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?