Positive Selection of Deleterious Alleles through Interaction with a Sex-Ratio Suppressor Gene in African Buffalo: A Plausible New Mechanism for a High Frequency Anomaly
Hooft, W.F. van; Greyling, B.J. ; Getz, W.M. ; Helden, P.D. van; Zwaan, B.J. ; Bastos, A.D.S. - \ 2014
PLoS ONE 9 (2014)11. - ISSN 1932-6203
heterozygosity-fitness correlations - bovine tuberculosis - syncerus-caffer - inbreeding depression - population-levels - complex traits - software - disease - wild - flow
Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in selective constraints. Here we present a possible new mechanism that explains the attainment of high frequencies of deleterious alleles in the African buffalo (Syncerus caffer) population of Kruger National Park, through positive selection of these alleles that is ultimately driven by a sex-ratio suppressor. We have previously shown that one in four Kruger buffalo has a Y-chromosome profile that, despite being associated with low body condition, appears to impart a relative reproductive advantage, and which is stably maintained through a sex-ratio suppressor. Apparently, this sex-ratio suppressor prevents fertility reduction that generally accompanies sex-ratio distortion. We hypothesize that this body-condition-associated reproductive advantage increases the fitness of alleles that negatively affect male body condition, causing genome-wide positive selection of these alleles. To investigate this we genotyped 459 buffalo using 17 autosomal microsatellites. By correlating heterozygosity with body condition (heterozygosity-fitness correlations), we found that most microsatellites were associated with one of two gene types: one with elevated frequencies of deleterious alleles that have a negative effect on body condition, irrespective of sex; the other with elevated frequencies of sexually antagonistic alleles that are negative for male body condition but positive for female body condition. Positive selection and a direct association with a Y-chromosomal sex-ratio suppressor are indicated, respectively, by allele clines and by relatively high numbers of homozygous deleterious alleles among sex-ratio suppressor carriers. This study, which employs novel statistical techniques to analyse heterozygosity-fitness correlations, is the first to demonstrate the abundance of sexually-antagonistic genes in a natural mammal population. It also has important implications for our understanding not only of the evolutionary and ecological dynamics of sex-ratio distorters and suppressors, but also of the functioning of deleterious and sexually-antagonistic alleles, and their impact on population viability
Rainfall-driven sex-ratio genes in African buffalo suggested by correlations between Y-chromosomal haplotype frequencies and foetal sex ratio
Hooft, W.F. van; Prins, H.H.T. ; Getz, W.M. ; Jolles, A.E. ; Wieren, S.E. van; Greyling, B.J. ; Helden, P.D. ; Bastos, A.D.S. - \ 2010
BMC Evolutionary Biology 10 (2010). - ISSN 1471-2148 - 11 p.
cattle bos-taurus - syncerus-caffer - male-fertility - meiotic drive - bovine tuberculosis - drosophila-melanogaster - microsatellite analysis - natural-populations - sperm - selection
Background - The Y-chromosomal diversity in the African buffalo (Syncerus caffer) population of Kruger National Park (KNP) is characterized by rainfall-driven haplotype frequency shifts between year cohorts. Stable Y-chromosomal polymorphism is difficult to reconcile with haplotype frequency variations without assuming frequency-dependent selection or specific interactions in the population dynamics of X- and Y-chromosomal genes, since otherwise the fittest haplotype would inevitably sweep to fixation. Stable Y-chromosomal polymorphism due one of these factors only seems possible when there are Y-chromosomal distorters of an equal sex ratio, which act by negatively affecting X-gametes, or Y-chromosomal suppressors of a female-biased sex ratio. These sex-ratio (SR) genes modify (suppress) gamete transmission in their own favour at a fitness cost, allowing for stable polymorphism. Results - Here we show temporal correlations between Y-chromosomal haplotype frequencies and foetal sex ratios in the KNP buffalo population, suggesting SR genes. Frequencies varied by a factor of five; too high to be alternatively explained by Y-chromosomal effects on pregnancy loss. Sex ratios were male-biased during wet and female-biased during dry periods (male proportion: 0.47-0.53), seasonally and annually. Both wet and dry periods were associated with a specific haplotype indicating a SR distorter and SR suppressor, respectively. Conclusions - The distinctive properties suggested for explaining Y-chromosomal polymorphism in African buffalo may not be restricted to this species alone. SR genes may play a broader and largely overlooked role in mammalian sex-ratio variation
Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo
Jolles, A.E. ; Ezenwa, V.O. ; Etienne, R.S. - \ 2008
Ecology 89 (2008)8. - ISSN 0012-9658 - p. 2239 - 2250.
kruger-national-park - fecal egg counts - bovine tuberculosis - syncerus-caffer - environmental-change - parasitic diseases - host populations - responses - wildlife - susceptibility
Epidemiological studies typically focus on single-parasite systems, although most hosts harbor multiple parasite species; thus, the potential impacts of co-infection on disease dynamics are only beginning to be recognized. Interactions between macroparasites, such as gastrointestinal nematodes, and microparasites causing diseases like TB, AIDS, and malaria are particularly interesting because co-infection may favor transmission and progression of these important diseases. Here we present evidence for strong interactions between gastrointestinal worms and bovine tuberculosis (TB) in free-ranging African buffalo (Syncerus caffer). TB and worms are negatively associated at the population, among-herd, and within-herd scales, and this association is not solely the result of demographic heterogeneities in infection. Combining data from 1362 buffalo with simple mechanistic models, we find that both accelerated mortality of co-infected individuals and TB transmission heterogeneity caused by trade-offs in immunity to the two types of parasites likely contribute to observed infection patterns. This study is one of the first to examine the relevance of within-host immunological trade-offs for understanding parasite distribution patterns in natural populations.
Genetic structure of African buffalo herds based on variation at the mitochondrial D-loop and autosomal microsatellite loci: Evidence for male-biased gene flow
Hooft, W.F. van; Groen, A.F. ; Prins, H.H.T. - \ 2003
Conservation Genetics 4 (2003)4. - ISSN 1566-0621 - p. 467 - 477.
syncerus-caffer - population-structure - markers - differentiation - dispersal - diversity - dna - relatedness - sequence - disease
Sexual differences in herding behaviour of African buffalo (Syncerus caffer) were studied by analysing at the herd level mitochondrial D-loop hypervariable region I and fourteen autosomal microsatellites. Three herds from Arusha National Park in Tanzania were analysed with mtDNA and five herds from Kruger National Park in South Africa with mtDNA and microsatellites. Significant mtDNA differentiation was observed among herds in Arusha NP (F-ST = 0.12, based on haplotype frequencies). Assignment tests with microsatellite data from Kruger NP showed that most frequent migration between herds is by males greater than or equal totwo years. This was confirmed by tests for herd differentiation and analyses with Lynch and Ritland's relatedness estimator. Within a herd, males younger than two years and females showed a higher relationship through a common father rather than a common mother, indicating that female herd members mate with only a few dominant males. This in turn suggests a female: male sex ratio larger than 5:1. The migration rate per generation between herds was estimated to be 5-20% for females and close to 100% for males. Finally, the implications for the management of buffalo populations are being discussed.