Abstract:
Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in
selective constraints. Here we present a possible new mechanism that explains the attainment of high frequencies of
deleterious alleles in the African buffalo (Syncerus caffer) population of Kruger National Park, through positive selection of
these alleles that is ultimately driven by a sex-ratio suppressor. We have previously shown that one in four Kruger buffalo
has a Y-chromosome profile that, despite being associated with low body condition, appears to impart a relative
reproductive advantage, and which is stably maintained through a sex-ratio suppressor. Apparently, this sex-ratio
suppressor prevents fertility reduction that generally accompanies sex-ratio distortion. We hypothesize that this bodycondition-
associated reproductive advantage increases the fitness of alleles that negatively affect male body condition,
causing genome-wide positive selection of these alleles. To investigate this we genotyped 459 buffalo using 17 autosomal
microsatellites. By correlating heterozygosity with body condition (heterozygosity-fitness correlations), we found that most
microsatellites were associated with one of two gene types: one with elevated frequencies of deleterious alleles that have a
negative effect on body condition, irrespective of sex; the other with elevated frequencies of sexually antagonistic alleles
that are negative for male body condition but positive for female body condition. Positive selection and a direct association
with a Y-chromosomal sex-ratio suppressor are indicated, respectively, by allele clines and by relatively high numbers of
homozygous deleterious alleles among sex-ratio suppressor carriers. This study, which employs novel statistical techniques
to analyse heterozygosity-fitness correlations, is the first to demonstrate the abundance of sexually-antagonistic genes in a
natural mammal population. It also has important implications for our understanding not only of the evolutionary and
ecological dynamics of sex-ratio distorters and suppressors, but also of the functioning of deleterious and sexuallyantagonistic
alleles, and their impact on population viability.
