Epistasis causes outbreeding depression in eucalypt hybrids

Tree Genetics and Genomes

Volumn 8, Issue 2, 2012, Pages 249-265

  Costa e Silva, João ^a,b   Potts, Brad M ^c   Tilyard, Paul ^c  

^a INSTITUTO SUPERIOR DE AGRONOMIA   (Portugal)

^b INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^c UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Epistasis; Eucalyptus globulus; Eucalyptus nitens; Genetic architecture; Hybrid fitness; Speciation

Indexed keywords

EUCALYPTUS; EUCALYPTUS GLOBULUS; EUCALYPTUS NITENS;

EID: 84858616168     PISSN: 16142942     EISSN: 16142950     Source Type: Journal    
DOI: 10.1007/s11295-011-0437-8     Document Type: Article

References (74)

1. Armbruster P, Bradshaw WE, Holzapfel CM (1997) Evolution of the genetic architecture underlying fitness in the pitcher-plant mosquito, Wyeomyia smithii. Evolution 51: 451-458.
2. Bartlett MS (1947) The use of transformations. Biometrics 3: 39-52.
3. Bradshaw WE, Holzapfel CM (2000) The evolution of genetic architectures and the divergence of natural populations. In: Wolf JB, Brodie ED, Wade MJ (eds) Epistasis and the evolutionary process. Oxford University Press, New York, pp 245-263.
4. Brooker MIH (2000) A new classification of the genus Eucalyptus L' Her. (Myrtaceae). Aust Syst Bot 13: 79-148.
5. Brooker MIH, Kleinig DA (1999) Field guide to eucalypts. Volume 1. South-eastern Australia. Bloomings Books, Hawthorn.
6. Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35: 31-52.
7. Carson HL (1975) The genetics of speciation at the diploid level. Am Nat 109: 83-92.
8. Costa e Silva J, Hardner C, Tilyard P, Potts BM (2011) The effects of age and environment on the expression of inbreeding depression in Eucalyptus globulus. Heredity 107: 50-60.
9. Coyne JA, Orr AH (2004) Speciation. Sinauer Associates, Sunderland.
10. Demuth JP, Wade MJ (2006) Experimental methods for measuring gene interactions. Annu Rev Ecol Evol Syst 37: 289-316.
11. Demuth JP, Wade MJ (2007) Population differentiation in the beetle Tribolium castaneum. I. Genetic architecture. Evolution 61: 494-509.
12. Dettman JR, Sirjusingh C, Kohn LM, Anderson JB (2007) Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447: 585-588.
13. Dobzhansky T (1936) Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21: 113-135.
14. Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution 53: 1757-1768.
15. Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16: 463-475.
16. Erickson DL, Fenster CB (2006) Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata. Evolution 60: 225-233.
17. Fenster CB, Galloway LF (2000) Population differentiation in an annual legume: genetic architecture. Evolution 54: 1157-1172.
18. Fenster CB, Galloway LG, Chao L (1997) Epistasis and its consequences for the evolution of natural populations. Trends Ecol Evol 12: 282-286.
19. Fishman L, Willis JH (2001) Evidence for Dobzhansky-Muller incompatibilites contributing to the sterility of hybrids between Mimulus guttatus and M. nasutus. Evolution 55: 1932-1942.
20. Fitzpatrick BM (2008a) Hybrid dysfunction: population genetics and quantitative genetic perspectives. Am Nat 171: 491-498.
21. Fitzpatrick BM (2008b) Dobzhansky-Muller model of hybrid dysfunction supported by poor burst-speed performance in hybrid tiger salamanders. J Evol Biol 21: 342-351.
22. Freeman JS, Whittock SP, Potts BM, Vaillancourt RE (2009) QTL influencing growth and wood properties in Eucalyptus globulus. Tree Genet Genomes 5: 713-722.
23. Fritz RS, Hochwender CG, Albrectsen BR, Czesak ME (2006) Fitness and genetic architecture of parent and hybrid willows in common gardens. Evolution 60: 1215-1227.
