A continent-wide high genetic load in African buffalo revealed by a
cline in the frequency of deleterious alleles and linkage disequilibrium
Abstract
Recent microsatellite studies of two African buffalo (Syncerus caffer)
populations in South Africa indicated a high genetic load due to
genome-wide high-frequency occurrence of deleterious alleles. These
alleles have a negative effect on two male traits: body condition and
bovine tuberculosis resistance. Here, we study the occurrence of these
male-deleterious alleles throughout most of the buffalo’s range using
previously published microsatellite data (2-17 microsatellite loci
genotyped on 1676 animals from 34 localities). We uncovered a
continent-wide frequency cline of microsatellite alleles associated with
male-deleterious traits, with frequencies decreasing from 25 °S to 5 °N
(adjusted R2 = 0.87). Further, there was a continent-wide presence of
linkage disequilibrium (LD) between male-deleterious-trait-associated
alleles at five linked locus pairs (interlocus distance: 0.5-28
Megabase). The fraction of positive interlocus associations among these
locus pairs was 0.65 (95% CI: 0.52-0.77; expected fraction with free
recombination: 0.5), indicating that many male-deleterious alleles
co-occur in haplotypes. We argue that the allele-frequency cline and LD
likely result from genome-wide balancing selection of male-deleterious
alleles with equilibrium allele and haplotype frequencies determined by
the activity of a sex-chromosomal gene-drive system, the latter which
was indicated in earlier studies and seemingly originated in southern
Africa. The selection pressures involved must be high to prevent
destruction of the allele-frequency cline and haplotypes by LD decay.
Since most buffalo populations are stable, our results indicate that
natural mammal populations can withstand a high genetic load.
Nevertheless, we expect that a high genetic load makes many buffalo
populations relatively sensitive to environmental stresses.