Genome-Wide Effects of Long-Term Divergent Selection

Johansson, Anna M.; Pettersson, Mats E.; Siegel, P. B.; Carlborg, Örjan

doi:10.1371/journal.pgen.1001188

Cited by 137 publications

(195 citation statements)

References 29 publications

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“…Evolution would seem likely to start with this variation, as long as it is relevant to selection and not unduly constrained by correlations with other traits. Fitting this expectation, the immediate and dramatic evolutionary responses often seen in artificial selection experiments suggest that plenty of relevant variation is present (Moose et al, 2004;Hill and Kirkpatrick, 2010;Johansson et al, 2010;Lango Allen et al, 2010). Although the results of these studies might seem of questionable relevance because the selection was not 'natural,' similarly rapid responses have been observed in natural populations experiencing environmental change (Hendry and Kinnison, 1999;Reznick and Ghalambor, 2001;Hendry et al, 2008).…”

Section: Ecosystem Functionmentioning

confidence: 83%

“…A scarcity of genes of large effect also appears to be the case for many other human traits, including susceptibility to diseases (Manolio et al, 2009). In addition, artificial selection studies clearly show that evolutionary changes are often driven by many genes (Hill and Kirkpatrick, 2010), with classic examples including oil and protein content in maize (Zea mays) (Moose et al, 2004) and body weight in chickens (Gallus gallus domesticus) (Johansson et al, 2010).…”

Section: Ecosystem Functionmentioning

confidence: 99%

“…Application of these approaches to the aforementioned selection experiments on maize (Moose et al, 2004) and chickens (Johansson et al, 2010) strongly implicates standing genetic variation. Application to natural populations often yields a similar conclusion, with examples including lactose tolerance in humans (Myles et al, 2005), warfarin resistance in brown rats (Rattus norvegicus) (Pelz et al, 2005), malathion resistance in blowflies (Lucilia spp.)…”

Section: Ecosystem Functionmentioning

confidence: 99%

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Key questions in the genetics and genomics of eco-evolutionary dynamics

Hendry

2013

Heredity

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Increasing acceptance that evolution can be 'rapid' (or 'contemporary') has generated growing interest in the consequences for ecology. The genetics and genomics of these 'eco-evolutionary dynamics' will be-to a large extent-the genetics and genomics of organismal phenotypes. In the hope of stimulating research in this area, I review empirical data from natural populations and draw the following conclusions. (1) Considerable additive genetic variance is present for most traits in most populations. (2) Trait correlations do not consistently oppose selection. (3) Adaptive differences between populations often involve dominance and epistasis. (4) Most adaptation is the result of genes of small-to-modest effect, although (5) some genes certainly have larger effects than the others. (6) Adaptation by independent lineages to similar environments is mostly driven by different alleles/genes. (7) Adaptation to new environments is mostly driven by standing genetic variation, although new mutations can be important in some instances. (8) Adaptation is driven by both structural and regulatory genetic variation, with recent studies emphasizing the latter. (9) The ecological effects of organisms, considered as extended phenotypes, are often heritable. Overall, the study of eco-evolutionary dynamics will benefit from perspectives and approaches that emphasize standing genetic variation in many genes of small-to-modest effect acting across multiple traits and that analyze overall adaptation or 'fitness'. In addition, increasing attention should be paid to dominance, epistasis and regulatory variation.

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Section: Ecosystem Functionmentioning

confidence: 83%

Section: Ecosystem Functionmentioning

confidence: 99%

Section: Ecosystem Functionmentioning

confidence: 99%

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Key questions in the genetics and genomics of eco-evolutionary dynamics

Hendry

2013

Heredity

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“…Subjecting populations to artificial selection provides an accelerated evolutionary process that may result in extreme phenotypes with accompanying changes across the genome [2][3][4]. Using such experiments, the contribution by mutational variance to the evolution of quantitative traits can be quantified by, for example, measuring the release of genetic variance during selection experiments from an inbred founder population [5].…”

Section: Introductionmentioning

confidence: 99%

Standing genetic variation as a major contributor to adaptation in the Virginia chicken lines selection experiment

