A continent-wide high genetic load in African buffalo revealed by clines in the frequency of deleterious alleles, genetic hitchhiking and linkage disequilibrium

Abstract

A high genetic load can negatively affect population viability and increase susceptibility to diseases and other environmental stressors. Prior microsatellite studies of two African buffalo (Syncerus caffer) populations in South Africa indicated substantial genome-wide genetic load due to high-frequency occurrence of deleterious alleles. The occurrence of these alleles, which negatively affect male body condition and bovine tuberculosis resistance, throughout most of the buffalo’s range were evaluated in this study. Using available microsatellite data (2–17 microsatellite loci) for 1676 animals from 34 localities (from 25˚S to 5˚N), we uncovered continent-wide frequency clines of microsatellite alleles associated with the aforementioned male traits. Frequencies decreased over a south-to-north latitude range (average per-locus Pearson r = -0.22). The frequency clines coincided with a multilocus-heterozygosity cline (adjusted R2 = 0.84), showing up to a 16% decrease in southern Africa compared to East Africa. Furthermore, continent-wide linkage disequilibrium (LD) at five linked locus pairs was detected, characterized by a high fraction of positive interlocus associations (0.66, 95% CI: 0.53, 0.77) between male-deleterious-trait-associated alleles. Our findings suggest continent-wide and genome-wide selection of male-deleterious alleles driven by an earlier observed sex-chromosomal meiotic drive system, resulting in frequency clines, reduced heterozygosity due to hitchhiking effects and extensive LD due to male-deleterious alleles co-occurring in haplotypes. The selection pressures involved must be high to prevent destruction of allele-frequency clines and haplotypes by LD decay. Since most buffalo populations are stable, these results indicate that natural mammal populations, depending on their genetic background, can withstand a high genetic load.S1 Text. Allele size standardization.S1 Table. Earlier reported associations of microsatellite alleles with low body condition and bovine tuberculosis (BTB) infection risk.S2 Table. Allele size standardization.S3 Table. Overview of alleles selected for analysis.S4 Table. p-MDTA allele frequencies per population.S5 Table. Per-locus Pearson correlation between ‘p-MDTA minus p-wildtype’ allele frequency difference and latitude, and between He and latitude.S6 Table. He per locus per population.S7 Table. Linkage disequilibrium per population.S8 Table. He per locus in KNP, HiP and Addo NP.S1 Fig. Increase of pairwise FST with geographic distance.S2 Fig. Multilocus-He cline based on twelve microsatellites per locality.S3 Fig. Multilocus-He cline based on seven microsatellites analysed in both East and southern Africa (microsatellite sets A, B and D) plus ABS010 and AGLA293.S4 Fig. Correlation between per-locus southern/northern KNP He ratio and He-latitude Pearson correlation, based on 19 microsatellites.http://www.plosone.orgam2022Zoology and Entomolog