Q(St) meets the G matrix: the dimensionality of adaptive divergence in multiple correlated quantitative traits.

The Q(ST)-F(ST) comparison has become an increasingly common method for inferring adaptive quantitative trait divergence among populations. For cases in which there is divergence in multiple traits, most studies have applied the method by performing multiple univariate Q(ST)-F(ST) comparisons. However, because traits are often genetically correlated, such univariate analyses are likely to paint a simplified picture of adaptive divergence. Here we show how the multivariate analogue of Q(ST), F(STq), which accounts for genetic correlations among traits, can be used to supply a more detailed picture of multitrait divergence. We apply the method to naturally occurring genetic variation for a suite of sexually selected display traits in Drosophila serrata. The analyses suggest the operation of divergent multivariate selection that has influenced multiple independent axes of genetic variance in a sex-specific manner. Finally, we show how a comparison of the components of F(STq), the average within and among population genetic variance-covariance matrices, G(W) and G(B), can be used as an additional test of the null expectation of neutral divergence, and allows for an investigation of whether natural populations have diverged along major or minor axes of genetic variance.     

Genetic variability at neutral markers,quantitative trait land trait in a subdivided population under selection

Genetic variability in a subdivided population under stabilizing and diversifying selection was investigated at three levels: neutral markers, QTL coding for a trait, and the trait itself. A quantitative model with additive effects was used to link genotypes to phenotypes. No physical linkage was introduced. Using an analytical approach, we compared the diversity within deme (H(S)) and the differentiation (F(ST)) at the QTL with the genetic variance within deme (V(W)) and the differentiation (Q(ST)) for the trait. The difference between F(ST) and Q(ST) was shown to depend on the relative amounts of covariance between QTL within and between demes. Simulations were used to study the effect of selection intensity, variance of optima among demes, and migration rate for an allogamous and predominantly selfing species. Contrasting dynamics of the genetic variability at markers, QTL, and trait were observed as a function of the level of gene flow and diversifying selection. The highest discrepancy among the three levels occurred under highly diversifying selection and high gene flow. Furthermore, diversifying selection might cause substantial heterogeneity among QTL, only a few of them showing allelic differentiation, while the others behave as neutral markers.     

Population differentiation in G matrix structure due to natural selection in Rana temporaria

The additive genetic variance-covariance matrix (G) is a concept central to discussions about evolutionary change over time in a suite of traits. However, at the moment we do not know how fast G itself changes as a consequence of selection or how sensitive it is to environmental influences. We investigated possible evolutionary divergence and environmental influences on G using data from a factorial common-garden experiment where common frog (Rana temporaria) tadpoles from two divergent populations were exposed to three different environmental treatments. G-matrices were estimated using an animal model approach applied to data from a NCII breeding design. Matrix comparisons using both Flury and multivariate analysis of variance methods revealed significant differences in G matrices both between populations and between treatments within populations, the former being generally larger than the latter. Comparison of levels of population differentiation in trait means using Q(ST) indices with that observed in microsatellite markers (F(ST)) revealed that the former values generally exceeded the neutral expectation set by F(ST). Hence, the results suggest that intraspecific divergence in G matrix structure has occurred mainly due to natural selection.     

Molecular and quantitative genetic divergence among populations of house mice with known evolutionary histories

Evolutionary biologists have long been interested in the processes influencing population differentiation, but separating the effects of neutral and adaptive evolution has been an obstacle for studies of population subdivision. A recently developed method allows tests of whether disruptive (ie, spatially variable) or stabilizing (ie, spatially uniform) selection is influencing phenotypic differentiation among subpopulations. This method, referred to as the F(ST) vs Q(ST) comparison, separates the total additive genetic variance into within- and among-population components and evaluates this level of differentiation against a neutral hypothesis. Thus, levels of neutral molecular (F(ST)) and quantitative genetic (Q(ST)) divergence are compared to evaluate the effects of selection and genetic drift on phenotypic differentiation. Although the utility of such comparisons appears great, its accuracy has not yet been evaluated in populations with known evolutionary histories. In this study, F(ST) vs Q(ST) comparisons were evaluated using laboratory populations of house mice with known evolutionary histories. In this model system, the F(ST) vs Q(ST) comparisons between the selection groups should reveal quantitative trait differentiation consistent with disruptive selection, while the F(ST) vs Q(ST) comparisons among lines within the selection groups should suggest quantitative trait differentiation in agreement with drift. We find that F(ST) vs Q(ST) comparisons generally produce the correct evolutionary inference at each level in the population hierarchy. Additionally, we demonstrate that when strong selection is applied between populations Q(ST) increases relative to Q(ST) among populations diverging by drift. Finally, we show that the statistical properties of Q(ST), a variance component ratio, need further investigation.     

