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. 2001 Dec;159(4):1701–1716. doi: 10.1093/genetics/159.4.1701

A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions.

L Fishman 1, A J Kelly 1, E Morgan 1, J H Willis 1
PMCID: PMC1461909  PMID: 11779808

Abstract

As part of a study of the genetics of floral adaptation and speciation in the Mimulus guttatus species complex, we constructed a genetic linkage map of an interspecific cross between M. guttatus and M. nasutus. We genotyped an F(2) mapping population (N = 526) at 255 AFLP, microsatellite, and gene-based markers and derived a framework map through repeated rounds of ordering and marker elimination. The final framework map consists of 174 marker loci on 14 linkage groups with a total map length of 1780 cM Kosambi. Genome length estimates (2011-2096 cM) indicate that this map provides thorough coverage of the hybrid genome, an important consideration for QTL mapping. Nearly half of the markers in the full data set (49%) and on the framework map (48%) exhibited significant transmission ratio distortion (alpha = 0.05). We localized a minimum of 11 transmission ratio distorting loci (TRDLs) throughout the genome, 9 of which generate an excess of M. guttatus alleles and a deficit of M. nasutus alleles. This pattern indicates that the transmission ratio distortion results from particular interactions between the heterospecific genomes and suggests that substantial genetic divergence has occurred between these Mimulus species. We discuss possible causes of the unequal representation of parental genomes in the F(2) generation.

