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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.

van Hooft P, Greyling BJ, Getz WM, van Helden PD, Zwaan BJ, Bastos AD - PLoS ONE (2014)

Bottom Line: Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in selective constraints.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.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.

View Article: PubMed Central - PubMed

Affiliation: Resource Ecology Group, Wageningen University, Wageningen, The Netherlands; Mammal Research Institute, Department of Zoology & Entomology, University of Pretoria, Hatfield, South Africa.

ABSTRACT
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.

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Correlation between LBC-minus-HBC group difference in PL-He and baseline PL-He.Baseline PL-He (expected heterozygosity per locus): PL-He of the pooled group of LBC and HBC individuals, error bars: 95% CI, vertical axis: 2(SE2LBC + SE2HBC)0.5, horizontal axis: 2SE; Spearman rank correlation coefficient: ρ = 0.80, nLBC = 230, nHBC = 90, nmicrosatellites = 17, Prandomization between body condition classes = 0.00034. Data are from southern Kruger. This figure shows that it was the microsatellites with low baseline PL-He (<0.56) that were associated with effects on body condition, i.e. a relatively large PL-He decrease in the LBC (low body condition) group relative to the HBC (high body condition) group. The positive correlation indicates that the HFCs (heterozygosity-fitness correlations) in southern Kruger can only be explained by LD between microsatellites and expressed genes.
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pone-0111778-g001: Correlation between LBC-minus-HBC group difference in PL-He and baseline PL-He.Baseline PL-He (expected heterozygosity per locus): PL-He of the pooled group of LBC and HBC individuals, error bars: 95% CI, vertical axis: 2(SE2LBC + SE2HBC)0.5, horizontal axis: 2SE; Spearman rank correlation coefficient: ρ = 0.80, nLBC = 230, nHBC = 90, nmicrosatellites = 17, Prandomization between body condition classes = 0.00034. Data are from southern Kruger. This figure shows that it was the microsatellites with low baseline PL-He (<0.56) that were associated with effects on body condition, i.e. a relatively large PL-He decrease in the LBC (low body condition) group relative to the HBC (high body condition) group. The positive correlation indicates that the HFCs (heterozygosity-fitness correlations) in southern Kruger can only be explained by LD between microsatellites and expressed genes.

Mentions: The PL-He decrease in the LBC group from southern Kruger (relative to the HBC group) declined with increasing baseline PL-He (Spearman rank correlation coefficient (ρ) = 0.80; Prandomization = 0.00034, nLBC = 230, nHBC = 90; northern Kruger: Prandomization = 0.53, nLBC = 68, nHBC = 70; Figure 1). As discussed above, this correlation cannot be explained by genetic drift due to population stratification, which is expected to result in an opposite pattern, namely an increase in PL-He decline with increasing baseline PL-He. The correlation seemed to occur independently of BTB status, considering that it was also significant among BTB-negative individuals from herds with a BTB prevalence lower than 10% (ρ = 0.72; Prandomization = 0.0039; nherds = 6, nLBC = 55, nHBC = 38). Furthermore, the correlation was significantly stronger than the correlation in the model, wherein allele frequencies were equalized between the LBC and HBC group in each herd (Prandomization per herd = 0.0057, nherds = 17, nLBC = 178, nHBC = 90). Because inbreeding and genetic drift due to population stratification cannot explain the differences in PL-He between the LBC and the HBC group, the most likely explanation is that LD with expressed genes is the cause (local effects hypothesis).


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.

van Hooft P, Greyling BJ, Getz WM, van Helden PD, Zwaan BJ, Bastos AD - PLoS ONE (2014)

Correlation between LBC-minus-HBC group difference in PL-He and baseline PL-He.Baseline PL-He (expected heterozygosity per locus): PL-He of the pooled group of LBC and HBC individuals, error bars: 95% CI, vertical axis: 2(SE2LBC + SE2HBC)0.5, horizontal axis: 2SE; Spearman rank correlation coefficient: ρ = 0.80, nLBC = 230, nHBC = 90, nmicrosatellites = 17, Prandomization between body condition classes = 0.00034. Data are from southern Kruger. This figure shows that it was the microsatellites with low baseline PL-He (<0.56) that were associated with effects on body condition, i.e. a relatively large PL-He decrease in the LBC (low body condition) group relative to the HBC (high body condition) group. The positive correlation indicates that the HFCs (heterozygosity-fitness correlations) in southern Kruger can only be explained by LD between microsatellites and expressed genes.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4221135&req=5

pone-0111778-g001: Correlation between LBC-minus-HBC group difference in PL-He and baseline PL-He.Baseline PL-He (expected heterozygosity per locus): PL-He of the pooled group of LBC and HBC individuals, error bars: 95% CI, vertical axis: 2(SE2LBC + SE2HBC)0.5, horizontal axis: 2SE; Spearman rank correlation coefficient: ρ = 0.80, nLBC = 230, nHBC = 90, nmicrosatellites = 17, Prandomization between body condition classes = 0.00034. Data are from southern Kruger. This figure shows that it was the microsatellites with low baseline PL-He (<0.56) that were associated with effects on body condition, i.e. a relatively large PL-He decrease in the LBC (low body condition) group relative to the HBC (high body condition) group. The positive correlation indicates that the HFCs (heterozygosity-fitness correlations) in southern Kruger can only be explained by LD between microsatellites and expressed genes.
Mentions: The PL-He decrease in the LBC group from southern Kruger (relative to the HBC group) declined with increasing baseline PL-He (Spearman rank correlation coefficient (ρ) = 0.80; Prandomization = 0.00034, nLBC = 230, nHBC = 90; northern Kruger: Prandomization = 0.53, nLBC = 68, nHBC = 70; Figure 1). As discussed above, this correlation cannot be explained by genetic drift due to population stratification, which is expected to result in an opposite pattern, namely an increase in PL-He decline with increasing baseline PL-He. The correlation seemed to occur independently of BTB status, considering that it was also significant among BTB-negative individuals from herds with a BTB prevalence lower than 10% (ρ = 0.72; Prandomization = 0.0039; nherds = 6, nLBC = 55, nHBC = 38). Furthermore, the correlation was significantly stronger than the correlation in the model, wherein allele frequencies were equalized between the LBC and HBC group in each herd (Prandomization per herd = 0.0057, nherds = 17, nLBC = 178, nHBC = 90). Because inbreeding and genetic drift due to population stratification cannot explain the differences in PL-He between the LBC and the HBC group, the most likely explanation is that LD with expressed genes is the cause (local effects hypothesis).

Bottom Line: Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in selective constraints.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.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.

View Article: PubMed Central - PubMed

Affiliation: Resource Ecology Group, Wageningen University, Wageningen, The Netherlands; Mammal Research Institute, Department of Zoology & Entomology, University of Pretoria, Hatfield, South Africa.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus