Bovine tuberculosis (BTB) is endemic to the African buffalo (Syncerus caffer) of HluhluweiMfolozi
Park (HiP) and Kruger National Park, South Africa. In HiP, the disease has been
actively managed since 1999 through a test-and-cull procedure targeting BTB-positive buffalo.
Prior studies in Kruger showed associations between microsatellite alleles, BTB and
body condition. A sex chromosomal meiotic drive, a form of natural gene drive, was hypothesized
to be ultimately responsible. These associations indicate high-frequency occurrence
of two types of male-deleterious alleles (or multiple-allele haplotypes). One type negatively
affects body condition and BTB resistance in both sexes. The other type has sexually antagonistic
effects: negative in males but positive in females. Here, we investigate whether a
similar gene drive system is present in HiP buffalo, using 17 autosomal microsatellites and
microsatellite-derived Y-chromosomal haplotypes from 401 individuals, culled in 2002–
2004. We show that the association between autosomal microsatellite alleles and BTB susceptibility
detected in Kruger, is also present in HiP. Further, Y-haplotype frequency dynamics
indicated that a sex chromosomal meiotic drive also occurred in HiP. BTB was
associated with negative selection of male-deleterious alleles in HiP, unlike positive selection
in Kruger. Birth sex ratios were female-biased. We attribute negative selection and
female-biased sex ratios in HiP to the absence of a Y-chromosomal sex-ratio distorter. This
distorter has been hypothesized to contribute to positive selection of male-deleterious
alleles and male-biased birth sex ratios in Kruger. As previously shown in Kruger, microsatellite
alleles were only associated with male-deleterious effects in individuals born after wet pre-birth years; a phenomenon attributed to epigenetic modification. We identified two additional
allele types: male-specific deleterious and beneficial alleles, with no discernible effect
on females. Finally, we discuss how our findings may be used for breeding disease-free buffalo
and implementing BTB test-and-cull programs.
S1 Text. Sex chromosomal meiotic drive can explain genome-wide high-frequency occurrence
of male-deleterious alleles.
S2 Text. Frequency differences of DEmajority and SAEpooled alleles between HiP and Kruger.
S1 Fig. Map with sampling localities.
S2 Fig. Monthly rainfall in HiP.
S3 Fig. Annual rainfall in HiP in the period 1979–2004.
S4 Fig. Frequencies of DEmajority and SAEpooled alleles in HiP compared with Kruger.
S5 Fig. Difference in Amale-spec between SAEindvN alleles from Kruger observed and not
observed in HIP.
S6 Fig. Allele frequency differences between northern Kruger and HiP per SAE allele type.
S1 Table. List of SAEpooled and DEmajority alleles.
S2 Table. List of individual alleles at the DE microsatellite loci.
S3 Table. List of individual alleles at the SAE microsatellite loci.
S4 Table. List of individual alleles at the SAE microsatellite loci with unknown linkage.
S5 Table. Logistic regression of BTB-infection risk for each sex separately.
S6 Table. Logistic regression of BTB-infection risk for dry and wet pre-birth years separately.
S7 Table. Logistic regression between sex (dependent) and age and 3yr-pre-birth rainfall.