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Selected References

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  1. Bradshaw H. D., Jr, Otto K. G., Frewen B. E., McKay J. K., Schemske D. W. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics. 1998 May;149(1):367–382. doi: 10.1093/genetics/149.1.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Buetow K. H. Influence of aberrant observations on high-resolution linkage analysis outcomes. Am J Hum Genet. 1991 Nov;49(5):985–994. [PMC free article] [PubMed] [Google Scholar]
  3. Chakravarti A., Lasher L. K., Reefer J. E. A maximum likelihood method for estimating genome length using genetic linkage data. Genetics. 1991 May;128(1):175–182. doi: 10.1093/genetics/128.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chetelat R. T., Meglic V., Cisneros P. A genetic map of tomato based on BC(1) Lycopersicon esculentum x Solanum lycopersicoides reveals overall synteny but suppressed recombination between these homeologous genomes. Genetics. 2000 Feb;154(2):857–867. doi: 10.1093/genetics/154.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Collins A., Teague J., Keats B. J., Morton N. E. Linkage map integration. Genomics. 1996 Aug 15;36(1):157–162. doi: 10.1006/geno.1996.0436. [DOI] [PubMed] [Google Scholar]
  6. Doebley J., Stec A., Gustus C. teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics. 1995 Sep;141(1):333–346. doi: 10.1093/genetics/141.1.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Doerge R. W., Churchill G. A. Permutation tests for multiple loci affecting a quantitative character. Genetics. 1996 Jan;142(1):285–294. doi: 10.1093/genetics/142.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dorweiler J., Stec A., Kermicle J., Doebley J. Teosinte glume architecture 1: A Genetic Locus Controlling a Key Step in Maize Evolution. Science. 1993 Oct 8;262(5131):233–235. doi: 10.1126/science.262.5131.233. [DOI] [PubMed] [Google Scholar]
  9. Ehm M. G., Kimmel M., Cottingham R. W., Jr Error detection for genetic data, using likelihood methods. Am J Hum Genet. 1996 Jan;58(1):225–234. [PMC free article] [PubMed] [Google Scholar]
  10. FISHER R. A., BAILEY N. T. J. The estimation of linkage with differential viability. Heredity (Edinb) 1949 Aug;Pt. 2 3:215–228. doi: 10.1038/hdy.1949.13. [DOI] [PubMed] [Google Scholar]
  11. Faris J. D., Laddomada B., Gill B. S. Molecular mapping of segregation distortion loci in Aegilops tauschii. Genetics. 1998 May;149(1):319–327. doi: 10.1093/genetics/149.1.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fishman L., Willis J. H. Evidence for Dobzhansky-Muller incompatibilites contributing to the sterility of hybrids between Mimulus guttatus and M. nasutus. Evolution. 2001 Oct;55(10):1932–1942. doi: 10.1111/j.0014-3820.2001.tb01311.x. [DOI] [PubMed] [Google Scholar]
  13. Jack T., Brockman L. L., Meyerowitz E. M. The homeotic gene APETALA3 of Arabidopsis thaliana encodes a MADS box and is expressed in petals and stamens. Cell. 1992 Feb 21;68(4):683–697. doi: 10.1016/0092-8674(92)90144-2. [DOI] [PubMed] [Google Scholar]
  14. Jeanmougin F., Thompson J. D., Gouy M., Higgins D. G., Gibson T. J. Multiple sequence alignment with Clustal X. Trends Biochem Sci. 1998 Oct;23(10):403–405. doi: 10.1016/s0968-0004(98)01285-7. [DOI] [PubMed] [Google Scholar]
  15. Jiang C., Zeng Z. B. Mapping quantitative trait loci with dominant and missing markers in various crosses from two inbred lines. Genetica. 1997;101(1):47–58. doi: 10.1023/a:1018394410659. [DOI] [PubMed] [Google Scholar]
  16. Karlin S., Burge C. Dinucleotide relative abundance extremes: a genomic signature. Trends Genet. 1995 Jul;11(7):283–290. doi: 10.1016/s0168-9525(00)89076-9. [DOI] [PubMed] [Google Scholar]
  17. Kim S. C., Rieseberg L. H. Genetic architecture of species differences in annual sunflowers: implications for adaptive trait introgression. Genetics. 1999 Oct;153(2):965–977. doi: 10.1093/genetics/153.2.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lander E. S., Green P., Abrahamson J., Barlow A., Daly M. J., Lincoln S. E., Newberg L. A., Newburg L. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics. 1987 Oct;1(2):174–181. doi: 10.1016/0888-7543(87)90010-3. [DOI] [PubMed] [Google Scholar]
  19. Lin J. Z., Ritland K. Construction of a genetic linkage map in the wild plant Mimulus using RAPD and isozyme markers. Genome. 1996 Feb;39(1):63–70. doi: 10.1139/g96-009. [DOI] [PubMed] [Google Scholar]
  20. Lincoln S. E., Lander E. S. Systematic detection of errors in genetic linkage data. Genomics. 1992 Nov;14(3):604–610. doi: 10.1016/s0888-7543(05)80158-2. [DOI] [PubMed] [Google Scholar]
  21. Luo D., Carpenter R., Vincent C., Copsey L., Coen E. Origin of floral asymmetry in Antirrhinum. Nature. 1996 Oct 31;383(6603):794–799. doi: 10.1038/383794a0. [DOI] [PubMed] [Google Scholar]
  22. Lyttle T. W. Segregation distorters. Annu Rev Genet. 1991;25:511–557. doi: 10.1146/annurev.ge.25.120191.002455. [DOI] [PubMed] [Google Scholar]
  23. Mackay T. F. Quantitative trait loci in Drosophila. Nat Rev Genet. 2001 Jan;2(1):11–20. doi: 10.1038/35047544. [DOI] [PubMed] [Google Scholar]
  24. Macnair M. R., Cumbes Q. J. The genetic architecture of interspecific variation in mimulus. Genetics. 1989 May;122(1):211–222. doi: 10.1093/genetics/122.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Paterson A. H., Damon S., Hewitt J. D., Zamir D., Rabinowitch H. D., Lincoln S. E., Lander E. S., Tanksley S. D. Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments. Genetics. 1991 Jan;127(1):181–197. doi: 10.1093/genetics/127.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Paterson A. H., Lin Y. R., Li Z., Schertz K. F., Doebley J. F., Pinson S. R., Liu S. C., Stansel J. W., Irvine J. E. Convergent domestication of cereal crops by independent mutations at corresponding genetic Loci. Science. 1995 Sep 22;269(5231):1714–1718. doi: 10.1126/science.269.5231.1714. [DOI] [PubMed] [Google Scholar]
  27. Remington D. L., O'Malley D. M. Whole-genome characterization of embryonic stage inbreeding depression in a selfed loblolly pine family. Genetics. 2000 May;155(1):337–348. doi: 10.1093/genetics/155.1.337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Remington D. L., Whetten R. W., Liu B. H., O'Malley D. M. Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda. Theor Appl Genet. 1999 Jun;98(8):1279–1292. doi: 10.1007/s001220051194. [DOI] [PubMed] [Google Scholar]
  29. Rieseberg L. H., Linder C. R., Seiler G. J. Chromosomal and genic barriers to introgression in Helianthus. Genetics. 1995 Nov;141(3):1163–1171. doi: 10.1093/genetics/141.3.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sweigart A, Karoly K, Jones A, Willis JH. The distribution of individual inbreeding coefficients and pairwise relatedness in a population of mimulus guttatus. Heredity (Edinb) 1999 Nov;83(Pt 5):625–632. doi: 10.1038/sj.hdy.6886020. [DOI] [PubMed] [Google Scholar]
  31. Sybenga J. Recombination and chiasmata: few but intriguing discrepancies. Genome. 1996 Jun;39(3):473–484. doi: 10.1139/g96-061. [DOI] [PubMed] [Google Scholar]
  32. Tanksley S. D. Mapping polygenes. Annu Rev Genet. 1993;27:205–233. doi: 10.1146/annurev.ge.27.120193.001225. [DOI] [PubMed] [Google Scholar]
  33. Vogl C., Xu S. Multipoint mapping of viability and segregation distorting loci using molecular markers. Genetics. 2000 Jul;155(3):1439–1447. doi: 10.1093/genetics/155.3.1439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Vos P., Hogers R., Bleeker M., Reijans M., van de Lee T., Hornes M., Frijters A., Pot J., Peleman J., Kuiper M. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995 Nov 11;23(21):4407–4414. doi: 10.1093/nar/23.21.4407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Voss S. R., Shaffer H. B. Adaptive evolution via a major gene effect: paedomorphosis in the Mexican axolotl. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):14185–14189. doi: 10.1073/pnas.94.25.14185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Weigel D., Alvarez J., Smyth D. R., Yanofsky M. F., Meyerowitz E. M. LEAFY controls floral meristem identity in Arabidopsis. Cell. 1992 May 29;69(5):843–859. doi: 10.1016/0092-8674(92)90295-n. [DOI] [PubMed] [Google Scholar]
  37. Whitkus R. Genetics of adaptive radiation in Hawaiian and Cook Islands species of Tetramolopium (Asteraceae). II. Genetic linkage map and its implications for interspecific breeding barriers. Genetics. 1998 Nov;150(3):1209–1216. doi: 10.1093/genetics/150.3.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Willis J. H. Inbreeding load, average dominance and the mutation rate for mildly deleterious alleles in Mimulus guttatus. Genetics. 1999 Dec;153(4):1885–1898. doi: 10.1093/genetics/153.4.1885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zeng Z. B., Liu J., Stam L. F., Kao C. H., Mercer J. M., Laurie C. C. Genetic architecture of a morphological shape difference between two Drosophila species. Genetics. 2000 Jan;154(1):299–310. doi: 10.1093/genetics/154.1.299. [DOI] [PMC free article] [PubMed] [Google Scholar]

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