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Life History Shapes Gene Expression in Salmonids Magazine R281 and from a Scottish hatchery strain distances between populations Life history of Atlantic salmon (Salmo salar). from genetic diversity at ten shapes gene Migratory individuals were sampled nuclear microsatellite loci. at the same age as sedentary The relationships between brown expression ones, just prior to leaving their trout populations are found to differ natal stream. Dissimilarities in drastically when considering gene in salmonids global gene expression were expression or genetic diversity computed between all pairs of (Figure 1). A neighbour-joining tree Thomas Giger1, Laurent populations, taking into account clusters all salmonid populations Excoffier1, Philip J. R. Day2, the variability between individuals according to their known historical Alexis Champigneulle3, Michael within populations by means of divergence (Figure 1A), while a M. Hansen4, Richard Powell5 and an analysis of variance (ANOVA). tree of global gene expression Carlo R. Largiadèr1,6* A similar ANOVA framework was relationships clusters brown trout used to assess evolutionary populations strictly according to Within species, individuals differ by gene expression, which A Atlantic lineage may translate into remarkable phenotypic differences. Between S. salar 2 species, gene expression levels 3 change linearly over evolutionary 54.0 time due to stochastic processes 53.5 [1,2], while intraspecific evolution 99.8 1 of transcriptional variation seems 73.2 to be dominated by stabilizing 4 selection [3]. We show that global gene expression levels within S. trutta juvenile brown trout from natural populations depend primarily on 5 their future life history — migratory versus residential — rather than their genetic relatedness. This suggests that a few major Mediterranean lineage genes have large effects on the transcriptome, as about one third of the examined genes contribute to the significant global expression 6 differences between individuals B 6 with alternative life histories. S. salar Salmonid fish show exceptional levels of life-history variation and resident and migratory types 1 81.9 often co-occur. Before reaching sexual maturity and leaving their natal stream, migratory individuals 57.2 3 undergo dramatic morphological, physiological and behavioral adaptations to open and salty 0.1 77.1 waters. This life-history variation 54.1 appears to be influenced by 2 complex interactions between 5 genetic and environmental factors [4]. Current Biology 4 To assess the relationship between global gene expression Figure 1. Genetic and gene expression relationships of salmonid fish at the individual and genetic as well as life-history and population level. variation, we assayed gene (A) Neighbour-joining tree summarizing the genetic relationship among six brown trout expression diversity using cDNA (S. trutta) and one Atlantic salmon (S. salar) population analyzed at ten nuclear micro- microarrays. We analysed 900 satellite loci. (B) Neighbour-joining tree summarizing global gene expression similarities randomly selected genes in the among the same populations based on cDNA microarray expression data at 900 genes. livers of 90 juvenile individuals Red branches indicate sedentary populations and black branches migratory popula- tions. Distances between populations and branch lengths represent the proportion of from six natural brown trout (Salmo total variance in genetic (A) or gene expression diversity (B) due to differences between trutta) populations located in populations. We only report in (A) and (B) the bootstrap values > 50% (of 1,000 pseudo Eastern France and in Denmark, replicates over loci). The two trees are drawn at the same scale. Current Biology Vol 16 No 8 R282 their future life style (Figure 1B). By performing a backward cluster together. It shows that one Indeed, genetically related elimination, we estimate that these can almost unambiguously classify populations of sedentary and few trans-acting genes, which individuals into life-history types migrant fish show very distinct remain to be identified, affect based on the expression levels of gene expression profiles, while about one third of the genes. a subset of genes that have been evolutionarily or geographically Indeed, 268 out of the 900 genes identified at the population level. distant populations sharing the analyzed need to be eliminated to same life history have very similar make gene expression difference Acknowledgements levels of mRNA transcripts. For statistically non-significant This work was supported by the Swiss instance, population ‘6’ belongs between migrant and sedentary National Science Foundation grant to a ‘Mediterranean’ lineage that brown trout. On the other hand, 3100-067136.01 to C.R.L. diverged more than 0.5 Myrs ago