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Evaluating the Role of Natural Selection in the Evolution of Gene Regulation

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Evaluating the Role of Natural Selection in the Evolution of Gene Regulation Heredity (2008) 100, 191–199 & 2008 Nature Publishing Group All rights reserved 0018-067X/08 $30.00 www.nature.com/hdy SHORT REVIEW Evaluating the role of natural selection in the evolution of gene regulation JC Fay1 and PJ Wittkopp2 1Department of Genetics, Washington University School of Medicine, St Louis, MO, USA and 2Department of Ecology and Evolutionary Biology and Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI, USA Surveys of gene expression reveal extensive variability both also discuss properties of regulatory systems relevant to within and between a wide range of species. Compelling neutral models of gene expression. Despite some potential cases have been made for adaptive changes in gene caveats, published studies provide considerable evidence for regulation, but the proportion of expression divergence adaptive changes in gene expression. Future challenges for attributable to natural selection remains unclear. Distinguish- studies of regulatory evolution will be to quantify the ing adaptive changes driven by positive selection from frequency of adaptive changes, identify the genetic basis of neutral divergence resulting from mutation and genetic drift expression divergence and associate changes in gene is critical for understanding the evolution of gene expression. expression with specific organismal phenotypes. Here, we review the various methods that have been used to Heredity (2008) 100, 191–199; doi:10.1038/sj.hdy.6801000; test for signs of selection in genomic expression data. We published online 23 May 2007 Keywords: gene expression; evolution; microarray; neutral models; quantitative traits Introduction Stern, 2000); pigmentation in Drosphila mediated by bric- a-brac (Kopp et al., 2000), yellow (Wittkopp et al., 2002; When and where a gene is expressed, and how much of Gompel et al., 2005) and ebony (Wittkopp et al., 2003); the gene product is made, can be as important as the butterfly eyespots mediated by Distal-less (Beldade et al., biochemical function of the encoded RNA or protein 2002) and beak size among Galapagos finches mediated (Raff, 1996; Carroll et al., 2001; Davidson, 2001). In 1969, by BMP4 (Abzhanov et al., 2004). Britten and Davidson (1969) proposed a theory of gene Experimental evolution in microorganisms also pro- regulation for eukaryotic cells that included a central role vides compelling evidence that regulatory evolution for regulatory divergence in phenotypic evolution. contributes to phenotypic divergence. Parallel mutations Subsequent comparisons of molecular and morphologi- observed in replicate populations are likely to have been cal phenotypes indicated that protein divergence was fixed by positive selection (Orr, 2005). Parallel expression insufficient to account for the extensive phenotypic divergence has been reported for experimental popula- differences observed between species, and prompted tions of both Saccharomyces cerevisiae and Escherichia coli the proposal that many adaptations may have arisen (Ferea et al., 1999; Cooper et al., 2003; Riehle et al., 2003; from changes in gene regulation rather than from Fong et al., 2005). In two populations of E. coli evolving changes in gene function (Wilson et al., 1974; King and independently for 20 000 generations in glucose-limited Wilson, 1975). Over the last 30 years, molecular studies of media, 59 genes acquired similar expression changes in development and evolution, combined with studies of both populations (Cooper et al., 2003). Similarly, three experimental evolution, have provided strong support strains of S. cerevisiae grown in glucose-limited media for for this hypothesis (for example Wray et al., 2003 and 250 generations showed over 50 genes whose expression Gompel et al., 2005). Nonetheless, the relative importance changed in parallel in all three lines, suggesting that of regulatory changes versus changes in protein function these changes were adaptive (Ferea et al., 1999). remains subject to debate. Finally, studies elucidating the molecular basis of Genetic and transgenic experiments have shown that adaptations in domesticated crops also indicate a changes in gene regulation often underlie morphological significant role for regulatory evolution in phenotypic differences between species. Examples include changes evolution. For example, in maize, changes in expression in pelvic structures in threespine sticklebacks mediated of the teosinte branched 1 (tb1) gene have evolved since it by Pitx1 (Shapiro et al., 2004); trichome patterning in shared a common ancestor with teosinte (Doebley et al., Drosophila mediated by Ubx (Stern, 1998); larval hairs in 1997). Mutations affecting