Divergent selection along climatic gradients in a rare central European endemic species,Saxifraga sponhemica

Background and Aims The effects of habitat fragmentation on quantitative genetic variation in plant populations are still poorly known. Saxifraga sponhemica is a rare endemic of Central Europe with a disjunct distribution, and a stable and specialized habitat of treeless screes and cliffs. This study therefore used S. sponhemica as a model species to compare quantitative and molecular variation in order to explore (1) the relative importance of drift and selection in shaping the distribution of quantitative genetic variation along climatic gradients; (2) the relationship between plant fitness, quantitative genetic variation, molecular genetic variation and population size; and (3) the relationship between the differentiation of a trait among populations and its evolvability.Methods Genetic variation within and among 22 populations from the whole distribution area of S. sponhemica was studied using RAPD (random amplified polymorphic DNA) markers, and climatic variables were obtained for each site. Seeds were collected from each population and germinated, and seedlings were transplanted into a common garden for determination of variation in plant traits.Key Results In contrast to previous results from rare plant species, strong evidence was found for divergent selection. Most population trait means of S. sponhemica were significantly related to climate gradients, indicating adaptation. Quantitative genetic differentiation increased with geographical distance, even when neutral molecular divergence was controlled for, and Q_ST exceeded F_ST for some traits. The evolvability of traits was negatively correlated with the degree of differentiation among populations (Q_ST), i.e. traits under strong selection showed little genetic variation within populations. The evolutionary potential of a population was not related to its size, the performance of the population or its neutral genetic diversity. However, performance in the common garden was lower for plants from populations with reduced molecular genetic variation, suggesting inbreeding depression due to genetic erosion.Conclusions The findings suggest that studies of molecular and quantitative genetic variation may provide complementary insights important for the conservation of rare species. The strong differentiation of quantitative traits among populations shows that selection can be an important force for structuring variation in evolutionarily important traits even for rare endemic species restricted to very specific habitats.     

Population genomics of parallel phenotypic evolution in stickleback across stream-lake ecological transitions

Understanding the genetics of adaptation is a central focus in evolutionary biology. Here, we use a population genomics approach to examine striking parallel morphological divergences of parapatric stream-lake ecotypes of threespine stickleback fish in three watersheds on the Haida Gwaii archipelago, western Canada. Genome-wide variation at greater than 1000 single nucleotide polymorphism loci indicate separate origin of giant lake and small-bodied stream fish within each watershed (mean F(ST) between watersheds = 0.244 and within = 0.114). Genome scans within watersheds identified a total of 21 genomic regions that are highly differentiated between ecotypes and are probably subject to directional selection. Most outliers were watershed-specific, but genomic regions undergoing parallel genetic changes in multiple watersheds were also identified. Interestingly, several of the stream-lake outlier regions match those previously identified in marine-freshwater and benthic-limnetic genome scans, indicating reuse of the same genetic loci in different adaptive scenarios. We also identified multiple new outlier loci, which may contribute to unique aspects of differentiation in stream-lake environments. Overall, our data emphasize the important role of ecological boundaries in driving both local and broadly occurring parallel genetic changes during adaptation.     

