Introduction
Several microsatellite studies on African buffalo (Syncerus caffe r) from Kruger National Park (KNP) and Hluhluwe-iMfolozi Park (HiP), South Africa, have identified deleterious alleles with a negative effect on male body condition and resistance to bovine tuberculosis (BTB) (van Hooft et al., 2018; van Hooft, Getz, Greyling, & Bastos, 2019; van Hooft et al., 2014). Two types of microsatellites were observed: one type containing alleles associated with negative phenotypic effects in both sexes (deleterious-effect—DE—associated loci and alleles), and one type containing alleles associated with negative phenotypic effects in males but positive phenotypic effects in females (sexually-antagonistic-effect—SAE—associated loci and alleles). These microsatellite alleles are probably linked to male-deleterious alleles (from hereon, DE, SAE and male-deleterious-trait-associated alleles will refer to microsatellite alleles and male-deleterious alleles to alleles at protein-coding genes). The male-deleterious alleles probably occur genome-wide at high frequencies in both populations and seem to be of large effect considering the notable frequency differences between year-cohorts and between unhealthy (BTB-positive and low body condition) and healthy (BTB-negative and high body condition) males.
Male-deleterious alleles seemed to have high frequencies and be under positive selection in KNP despite the negative phenotypic effects (van Hooft et al., 2014). Positive selection has been attributed to a sex-ratio meiotic gene-drive system (van Hooft et al., 2018; van Hooft et al., 2019; van Hooft et al., 2014; van Hooft et al., 2010). It was hypothesized that poor health (due to low body condition and BTB infection) in males suppresses sex-ratio distortion genes in this gene-drive system, which when active results in reduced fertility. As a consequence, any allele that has a negative effect on male health may have a positive effect on male relative fertility and thereby be under positive selection if the net fitness effect on health and fertility across both sexes is positive. However, in contrast to positive selection of male-deleterious alleles in KNP, selection of male-deleterious alleles appears to be negative in HiP, which is situated just 280 km further south, resulting in relatively low male-deleterious allele frequencies compared to KNP (van Hooft et al., 2019). This negative selection has been attributed to incompleteness of the gene-drive system, as discussed elsewhere (van Hooft et al., 2018; van Hooft et al., 2019).
It is unlikely that the male-deleterious alleles are restricted to just KNP and HiP. Positive selection and movement of individuals (both diffusive and migratory) may have spread these alleles, together with the linked (hitchhiking) DE and SAE microsatellite alleles, across a large part of southern Africa (van Hooft et al., 2018). Their range possibly extends as far as East Africa, considering the high DE allele frequencies in this region (average frequency Kruger: 0.69, average frequency East Africa: 0.47) (van Hooft et al., 2014). The interplay between migration (gene flow) and selection may have resulted in allele-frequency clines, which would be a strong indicator of selection acting across a wide geographic range (Charlesworth & Charlesworth, 2010; May, Endler, & McMurtrie, 1975; Slatkin, 1973). Such clines have previously been observed in KNP, not only for the DE and SAE alleles but also for a Y-chromosomal haplotype hypothesized to be linked to a suppressor gene from the gene-drive system (van Hooft et al., 2014). Further, multilocus selection of male-deleterious alleles at short chromosomal distances may have resulted in linkage disequilibrium (LD) due to increased frequencies of haplotypes consisting of multiple male-deleterious alleles (relative to haplotype frequencies expected under linkage equilibrium) (Hastings, 1984). This may be particularly so if sex-specific selection results in admixture LD due to different allele frequencies in male and female gametes (Úbeda, Haig, & Patten, 2011). Such differences have earlier been hypothesized in KNP for both DE and SAE alleles based on genetic data from male and female calves (van Hooft et al., 2018). In combination with a selection gradient, multilocus sex-specific selection may have resulted in an LD cline with highest LD where selection is strongest. A wide distribution of male-deleterious alleles may have substantial management implications, because it suggests that many African buffalo populations experience a high genetic load (reduction in relative fitness due to genetic factors) and thereby may be relatively sensitive to environmental stresses.
In this study, we analysed previously published microsatellite data from 1676 African buffalo from 34 localities across the African continent (Figure 1). We addressed the following four questions. 1) Do DE and SAE alleles occur throughout the range of African buffalo? 2) Do the spatial distributions of alleles constitute allele-frequency clines? 3) Can allele-frequency clines, if present, be attributed to selection? 4) Did selection result in an additional LD cline?