In the early 1970s, a couple of hundred wild rats near the Siberian city of Novosibirsk were rounded up by scientists for an ambitious experiment to understand how animals evolve during domestication. Dimitry Belyaev and his colleagues—known for their related project on domesticating foxes—split the rats into two groups.

With one group, the researchers tried to replicate the way human ancestors had tamed wild animals over generations. At each generation, only the tamest of the rats were selected for breeding. With the other group, they did the opposite, breeding only the rats that were most wary of and aggressive towards humans. After more than sixty generations of selection, the immediate response of rats from the “aggressive” line is to escape or attack. In contrast, the rats from the “tame” line can be handled and even petted.

In this month’s issue of GENETICS, Heyne et al. report quantitative trait loci (QTLs) contributing to this rapidly-evolved behavior difference, including genetic influences on gene expression in the brain. Their results show that the genetic architecture of tameness in these rats is more complex than once thought.

Albert et al. had previously mapped QTLs contributing to the difference in tameness by crossing the two rat lines (using an F2 intercross design). But the analysis method they used assumed the causative alleles were fixed in each population — that is, in the tame population, all rats were homozygous for the “tameness” alleles and in the aggressive population, all rats were homozygous for the corresponding “aggression” alleles.

In the new study, the authors reasoned that both rat lines were genetically diverse enough to violate this assumption. Because the founders came from a wild population, and matings between close relatives were avoided over the generations of selection, multiple alleles at the causative loci may still be present within each line. Heyne et al. revisited the mapping data using an analysis method (FIA) that can account for such segregating—as opposed to fixed—variation, and found eight QTLs, including the two discovered previously.

Given that effects on behavior are likely to involve the brain, the authors also applied the FIA method to identify hundreds of QTLs affecting differences in brain gene expression between the lines (a.k.a. eQTLs). They used this information to select good candidates for causative genes within the “tameness” QTL regions. First, they looked for genes in the behavior QTLs that overlapped one of the gene expression QTLs, then narrowed down the list to those genes that were expressed at different levels in the brains of tame vs. aggressive rats.

The most plausible candidate genes would not only have overlapping behavior and expression QTLs, but both QTLs would be caused by the same underlying variants. The authors looked for evidence for shared underlying variants using the ability of the FIA method to estimate the effects for multiple alleles per QTL. In those cases where multiple alleles are involved, the relative effect of each of the different alleles should be correlated across the two traits being measured, i.e. behavior and gene expression. Five of the candidate genes showed significant correlations and the authors consider these genes the most likely to play key roles in shaping behavior differences between the two populations.

These candidates look promising so far. Three of the genes are involved in nervous system development and one, Slc17a7, has previously been implicated in fear and stress behavior in mice. Further work is needed to test which genes contribute significantly to the remarkable behavior differences between the two types of rat.

Mark Johnston, Editor-in-Chief of GENETICS commented on the study in a press statement: “These rats are one of those rich experimental resources that keeps providing new insights as our methods and technology advance. Thanks to the authors’ excellent work and to Belyaev’s foresight in 1972, we are finally starting to understand the genetic details of a biological process that has been pivotal to human history.”

 

CITATION:
Heyne H.O., R. Nelson, F. Besnier, M. Rotival, A. Cagan, R. Kozhemyakina, I. Z. Plyusnina, L. Trut, O. Carlborg, E. Petretto, L. Kryuglyak, S. Pääbo, T. Schöneberg, & F.W. Albert (2014). Genetic Influences on Brain Gene Expression in Rats Selected for Tameness and Aggression, Genetics, 198 (3) 1277-1290. http://www.genetics.org/content/198/3/1277.full
DOI: http://dx.doi.org/10.1534/genetics.114.168948

 

More:

Read the press release: Genes contribute to behavior differences between fierce and friendly rats.

Listen to co-author Alex Cagan talk about this work in an interview with NPR’s Science Friday.

Read about why domesticated mammals may share so many traits in Does neural crest development drive domestication syndrome?

Read about how an endogenous retrovirus gave many domestic cats their distinctive coat patterns How the cat got its spots (and hearing problems).

, , , , ,

Cristy Gelling is a science writer, lapsed yeast geneticist, and former Communications Director at the GSA.