The genetic differentiation at quantitative trait loci under local adaptation

Most adaptive traits are controlled by large number of genes that may all together be the targets of selection. Adaptation may thus involve multiple but not necessarily substantial allele frequency changes. This has important consequences for the detection of selected loci and implies that a quantitative genetics framework may be more appropriate than the classical 'selective sweep' paradigm. Preferred methods to detect loci involved in local adaptation are based on the detection of 'outlier' values of the allelic differentiation F(ST) . A quantitative genetics framework is adopted here to review theoretical expectations for how allelic differentiation at quantitative trait loci (F(STQ) ) relates to (i), neutral genetic differentiation (F(ST) ) and (ii), phenotypic differentiation (Q(ST) ). We identify cases where results of outlier-based methods are likely to be poor and where differentiation at selected loci conveys little information regarding local adaptation. A first case is when neutral differentiation is high, so that local adaptation does not necessitate increased differentiation. A second case is when local adaptation is reached via an increased covariance of allelic effects rather than via allele frequency changes, which is more likely under high gene flow when the number of loci is high and selection is recent. The comparison of theoretical predictions with observed data from the literature suggests that polygenic local adaptation involving only faint allele frequency changes are very likely in some species such as forest trees and for climate-related traits. Recent methodological improvements that may alleviate the weakness of F(ST) -based detection methods are presented.     

Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. and Q. petraea (Matt.) Liebl.

Interspecific differentiation values (G(ST)) between two closely related oak species (Quercus petraea and Q. robur) were compiled across different studies with the aim to explore the distribution of differentiation at the genome level. The study was based on a total set of 389 markers (isozymes, AFLPs, SCARs, microsatellites, and SNPs) for which allelic frequencies were estimated in pairs of populations sampled throughout the sympatric distribution of the two species. The overall distribution of G(ST) values followed an L-shaped curve with most markers exhibiting low species differentiation (G(ST) < 0.01) and only a few loci reaching >10% levels. Twelve percent of the loci exhibited significant G(ST) deviations to neutral expectations, suggesting that selection contributed to species divergence. Coding regions expressed higher differentiation than noncoding regions. Among the 389 markers, 158 could be mapped on the 12 linkage groups of the existing Q. robur genetic map. Outlier loci with large G(ST) values were distributed over 9 linkage groups. One cluster of three outlier loci was found within 0.51 cM; but significant autocorrelation of G(ST) was observed at distances <2 cM. The size and distribution of genomic regions involved in species divergence are discussed in reference to hitchhiking effects and disruptive selection.     

Comparing Bayesian estimates of genetic differentiation of molecular markers and quantitative traits: an application to Pinus sylvestris

Comparison of the level of differentiation at neutral molecular markers (estimated as F(ST) or G(ST)) with the level of differentiation at quantitative traits (estimated as Q(ST)) has become a standard tool for inferring that there is differential selection between populations. We estimated Q(ST) of timing of bud set from a latitudinal cline of Pinus sylvestris with a Bayesian hierarchical variance component method utilizing the information on the pre-estimated population structure from neutral molecular markers. Unfortunately, the between-family variances differed substantially between populations that resulted in a bimodal posterior of Q(ST) that could not be compared in any sensible way with the unimodal posterior of the microsatellite F(ST). In order to avoid publishing studies with flawed Q(ST) estimates, we recommend that future studies should present heritability estimates for each trait and population. Moreover, to detect variance heterogeneity in frequentist methods (ANOVA and REML), it is of essential importance to check also that the residuals are normally distributed and do not follow any systematically deviating trends.     

Genome-wide polymorphisms show unexpected targets of natural selection

Natural selection can act on all the expressed genes of an individual, leaving signatures of genetic differentiation or diversity at many loci across the genome. New power to assay these genome-wide effects of selection comes from associating multi-locus patterns of polymorphism with gene expression and function. Here, we performed one of the first genome-wide surveys in a marine species, comparing purple sea urchins, Strongylocentrotus purpuratus, from two distant locations along the species' wide latitudinal range. We examined 9112 polymorphic loci from upstream non-coding and coding regions of genes for signatures of selection with respect to gene function and tissue- and ontogenetic gene expression. We found that genetic differentiation (F(ST)) varied significantly across functional gene classes. The strongest enrichment occurred in the upstream regions of E3 ligase genes, enzymes known to regulate protein abundance during development and environmental stress. We found enrichment for high heterozygosity in genes directly involved in immune response, particularly NALP genes, which mediate pro-inflammatory signals during bacterial infection. We also found higher heterozygosity in immune genes in the southern population, where disease incidence and pathogen diversity are greater. Similar to the major histocompatibility complex in mammals, balancing selection may enhance genetic diversity in the innate immune system genes of this invertebrate. Overall, our results show that how genome-wide polymorphism data coupled with growing databases on gene function and expression can combine to detect otherwise hidden signals of selection in natural populations.     

