López-Fanjul C, Fernández A, Toro MA. The effect of neutral nonadditive gene action on the quantitative index of population divergence. Genetics 164: 1627-1633

Departamento de Genética, Facultad de Ciencias Biológicas, Universidad Complutense, 28040 Madrid, Spain.
Genetics (Impact Factor: 5.96). 08/2003; 164(4):1627-33.
Source: PubMed


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.

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    • "Including dominance variance is appropriate for understanding evolutionary change in clonal or highly selfing species, but not for sexual ones, and including nonadditive variance in estimates can either increase or decrease Q ST (Whitlock 1999; Lopez-Fanjul et al. 2003). Sampling error for Q ST is also likely to be reduced for a given number of individuals by using full-sib families rather than estimating additive variation; this may be why the standard errors of our estimates of Q ST are larger than those of previous studies. "
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    ABSTRACT: 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.
    Full-text · Article · Nov 2008 · Genetics
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    • "However, here Q ST > F ST was observed, and thus, other biological phenomena or violations of assumptions likely are of greater relevance. However, this topic remains disputed (Lopez Fanjul and Toro, 2007; Lopez-Fanjul et al., 2003) and more studies on additivity and epistasis of gene expression in natural populations are needed. Third, contrasts between Q ST and G ST provide insights into the importance of selection as a cause for differentiation . "
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    ABSTRACT: Owing to the relevance to evolutionary theories of genotypic and phenotypic evolution, the correspondence of differentiation among natural populations in complex phenotypic traits and genetic markers has been studied extensively, and generally found to be poor. In contrast, the correspondence of differentiation among natural populations in gene expression, now often considered a genomic era proxy for the phenotype, and genetic markers, remains largely unexplored. Here, an analysis of expression and nucleotide sequence polymorphism of 106 genes in Drosophila melanogaster strains of the Cosmopolitan (M) and Zimbabwe, Africa (Z) mating races showed that differentiation of gene expression and of coding sequences, measured as QST and GST, respectively, were uncorrelated and, generally, QST > GST. However, an exploratory analysis showed that GST of the 5 prime sequences of genes was correlated with QST calculated from expression data, while GST of the coding sequences remained uncorrelated with QST. This scenario is consistent with the population differentiation at cis-regulatory regions that is decoupled from differentiation of the coding regions. However, despite evidence for selection on global levels of gene expression (deduced from QST > GST), 5 prime sequence polymorphisms generally were compatible with selective neutrality, suggesting differentiation in cis-regulated gene expression for these genes has been promoted by drift or selection too weak or too long ago to be detected, or higher organizational levels underlying the genetic architecture of expression are targets of selection. In all, this raises the question how selection on the expression changes (i.e. the phenotype) can be so obvious yet elusive at the level of the nucleotide sequence. Our contrasts between genetic differentiation of populations in expression and sequences revealed that even when genotype and phenotype can be connected the sources of variation that are the target of selection remain to be identified.
    Full-text · Article · Jun 2008 · Genes & Genetic Systems
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    • "Theoretical studies focussing on the assumptions and properties of Q ST have been rather slow to appear (Fig. 1), starting with Whitlock's (1999) simulations of effects of nonadditive genetic effects on the difference between F ST and Q ST . This work has been recently extended by several authors (Le Corre & Kremer, 2003; Lopez-Fanjul et al., 2003; Goudet & Buchi, 2006), the main practical conclusion being that nonadditive genetic effects are unlikely to bias Q ST estimates considerably. An important concern in comparative studies of quantitative trait and marker gene differentiation is also the distinction between Q ST for a quantitative trait and individual quantitative trait loci (Latta, 1998; McKay & Latta, 2002). "
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    ABSTRACT: 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.
    Full-text · Article · Feb 2008 · Journal of Evolutionary Biology
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