Introducing mother's curse: Low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares

Molecular Ecology

Volumn 19, Issue 1, 2010, Pages 36-43

  Smith, Steve ^a   Turbill, Christopher ^a   Suchentrunk, Franz ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

Author keywords

Captive breeding; Mother's curse; MtDNA; Reproductive success

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; DNA SEQUENCE; FEMALE; FERTILITY; GENETIC FITNESS; GENETICS; HAPLOTYPE; HARE; MALE; MALE INFERTILITY; PHYLOGENY; POPULATION GENETICS; SEQUENCE ALIGNMENT;

ANIMALS; DNA, MITOCHONDRIAL; FEMALE; FERTILITY; GENETIC FITNESS; GENETICS, POPULATION; HAPLOTYPES; HARES; INFERTILITY, MALE; MALE; MODELS, GENETIC; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

LEPUS; LEPUS CAPENSIS;

EID: 72849116778     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04444.x     Document Type: Article

References (43)

1. Allendorf FW, Ryman N (2002) The role of genetics in population viability analysis. In : Population Viability Analysis (eds Beissinger SR, McCullough DR). pp. 50 85, University of Chicago Press, Boston.
2. Arnason U, Adegoke JA, Bodin K et al. (2002) Mammalian mitogenomic relationships and the root of the eutherian tree. Proceedings of the National Academy of Sciences of the United States of America, 99, 8151 8156.
3. Avise JC, Arnold J, Ball RM et al. (1987) Intraspecific phylogeography - the mitochondrial-dna bridge between population-genetics and systematics. Annual Review of Ecology and Systematics, 18, 489 522.
4. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Molecular Ecology, 13, 729 744.
5. Ben Slimen H, Suchentrunk F, Shahin AB, Elgaaied ABA (2007) Phylogenetic analysis of mtCR-1 sequences of Tunisian and Egyptian hares (Lepus sp or spp., Lagomorpha) with different coat colours. Mammalian Biology, 72, 224 239.
6. Burton RS, Ellison CK, Harrison JS (2006) The Sorry State of F2 Hybrids: consequences of rapid mitochondrial DNA evolution in allopatric populations. The American Naturalist, 168, S14 S24.
7. Carra E, Sangiorgi D, Gattuccio F, Rinaldi AM (2004) Male infertility and mitochondrial DNA. Biochemical and Biophysical Research Communications, 322, 333 339.
8. Chinnery PF, Thorburn DR, Samuels DC et al. (2000) The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends in Genetics, 16, 500 505.
9. Clement M, Posada D, Crandall KA (2000) TCS: A computer program to estimate gene genealogies. Molecular Ecology, 9, 1657 1659.
10. Cummins J (1998) Mitochondrial DNA in mammalian reproduction. Review of Reproduction, 3, 172 182.
11. Diez-Sanchez C, Ruiz-Pesini E, Lapena AC et al. (2003) Mitochondrial DNA content of human spermatozoa. Biology of Reproduction, 68, 180 185.
12. Dowling DK, Friberg U, Arnqvist G (2007a) A comparison of nuclear and cytoplasmic genetic effects on sperm competitiveness and female remating in a seed beetle. Journal of Evolutionary Biology, 20, 2113 2125.
13. Dowling DK, Nowostawski AL, Arnqvist G (2007b) Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory? Journal of Evolutionary Biology, 20, 358 368.
14. Dowling DK, Friberg U, Lindell J (2008) Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology & Evolution, 23, 546.
15. Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Molecular Ecology, 16, 463 475.
16. Ellison CK, Burton RS (2008) Interpopulation hybrid breakdown maps to the mitochondrial genome. Evolution, 62, 631 638.
17. da Fonseca RR, Johnson WE, O'Brien SJ, Ramos MJ, Antunes A (2008) The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics, 9, 119.
18. Friberg U, Dowling DK (2008) No evidence of mitochondrial genetic variation for sperm competition within a population of Drosophila melanogaster. Journal of Evolutionary Biology, 21, 1798 1807.
