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Rainfall-driven sex-ratio genes in African buffalo suggested by correlations between Y-chromosomal haplotype frequencies and foetal sex ratio.

van Hooft P, Prins HH, Getz WM, Jolles AE, van Wieren SE, Greyling BJ, van Helden PD, Bastos AD - BMC Evol. Biol. (2010)

Bottom Line: Frequencies varied by a factor of five; too high to be alternatively explained by Y-chromosomal effects on pregnancy loss.Both wet and dry periods were associated with a specific haplotype indicating a SR distorter and SR suppressor, respectively.SR genes may play a broader and largely overlooked role in mammalian sex-ratio variation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Resource Ecology Group, Wageningen University, 6708 PB Wageningen, The Netherlands. pim.vanhooft@wur.nl

ABSTRACT

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.

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Related in: MedlinePlus

Mean monthly foetal sex ratios. Green bars: wet season, Yellow bars: dry season, Error bars: 90% CI. Sample size is given in brackets. Monthly data are pooled across years (1978-1998).
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Figure 3: Mean monthly foetal sex ratios. Green bars: wet season, Yellow bars: dry season, Error bars: 90% CI. Sample size is given in brackets. Monthly data are pooled across years (1978-1998).

Mentions: If haplotypes 112 and 557 are linked to SR distorters or SR suppressors then one would expect an alternating seasonal pattern with sex ratios (male proportion) as well, which was indeed observed (Figure 2). In the same age cohorts as were used in the genetic analyses the sex ratio was higher among individuals conceived during the wet seasons than among those conceived during the dry seasons (Pexact = 0.096, n = 291; calves culled in 1998 plus foetuses collected in 1996). There was an identical pattern in earlier age cohorts. Among 0-4 months old calves culled between June 1982 and February 1983, the sex ratio was only 0.27 (8/30) among those conceived in the dry season of 1981 (culled in June-November) but as high as 0.69 (9/13) among those conceived in the subsequent wet season (culled in January-February) (Pexact = 0.016) [33]. Most importantly, a significant seasonal difference in sex ratio, with an effect size of 0.045 (absolute difference between two sex ratios), was observed among the foetuses collected between 1978 and 1998 (Figure 3 and Table 1; Pexact = 0.025; data pooled across years). The sex ratio was female-biased during the dry season (PWilsonscore = 0.049, one-sided) and male-biased during the wet season (PWilsonscore = 0.056, one-sided). The largest difference was observed at the change of seasons between March and April. The seasonal difference in sex ratio was already present among foetuses ≤ 4 months old (Table 1; Pexact = 0.035; data pooled across years), ruling out late-term foetal loss as an explanation.


Rainfall-driven sex-ratio genes in African buffalo suggested by correlations between Y-chromosomal haplotype frequencies and foetal sex ratio.

van Hooft P, Prins HH, Getz WM, Jolles AE, van Wieren SE, Greyling BJ, van Helden PD, Bastos AD - BMC Evol. Biol. (2010)

Mean monthly foetal sex ratios. Green bars: wet season, Yellow bars: dry season, Error bars: 90% CI. Sample size is given in brackets. Monthly data are pooled across years (1978-1998).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2875233&req=5

Figure 3: Mean monthly foetal sex ratios. Green bars: wet season, Yellow bars: dry season, Error bars: 90% CI. Sample size is given in brackets. Monthly data are pooled across years (1978-1998).
Mentions: If haplotypes 112 and 557 are linked to SR distorters or SR suppressors then one would expect an alternating seasonal pattern with sex ratios (male proportion) as well, which was indeed observed (Figure 2). In the same age cohorts as were used in the genetic analyses the sex ratio was higher among individuals conceived during the wet seasons than among those conceived during the dry seasons (Pexact = 0.096, n = 291; calves culled in 1998 plus foetuses collected in 1996). There was an identical pattern in earlier age cohorts. Among 0-4 months old calves culled between June 1982 and February 1983, the sex ratio was only 0.27 (8/30) among those conceived in the dry season of 1981 (culled in June-November) but as high as 0.69 (9/13) among those conceived in the subsequent wet season (culled in January-February) (Pexact = 0.016) [33]. Most importantly, a significant seasonal difference in sex ratio, with an effect size of 0.045 (absolute difference between two sex ratios), was observed among the foetuses collected between 1978 and 1998 (Figure 3 and Table 1; Pexact = 0.025; data pooled across years). The sex ratio was female-biased during the dry season (PWilsonscore = 0.049, one-sided) and male-biased during the wet season (PWilsonscore = 0.056, one-sided). The largest difference was observed at the change of seasons between March and April. The seasonal difference in sex ratio was already present among foetuses ≤ 4 months old (Table 1; Pexact = 0.035; data pooled across years), ruling out late-term foetal loss as an explanation.

Bottom Line: Frequencies varied by a factor of five; too high to be alternatively explained by Y-chromosomal effects on pregnancy loss.Both wet and dry periods were associated with a specific haplotype indicating a SR distorter and SR suppressor, respectively.SR genes may play a broader and largely overlooked role in mammalian sex-ratio variation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Resource Ecology Group, Wageningen University, 6708 PB Wageningen, The Netherlands. pim.vanhooft@wur.nl

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus