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.
Highlights
The presence of deleterious alleles in wildlife populations can result in genetic load: a decrease of the fitness of the average genotype relative to the fittest genotype present in a population [1]
The Hluhluwe-iMfolozi Park (HiP) population deviated from the overall trend, showing a clear frequency decrease of p-MDTA alleles relative to p-wildtype alleles (0.10 decrease) in sharp contrast to the other southern African populations
A substantial number of high-frequency deleterious alleles of seemingly large effect [21, 22], with many co-occurring in haplotypes, indicates a high genetic load
Summary
The presence of deleterious alleles in wildlife populations can result in genetic load: a decrease of the fitness of the average genotype relative to the fittest genotype present in a population [1]. A high genetic load can strongly increase local extinction risk via inbreeding depression, in small populations [2, 3]. Inbreeding depression, which is characterized by lower fertility, survival and growth rates, is generally caused by increased homozygosity for partially recessive deleterious mutations (dominance hypothesis) [4]. It has been argued that in many cases deleterious alleles have a limited impact because of density-dependent processes [6]. According to this argumentation selection is typically soft, where selective death due to deleterious alleles would otherwise be replaced by nonselective death due to environmental and ecological conditions (e.g., droughts and intraspecific resource competition). Population size and persistence often do not seem to be affected by the presence of deleterious alleles, even when they are clearly expressed [7]
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