Species and Recombination Effects on DNA Variability in the Tomato Genus

Corresponding author: Wolfgang Stephan, Department of Evolutionary Biology, University of Munich, Luisenstr. 14, 80333 Munich, Germany., stephan{at}zi.biologie.uni-muenchen.de (E-mail)

Communicating editor: O. SAVOLAINEN

Population genetics theory predicts that strong selection for rare, beneficial mutations or against frequent, deleterious mutations reduces polymorphism at linked neutral (or weakly selected) sites. The reduction of genetic variation is expected to be more severe when recombination rates are lower. In outbreeding species, low recombination rates are usually confined to certain chromosomal regions, such as centromeres and telomeres. In contrast, in predominantly selfing species, the rarity of double heterozygotes leads to a reduced effective recombination rate in the whole genome. We investigated the effects of restricted recombination on DNA polymorphism in these two cases, analyzing five Lycopersicon species with contrasting mating systems: L. chilense, L. hirsutum, L. peruvianum, L. chmielewskii, and L. pimpinellifolium, of which only the first three species have self-incompatibility alleles. In each species, we determined DNA sequence variation of five single-copy genes located in chromosomal regions with either high or low recombination rate. We found that the mating system has a highly significant effect on the level of polymorphism, whereas recombination has only a weak influence. The effect of recombination on levels of polymorphism in Lycopersicon is much weaker than in other well-studied species, including Drosophila. To explain these observations, we discuss a number of hypotheses, invoking selection, recombination, and demographic factors associated with the mating system. We also provide evidence that L. peruvianum, showing a level of polymorphism (almost 3%) that is comparable to the level of divergence in the whole genus, is the ancestral species from which the other species of the genus Lycopersicon have originated relatively recently.

This article has been cited by other articles:

				A. Kawabe, A. Forrest, S. I. Wright, and D. Charlesworth High DNA Sequence Diversity in Pericentromeric Genes of the Plant Arabidopsis lyrata Genetics, June 1, 2008; 179(2): 985 - 995. [Abstract] [Full Text] [PDF]

				A. D. Cutter Multilocus Patterns of Polymorphism and Selection Across the X Chromosome of Caenorhabditis remanei Genetics, March 1, 2008; 178(3): 1661 - 1672. [Abstract] [Full Text] [PDF]

				T. Stadler, U. Arunyawat, and W. Stephan Population Genetics of Speciation in Two Closely Related Wild Tomatoes (Solanum Section Lycopersicon) Genetics, January 1, 2008; 178(1): 339 - 350. [Abstract] [Full Text] [PDF]

				U. Arunyawat, W. Stephan, and T. Stadler Using Multilocus Sequence Data to Assess Population Structure, Natural Selection, and Linkage Disequilibrium in Wild Tomatoes Mol. Biol. Evol., October 1, 2007; 24(10): 2310 - 2322. [Abstract] [Full Text] [PDF]

				S.-B. Chang, L. K. Anderson, J. D. Sherman, S. M. Royer, and S. M. Stack Predicting and Testing Physical Locations of Genetically Mapped Loci on Tomato Pachytene Chromosome 1 Genetics, August 1, 2007; 176(4): 2131 - 2138. [Abstract] [Full Text] [PDF]

				L. E. Rose, R. W. Michelmore, and C. H. Langley Natural Variation in the Pto Disease Resistance Gene Within Species of Wild Tomato (Lycopersicon). II. Population Genetics of Pto Genetics, March 1, 2007; 175(3): 1307 - 1319. [Abstract] [Full Text] [PDF]

				S. Glemin, E. Bazin, and D. Charlesworth Impact of mating systems on patterns of sequence polymorphism in flowering plants Proc R Soc B, December 7, 2006; 273(1604): 3011 - 3019. [Abstract] [Full Text] [PDF]

				S. I. Wright, J. P. Foxe, L. DeRose-Wilson, A. Kawabe, M. Looseley, B. S. Gaut, and D. Charlesworth Testing for Effects of Recombination Rate on Nucleotide Diversity in Natural Populations of Arabidopsis lyrata Genetics, November 1, 2006; 174(3): 1421 - 1430. [Abstract] [Full Text] [PDF]

				I. Simko, K. G. Haynes, and R. W. Jones Assessment of Linkage Disequilibrium in Potato Genome With Single Nucleotide Polymorphism Markers Genetics, August 1, 2006; 173(4): 2237 - 2245. [Abstract] [Full Text] [PDF]

				K. Roselius, W. Stephan, and T. Stadler The Relationship of Nucleotide Polymorphism, Recombination Rate and Selection in Wild Tomato Species Genetics, October 1, 2005; 171(2): 753 - 763. [Abstract] [Full Text] [PDF]

				S. I. Wright and B. S. Gaut Molecular Population Genetics and the Search for Adaptive Evolution in Plants Mol. Biol. Evol., March 1, 2005; 22(3): 506 - 519. [Abstract] [Full Text] [PDF]

				M. T. Hamblin, S. E. Mitchell, G. M. White, J. Gallego, R. Kukatla, R. A. Wing, A. H. Paterson, and S. Kresovich Comparative Population Genetics of the Panicoid Grasses: Sequence Polymorphism, Linkage Disequilibrium and Selection in a Diverse Sample of Sorghum bicolor Genetics, May 1, 2004; 167(1): 471 - 483. [Abstract] [Full Text] [PDF]

				S. E. Ramos-Onsins, B. E. Stranger, T. Mitchell-Olds, and M. Aguade Multilocus Analysis of Variation and Speciation in the Closely Related Species Arabidopsis halleri and A. lyrata Genetics, January 1, 2004; 166(1): 373 - 388. [Abstract] [Full Text] [PDF]

				H. Innan and W. Stephan Distinguishing the Hitchhiking and Background Selection Models Genetics, December 1, 2003; 165(4): 2307 - 2312. [Abstract] [Full Text] [PDF]

				N. Frankel, E. Hasson, N. D. Iusem, and M. S. Rossi Adaptive Evolution of the Water Stress-Induced Gene Asr2 in Lycopersicon Species Dwelling in Arid Habitats Mol. Biol. Evol., December 1, 2003; 20(12): 1955 - 1962. [Abstract] [Full Text] [PDF]

				A. D. Cutter and B. A. Payseur Selection at Linked Sites in the Partial Selfer Caenorhabditis elegans Mol. Biol. Evol., May 1, 2003; 20(5): 665 - 673. [Abstract] [Full Text] [PDF]

				M. I. Tenaillon, M. C. Sawkins, L. K. Anderson, S. M. Stack, J. Doebley, and B. S. Gaut Patterns of Diversity and Recombination Along Chromosome 1 of Maize (Zea mays ssp. mays L.) Genetics, November 1, 2002; 162(3): 1401 - 1413. [Abstract] [Full Text] [PDF]

				S. I. Wright, B. Lauga, and D. Charlesworth Rates and Patterns of Molecular Evolution in Inbred and Outbred Arabidopsis Mol. Biol. Evol., September 1, 2002; 19(9): 1407 - 1420. [Abstract] [Full Text] [PDF]

				A. Graustein, J. M. Gaspar, J. R. Walters, and M. F. Palopoli Levels of DNA Polymorphism Vary With Mating System in the Nematode Genus Caenorhabditis Genetics, May 1, 2002; 161(1): 99 - 107. [Abstract] [Full Text] [PDF]