Targeted resequencing of a genomic region influencing tameness and aggression reveals multiple signals of positive selection

Albert, Frank W.; Hodges, Emily; Jensen, Jeffrey D.; Besnier, François; Xuan, Zhenyu; Rooks, Michelle; Bhattacharjee, Arindam; Brizuela, Leonardo; Good, Jeffrey M.; Green, Edward; Burbano, Hernán A.; Plyusnina, I. Z.; Trut, Lyudmila N.; Andersson, Leif; Schöneberg, Torsten; Carlborg, Örjan; Hannon, Gregory J.; Pääbo, Svante

doi:10.1038/hdy.2011.4

Cited by 30 publications

(23 citation statements)

References 48 publications

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“…Instead, most genetic variants that were selected are expected to be due to standing variation already present in the wild population. We earlier confirmed the existence of considerable DNA sequence variation both between and within each of the two lines (Albert et al 2011). Therefore, it seems plausible that alleles influencing behavior segregate not only between but also within the lines.…”

supporting

confidence: 58%

“…Using this method, we identified two tameness QTL (Albert et al 2009) and hundreds of eQTL. Because the two selection lines are outbred and display considerable within-line genetic variation (Albert et al 2011), we also used a QTL mapping method that does not require causative alleles to be fixed between the tame and aggressive founders (Rönnegård et al 2008). Using this method, many additional tameness QTL and eQTL were detected.…”

Section: Discussionmentioning

confidence: 99%

“…At the most significant FIA tameness QTL on chromosome 1 (corresponding to the "Tame-1" locus identified in Albert et al (2009), the alleles carried by the tame and the aggressive individuals used to found the F 2 pedigree have clearly different effects on tameness (Figure 1). However, more than one "aggressive" allele appears to exist among the four aggressive founder animals (Albert et al 2011), and one of the four tame founders appears to be heterozygous for one "tame" and one aggressive allele. Nevertheless, the overall allelic differentiation between the tame and the aggressive founder individuals explains why this locus was also the strongest QTL identified by HKR.…”

Section: Genetic Variation Within the Selection Lines Influences Tamementioning

confidence: 99%

“…Inbreeding was avoided in both strains by avoiding mating between close relatives. In 2005, subpopulations from both lines were transferred to Leipzig to study the genetic basis of the tameness (Albert et al 2008(Albert et al , 2009(Albert et al , 2011(Albert et al , 2012. During all care-taking procedures and experiments, animals from different lines and generations were treated identically.…”

Section: Rat Populationsmentioning

confidence: 99%

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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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supporting

confidence: 58%

Section: Discussionmentioning

confidence: 99%

Section: Genetic Variation Within the Selection Lines Influences Tamementioning

confidence: 99%

Section: Rat Populationsmentioning

confidence: 99%

See 2 more Smart Citations

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

Heyne

Lautenschlaeger²,

Nelson

et al. 2014

Preprint

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“…Further, polygenic traits will more likely only slightly change in frequency instead of going to fixation. Such selection will also be accompanied by strong linkage disequilibrium [174], which may cause morphological changes that do not appear to have a direct phenotypic correlation with the behavioral traits under selection [167].…”

Section: Factors Affecting Selectionmentioning

confidence: 99%

Chicken domestication : Effects of tameness on brain gene expression and DNA methylation

Bélteky¹

2016

Linköping Studies in Science and Technology. Dissertations

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Domestication greatly increases phenotypic variation in a short time span, with selection for a single phenotype and a plethora of associated phenotypic changes as an outcome of the process. The domestication process influences the underlying genomic architecture of a species, and the success and speed of the process is likely influenced by it. The main aims of my thesis was to study how domestication affects the brain of chickens: specifically changes in morphology, gene expression, and DNA methylation. Differences in gene expression and DNA methylation between White Leghorn and Red Junglefowl chickens were mapped, and inheritance of these patterns were quantified, indicating a faithful transmission of breed-specific epigenetic markers. Selection on the behavioral trait fearfulness, generated high and low fearful lines of Red Junglefowl. Both the parental population and the fifth selected generation were used for the analyses in this thesis. One experiment studied morphological changes in the brain and other vital organs, and found that relative total brain size increased in high fearful birds, as a consequence of an increase in cerebral hemisphere size in high fearful birds and not in low fearful birds. Also, the relative heart, liver, spleen and testis size increased in high fearful birds, indicating correlated morphological changes with selection for fearfulness. Two additional experiments examined differential gene expression in the hypothalamus and the anterior cerebral hemisphere. The hypothalamus differed in expression of genes with reproductive and immunological functions, whilst the cerebral hemisphere differed in expression of genes related to social behaviors and neurological functions especially those upregulated in low fearful birds. These results indicate the occurrence of tissue-and species-specific changes in gene expression as overlap with other domestication events were nearly nonexistent. A fourth experiment sought to associate the change in fear levels and gene expression differences with DNA methylation. Chromosomal regions with differential DNA methylation between high and low fearful birds were identified, and genes in these regions had annotated functions relevant to phenotypic differences between the selection lines. This thesis is the first to study the genetic alterations of domestication using the wild ancestor of an already domesticated species to repeat the domestication process selecting against fear of humans. The findings corroborate results from previous comparisons of wild and domestic animals, and further support the theory that rigorous selection for a behavioral trait can cause a cascade of genetic and epigenetic changes facilitating the domestication of a population. Populärvetenskaplig sammanfattningDomesticering, när en population djur anpassas till ett liv i fångenskap och nära kontakt med människor, är en process som under kort tid ger upphov till stora förändringar hos djuret under selektion, såsom skillnader i beteende, fysiologi, storlek, reproduktion och fä...

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Rapid behavioral assay using handling test provides breed and sex differences in tameness of chickens

et al. 2019

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Background Japanese indigenous chicken breeds are often used to improve meat quality rather than broilers in the Jidori industry. There are sometimes severe crowding accidents caused by many birds frightened by environmental stimuli. To prevent the economic loss, the chickens need to be more gentle, tame, and imperturbable. Methods In this study, a new handling test for tameness in adult chickens in individual cages was performed with 100 birds from each sex of Shamo, Rhode Island Red, Nagoya, Australorp, and Ukokkei, as well as 10 hens of F1 hybrid between Shamo and Rhode Island Red, to measure both active and passive tameness. We counted the number heading toward human hands (heading) and retreating in other directions (avoiding) in both active and passive tameness phases, as well as the number of steps taken (step) during the handling test. Results Male chickens exhibited higher avoidance behavior than females. Nagoya females displayed the lowest level of avoidance behavior, which implies passive tameness. In terms of active tameness, a variety of phenotypes can be obtained in different combinations of breed and sex. These results suggested the handling test will be good method for rapid screening of individual differences in tameness. In addition, there were heterosis effects on avoidance and locomotive behaviors. Since F1 is often used in the Jidori industry, the breeders should be tested not only for meat production but also for tameness. Conclusions In the future, combining both the behavioral screening and the population genomics will establish typical evidence about mechanisms of tameness and domestication in animals.

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Targeted resequencing of a genomic region influencing tameness and aggression reveals multiple signals of positive selection

Cited by 30 publications

References 48 publications

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

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

Chicken domestication : Effects of tameness on brain gene expression and DNA methylation

Rapid behavioral assay using handling test provides breed and sex differences in tameness of chickens

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