Sheng

Pettersson

Honaker

et al. 2015

Preprint

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Background: Artificial selection provides a powerful approach to study the genetics of adaptation. Using selectivesweep mapping, it is possible to identify genomic regions where allele-frequencies have diverged during selection. To avoid false positive signatures of selection, it is necessary to show that a sweep affects a selected trait before it can be considered adaptive. Here, we confirm candidate, genome-wide distributed selective sweeps originating from the standing genetic variation in a long-term selection experiment on high and low body weight of chickens. Results: Using an intercross between the two divergent chicken lines, 16 adaptive selective sweeps were confirmed based on their association with the body weight at 56 days of age. Although individual additive effects were small, the fixation for alternative alleles across the loci contributed at least 40 % of the phenotypic difference for the selected trait between these lines. The sweeps contributed about half of the additive genetic variance present within and between the lines after 40 generations of selection, corresponding to a considerable portion of the additive genetic variance of the base population. Conclusions: Long-term, single-trait, bi-directional selection in the Virginia chicken lines has resulted in a gradual response to selection for extreme phenotypes without a drastic reduction in the genetic variation. We find that fixation of several standing genetic variants across a highly polygenic genetic architecture made a considerable contribution to long-term selection response. This provides new fundamental insights into the dynamics of standing genetic variation during long-term selection and adaptation.

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“…Based on work on complex traits in other species, we might expect many more loci with effects too small to be detected in our current sample to influence a complex behavioral trait like tameness (e.g., Yang et al 2010;Hunt et al 2013). Further, selection experiments in multiple species (Drosophila (Burke et al 2010), maize (Laurie et al 2004), and chickens (Johansson et al 2010;Pettersson et al 2013) demonstrated that many loci typically respond to strong selection, as expected when trait variation is due to variants at many genes. It thus seems plausible that many genetic variants with small effects contribute to differences in several biological pathways that together shape complex behavioral traits such as tameness and defensive aggression.…”

Section: Discussionmentioning

confidence: 81%

Genetic Influences on Brain Gene Expression in Rats Selected for Tameness and Aggression

Heyne

Lautenschlaeger²,

Nelson

et al. 2014

Preprint

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Interindividual differences in many behaviors are partly due to genetic differences, but the identification of the genes and variants that influence behavior remains challenging. Here, we studied an F 2 intercross of two outbred lines of rats selected for tame and aggressive behavior toward humans for .64 generations. By using a mapping approach that is able to identify genetic loci segregating within the lines, we identified four times more loci influencing tameness and aggression than by an approach that assumes fixation of causative alleles, suggesting that many causative loci were not driven to fixation by the selection. We used RNA sequencing in 150 F 2 animals to identify hundreds of loci that influence brain gene expression. Several of these loci colocalize with tameness loci and may reflect the same genetic variants. Through analyses of correlations between allele effects on behavior and gene expression, differential expression between the tame and aggressive rat selection lines, and correlations between gene expression and tameness in F 2 animals, we identify the genes Gltscr2, Lgi4, Zfp40, and Slc17a7 as candidate contributors to the strikingly different behavior of the tame and aggressive animals. B EHAVIORAL differences among members of a species are in part due to genetic variation. The identification of the genes and variants that influence behavior remains challenging. In human genome-wide association studies of psychiatric and cognitive traits, the identified loci typically explain only a small fraction of the heritability, i.e., the additive genetic contribution to the trait (Watanabe et al. 2007;Hovatta and Barlow 2008;Deary et al. 2009;Otowa et al. 2009;Calboli et al. 2010;Terracciano et al. 2010;Flint and Munafo 2013;Rietveld et al. 2013;Sokolowska and Hovatta 2013). In experimental crosses in model species, especially between inbred lines, the identified loci (termed quantitative trait loci, QTL), often explain much more of the heritability (Lynch and Walsh 1998). However, in this design the spatial resolution is limited-the QTL are wide and contain many, sometimes hundreds of genes. With the exception of a handful of identified genes with quantitative effects on behavioral traits (Yalcin et al. 2004;Watanabe et al. 2007;McGrath et al. 2009;Bendesky et al. 2012;Goodson et al. 2012), gene identification is particularly difficult for behavioral QTL that often have modest effect sizes (Flint 2003;Willis-Owen and Flint 2006;Wright et al. 2006;Hovatta and Barlow 2008).The causal variants within a QTL can alter the protein sequence encoded by a gene or affect gene expression. Such Musunuru et al. 2010). A few eQTL studies have also recently been carried out to identify candidate genes for behavioral QTL (Hitzemann et al. 2004;De Jong et al. 2011;Saba et al. 2011;Kelly et al. 2012).Here, we studied two lines of rats (Rattus norvegicus) that, starting from one wild population, have been selected for increased tameness and increased aggression toward humans, respectively. These experimental...

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Genome-Wide Effects of Long-Term Divergent Selection

Cited by 137 publications

References 29 publications

Key questions in the genetics and genomics of eco-evolutionary dynamics

Key questions in the genetics and genomics of eco-evolutionary dynamics

Standing genetic variation as a major contributor to adaptation in the Virginia chicken lines selection experiment

Genetic Influences on Brain Gene Expression in Rats Selected for Tameness and Aggression

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