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

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Van Hooft, Pim ^a,b   Prins, Herbert Ht ^a   Getz, Wayne M ^b,c   Jolles, Anna E ^d   Van Wieren, Sipke E ^a   Greyling, Barend J ^b,e   Van Helden, Paul D ^f   Bastos, Armanda Ds ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d OREGON STATE UNIVERSITY   (United States)

^e AGRICULTURAL RESEARCH COUNCIL   (South Africa)

^f UNIVERSITY OF STELLENBOSCH   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME; FITNESS; GENE FLOW; GENETIC ANALYSIS; GENETICS; GENOTYPE; POPULATION DYNAMICS; RAINFALL; RUMINANT; SEX RATIO;

MAMMALIA; SYNCERUS CAFFER;

MICROSATELLITE DNA;

ANIMAL; ARTICLE; BUFFALO; CLIMATE; FEMALE; FETUS; GENETICS; HAPLOTYPE; MALE; METABOLISM; SEX RATIO; SOUTH AFRICA; Y CHROMOSOME;

ANIMALS; BUFFALOES; CLIMATE; FEMALE; FETUS; HAPLOTYPES; MALE; MICROSATELLITE REPEATS; SEX RATIO; SOUTH AFRICA; Y CHROMOSOME;

EID: 77951129697     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-106     Document Type: Article

References (61)