24. Gilmour AR, Thompson R, Cullis BR (1995) Average information REML. An efficient algorithm for variance parameter estimation in linear mixed models. Biometrics 51: 1440-1450.
25. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2006) ASReml user guide release 2. 0. VSN International, Hemel Hempstead.
26. Goodnight CJ (2000) Quantitative trait loci and gene interaction: the quantitative genetics of metapopulations. Heredity 84: 587-598.
27. Gore PL, Potts BM, Volker PW, Megalos J (1990) Unilateral cross-incompatibility in Eucalyptus: the case of hybridisation between E. globulus and E. nitens. Aust J Bot 38: 383-394.
28. Griffin AR, Burgess IP, Wolf L (1988) Patterns of natural and manipulated hybridization in the genus Eucalyptus L'Herit.: a review. Aust J Bot 36: 41-66.
29. Hansen TF (2006) The evolution of genetic architecture. Annu Rev Ecol Evol Syst 37: 123-157.
30. Hansen TF, Álvarez-Castro JM, Carter AJR, Hermisson J, Wagner GP (2006) Evolution of genetic architecture under directional selection. Evolution 60: 1523-1536.
31. Henderson CR (1984) Applications of linear models in animal breeding. University of Guelph, Guelph.
32. Hill WG (1982) Dominance and epistasis as components of heterosis. Zeitschrift für Tierzüchtung und Züchtungsbiologie 99: 161-168.
33. Hudson CJ, Kullan ARK, Freeman JS, Faria DA, Grattapaglia D, Kilian A, Myburg AA, Potts BM, Vaillancourt RE (2011) High synteny and colinearity among Eucalyptus genomes revealed by high-density comparative genetic mapping. Tree Genet Genom (in press).
34. Kenward MG, Roger JH (1997) The precision of fixed effects estimates from restricted maximum likelihood. Biometrics 53: 983-997.
35. Koch RM, Dickerson GE, Cundiff LV, Gregory KE (1985) Heterosis retained in advanced generations of crosses among Angus and Hereford cattle. J Anim Sci 60: 1117-1132.
36. Komender P, Hoeschele I (1989) Use of mixed-model methodology to improve estimation of crossbreeding parameters. Livest Prod Sci 21: 101-113.
37. Lair KP, Bradshaw WE, Holzapfel CM (1997) Evolutionary divergence of the genetic architecture underlying photoperiodism in the pitcher-plant mosquito, Wyeomyia smithii. Genetics 147: 1873-1883.
38. Lawrence R, Potts BM, Whitham TG (2003) Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore. Ecology 84: 1171-1178.
39. Li L, Lu K, Chen Z, Mu T, Hu Z, Li X (2008) Dominance, overdominance and epistasis condition the heterosis in two heterotic rice hybrids. Genetics 180: 1725-1742.
40. Lopez GA, Potts BM, Tilyard PA (2000) F1 hybrid inviability in Eucalyptus: the case of E. ovata × E. globulus. Heredity 85: 242-250.
41. Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622-629.
42. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland.
43. Mather K, Jinks JL (1982) Biometrical genetics. Chapman and Hall, New York.
44. Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge.
45. McKinnon GE, Vaillancourt RE, Steane DA, Potts BM (2008) An AFLP marker approach to lower-level systematics in Eucalyptus (Myrtaceae). Am J Bot 95: 368-380.
46. McKinnon GE, Smith JJ, Potts BM (2010) Recurrent nuclear DNA introgression accompanies chloroplast DNA exchange between two eucalypt species. Mol Ecol 19: 1367-1380.
47. Muller HJ (1942) Isolating mechanisms, evolution, and temperature. Biol Symp 6: 71-125.
48. Myburg AA, Vogl C, Griffin AR, Sederoff RR, Whetten RW (2004) Genetics of postzygotic isolation in Eucalyptus: whole-genome analysis of barriers to introgression in a wide interspecific cross of Eucalyptus grandis and E. globulus. Genetics 166: 1405-1418.