19. Froman DP, Kirby JD (2005) Sperm mobility: phenotype in roosters (Gallus domesticus) determined by mitochondrial function. Biology of Reproduction, 72, 562 567.
20. Froman DP, Feltmann AJ, Rhoads ML, Kirby JD (1999) Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus). Biology of Reproduction, 61, 400 405.
21. Gemmell NJ, Metcalf VJ, Allendorf FW (2004) Mother's curse: the effect of mtDNA on individual fitness and population viability. Trends in Ecology & Evolution, 19, 238.
22. Grantham R (1974) Amino acid difference formula to help explain protein evolution. Science, 185, 862 864.
23. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 9598NT. Nucleic Acids Symposium Series, 41, 95 98.
24. Hartl GB, Vodnansky M, Suchentrunk F, Steineck T, Willing R, Tataruch F, Oberwalder U (1991) Fortpflanzungsstörungen in einer Feldhasenzucht - Folge einer Inzuchtdepression Verhandlungsbericht über die Erkrankungender Zoo - und Wildtiere, 33, 17 26.
25. Holyoake AJ, Sin IL, Benny PS, Sin FYT (1999) Association of a novel human mtDNA ATPase6 mutation with immature sperm cells. Andrologia, 31, 339 345.
26. Holyoake AJ, McHugh P, Wu M et al. (2001) High incidence of single nucleotide substitutions in the mitochondrial genome is associated with poor semen parameters in men. International Journal Of Andrology, 24, 175 182.
27. Kasapidis P, Suchentrunk F, Magoulas A, Kotoulas G (2005) The shaping of mitochondrial DNA phylogeographic patterns of the brown hare (Lepus europaeus) under the combined influence of Late Pleistocene climatic fluctuations and anthropogenic translocations. Molecular Phylogenetics And Evolution, 34, 55 66.
28. Liau WS, Gonzalez-Serricchio AS, Deshommes C, Chin K, LaMunyon CW (2007) A persistent mitochondrial deletion reduces fitness and sperm performance in heteroplasmic populations of C. elegans. BMC Genetics, 8, 8.
29. Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution, 45, 622 629.
30. Moore F, Reijo-Pera R (2000) Male sperm motility dictated by mother's mtDNA. American Journal of Human Genetics, 67, 543 548.
31. Pereira L, Goncalves J, Franco-Duarte R et al. (2007) No evidence for an mtdna role in sperm motility: data from complete sequencing of asthenozoospermic males. Molecular Biology and Evolution, 24, 868 874.
32. Pierpaoli M, Riga F, Trocchi V, Randi E (1999) Species distinction and evolutionary relationships of the Italian hare (Lepus corsicanus) as described by mitochondrial DNA sequencing. Molecular Ecology, 8, 1805 1817.
33. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817 818.
34. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572 1574.
35. Ruiz-Pesini E, Diez C, Lapena AC et al. (1998) Correlation of sperm motility with mitochondrial enzymatic activities. Clinical Chemistry, 44, 1616 1620.
36. Ruiz-Pesini E, Lapena AC, Diez-Sanchez C et al. (2000) Human mtDNA haplogroups associated with high or reduced spermatozoa motility. American Journal of Human Genetics, 67, 682 696.
37. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science, 303, 223 226.
38. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 57, 758 771.
39. Stamatis C, Suchentrunk F, Moutou KA et al. (2009) Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south-eastern Mediterranean refugia? Journal of Biogeography, 36, 515 528.
40. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends in Ecology & Evolution, 19, 489 496.
41. Wade MJ, Brandvain Y (2009) Reversing mother's curse: selection on mitochondrial fitness effects. Evolution, 63, 1084 1089.
42. Willett CS, Burton RS (2001) Viability of cytochrome C genotypes depends on cytoplasmic backgrounds in Tigriopus californicus. Evolution, 55, 1592 1599.
43. Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology, 17, 2107 2121.