Reduced sperm performance in backcross hybrids between species pairs of whitefish (Coregonus clupeaformis)

Canadian Journal of Zoology

Volumn 87, Issue 7, 2009, Pages 566-572

  Whiteley, A R ^a   Persaud, K N ^b,c   Derome, N ^a   Montgomerie, R ^b   Bernatchez, L ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DIVERGENCE; GROUP BEHAVIOR; HYBRID; PERFORMANCE ASSESSMENT; REPRODUCTIVE ISOLATION; SALMONID; SPAWNING; SPERM; SWIMMING BEHAVIOR;

COREGONUS CLUPEAFORMIS;

EID: 68949114836     PISSN: 00084301     EISSN: None     Source Type: Journal    
DOI: 10.1139/Z09-042     Document Type: Article

References (51)

1. Anderson, M.J., and Dixson, A.F. 2002. Sperm competition: motility and the midpiece in primates. Nature (London), 416(6880): 496. doi:10.1038/416496a. PMID:11932733.
2. Armbruster, P., Bradshaw, W.E., Steiner, A.L., and Holzapfel, C.M. 1999. Evolutionary responses to environmental stress by the pitcher-plant mosquito, Wyeomyia smithii. Heredity, 83(5): 509-519. doi:10.1038/sj.hdy. 6886040. PMID:10620022.
3. Ball, M.A., and Parker, G.A. 1996. Sperm competition games: external fertilization and "adaptive" infertility. J. Theor. Biol. 180(2): 141-150. doi:10.1006/jtbi.1996.0090. PMID:8763365.
4. Bernatchez, L. 2004. Ecological theory of adaptive radiation: an empirical assessment from Coregonine fishes (Salmoniformes). In Evolution illuminated: salmon and their relatives. Edited by A.P. Hendry and S.C. Stearns. Oxford University Press, Oxford.pp. 175-207.
5. Bernatchez, L., and Dodson, J.J. 1990. Allopatric origin of sympatric populations of lake whitefish (Coregonus clupeaformis) as revealed by mitochondrial-DNA restriction analysis. Evolution, 44(5): 1263-1271. doi:10.2307/2409287.
6. Birkhead, T.R., Martínez, J.G., Burke, T., and Froman, D.P. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. Lond. B Biol. Sci. 266: 1759-1764. doi:10.1098/rspb.1999. 0843.
7. Birkhead, T.R., Pellatt, E.J., Brekke, P., Yeates, R., and Castillo- Juarez, H. 2005. Genetic effects on sperm design in the zebra finch. Nature (London), 434(7031): 383-387. doi:10.1038/ nature03374. PMID:15772662.
8. Brideau, N.J., Flores, H.A., Wang, J., Maheshwari, S., Wang, X., and Barbash, D.A. 2006. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science (Washington, D.C.), 314(5803): 1292-1295. doi:10.1126/science. 1133953. PMID:17124320.
9. Burness, G., Casselman, S.J., Schulte-Hostedde, A.I., Moyes, C.D., and Montgomerie, R. 2004. Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav. Ecol. Sociobiol. 56(1): 65-70. doi:10.1007/s00265-003-0752-7.
10. Campbell, D., and Bernatchez, L. 2004. Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21(5): 945-956. doi:10.1093/molbev/msh101. PMID:15014172.
11. Cardullo, R.A., and Baltz, J.M. 1991. Metabolic regulation in mammalian sperm: mitochondrial volume determines sperm length and flagellar beat frequency. Cell Motil. Cytoskeleton, 19(3): 180-188. doi:10.1002/cm. 970190306. PMID:1878988.
12. Casselman, S.J., Schulte-Hostedde, A.I., and Montgomerie, R. 2006. Sperm quality influences male fertilization success in walleye (Sander vitreus). Can. J. Fish. Aquat. Sci. 63(9): 2119- 2125. doi:10.1139/F06-108.
13. Coyne, J.A., and Orr, H.A. 2004. Speciation. Sinauer Associates, Inc., Sunderland, Mass.
14. Derome, N., Duchesne, P., and Bernatchez, L. 2006. Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol. Ecol. 15(5): 1239-1249. doi:10.1111/j.1365-294X. 2005.02968.x. PMID:16626451.
15. Edmands, S. 1999. Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution, 53(6): 1757-1768. doi:10.2307/2640438.