The effect of neutral nonadditive gene action on the quantitative index of population divergence

For neutral additive genes, the quantitative index of population divergence (Q(ST)) is equivalent to Wright's fixation index (F(ST)). Thus, divergent or convergent selection is usually invoked, respectively, as a cause of the observed increase (Q(ST) > F(ST)) or decrease (Q(ST) < F(ST)) of Q(ST) from its neutral expectation (Q(ST) = F(ST)). However, neutral nonadditive gene action can mimic the additive expectations under selection. We have studied theoretically the effect of consecutive population bottlenecks on the difference F(ST) - Q(ST) for two neutral biallelic epistatic loci, covering all types of marginal gene action. With simple dominance, Q(ST) < F(ST) for only low to moderate frequencies of the recessive alleles; otherwise, Q(ST) > F(ST). Additional epistasis extends the condition Q(ST) < F(ST) to a broader range of frequencies. Irrespective of the type of nonadditive action, Q(ST) < F(ST) generally implies an increase of both the within-line additive variance after bottlenecks over its ancestral value (V(A)) and the between-line variance over its additive expectation (2F(ST)V(A)). Thus, both the redistribution of the genetic variance after bottlenecks and the F(ST) - Q(ST) value are governed largely by the marginal properties of single loci. The results indicate that the use of the F(ST) - Q(ST) criterion to investigate the relative importance of drift and selection in population differentiation should be restricted to pure additive traits.     

Heritability and quantitative genetic divergence of serotiny,a fire-persistence plant trait

Background and Aims

Although it is well known that fire acts as a selective pressure shaping plant phenotypes, there are no quantitative estimates of the heritability of any trait related to plant persistence under recurrent fires, such as serotiny. In this study, the heritability of serotiny in Pinus halepensis is calculated, and an evaluation is made as to whether fire has left a selection signature on the level of serotiny among populations by comparing the genetic divergence of serotiny with the expected divergence of neutral molecular markers (Q_ST–F_ST comparison).

Methods

A common garden of P. halepensis was used, located in inland Spain and composed of 145 open-pollinated families from 29 provenances covering the entire natural range of P. halepensis in the Iberian Peninsula and Balearic Islands. Narrow-sense heritability (h²) and quantitative genetic differentiation among populations for serotiny (Q_ST) were estimated by means of an ‘animal model’ fitted by Bayesian inference. In order to determine whether genetic differentiation for serotiny is the result of differential natural selection, Q_ST estimates for serotiny were compared with F_ST estimates obtained from allozyme data. Finally, a test was made of whether levels of serotiny in the different provenances were related to different fire regimes, using summer rainfall as a proxy for fire regime in each provenance.

Key Results

Serotiny showed a significant narrow-sense heritability (h²) of 0·20 (credible interval 0·09–0·40). Quantitative genetic differentiation among provenances for serotiny (Q_ST = 0·44) was significantly higher than expected under a neutral process (F_ST = 0·12), suggesting adaptive differentiation. A significant negative relationship was found between the serotiny level of trees in the common garden and summer rainfall of their provenance sites.

Conclusions

Serotiny is a heritable trait in P. halepensis, and selection acts on it, giving rise to contrasting serotiny levels among populations depending on the fire regime, and supporting the role of fire in generating genetic divergence for adaptive traits.     