the remarkable similarity in gene Supplemental data [5] from the ‘Atlantic’ lineage to expression between populations Supplemental data including which populations ‘1–5’ belong. with the same life history suggests Experimental Procedures are available However, the gene expression that this programme is highly at http://www.current-biology.com/cgi/ profile of this sedentary population selected for in brown trout. content/full/16/8/R281/DC1/ is very similar to that of other Importantly, despite the sedentary Atlantic populations differences between populations References 1. Khaitovich, P., Weiss, G., Lachmann, from Eastern France or Denmark differing in life history, we do M., Hellmann, I., Enard, W., Muetzel, B., (Figure 1B). By contrast, the not find that individuals are Wirkner, U., Ansorge, W., and Paabo, S. migrant population ‘2’ and the more similar in expression levels (2004). A neutral model of transcriptome evolution. Plos Biol. 2, 682–689. sedentary population ‘1’ have very within than between populations. 2. Rifkin, S.A., Kim, J., and White, K.P. different transcriptomes, despite Individual migratory and sedentary (2003). Evolution of gene expression in the Drosophila melanogaster subgroup. living in the same French river. fish neither strictly cluster Nat. Genet. 33, 138–144. Thus, even though some gene according to their life history nor 3. Denver, D.R., Morris, K., Streelman, J.T., expression differences between according to their populations Kim, S.K., Lynch, M., and Thomas, W.K. (2005). The transcriptional consequences pre-migratory fish and resident (Supplemental Data). Even Atlantic of mutation and natural selection in fish were expected, it appears salmon individuals, which are Caenorhabditis elegans. Nat. Genet. 37, 544–548. remarkable that these differences strongly differentiated from brown 4. Hendry, A.P., Bohlin, T., Jonsson, B., affect the whole transcriptome and trout at the population level (Figure and Berg, O.K. (2004). To sea or not to lead to such a clear distinction 1B), do not cluster as a distinct sea? Anadromy versus non-anadromy in salmonids. In Evolution Illuminated. between migrant and resident group. This is due to the fact that Salmon and their relatives, A.P. Hendry populations. only a minor fraction (7–29%) of and S.C. Stearns, eds. (NY: Oxford University Press), pp. 92–125. We quantified the respective the diversity in gene expression 5. Bernatchez, L., Guyomard, R., and importance of life history and levels is due to differences Bonhomme, F. (1992). DNA sequence genetic relatedness for predicting between populations of brown variation of the mitochondrial control region among geographically and transcriptome profiles by a trout (Supplemental Data). This morphologically remote European brown multivariate regression analysis. is a common phenomenon, as in trout Salmo trutta populations. Mol. Ecol. 1, 161–173. Within brown trout, life-history general most molecular diversity 6. Wittkopp, P.J., Haerum, B.K., and Clark, difference explains 45% of the occurs within rather than between A.G. (2004). Evolutionary changes in cis total variability in gene expression populations [8]. A similarly high and trans gene regulation. Nature 430, 85–88. levels (Mantel test, p = 0.022), diversity has been described in 7. Morley, M., Molony, C.M., Weber, T.M., whereas three times less of the freshwater populations of the Devlin, J.L., Ewens, K.G., Spielman, R.S., and Cheung, V.G. (2004). Genetic analysis variability (14.4%) is explained by genus Fundulus [9,10], implying of genome-wide variation in human gene genetic diversity (p = 0.028). When that relatively large samples expression. Nature 430, 743–747. we include S. salar in the analysis, are necessary to distinguish 8. Nichols, R. (2001). Gene trees and species trees are not the same. Trends Ecol. Evol. more than half (51.9%) of the total populations with different life 16, 358–364. variance in transcriptome profiles histories. 9. Oleksiak, M.F., Churchill, G.A., and Crawford, D.L. (2002). Variation in gene is explained by genetic diversity A re-sampling study of our expression within and among natural (Mantel test, p = 0.019), while less material shows (Supplemental populations. Nat. Genet. 32, 261–266. than 3% (p = 0.039) is explained Data) that the transcriptome of 10. Whitehead, A., and Crawford, D.L. (2005). Variation in tissue-specific gene by life-history differences. The two about 10 individuals needs to expression among natural populations. species show extremely distinct be examined per population to Genome Biol. 6, R13. gene expression profiles, which observe a stable segregation of 1 is in keeping with the hypothesis brown trout populations according CMPG, Zoological Institute, University of Bern, 3012 Bern, Switzerland. that interspecific expression
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