Fitness effects of a selfish gene (the Mus t complex) are revealed in an ecological context.
In wild house mice, genes linked to the t transmission distortion complex cause meiotic drive by sabotaging wild-type gametes. The t complex is consequently inherited at frequencies higher than 90%. Yet, for unclear reasons, in wild mouse populations this selfish DNA is found at frequencies much lower than expected. Here, we examine selection on the t complex in 10 seminatural populations of wild mice based on data from 234 founders and nearly 2000 progeny. Eight of the 10 populations decreased in t frequency over one generation, and the overall frequency of t haplotypes across all 10 populations was 48.5% below expectations based on transmission distortion and 34.3% below Mendelian (or Hardy-Weinberg) expectations. Behavioral and reproductive data were collected for 10 months for each population, and microsatellite genotyping was performed on seven of the populations to determine parentage. These combined data show t-associated fitness declines in both males and females. This is the first study to show evidence for a reduction in the ability of +/t males to maintain territories. Because females tend to mate with dominant males, impairment of territorial success can explain much of the selection against t observed in our populations. In nature, selection against heterozygote carriers of the t complex helps solve the puzzlingly low t frequencies found in wild populations. This ecological approach for determining fitness consequences of genetic variants has broad application for the discovery of gene function in general.
Carroll
Lara S
LS
Howard Hughes Medical Institute, University of Utah, 15 North 2030 East, Room 5100, Salt Lake City, Utah 84112, USA. lsc3@utah.edu
Meagher
Shawn
S
Morrison
Linda
L
Penn
Dustin J
DJ
Potts
Wayne K
WK
D000704:Analysis of Variance; D000818:Animals; D005298:Fertility / Q000502:physiology*; D005431:Florida; D005828:Genetics, Population; D005838:Genotype; D006239:Haplotypes / Q000235:genetics; D007178:Inbreeding; D051379:Mice / Q000235:genetics* / Q000502:physiology; D018895:Microsatellite Repeats / Q000235:genetics; D008869:Microtubule-Associated Proteins / Q000235:genetics*; D009687:Nuclear Proteins / Q000235:genetics*; D019370:Observation; D012091:Repetitive Sequences, Nucleic Acid / Q000235:genetics*; D012641:Selection, Genetic; D012930:Social Dominance; D013731:Territoriality; D056427:t-Complex Genome Region
D008869:Microtubule-Associated Proteins; D009687:Nuclear Proteins