16. Fabricius, E., and Lindroth, A. 1954. Experimental observations on the spawning of whitefish, Coregonus lavaretus L., in the stream aquarium of the Hölle Laboratory at River Indalsälven. Rep. Inst. Freshw. Res. Drottningholm, 35: 105-112.
17. Fenster, C.B., and Galloway, L.F. 2000. Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculata (Fabaceae). Conserv. Biol. 14(5): 1406-1412. doi:10.1046/j.1523-1739.2000.99234.x.
18. Fitzpatrick, J.L., Desjardins, J.K., Milligan, N., Montgomerie, R., and Balshine, S. 2007. Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid. Biol. Reprod. 77(2): 280-284. doi:10.1095/biolreprod.106.059550. PMID:17460159.
19. Fitzpatrick, J.L., Montgomerie, R., Desjardins, J.K., Stiver, K.A., Kolm, N., and Balshine, S. 2009. Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc. Natl. Acad. Sci. U.S.A. 106(4): 1128-1132. doi:10.1073/pnas.0809990106. PMID:19164576.
20. Froman, D.P., Pizzari, T., Feltmann, A.J., Castillo-Juarez, H., and Birkhead, T.R. 2002. Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc. R. Soc. Lond. B Biol. Sci. 269(1491): 607-612. doi:10. 1098/rspb.2001.1925.
21. Gage, M.J.G., Macfarlane, C.P., Yeates, S., Ward, R.G., Searle, J.B., and Parker, G.A. 2004. Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14(1): 44-47. PMID:14711413.
22. Gemmell, N.J., Metcalf, V.J., and Allendorf, F.W. 2004. Mother's curse: the effect of mtDNA on individual fitness and population viability. Trends Ecol. Evol. 19(5): 238-244. doi:10.1016/j.tree. 2004.02.002. PMID:16701262.
23. Gharrett, A.J., Smoker, W.W., Reisenbichler, R.R., and Taylor, S.G. 1999. Outbreeding depression in hybrids between odd- and even-broodyear pink salmon. Aquaculture, 173(1-4): 117-129. doi:10.1016/S0044-8486(98)00480-3.
24. Gomendio, M., and Roldan, E.R.S. 1991. Sperm competition influences sperm size in mammals. Proc. R. Soc. Lond. B Biol. Sci. 243(1308): 181-185. doi:10.1098/rspb.1991.0029.
25. Gow, J.L., Peichel, C.L., and Taylor, E.B. 2007. Ecological selection against hybrids in natural populations of sympatric threespine sticklebacks. J. Evol. Biol. 20(6): 2173-2180. doi:10. 1111/j.1420-9101.2007.01427.x. PMID:17887972.
26. Hatfield, T., and Schluter, D. 1999. Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution, 53(3): 866-873. doi:10.2307/2640726.
27. Hoysak, D.J., and Liley, N.R. 2001. Fertilization dynamics in sockeye salmon and a comparison of sperm from alternative male phenotypes. J. Fish Biol. 58(5): 1286-1300. doi:10.1111/j.1095-8649.2001.tb02286.x.
28. Landry, L., Vincent, W.F., and Bernatchez, L. 2007. Parallel evolution of lake whitefish dwarf ecotypes in association with limnological features of their adaptive landscape. J. Evol. Biol. 20(3): 971-984. doi:10.1111/j.1420-9101.2007.01304.x. PMID:17465908.
29. Levitan, D.R. 2000. Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc. R. Soc. Lond. B Biol. Sci. 267(1443): 531-534. doi:10.1098/rspb.2000. 1032.
30. Lu, G., and Bernatchez, L. 1998. Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis). Proc. R. Soc. Lond. B Biol. Sci. 265(1400): 1025-1030. doi:10.1098/rspb.1998.0394.
31. Lu, G.Q., and Bernatchez, L. 1999. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution, 53(5): 1491-1505. doi:10.2307/2640895.
32. Lu, G., Basley, D.J., and Bernatchez, L. 2001. Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridization between lineages of lake whitefish (Coregonus clupeaformis); relevance for speciation. Mol. Ecol. 10(4): 965-985.doi:10.1046/j.1365-294X.2001.01252. x. PMID:11348504.
33. Ludlow, A.M., and Magurran, A.E. 2006. Gametic isolation in guppies (Poecilia reticulata). Proc. R. Soc. Lond. B Biol. Sci. 273(1600): 2477-2482. doi:10.1098/rspb.2006.3605.