The influence of stochastic and selective forces in the population divergence of female colour polymorphism in damselflies of the genus Ischnura

Disentangling the relative importance and potential interactions of selection and genetic drift in driving phenotypic divergence of species is a classical research topic in population genetics and evolutionary biology. Here, we evaluate the role of stochastic and selective forces on population divergence of a colour polymorphism in seven damselfly species of the genus Ischnura, with a particular focus on I. elegans and I. graellsii. Colour-morph frequencies in Spanish I. elegans populations varied greatly, even at a local scale, whereas more similar frequencies were found among populations in eastern Europe. In contrast, I. graellsii and the other five Ischnura species showed little variation in colour-morph frequencies between populations. F(ST)-outlier analyses revealed that the colour locus deviated strongly from neutral expectations in Spanish populations of I. elegans, contrasting the pattern found in eastern European populations, and in I. graellsii, where no such discrepancy between morph divergence and neutral divergence could be detected. This suggests that divergent selection has been operating on the colour locus in Spanish populations of I. elegans, whereas processes such as genetic drift, possibly in combination with other forms of selection (such as negative frequency-dependent selection), appear to have been present in other regions, such as eastern Europe. Overall, the results indicate that both selective and stochastic processes operate on these colour polymorphisms, and suggest that the relative importance of factors varies between geographical regions.     

Migration-induced phenotypic divergence: the migration-selection balance of correlated traits

Genetically correlated traits are known to respond to indirect selection pressures caused by directional selection on other traits. It is however unclear how local adaptation in populations diverging along some phenotypic traits but not others is affected by the joint action of gene flow and genetic correlations among traits. This simulation study shows that although gene flow is a potent constraining mechanism of population adaptive divergence, it may induce phenotypic divergence in traits under homogeneous selection among habitats if they are genetically correlated with traits under divergent selection. This correlated phenotypic divergence is a nonmonotonous function of migration and increases with mutational correlation among traits. It also increases with the number of divergently selected traits provided their genetic autonomy relative to the uniformly selected trait is reduced by specific patterns of genetic covariances: populations with lower effective trait dimensionality are more likely to generate very large correlated divergence. The correlated divergence is likely to be picked up by Q(ST)-F(ST) analysis of population genetic differentiation and be erroneously ascribed to adaptive divergence under divergent selection. This study emphasizes the necessity to understand the interaction between selection and the genetic basis of adaptation in a multivariate rather than univariate context.     

Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis

Comparative studies of quantitative genetic and neutral marker differentiation have provided means for assessing the relative roles of natural selection and random genetic drift in explaining among-population divergence. This information can be useful for our fundamental understanding of population differentiation, as well as for identifying management units in conservation biology. Here, we provide comprehensive review and meta-analysis of the empirical studies that have compared quantitative genetic (Q(ST)) and neutral marker (F(ST)) differentiation among natural populations. Our analyses confirm the conclusion from previous reviews - based on ca. 100% more data - that the Q(ST) values are on average higher than F(ST) values [mean difference 0.12 (SD 0.27)] suggesting a predominant role for natural selection as a cause of differentiation in quantitative traits. However, although the influence of trait (life history, morphological and behavioural) and marker type (e.g. microsatellites and allozymes) on the variance of the difference between Q(ST) and F(ST) is small, there is much heterogeneity in the data attributable to variation between specific studies and traits. The latter is understandable as there is no reason to expect that natural selection would be acting in similar fashion on all populations and traits (except for fitness itself). We also found evidence to suggest that Q(ST) and F(ST) values across studies are positively correlated, but the significance of this finding remains unclear. We discuss these results in the context of utility of the Q(ST)-F(ST) comparisons as a tool for inferring natural selection, as well as associated methodological and interpretational problems involved with individual and meta-analytic studies.     

Adaptive differentiation of quantitative traits in the globally distributed weed, wild radish (Raphanus raphanistrum)

Weedy species with wide geographical distributions may face strong selection to adapt to new environments, which can lead to adaptive genetic differentiation among populations. However, genetic drift, particularly due to founder effects, will also commonly result in differentiation in colonizing species. To test whether selection has contributed to trait divergence, we compared differentiation at eight microsatellite loci (measured as F(ST)) to differentiation of quantitative floral and phenological traits (measured as Q(ST)) of wild radish (Raphanus raphanistrum) across populations from three continents. We sampled eight populations: seven naturalized populations and one from its native range. By comparing estimates of Q(ST) and F(ST), we found that petal size was the only floral trait that may have diverged more than expected due to drift alone, but inflorescence height, flowering time, and rosette formation have greatly diverged between the native and nonnative populations. Our results suggest the loss of a rosette and the evolution of early flowering time may have been the key adaptations enabling wild radish to become a major agricultural weed. Floral adaptation to different pollinators does not seem to have been as necessary for the success of wild radish in new environments.     