tb1 expression alter branching, Drosophila mediated by ovo/shaven-baby (Sucena and consistent with morphological differences between do- mesticated corn and its wild relative (Hubbard et al., Correspondence: Dr JC Fay, Department of Genetics, Washington 2002). Evidence of directional selection has been found in University School of Medicine, 4444 Forest Park Ave., St Louis, MO the upstream cis-regulatory regions of noncoding region 63108, USA. E-mail: [email protected] of tb1, suggesting adaptive changes in expression of Received 10 July 2006; revised 27 December 2006; accepted 19 April this gene (Clark et al., 2006). Regulatory changes have 2007; published online 23 May 2007 also been implicated in the evolution of naked grains Evaluating neutral models for regulatory evolution JC Fay and PJ Wittkopp 192 in maize (Wang et al., 2005) and in the loss of seed The role of selection and genetic drift in the shattering in rice (Konishi et al., 2006). These compelling examples illustrate that regulatory evolution of gene expression changes can underlie adaptations. But, do all changes in Evolution has many causes. Darwin (1876) poignantly gene expression contribute to phenotypic evolution and argued that evolution is caused by natural selection. how often is regulatory divergence adaptive? One way Since then, considerable efforts have been made to to obtain insight into this question is by using DNA examine an alternative explanation: genetic drift, or the microarrays to examine genomic patterns of gene stochastic changes that occur as a consequence of finite expression within and between species and using population size (Kimura, 1983). Three primary methods statistical methods to distinguish neutral and nonneutral have been used to distinguish between these possibili- patterns of gene expression divergence. Indeed, methods ties. First, the comparative method examines the evolu- originally developed to detect signs of selection on tion of a character in relation to the evolution of other morphological characters and DNA sequences have now characters or environmental variables in a phylogenetic been applied to genomic expression data. Here, we context (Martins, 2000). Second, neutral models of review these tests, their applications and assumptions of evolutionary change can be used to test for selection on the underlying models. We discuss features of regulatory quantitative characters (Turelli et al., 1988). Finally, the evolution that may complicate the interpretation of these empirical rate of expression divergence across lineages tests, including correlated changes in expression among can be used to distinguish between selection and drift genes, the relationship between genotype and gene (Rifkin et al., 2005). Each of these methods has recently expression and the dependency of mutational effects on been applied to gene expression data with the hope of current expression levels. We conclude by anticipating addressing the long-standing idea that changes in gene future directions for studies investigating the evolution regulation play a substantial role in adaptive evolution. of gene expression, including the identification of specific phenotypes affected by genes showing evidence of adaptive regulatory divergence. Comparative methods The comparative method is based on the correlated Genomic variation in gene expression evolution of a phenotype with some other trait or Genome-wide measurements have revealed high rates of environmental variable. Two classic examples are the genetic variation in gene expression (typically 410% of association between white coat coloration and animals genes) in humans (Enard et al., 2002; Rockman and Wray, living in snowy environments, and between large testis 2002; Bray et al., 2003; Lo et al., 2003; Whitney et al., 2003; size and polygynous primate species (Harvey and Pagel, Morley et al., 2004; Pastinen et al., 2004; Radich et al., 1991). Although the repeated evolution of a trait is 2004), mice (Cowles et al., 2002; Schadt et al., 2003; indicative of adaptation, correlated patterns of change Shockley and Churchill, 2006), fish (Oleksiak et al., 2002, can also arise for other reasons. First, shared ancestry 2005), flies (Jin et al., 2001; Wayne and McIntyre, 2002; causes correlations among characters in the absence of Meiklejohn et al., 2003; Rifkin et al., 2003; Nuzhdin et al., selection (Felsenstein, 1985). If the evolutionary history 2004; Ranz et al., 2004), yeast (Cavalieri et al., 2000; Brem of the species under study is known, it can be taken into et al., 2002; Townsend et al., 2003; Yvert et al., 2003; Fay account by using independent contrasts that examine et al., 2004), plants (Kirst et al., 2005; Vuylsteke et al., 2005; subsets of the tree (Felsenstein, 1985), by partitioning Lai et al., 2006) and bacteria (Le et al., 2005). Patterns of phenotypic changes
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