View all posts by Cristy Gelling »

Read more in

  • Ed Grell at his dissecting microscope using ether to anesthetize his flies.

    In Memoriam: Ellsworth Herman Grell (1932–2023), a pioneer of Drosophila genome engineering and annotation

    Ellsworth (Ed) Grell blessed the Drosophila community through three enduring legacies: as a pioneer of chromosome mechanics, as a primary organizer and synthesizer of genetic knowledge in Drosophila, and as a graceful mentor to those fortunate to have known him personally. Ed grew up in rural Nebraska, completed his undergraduate studies at Iowa State, and…

  • Congratulations to the #Fungal24 Poster Award winners!

    We are pleased to announce the recipients of the GSA Poster Awards for posters presented at the 32nd Fungal Genetics Conference! Undergraduate and graduate student members of GSA were eligible for the awards, and a hard-working team of judges made the determinations. Congratulations to all! Felicia Ebot Ojong, The University of Georgia My research is focused…

  • Poster presentation tips for TAGC 2024

    You’ve been selected to present a poster at The Allied Genetics Conference 2024 in March—you’ve celebrated, made plans to attend, now what? This is an exciting opportunity to showcase your research and engage with fellow members of the genetics community, so you want to make sure you’re prepared. We wanted to offer you some tips…

  • Maximize your TAGC 2024 experience 

    A guide to all that National Harbor & DC have to offer Are you joining us for The Allied Genetics Conference 2024 in March? Make the most of your #TAGC24 experience in National Harbor! We know the science will keep you busy, but you deserve to unwind and have some fun, so we’ve curated a…

  • Early Career Leadership Spotlight: Sarah Petrosky

    We’re taking time to get to know the members of the GSA’s Early Career Scientist Committees. Join us to learn more about our early career scientist advocates. Sarah PetroskyMultimedia SubcommitteeUniversity of Pittsburgh Research Interest I am interested in understanding adaptation that has been happening recently in populations by dissecting the ways that genes underlying an adaptation…

  • TAGC 2024 Early Career Award Winners

    GSA is pleased to announce the winners of the early career awards presented at The Allied Genetics Conference 2024. These awards are specific to particular TAGC communities and recognize early career scientists’ outstanding work on their respective research organisms. The awardees will present their talks in keynote sessions at TAGC 2024.  Don’t miss the opportunity…

  • Preeminent geneticists recognized with revamped GSA Awards

    In 2022, GSA’s Board of Directors launched an audit to review the five major awards conferred by the Society. Today, we are thrilled to announce the recipients of the reimagined GSA Awards, including the new Genetics Society of America Early Career Medal. The scientists honored this year are recognized by their peers for their outstanding…

  • Fly Board funds outreach programs to spread the word about Drosophila research

    In 2020, the Fly Board voted to use part of its reserve fund to support efforts to increase trainee participation as well as equity and diversity in the Drosophila community. An awards committee decides how the money will be spent each year, and from 2020–2022, the committee posted a very broad call for applications from…

  • New members of the GSA Board of Directors: 2024–2026

    We are pleased to announce the election of four new leaders to the GSA Board of Directors: 2024 Vice President/2025 President Brenda Andrews Professor, University of Toronto It’s an honor to continue my association with the Society by serving as Vice President of the Board of Directors. I have broad knowledge of the ongoing activities…

  • A rose-ringed parakeet, one of three parrot species used in the study.

    Parrot plumage study aids breeders and endangered natural populations

    Yellow coloration is maladaptive in the wild but prized by breeders. People have long been fascinated with birds, which exhibit one of the widest ranges of coloration among vertebrates. Parrots, in particular, have captivated humans by their ability to mimic human speech and spectacular plumage. Brightly colored feathers are used primarily to attract mates, intimidate…

  • Early Career Leadership Spotlight: Sarah Gilmour

    We’re taking time to get to know the members of the GSA’s Early Career Scientist Committees. Join us to learn more about our early career scientist advocates. Sarah GilmourMultimedia SubcommitteeStowers Institute for Medical Research Research Interest Questions of evolution have always fascinated me. I am extremely fortunate to be starting out my research career in a…