Adaptive divergence in moor frog (Rana arvalis) populations along an acidification gradient: inferences from Q(st) -F(st) correlations

Microevolutionary responses to spatial variation in the environment seem ubiquitous, but the relative role of selection and neutral processes in driving phenotypic diversification remain often unknown. The moor frog (Rana arvalis) shows strong phenotypic divergence along an acidification gradient in Sweden. We here used correlations among population pairwise estimates of quantitative trait (P(ST) or Q(ST) from common garden estimates of embryonic acid tolerance and larval life-history traits) and neutral genetic divergence (F(ST) from neutral microsatellite markers), as well as environmental differences (pond pH, predator density, and latitude), to test whether this phenotypic divergence is more likely due to divergent selection or neutral processes. We found that trait divergence was more strongly correlated with environmental differences than the neutral marker divergence, suggesting that divergent natural selection has driven phenotypic divergence along the acidification gradient. Moreover, pairwise P(ST) s of embryonic acid tolerance and Q(ST) s of metamorphic size were strongly correlated with breeding pond pH, whereas pairwise Q(ST) s of larval period and growth rate were more strongly correlated with geographic distance/latitude and predator density, respectively. We suggest that incorporating measurements of environmental variation into Q(ST) -F(ST) studies can improve our inferential power about the agents of natural selection in natural populations.     

Local adaptation in brown trout early life-history traits: implications for climate change adaptability

Knowledge of local adaptation and adaptive potential of natural populations is becoming increasingly relevant due to anthropogenic changes in the environment, such as climate change. The concern is that populations will be negatively affected by increasing temperatures without the capacity to adapt. Temperature-related adaptability in traits related to phenology and early life history are expected to be particularly important in salmonid fishes. We focused on the latter and investigated whether four populations of brown trout (Salmo trutta) are locally adapted in early life-history traits. These populations spawn in rivers that experience different temperature conditions during the time of incubation of eggs and embryos. They were reared in a common-garden experiment at three different temperatures. Quantitative genetic differentiation (QST) exceeded neutral molecular differentiation (FST) for two traits, indicating local adaptation. A temperature effect was observed for three traits. However, this effect varied among populations due to locally adapted reaction norms, corresponding to the temperature regimes experienced by the populations in their native environments. Additive genetic variance and heritable variation in phenotypic plasticity suggest that although increasing temperatures are likely to affect some populations negatively, they may have the potential to adapt to changing temperature regimes.     

Past climate changes explain the phylogeography of Vitellaria paradoxa over Africa

The evolution of the savanna biome has been deeply marked by repeated contraction/expansion phases due to climate perturbations during the Quaternary period. In this study, we investigated the impact of the last glacial maximum (LGM) on the present genetic pattern of Vitellaria paradoxa (shea tree), a major African savanna tree. A range-wide sampling of the species enabled us to sample 374 individuals from 71 populations distributed throughout sub-Sahelian Africa. Trees were genotyped using 3 chloroplasts and 12 nuclear microsatellites, and were sequenced for 2 polymorphic chloroplast intergenic spacers. Analyses of genetic diversity and structure were based on frequency-based and Bayesian methods. Potential distributions of V. paradoxa at present, during the LGM and the last interglacial period, were examined using DIVA-GIS ecological niche modelling (ENM). Haplotypic and allelic richness varied significantly across the range according to chloroplast and nuclear microsatellites, which pointed to higher diversity in West Africa. A high but contrasted level of differentiation was revealed among populations with a clear phylogeographic signal, with both nuclear (F(ST) = 0.21; R(ST) = 0.28; R(ST) > R(ST) (permuted)) and chloroplast simple sequence repeats (SSRs) (G(ST) = 0.81; N(ST) = 0.90; N(ST) > N(ST) (permuted)). We identified a strong geographically related structure separating western and eastern populations, and a substructure in the eastern part of the area consistent with subspecies distinction. Using ENM, we deduced that perturbations during the LGM fragmented the potential eastern distribution of shea tree, but not its distribution in West Africa. Our main results suggest that climate variations are the major factor explaining the genetic pattern of V. paradoxa.