34. Malo, A.F., Garde, J.J., Soler, A.J., García, A.J., Gomendio, M., and Roldan, E.R.S. 2005. Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol. Reprod. 72(4): 822-829. doi:10.1095/biolreprod.104.036368. PMID:15576823.
35. Marr, A.B., Keller, L.F., and Arcese, P. 2002. Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution, 56(1): 131-142. PMID:11913658.
36. Marshall, T.C., and Spalton, J.A. 2000. Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Anim. Conserv. 3(3): 241-248. doi:10.1111/j.1469-1795.2000.tb00109.x.
37. Montgomerie, R., and Fitzpatrick, J.L. 2009. Testes, sperm, and sperm competition. In Reproductive biology and phylogeny of fishes (agnathans and bony fishes). Part B. Edited by B.G.M. Jamieson. Science Publishers, Enfield, N.H. pp. 1-56.
38. Pigeon, D., Chouinard, A., and Bernatchez, L. 1997. Multiple modes of speciation involved in the parallel evolution of sympatric morphotypes of lake whitefish (Coregonus clupeaformis, Salmonidae). Evolution, 51(1): 196-205. doi:10.2307/2410973.
39. Rogers, S.M., and Bernatchez, L. 2005. Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Mol. Ecol. 14(2): 351-361. doi:10.1111/j.1365-294X.2004.02396.x. PMID:15660930.
40. Rogers, S.M., and Bernatchez, L. 2006. The genetic basis of intrinsic and extrinsic post-zygotic reproductive isolation jointly promoting speciation in the lake whitefish species complex (Coregonus clupeaformis). J. Evol. Biol. 19(6): 1979-1994.doi:10.1111/j.1420-9101.2006.01150.x. PMID:17040396.
41. Rogers, S.M., and Bernatchez, L. 2007. The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs. Mol. Biol. Evol. 24(6): 1423-1438. doi:10.1093/ molbev/msm066. PMID:17404398.
42. Rogers, S.M., Gagnon, V., and Bernatchez, L. 2002. Genetically based phenotype-environment association for swimming behavior in lake whitefish ecotypes (Coregonus clupeaformis Mitchill). Evolution, 56(11): 2322-2329. PMID:12487361.
43. Rudolfsen, G., Muller, R., Urbach, D., and Wedekind, C. 2008. Predicting the mating system from phenotypic correlations between life-history and sperm quality traits in the Alpine whitefish Coregonus zugensis. Behav. Ecol. Sociobiol. 62(4): 561-567. doi:10.1007/s00265-007-0480-5.
44. Rundle, H.D. 2002. A test of ecologically dependent postmating isolation between sympatric sticklebacks. Evolution, 56(2): 322-329. PMID:11926500.
45. Rundle, H.D., and Nosil, P. 2005. Ecological speciation. Ecol. Lett. 8(3): 336-352. doi:10.1111/j.1461-0248.2004.00715.x.
46. Schluter, D. 2000. The ecology of adaptive radiation. Oxford University Press, New York.
47. St-Cyr, J., Derome, N., and Bernatchez, L. 2008. The transcriptomics of life-history trade-offs in whitefish species pairs (Coregonus sp.). Mol. Ecol. 17(7): 1850-1870. doi:10.1111/j.1365-294X.2008.03696.x. PMID:18312278.
48. Stoltz, J.A., and Neff, B.D. 2006. Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length. J. Evol. Biol. 19(6): 1873-1881. doi:10.1111/j.1420-9101.2006.01165.x. PMID:17040384.
49. Sutton, S.G., Bult, T.P., and Haedrich, R.L. 2000. Relationships among fat weight, body weight, water weight, and condition factors in wild Atlantic salmon parr. Trans. Am. Fish. Soc. 129(2): 527-538. doi:10.1577/1548- 8659(2000)129<0527:RAFWBW>2.0.CO;2.
50. Tallmon, D.A., Luikart, G., and Waples, R.S. 2004. The alluring simplicity and complex reality of genetic rescue. Trends Ecol. Evol. 19(9): 489-496. doi:10.1016/j.tree.2004.07.003. PMID: 16701312.
51. Trudel, M., Tremblay, A., Schetagne, R., and Rasmussen, J.B. 2001. Why are dwarf fish so small? An energetic analysis of polymorphism in lake whitefish (Coregonus clupeaformis). Can. J. Fish. Aquat. Sci. 58(2): 394-405. doi:10.1139/cjfas-58-2-394.