Genetica

, Volume 129, Issue 2, pp 167–177

Hybridization, recombination, and the genetic basis of fitness variation across environments in Avena barbata

  • Robert G. Latta
  • Kyle M. Gardner
  • April D. Johansen-Morris
Original Paper

Abstract

We created Recombinant Inbred Lines (RILs) derived from a cross between ecotypes of Avena barbata associated with moist (mesic) and dry (xeric) habitats in California. Traits which were correlated with fitness across RILs mapped to the same Quantitative Trait Loci (QTLs) as fitness. However, different QTL affected fitness in different environments so that fitness was weakly correlated across environments. Recombination released considerable heritable variation both in fitness, and in ecologically relevant traits. Many traits showed transgressive segregation caused by recombination of QTL associated in repulsion phase in the parents. In addition, some traits were uncorrelated, allowing novel combinations of those traits to be created. Recombination also created heritable variation in reaction norms for at least one trait (root allocation). Altogether these results suggest that recombination can combine the most selectively advantageous genes and traits of the parents to produce broadly adapted genotypes that are capable of outperforming the parents. Indeed, two of the RILs showed higher fitness than the parental ecotypes across a range of environmental treatments in the greenhouse, but their superiority was less pronounced in the field. Although late-generation recombinants exhibited hybrid breakdown, being less fit, on average, than the mid-parent, early generation hybrids appear to exhibit hybrid vigour through the expression of dominance effects in the heterozyotes. This vigour may offset the effects of hybrid breakdown in the early generations following a cross, enhancing the opportunity for recombination to create broadly adapted genotypes. We discuss the implications of these findings to the evolution of colonizing species.

Keywords

Coadapted gene complex Epistasis Generalist/specialist Line cross analysis QTL mapping Transgressive segregation 

