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The parallel evolution of dwarfism in Arctic charr is accompanied by adaptive divergence in mTOR-pathway gene expression

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Abstract

Ecological factors have a major role shaping natural variation in body-size, although the underlying mechanisms are poorly understood. Icelandic Arctic charr (Salvelinus alpinus L.) populations represent an ideal model to understand body-size evolution, since adult-dwarfism has arisen independently on multiple occasions in response to parallel environmental pressures. The mechanistic target of rapamycin (mTOR)-pathway transmits signals from the environment to control cellular-growth and is a primary candidate to be under selection for the dwarf phenotype. To test this hypothesis, we modified ‘inputs’ to this pathway in 5 dwarf and 2 generalist populations (with ancestral life-history and body-size traits), using a standardised manipulation of food-intake in a common environment. The skeletal-muscle transcript levels of 21 mTOR-pathway genes were quantified in 274 individuals (ca. 6000 datapoints) and statistical modelling used to elucidate sources of variation. Constitutive expression differences between-populations were the main component of variation for around three-quarters of the studied genes, irrespective of nutritional-state and body-size phenotype. There was evidence for stabilizing-selection acting among-populations, conserving the nutritionally-dependent regulation of pathway genes controlling muscle-atrophy. There were 3 genes (mTOR, 4E-BP-1 and IGFBP4), where the expression-variation between dwarf and generalist populations exceeded the between-population variation. Divergence in expression of these candidate adaptive genes was most evident during a period of rapid growth following sustained-fasting and was directionally consistent with their functions regulating growth and protein-synthesis. We concluded that selection has operated efficiently to shape gene expression evolution in Icelandic charr populations and that the regulation of certain mTOR-pathway genes evolved adaptively in locations favouring dwarfism, resulting in reduced muscle protein-accretion under growth-favouring conditions.
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Original languageEnglish
Pages (from-to)3167-3184
Number of pages17
JournalMolecular Ecology
Volume20
Issue number15
DOIs
Publication statusPublished - 2011

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