1. Sex chromosome meiotic drive. J Jaenike, Annu Rev Ecol Syst 2001 32 25 49 10.1146/annurev.ecolsys.32.081501.113958 (Pubitemid 34043155)
2. Haploid selection in animals. SB Joseph M Kirkpatrick, Trends Ecol Evol 2004 19 11 592 597 10.1016/j.tree.2004.08.004
3. Transmission ratio distortion in mice. MF Lyon, Annu Rev Genet 2003 37 393 408 10.1146/annurev.genet.37.110801.143030 14616067
4. Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells. KC Kleene, Dev Biol 2005 277 1 16 26 10.1016/j.ydbio.2004.09.031 15572136
5. Selfish genetic elements and sexual selection: their impact on male fertility. TAR Price N Wedell, Genetica 2008 132 3 295 307 10.1007/s10709-007- 9173-2 17647082
6. Suppression of sex-ratio meiotic drive and the maintenance of Y-chromosome polymorphism in Drosophila. J Jaenike, Evolution 1999 53 1 164 174 10.2307/2640929
7. A sex-ratio meiotic drive system in Drosophila simulans. I: an autosomal suppressor. Y Tao JP Masly L Araripe Y Ke DL Hartl, PLoS Biol 2007 5 11 2560 2575 (Pubitemid 350276930)
8. Distorted sex ratios: a window into RNAi-mediated silencing. PM Ferree DA Barbash, PLoS Biol 2007 5 11 2453 2457 10.1371/journal.pbio.0050303 (Pubitemid 350276920)
9. Truncated RanGAP encoded by the segregation distorter locus of Drosophila. C Merrill L Bayraktaroglu A Kusano B Ganetzky, Science 1999 283 5408 1742 1745 10.1126/science.283.5408.1742 10073941
10. Sex-ratio meiotic drive in Drosophila simulans : cellular mechanism, candidate genes and evolution. C Montchamp-Moreau, Biochem Soc Trans 2006 34 562 565 10.1042/BST0340562 16856861
11. A single gene causes both male sterility and segregation distortion in Drosophila hybrids. N Phadnis HA Orr, Science 2009 323 5912 376 379 10.1126/science.1163934 19074311
12. A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. Y Tao L Araripe SB Kingan Y Ke H Xiao DL Hartl, PLoS Biol 2007 5 11 2576 2588 (Pubitemid 350276931)
13. Natural selection and Y-linked polymorphism. AG Clark, Genetics 1987 115 3 569 577 3569883
14. Two tests of Y chromosomal variation in male fertility of Drosophila melanogaster. AG Clark, Genetics 1990 125 3 527 534 2116355
15. Protecting haploid polymorphisms in temporally variable environments. AM Dean, Genetics 2005 169 2 1147 1156 10.1534/genetics.104.036053 15545644
16. Evolutionary ecology of the prezygotic stage. G Bernasconi TL Ashman TR Birkhead JDD Bishop U Grossniklaus E Kubli DL Marshall B Schmid I Skogsmyr RR Snook D Taylor I Till-Bottraud PI Ward DW Zeh B Hellriegel, Science 2004 303 5660 971 975 10.1126/science.1092180 14963320
17. Sex ratio distorter reduces sperm competitive ability in an insect. TAR Price AJ Bretman TD Avent RR Snook GDD Hurst N Wedell, Evolution 2008 62 7 1644 1652 10.1111/j.1558-5646.2008.00386.x 18373627
18. The Y chromosomes of Drosophila simulans are highly polymorphic for their ability to suppress sex-ratio drive. C Montchamp-Moreau V Ginhoux A Atlan, Evolution 2001 55 4 728 737 10.1554/0014-3820(2001)055[0728:TYCODS]2.0.CO;2 11392391
19. Polymorphism for Y-linked suppressors of sex-ratio in two natural populations of Drosophila mediopunctata. AB Carvalho SC Vaz LB Klaczko, Genetics 1997 146 3 891 902 9215895
20. Sperm competition and the dynamics of X chromosome drive: Stability and extinction. JE Taylor J Jaenike, Genetics 2002 160 4 1721 1731 11973324
21. Meiotic drive and sex chromosome cycling. DW Hall, Evolution 2004 58 5 925 931 15212373
22. Evaluation of population effects of bovine tuberculosis in free-ranging African buffalo (Syncerus caffer). TC Rodwell IJ Whyte WM Boyce, J Mammal 2001 82 1 231 238 10.1644/1545-1542(2001)082<0231:EOPEOB>2.0.CO;2
23. Kruger NP buffalo census. I Whyte, Gnusletter 2005 24 2 14 16
24. Disentangling association patterns in fission-fusion societies using African buffalo as an example. PC Cross JO Lloyd-Smith WM Getz, Anim Behav 2005 69 499 506 10.1016/j.anbehav.2004.08.006 (Pubitemid 40084849)
25. Ecology and behaviour of the African buffalo: Social inequality and decision making. HHT Prins, London: Chapman and Hall 1996
26. Ecological cues, gestation length, and birth timing in African buffalo (Syncerus caffer). SJ Ryan CU Knechtel WM Getz, Behav Ecol 2007 18 4 635 644 10.1093/beheco/arm028 (Pubitemid 47216475)
27. Environmental and maternal correlates of foetal sex ratios in the African buffalo (Syncerus caffer) and savanna elephant (Loxodonta africana). DR Visscher RJ van Aarde I Whyte, J Zool 2004 264 111 116 10.1017/S0952836904005436 (Pubitemid 39384574)
28. The genetical theory of natural selection. RA Fisher, Oxford: Claredon Press 1930
29. Selection at the Y chromosome of the African buffalo driven by rainfall. P van Hooft BJ Greyling HHT Prins WM Getz AE Jolles ADS Bastos, PLoS ONE 2007 10.1371/journal.pone.0001086(10) 17971851
30. Maternal and paternal genealogy of Eurasian taurine cattle (Bos taurus). J Kantanen CJ Edwards DG Bradley H Viinalass S Thessler Z Ivanova T Kiselyova M Cinkulov R Popov S Stojanovic I Ammosov J Vilkki, Heredity 2009 103 5 404 415 10.1038/hdy.2009.68 19603063
31. Microsatellite analysis of genetic diversity in African buffalo (Syncerus caffer) populations throughout Africa. WF van Hooft AF Groen HHT Prins, Mol Ecol 2000 9 12 2017 2025 10.1046/j.1365-294X.2000.01101.x 11123614
32. Assessing vaccination as a control strategy in an ongoing epidemic: Bovine tuberculosis in African buffalo. PC Cross WM Getz, Ecol Model 2006 196 3-4 494 504 10.1016/j.ecolmodel.2006.02.009
33. Sex and age data from cropping of buffalo Syncerus caffer in the Kruger National Park. DR Mason, Koedoe 1984 27 73 78
