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Open Access Highly Accessed Research article

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

Pim van Hooft12*, Herbert HT Prins1, Wayne M Getz23, Anna E Jolles4, Sipke E van Wieren1, Barend J Greyling25, Paul D van Helden6 and Armanda DS Bastos2

Author Affiliations

1 Resource Ecology Group, Wageningen University, Droevendaalsesteeg 3a, 6708 PB Wageningen, The Netherlands

2 Mammal Research Institute, Department of Zoology & Entomology, University of Pretoria, Pretoria 0002, South Africa

3 Department of Environmental Science Policy & Management, University of California at Berkeley, 140 Mulford Hall, CA 94720-3112, USA

4 Department of Biomedical Sciences, College of Veterinary Medicine, Oregon State University, Corvallis OR 97331, USA

5 Agricultural Research Council, Irene 0062, South Africa

6 DST/NRF Centre of Excellence for Biomedical TB Research, US/MRC Centre for Molecular and Cellular Biology, Division of Molecular Biology and Human Genetics, Faculty of Health Sciences, Stellenbosch University, Tygerberg 7505, South Africa

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BMC Evolutionary Biology 2010, 10:106  doi:10.1186/1471-2148-10-106

Published: 23 April 2010

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.