Abbreviations

QTL

Quantitative trait locus

RIL

Recombinant inbred line

RMR

Root mass ratio

GxE

Genotype by environment interaction

HREC

Hopland Research and Extension Center

SFREC

Sierra Foothills Research and Extension Center

AFLP

Amplified fragment length polymorphism

References

  1. Ainouche ML, Baumel A, Salmon A, Yannic G (2004) Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol 161:165–172CrossRefGoogle Scholar
  2. Allard RW (1965) Genetic systems associated with colonizing ability in predominantly self-pollinated species. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 50–78Google Scholar
  3. Allard RW (1999) History of plant population genetics. Annu Rev Genet 33:1–27PubMedCrossRefGoogle Scholar
  4. Allard RW, Babbel GR, Clegg MT, Kahler AL (1972) Evidence for coadaptation in Avena barbata. Proc Natl Acad Sci USA 69:3043–3048PubMedCrossRefGoogle Scholar
  5. Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution and control of invasive species. Conserv Biol 17:24–30CrossRefGoogle Scholar
  6. Anderson E, Stebbins GL (1954) Hybridization as an evolutionary stimulus. Evolution 8:378–388CrossRefGoogle Scholar
  7. Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New YorkGoogle Scholar
  8. Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds), The genetics of colonizing species. Academic Press, New York, pp. 147–172Google Scholar
  9. Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568PubMedCrossRefGoogle Scholar
  10. Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52PubMedCrossRefGoogle Scholar
  11. Clausen J (1949) Genetics of climatic races of Potentilla glandulosa. Hereditas (Suppl.) pp 162–172Google Scholar
  12. Clausen J (1953) New bluegrasses by combining and rearranging genomes of contrasting Poa species. Proc 6th Int Grassland Congr, Univ. Park, Pa., 1952, pp 216–221Google Scholar
  13. Clausen JC, Keck D, Heisey WM (1948) Experimental studies on the nature of plant species. III. Environmental responses of climatic races of Achillea. Carnegie Institution of Washington, Washington DC, USA, Publication 581Google Scholar
  14. Clegg MT, Allard RW (1972) Patterns of genetic differentiation in the slender wild oat species Avena barbata. Proc Natl Acad Sci USA 69:1820–1824PubMedCrossRefGoogle Scholar
  15. Dyer AR, Rice KJ (1999) Effects of competition on resource availability and growth of a California bunchgrass. Ecology 80:2697–2710CrossRefGoogle Scholar
  16. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050PubMedCrossRefGoogle Scholar
  17. Fenster CB, Galloway LF (2000) Population differentiation in an annual legume: genetic architecture. Evolution 54:1157–1172PubMedGoogle Scholar
  18. Fry JD (1996) The evolution of host specialization: are trade-offs overrated? Am Nat 148:S84–S107CrossRefGoogle Scholar
  19. Fry JD, Nuzhdin SV, Pasyukova EG, McKay TFC (1998) QTL mapping of genotype–environment interaction for fitness in Drosophila melanogaster. Genet Res 71:133–141PubMedCrossRefGoogle Scholar
  20. Futuyma DJ (2001) Ecological specialization and generalization. In: Fox CW, Roff DA, Fairbairn DJ (eds) Evolutionary ecology: concepts and case studeis. Oxford University Press, London UK, pp 177–189Google Scholar
  21. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–223CrossRefGoogle Scholar
  22. Garcia P, Vences FJ, Perez de la Vega M, Allard RW (1989) Allelic and genotypic composition of ancestral spanish and colonial Californian gene pools of Avena barbata: evolutionary implications. Genetics 122:687–694PubMedGoogle Scholar
  23. Gardner KM (2004) The genetic architecture of fitness related traits in Avena barbata. PhD Dissertation, Dalhousie UniversityGoogle Scholar
  24. Gardner KM, Latta RG (2006) Identifying loci under selection across contrasting environments in Avena barbata using quantitative trait locus mapping. Mol Ecol 15:1321–1333PubMedCrossRefGoogle Scholar
  25. Grant V (1981) Plant speciation, 2nd edn. Columbia University Press, New York, USAGoogle Scholar
  26. Hamrick JL, Holden L (1979) Influence of microhabitat heterogeneity on gene frequency distribution and gametic phase disequilibrium in Avena barbata. Evolution 33:521–533CrossRefGoogle Scholar
  27. Hawthorne DJ, Via S (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412:904–907PubMedCrossRefGoogle Scholar
  28. Hedrick PW, Holden L (1979) Hitch-hiking: an alternative to coadaptation for the barley and slender wild oat examples. Heredity 43:79–86Google Scholar
  29. Holmes TH, Rice KJ (1996) Patterns of growth and soil–water utilization in some exotic annuals and native perennial bunchgrasses of California. Ann Bot 78:233–243CrossRefGoogle Scholar
  30. Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155CrossRefGoogle Scholar
  31. Hutchings MJ, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. Adv Ecol Res 25:159–238CrossRefGoogle Scholar