34. Microsatellite analysis of genetic diversity in fragmented South African buffalo populations. C O'Ryan EH Harley MW Bruford M Beaumont RK Wayne MI Cherry, Animal Conservation 1998 1 2 85 94 10.1111/j.1469-1795.1998.tb00015.x
35. Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. WH James, J Endocrinol 2008 198 1 3 15 10.1677/JOE-07-0446 18577567
36. Some comments on the paper of Grant (2007). WH James, J Theor Biol 2008 253 2 401 404 10.1016/j.jtbi.2008.03.014 18455193
37. Consequences for the bovine embryo of being derived from a spermatozoon subjected to post-ejaculatory aging and heat shock: development to the blastocyst stage and sex ratio. KEM Hendricks L Martins PJ Hansen, J Reprod Dev 2009 55 1 69 74 10.1262/jrd.20097 18957823
38. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. M Perez-Crespo B Pintado A Gutierrez-Adan, Mol Reprod Dev 2008 75 1 40 47 10.1002/mrd.20759 17474098
39. Y chromosome polymorphism is a strong determinant of male fitness in Drosophila melanogaster. AK Chippindale WR Rice, Proc Natl Acad Sci USA 2001 98 10 5677 5682 10.1073/pnas.101456898 11320221
40. Mitochondrial DNA and the Y chromosome: parallels and paradoxes. J Cummins, Reprod Fertil Dev 2001 13 7-8 533 542 10.1071/RD01064 11999303
41. The human Y chromosome: function, evolution and disease. L Quintana-Murci C Krausz K McElreavey, Forensic SciInt 2001 118 2-3 169 181 10.1016/S0379-0738(01)00387-5 (Pubitemid 32331908)
42. The Y chromosome as a battle ground for sexual selection. ERS Roldan M Gomendio, Trends Ecol Evol 1999 14 2 58 62 10.1016/S0169-5347(98)01567-5 10234253
43. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. H Skaletsky T Kuroda-Kawaguchi PJ Minx HS Cordum L Hillier LG Brown S Repping T Pyntikova J Ali T Bieri A Chinwalla A Delehaunty K Delehaunty H Du G Fewell L Fulton R Fulton T Graves SF Hou P Latrielle S Leonard E Mardis R Maupin J McPherson T Miner W Nash C Nguyen P Ozersky K Pepin S Rock T Rohlfing K Scott B Schultz C Strong A Tin-Wollam SP Yang RH Waterston RK Wilson S Rozen DC Page, Nature 2003 423 6942 825 U822 10.1038/nature01722 12815422
44. Polymorphic Y chromosomes harbor cryptic variation with manifold functional consequences. B Lemos LO Araripe DL Hartl, Science 2008 319 5859 91 93 10.1126/science.1148861 18174442
45. Impact of season on seminal characteristics and endocrine status of adult free-ranging African buffalo (Syncerus caffer). JL Brown DE Wildt JR Raath V Devos JG Howard DL Janssen SB Citino M Bush, J Reprod Fertil 1991 92 1 47 57 1905353
46. Collection frequency affects percent Y-chromosome bearing sperm, sperm head area and quality of bovine ejaculates. JE Chandler AM Canal JB Paul EB Moser, Theriogenology 2002 57 4 1327 1346 10.1016/S0093-691X(01)00721-X 12013453
47. Male fertility and sex ratio at birth in red deer. M Gomendio AF Malo AJ Soler MR Fernandez-Santos MC Esteso AJ Garcia ERS Roldan J Garde, Science 2006 314 5804 1445 1447 10.1126/science.1133064 17138900
48. Panax ginseng improves survival and sperm quality in guinea pigs exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. SY Hwang WJ Kim JJ Wee JS Choi SK Kim, BJU International 2004 94 4 663 668 10.1111/j.1464-410X.2004.05019.x 15329132
49. Experimental demonstration that pre- and post-conceptional mechanisms influence sex ratio in mouse embryos. A Jimenez R Fernandez N Madrid-Bury PN Moreira C Borque B Pintado A Gutierrez-Adan, Mol Reprod Dev 2003 66 2 162 165 10.1002/mrd.10345 12950103
50. Decline in sex ratio at birth after 10-day war in Slovenia. B Zorn V Sucur J Stare H Meden-Vrtovec, Hum Reprod 2002 17 12 3173 3177 10.1093/humrep/17.12.3173 12456620
51. Sperm traits and male fertility in natural populations. M Gomendio AF Malo J Garde ERS Roldan, Reproduction 2007 134 1 19 29 10.1530/REP-07-0143 17641085
52. A review of nutritional influences on reproduction in boars, bulls and rams. BW Brown, Reprod Nutr Dev 1994 34 2 89 114 10.1051/rnd:19940201 8179818
53. Correlates of survival rates for 10 African ungulate populations: density, rainfall and predation. N Owen-Smith DR Mason JO Ogutu, J Anim Ecol 2005 74 4 774 788 10.1111/j.1365-2656.2005.00974.x (Pubitemid 41576946)
54. Prevalence of bovine tuberculosis in African buffalo at Kruger National Park. TC Rodwell NP Kriek RG Bengis IJ Whyte PC Viljoen V de Vos WM Boyce, J Wildl Dis 2001 37 2 258 264 11310876
55. Study of fetal sex determination based on external genitalia and gonadal differentiation in water buffalos. R Ranjbar SH Rashidi N Alboghobeish RA Sadrkhanloo Y Mazaheri, Internet J Vet Med 2007 3
56. Ultrasonographic fetometry and determination of fetal sex in buffaloes (Bubalus bubalis). A Ali S Fahmy, Anim Reprod Sci 2008 106 1-2 90 99 10.1016/j.anireprosci.2007.04.010 17544605
57. Growth of fetal calf and its arterial pressure, blood gases and hematologic data. JT Reeves M Gentry FS Daoud, J Appl Physiol 1972 32 2 240 244 5061739
58. Histo-morphology of the uterus and early placenta of the African buffalo (Syncerus caffer) and comparative placentome morphology of the African buffalo and cattle (Bos taurus). S Schmidt D Gerber JT Soley TA Aire A Boos, Placenta 2006 27 8 899 911 10.1016/j.placenta.2005.09.008 16293303
59. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995). J Goudet, 2001
60. FSTAT (Version 1.2): A computer program to calculate F-statistics. J Goudet, J Hered 1995 86 6 485 486
61. Interval estimation for a binomial proportion - Comment - Rejoinder. LD Brown TT Cai A DasGupta A Agresti BA Coull G Casella C Corcoran C Mehta M Ghosh TJ Santner LD Brown TT Cai A DasGupta, Stat Sci 2001 16 2 101 133