. Selection and its simulation were applied to the fieldtest results of two tree species. Optimum restriction on family number is very close to P/P ₁, especially when heritability is low. In the real world of tree breeding, P ₂ ^* is given, or approximated, by P/P ₁+1/ _tm where m is the initial family number. The improvement of gain and the conservation of inbreeding effective population size are easy with high heritability and could be simultaneously obtained by using intense selection with a relatively low P ₁.     

Genetic and phenotypic variation of foot-and-mouth disease virus during serial passages in a natural host

Foot-and-mouth disease virus (FMDV), like other RNA viruses, exhibits high mutation rates during replication that have been suggested to be of adaptive value. However, even though genetic variation in RNA viruses and, more specifically, FMDV has been extensively examined during virus replication in a wide variety of in vitro cell cultures, very little is known regarding the generation and effects of genetic variability of virus replication in the natural host under experimental conditions and no genetic data are available regarding the effects of serial passage in natural hosts. Here, we present the results of 20 serial contact transmissions of the highly pathogenic, pig-adapted O Taiwan 97 (O Tw97) isolate of FMDV in swine. We examined the virus genomic consensus sequences for a total of 37 full-length viral genomes recovered from 20 in vivo passages. The characteristics and distributions of changes in the sequences during the series of pig infections were analyzed in comparison to the O Tw97 genomes recovered from serially infected BHK-21 cell cultures. Unexpectedly, a significant reduction of virulence upon pig passages was observed, and finally, interruption of the viral transmission chain occurred after the14th pig passage (T14). Virus was, however, isolated from the tonsils and nasal swabs of the asymptomatic T15 pigs at 26 days postcontact, consistent with a natural establishment of the carrier state previously described only for ruminants. Surprisingly, the region encoding the capsid protein VP1 (1D) did not show amino acid changes during in vivo passages. These data demonstrate that contact transmission of FMDV O Tw97 in pigs mimics the fitness loss induced by the bottleneck effect, which was previously observed by others during plaque-to-plaque FMDV passage in vitro, suggesting that unknown mechanisms of virulence recovery might be necessary during the evolution and perpetuation of FMDV in nature.     

Genetic constraints on the evolution of mate recognition under natural selection

Field populations of Drosophila serrata display reproductive character displacement in cuticular hydrocarbons (CHCs) when sympatric with Drosophila birchii. We have previously shown that the naturally occurring pattern of reproductive character displacement can be experimentally replicated by exposing field allopatric populations of D. serrata to experimental sympatry with D. birchii. Here, we tested whether the repeated evolution of reproductive character displacement in natural and experimental populations was a consequence of genetic constraints on the evolution of CHCs. The genetic variance-covariance (G) matrices for CHCs were determined for populations of D. serrata that had evolved in either the presence or absence of D. birchii under field and experimental conditions. Natural selection on mate recognition under both field and experimental sympatric conditions increased the genetic variance in CHCs consistent with a response to selection based on rare alleles. A close association between G eigenstructure and the eigenstructure of the phenotypic divergence (D) matrix in natural and experimental populations suggested that G matrix eigenstructure may have determined the direction in which reproductive character displacement evolved during the reinforcement of mate recognition.     

Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum.

We have studied the genetic polymorphism at 10 Plasmodium falciparum loci that are considered potential targets for specific antimalarial vaccines. The polymorphism is unevenly distributed among the loci; loci encoding proteins expressed on the surface of the sporozoite or the merozoite (AMA-1, CSP, LSA-1, MSP-1, MSP-2, and MSP-3) are more polymorphic than those expressed during the sexual stages or inside the parasite (EBA-175, Pfs25, PF48/45, and RAP-1). Comparison of synonymous and nonsynonymous substitutions indicates that natural selection may account for the polymorphism observed at seven of the 10 loci studied. This inference depends on the assumption that synonymous substitutions are neutral, which we test by analyzing codon bias and G+C content in a set of 92 gene loci. We find evidence for an overall trend towards increasing A+T richness, but no evidence for mutation bias. Although the neutrality of synonymous substitutions is not definitely established, this trend towards an A+T rich genome cannot explain the accumulation of substitutions at least in the case of four genes (AMA-1, CSP, LSA-1, and PF48/45) because the Gleft and right arrow C transversions are more frequent than expected. Moreover, the Tajima test manifests positive natural selection for the MSP-1 and, less strongly, MSP-3 polymorphisms; the McDonald-Kreitman test manifests natural selection at LSA-1 and PF48/45. We conclude that there is definite evidence for positive natural selection in the genes encoding AMA-1, CSP, LSA-1, MSP-1, and Pfs48/45. For four other loci, EBA-175, MSP-2, MSP-3, and RAP-1, the evidence is limited. No evidence for natural selection is found for Pfs25.     

How selection affects phenotypic fluctuation

The large degree of phenotypic fluctuation among isogenic cells highlighted by recent studies on stochastic gene expression confers fitness on some individuals through a ‘bet‐hedging’ strategy, when faced with different selective environments. Under a single selective environment, the fluctuation may be suppressed through evolution, as it prevents maintenance of individuals around the fittest state and/or function. However, as fluctuation can increase phenotypic diversity, similar to mutation, it may contribute to the survival of individuals even under a single selective environment. To discuss whether the fluctuation increases over the course of evolution, cycles of mutation and selection for higher GFP fluorescence were carried out in Escherichia coli. Mutant genotypes possessing broad GFP fluorescence distributions with low average values emerged under strong selection pressure. These ‘broad mutants’ appeared independently on the phylogenetic tree and increased fluctuations in GFP fluorescence were attributable to the variance in mRNA abundance. In addition to the average phenotypic change by genetic mutation, the observed increase in phenotypic fluctuation acts as an evolutionary strategy to produce an extreme phenotype under severe selective environments.     

Phenology and phenotypic natural selection on the flowering time of a deceit-pollinated tropical orchid, Myrmecophila christinae

BACKGROUND AND AIMS: Flowering phenology is described and the effect of flowering time on pollination success is evaluated in the deceit-pollinated tropical orchid, Myrmecophila christinae. It was expected that, due to this species' deceit pollination strategy and low observed pollinator visit rate, there would be a higher probability of natural selection events favouring individuals flowering away from the population flowering peak. METHODS: The study covers two consecutive years and four populations of M. christinae located along the north coast of the Yucatán Peninsula. For phenological and pollination success data, a total of 110 individuals were monitored weekly in 1998, and 83 individuals in 1999, during all the flowering and fruiting season. KEY RESULTS: The results showed significant differences in the probability of donating and receiving pollen throughout the flowering season. The probability of receiving or donating pollen increased the further an individual flowering was from the flowering peak. Regression analysis showed directional and disruptive phenotypic natural selection gradients, suggesting the presence of selection events unfavourable to flowering during flowering peak, for both male success (pollen removal) and female success (fruit production). However, the intensity and significance of the natural selection events varied between populations from year to year. The variation between seasons and populations was apparently due to variations in the density of reproductive individuals in each population and each season. CONCLUSIONS: As in other deceit-pollinated orchids, natural selection in M. christinae favours individuals flowering early or late in relation to population peak flowering. However, results also suggested a fluctuating regime of selective events act on flowering time of M. christinae.