  32. Hutchinson ES (1982) Genetic markers and ecotypic differentiation of Avena barbata Pott. ex Link. PhD Dissertation, University of California, DavisGoogle Scholar
  33. Hutchinson ES, Hakim-Elahi A, Miller RD, Allard RW (1983) The genetics of diploidized tetraploid Avena barbata. J Hered 74:325–330Google Scholar
  34. Jain SK, Rai KN (1980) Population biology of Avena. VIII. Colonization experiment as a test of the role of natural selection in population divergence. Am J Bot 67:1342–1346CrossRefGoogle Scholar
  35. Jin H, Domier LL, Shen XJ, Kolb FL (2003) Combined AFLP and RFLP mapping in two hexaploid oat recombinant inbred populations. Genome 43:94–101CrossRefGoogle Scholar
  36. Johansen AD (2004) Fitness consequences of hybridization between ecotypes of Avena barbata. PhD Dissertation, Dalhousie UniversityGoogle Scholar
  37. Johansen-Morris AD, Latta RG (2006) Fitness consequences of hybridization between ecotypes of Avena barbata: hybrid breakdown, hybrid vigour and transgressive segregation. Evolution (in press)Google Scholar
  38. Kassen R, Bell G (2000) The ecology and genetics of fitness in Chlamydomonas. X. The relationship between genetic correlation and genetic distance. Evolution 54:425–432PubMedGoogle Scholar
  39. Kawecki TJ, Barton NH, Fry JD (1997) Mutation collapse of fitness in marginal habitats and the evolution of ecological specialization. J Evol Biol 10:407–429CrossRefGoogle Scholar
  40. Kremer CA, Lee M, Holland JB (2001) A restriction fragment length polymorphism based linkage map of a diploid Avena recombinant inbred line population. Genome 44:192–204PubMedCrossRefGoogle Scholar
  41. Latta RG, MacKenzie JL, Vats A, Schoen DJ (2004) Divergence and segregation of quantitative traits between allozyme genotypes of Avena barbata from contrasting habitats. J Ecol 92:57–71CrossRefGoogle Scholar
  42. Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391CrossRefGoogle Scholar
  43. Lee CE, Remfert JL, Gelembiuk GW (2003) Evolution of physiological tolerance and performance during freshwater invasions. Integ Comp Biol 43:439–449CrossRefGoogle Scholar
  44. Lexer C, Randell RA, Rieseberg LH (2003) Experimental hybridization as a tool for studying selection in the wild. Ecology 84:1688–1699CrossRefGoogle Scholar
  45. Lynch M, Gabriel W (1983) Phenotypic evolution and parthenogenesis. Am Nat 122:745–764CrossRefGoogle Scholar
  46. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, Inc., SunderlandGoogle Scholar
  47. MacKay TFC (2001) The genetic architecture of quantitative traits. Annu Rev Genet 35:303–339PubMedCrossRefGoogle Scholar
  48. MacKenzie A (1996) A trade-off for host plant utilization in the black bean aphid Aphis fabae. Evolution 50:155–162CrossRefGoogle Scholar
  49. Mather K, Jinks JL (1982) Biometrical genetics: the study of continuous variation. Chapman and Hall, LondonGoogle Scholar
  50. Nagy ES (1997) Selection for native characters in hybrids between two locally adapted plant subspecies. Evolution 51:1469–1480CrossRefGoogle Scholar
  51. Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389CrossRefGoogle Scholar
  52. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372PubMedCrossRefGoogle Scholar
  53. Rieseberg LH, Widmer A, Arntz AM, Burke JM (2003) The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Phil Trans R Soc Lond B 358:1141–1147CrossRefGoogle Scholar
  54. Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New YorkGoogle Scholar
  55. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  56. van Tienderen PH (1992) Variation in a population of Plantago-lanceolata along a topographical gradient. Oikos 64:560–572CrossRefGoogle Scholar
  57. Verhoeven KJF, Vanhala TK, Biere A, Nevo E, Van Damme JMM (2004) The genetic baiss of adaptive population differentiation: a quantitative trait locus analysis of fitness traits in two wild barley populations from contrasting habitats. Evolution 58:270–283PubMedGoogle Scholar
  58. Via S, Lande R (1985) Genotype–environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522CrossRefGoogle Scholar
  59. Vos P, Hogers R, Bleeker M, Reijans M, Vandalee T, Hornes M, Fijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP—a new technique for DNA fingerprinting. Nucl Acids Res 23:4407–4414PubMedCrossRefGoogle Scholar
  60. Weinig C, Dorn LA, Kane NC, German ZM, Halldorsdottir SS, Ungerer MC, Toyonaga Y, Mackay TFC, Purugganan MD, Schmitt J (2003) Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Genetics 165:321–329PubMedGoogle Scholar
  61. Williamson M (1996) Biological invasions. Chapman and Hall, New YorkGoogle Scholar
  62. Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Robert G. Latta
    • 1
  • Kyle M. Gardner
    • 1
  • April D. Johansen-Morris
    • 1
  1. 1.Department of BiologyDalhousie UniversityHalifaxCanada

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