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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.Apparently, this sex-ratio suppressor prevents fertility reduction that generally accompanies sex-ratio distortion.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.

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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Allele clines in Kruger for two classes of microsatellites.Allele frequencies were averaged across individuals and across microsatellites. Black diamonds: average majority allele frequency per herd, Z = 3.51, PStouffer-Z = 0.00044, nmicrosatellites = 8, ρ = −0.60, nherds = 30, nindividuals = 459; grey diamonds: average frequency per herd of the pooled three most frequent alleles per microsatellite (microsatellites without majority allele), Z = 3.58, PStouffer-Z = 0.00034, nmicrosatellites = 9, ρ = −0.52, nherds = 30, nindividuals = 459, latitude <−24: southern Kruger. Allele clines with increasing frequencies going from north to south were observed for all eight autosomal microsatellites with a majority allele and eight out of nine autosomal microsatellites without a majority allele. These allele clines are indicative of positive selection.
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pone-0111778-g005: Allele clines in Kruger for two classes of microsatellites.Allele frequencies were averaged across individuals and across microsatellites. Black diamonds: average majority allele frequency per herd, Z = 3.51, PStouffer-Z = 0.00044, nmicrosatellites = 8, ρ = −0.60, nherds = 30, nindividuals = 459; grey diamonds: average frequency per herd of the pooled three most frequent alleles per microsatellite (microsatellites without majority allele), Z = 3.58, PStouffer-Z = 0.00034, nmicrosatellites = 9, ρ = −0.52, nherds = 30, nindividuals = 459, latitude <−24: southern Kruger. Allele clines with increasing frequencies going from north to south were observed for all eight autosomal microsatellites with a majority allele and eight out of nine autosomal microsatellites without a majority allele. These allele clines are indicative of positive selection.

Mentions: Positive selection of deleterious and sexually antagonistic alleles was strongly supported by the observation of an allele cline at 16 of the 17 microsatellites, with frequencies increasing in a north-south direction. Allele clines are generally considered as a strong indicator of positive selection [36]–[38]. All eight majority microsatellite alleles showed a negative Spearman rank correlation with latitude (Z = 3.51, PStouffer-Z = 0.00044, nmicrosatellites = 8; Table S9, Figure 5). They increased in frequency from around 0.67 in the far north to around 0.74 in the far south. Allele clines were also observed at the remaining microsatellites (baseline PL-He >0.75) when the three most frequent alleles per locus were pooled. This pooling assumes that these frequent alleles, considering the relatively large positive effect size for most of them (21 out of 27 alleles with frequencies ≥0.125 showed a positive effect size; Figure 4), are much more likely to be linked to a sexually antagonistic allele than the remaining less frequent alleles. Because of this linkage, these microsatellite alleles may to a large extent behave as a single allele. Indeed, eight of the nine pooled alleles showed a negative Spearman rank correlation with latitude (Z = 3.58, PStouffer-Z = 0.00034, nmicrosatellites = 9; Table S10, Figure 5). The significance of the latter result cannot be explained by a negative bias on the P-value because of LD among three of the microsatellites, considering that the correlation between latitude and the ‘average allele frequency across loci’ (after pooling within loci) was also highly significant (ρ = −0.52, P = 0.0030, nherds = 30). The pooled alleles increased in frequency from around 0.56 in the far north to around 0.64 in the far south.


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)

Allele clines in Kruger for two classes of microsatellites.Allele frequencies were averaged across individuals and across microsatellites. Black diamonds: average majority allele frequency per herd, Z = 3.51, PStouffer-Z = 0.00044, nmicrosatellites = 8, ρ = −0.60, nherds = 30, nindividuals = 459; grey diamonds: average frequency per herd of the pooled three most frequent alleles per microsatellite (microsatellites without majority allele), Z = 3.58, PStouffer-Z = 0.00034, nmicrosatellites = 9, ρ = −0.52, nherds = 30, nindividuals = 459, latitude <−24: southern Kruger. Allele clines with increasing frequencies going from north to south were observed for all eight autosomal microsatellites with a majority allele and eight out of nine autosomal microsatellites without a majority allele. These allele clines are indicative of positive selection.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4221135&req=5

pone-0111778-g005: Allele clines in Kruger for two classes of microsatellites.Allele frequencies were averaged across individuals and across microsatellites. Black diamonds: average majority allele frequency per herd, Z = 3.51, PStouffer-Z = 0.00044, nmicrosatellites = 8, ρ = −0.60, nherds = 30, nindividuals = 459; grey diamonds: average frequency per herd of the pooled three most frequent alleles per microsatellite (microsatellites without majority allele), Z = 3.58, PStouffer-Z = 0.00034, nmicrosatellites = 9, ρ = −0.52, nherds = 30, nindividuals = 459, latitude <−24: southern Kruger. Allele clines with increasing frequencies going from north to south were observed for all eight autosomal microsatellites with a majority allele and eight out of nine autosomal microsatellites without a majority allele. These allele clines are indicative of positive selection.
Mentions: Positive selection of deleterious and sexually antagonistic alleles was strongly supported by the observation of an allele cline at 16 of the 17 microsatellites, with frequencies increasing in a north-south direction. Allele clines are generally considered as a strong indicator of positive selection [36]–[38]. All eight majority microsatellite alleles showed a negative Spearman rank correlation with latitude (Z = 3.51, PStouffer-Z = 0.00044, nmicrosatellites = 8; Table S9, Figure 5). They increased in frequency from around 0.67 in the far north to around 0.74 in the far south. Allele clines were also observed at the remaining microsatellites (baseline PL-He >0.75) when the three most frequent alleles per locus were pooled. This pooling assumes that these frequent alleles, considering the relatively large positive effect size for most of them (21 out of 27 alleles with frequencies ≥0.125 showed a positive effect size; Figure 4), are much more likely to be linked to a sexually antagonistic allele than the remaining less frequent alleles. Because of this linkage, these microsatellite alleles may to a large extent behave as a single allele. Indeed, eight of the nine pooled alleles showed a negative Spearman rank correlation with latitude (Z = 3.58, PStouffer-Z = 0.00034, nmicrosatellites = 9; Table S10, Figure 5). The significance of the latter result cannot be explained by a negative bias on the P-value because of LD among three of the microsatellites, considering that the correlation between latitude and the ‘average allele frequency across loci’ (after pooling within loci) was also highly significant (ρ = −0.52, P = 0.0030, nherds = 30). The pooled alleles increased in frequency from around 0.56 in the far north to around 0.64 in the far south.

Bottom Line: Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in selective constraints.Apparently, this sex-ratio suppressor prevents fertility reduction that generally accompanies sex-ratio distortion.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.

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