49. Orr HA (1995) The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805-1813.
50. Orr HA, Irving S (2001) Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics 158: 1089-1100.
51. Oudjehih B, Bentouati A (2006) Chromosome numbers of the 59 species of Eucalyptus L'Herit. (Myrtaceae). Caryologia 59: 207-212.
52. Potts BM, Dungey HS (2004) Interspecific hybridization of Eucalyptus: key issues for breeders and geneticists. New For 27: 115-138.
53. Potts BM, Volker PW, Tilyard PA, Joyce K (2000) The genetics of hybridisation in the temperate Eucalyptus. In: Dungey HSD, Dieters MJ, Nikles DG (eds) Hybrid breeding and genetics of forest trees. Proceedings of QFRI/CRC-SPF Symposium, Noosa, Queensland, Australia, April 9-14, 2000. Department of Primary Industries, Brisbane, pp 200-211.
54. Potts BM, Barbour RC, Hingston A, Vaillancourt RE (2003) Turner review no. 6: genetic pollution of native eucalypt gene pools-identifying the risks. Aust J Bot 51: 1-25.
55. Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16: 351-358.
56. Rieseberg LH, Willis JH (2007) Plant speciation. Science 317: 910-914.
57. Roff DA, Emerson K (2006) Epistasis and dominance: evidence for differential effects in life-history versus morphological traits. Evolution 60: 1981-1990.
58. SAS Institute Inc (2004) SAS/STAT 9. 1 user's guide. SAS Institute, Cary.
59. Shapiro SS, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52: 591-611.
60. Taylor SJ, Arnold M, Martin NH (2009) The genetic architecture of reproductive isolation in Louisiana irises: hybrid fitness in nature. Evolution 63: 2581-2594.
61. Thumma BR, Southerton SG, Bell JC, Owen JV, Henery ML, Moran GF (2010) Quantitative trait locus (QTL) analysis of wood quality traits in Eucalyptus nitens. Tree Genet Genomes 6: 305-317.
62. Tiffin P, Olson MS, Moyle LC (2001) Asymmetrical crossing barriers in angiosperms. Proc Royal Soc London B 268: 861-867.
63. Tomé M, Tomé JA, Araújo MC, Pereira JS (1994) Intraspecific competition in irrigated and fertilized eucalypt plantations. For Ecol Manag 69: 211-218.
64. Turelli M, Orr HA (2000) Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154: 1663-1679.
65. Volker PW, Owen JV, Borralho NMG (1994) Genetic variances and covariances for frost tolerance in Eucalyptus globulus and E. nitens. Silvae Genetica 43: 366-372.
66. Volker PW, Potts BM, Borralho NMG (2008) Genetic parameters of intra- and inter-specific hybrids of Eucalyptus globulus and E. nitens. Tree Genet Genomes 4: 445-460.
67. Wegner KM, Berenos C, Schmid-Hempel P (2008) Nonadditive genetic components in resistance of the red flour beetle Tribolium castanaeum against parasite infection. Evolution 62: 2381-2392.
68. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK, Leroy CJ, Lonsdorf EV, Allan GJ, DiFazio SP, Potts BM, Fischer DG, Gehring CA, Lindroth RL, Marks JC, Hart SC, Wimp GM, Wooley SC (2006) A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7: 510-523.
69. Whitlock MC, Phillips PC, Moore FBG, Tonsor SJ (1995) Multiple fitness peaks and epistasis. Annu Rev Ecol Syst 26: 601-629.
70. Willham RL, Pollak E (1985) Theory of heterosis. J Dairy Sci 68: 2411-2417.
71. Williams DR, Potts BM, Black PG (1999) Testing single visit pollination procedures for Eucalyptus globulus and E. nitens. Aust For 62: 346-352.
72. Wright S (1978) Evolution and the genetics of populations, vol 4: variability within and among natural populations. University of Chicago Press, Chicago.
73. Wu CI (2001) The genic view of the process of speciation. J Evol Biol 14: 851-865.
74. Wu CI, Ting CT (2004) Genes and speciation. Nat Rev Genet 5: 114-122.