Genetic Architecture of Tameness in a Rat Model of Animal Domestication

Albert, Frank W.; Carlborg, Örjan; Plyusnina, I. Z.; Besnier, François; Hedwig, Daniela; Lautenschläger, Susann; Lorenz, Doreen; McIntosh, Jenny; Neumann, Christof; Richter, Henning; Zeising, Claudia; Kozhemyakina, R. V.; Shchepina, Olesya; Kratzsch, Jürgen; Trut, Lyudmila N.; Teupser, Daniel; Thiery, Joachim; Schöneberg, Torsten; Andersson, Leif; Pääbo, Svante

doi:10.1534/genetics.109.102186

Cited by 118 publications

(143 citation statements)

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“…These data were used to map eQTL influencing differences in expression levels, using a QTL mapping method (flexible intercross analysis, FIA) (Rönnegård et al 2008) that can account for segregating variation within the founders of a cross between two outbred lines. Using FIA, we also found four times as many loci influencing tameness than previously seen (Albert et al 2009). We identify multiple genes within the tameness QTL whose expression in the brain is influenced by the genetic variants from the tame-and aggressive lines.…”

supporting

confidence: 66%

“…The first principal component provides a quantitative measurement for tameness (Albert et al 2009). For the present study, we used stored organs from the 75 tamest and the 75 most aggressive F 2 animals. …”

mentioning

confidence: 99%

“…eQTL were treated as local when the gene's physical position overlapped their confidence interval. Genetic positions in centimorgans were interpolated to the physical megabase scale and vice versa with the approx.fun function using coordinates given in table S2 of Albert et al (2009) that contains the genetic and physical position of the markers that were used to build the genetic map.eQTL and tameness QTL were treated as overlapping when their confidence intervals overlapped by at least 1 cM. In the test of whether windows within tameness QTL had more eQTL than the rest of the genome, we used nonoverlapping sliding windows with a width of 18 cM, which is the median confidence interval size of HKR eQTL.…”

mentioning

confidence: 99%

“…To gain insight into the genetic basis of tameness and associated phenotypes, we earlier bred an F 2 intercross between the tame and aggressive rat lines (Albert et al 2009). Genetic mapping in 700 rats from this population revealed two genome-wide significant QTL for tameness.…”

mentioning

confidence: 99%

“…Genetic mapping in 700 rats from this population revealed two genome-wide significant QTL for tameness. Three additional loci were found as part of an epistatic network influencing tameness (Albert et al 2009). However, these QTL harbor hundreds of genes, and individual genes influencing the behavior remain unknown.…”

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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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confidence: 66%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

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

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Genetics of Aggression in Nonhuman Animals

Kukekova

2017

The Wiley Handbook of Violence and Aggression

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The range of aggressive behaviors observed in humans cannot be studied in a single animal model, but a spectrum of animal models can facilitate an understanding of the genetic regulation of aggression. This chapter discusses recent discoveries in the genetics of aggression in rodents, canids, and primates. Rodents, often used to study intermale aggression, provide advantages for functional studies using gene modification techniques. Dramatic changes in aggressive behavior, which took place during dog and fox domestication, allow the investigation of a wider array of aggressive behaviors. Finally, studies of individual differences in the behavior of rhesus monkeys and other primates provide insight into developmental aspects of aggression and gene–environment interactions. Although studies of human social behavior using animal models present challenges, a spectrum of such models, each of which provides its own unique information, can work synergistically to yield robust insights into human aggressive behavior.

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Trabecular bone in domestic dogs and wolves: Implications for understanding human self‐domestication

Chirchir

2020

The Anatomical Record

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The process of domestication is complex and results in significant morphological, cognitive, and physiological changes. In canids, some of the traits indicative of domestication of domestic dogs compared to their wild counterparts the wolves are prosociality toward humans, reduced stress hormone levels, and reduced cranial capacity. Research suggests that selection for prosociality among dogs resulted in morphological changes such as reduction in cranial capacity, juvenilization of the face, and overall gracile morphology. Interestingly, similar features have been described in modern humans compared to extinct species of Homo, for example, Neanderthals. Therefore, the human self‐domestication hypothesis has been proposed to partially explain the gracile modern human skeleton. Specifically, that as modern humans settled in communities, there was increased selection for prosociality (intergroup cooperation); and one of the by‐products of this selection was the evolution of a gracile skeleton, including a slight reduction in cranial capacity, reduced brow ridge and tooth size, and low trabecular bone fraction (TBF). However, TBF variation has not been tested between domestic dogs and wolves, who underwent self‐domestication. Thus, this study tests the hypothesis that dogs have low TBF as a consequence of domestication compared to their wild counterparts, the wolves, by comparing TBF in the hindlimbs—proximal femur and distal tibia‐ of the two species. Wilcoxon rank sum tests show that dogs have lower TBF values than wolves in both elements. These preliminary results add to the literature documenting changes in self‐domesticated species and provide a potential analog to further the understanding of self‐domestication.

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Genetic Architecture of Tameness in a Rat Model of Animal Domestication

Cited by 118 publications

References 61 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

Genetics of Aggression in Nonhuman Animals

Trabecular bone in domestic dogs and wolves: Implications for understanding human self‐domestication

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