The Relationship of Nucleotide Polymorphism, Recombination Rate and Selection in Wild Tomato Species

Abstract

We analyzed the effects of mating system and recombination rate on single nucleotide polymorphisms using 14 single-copy nuclear loci from single populations of five species of wild tomatoes (Solanum section Lycopersicon). The taxa investigated comprise two self-compatible (SC) and three self-incompatible (SI) species. The observed reduction in nucleotide diversity in the SC populations compared to the SI populations is much stronger than expected under the neutral effects of the mating system on effective population size. Importantly, outgroup sequences available for 11 of the 14 loci yield strong positive correlations between silent nucleotide diversity and silent divergence, indicative of marked among-locus differences in mutation rates and/or selective constraints. Furthermore, using a physical estimate of local recombination rates, we find that silent nucleotide diversity (but not divergence) is positively correlated with recombination rate in two of the SI species. However, this correlation is not nearly as strong as in other well-characterized species (in particular, Drosophila). We propose that nucleotide diversity in Lycopersicon is dominated mainly by differences in neutral mutation rates and/or selective constraints among loci, demographic processes (such as population subdivision), and background selection. In addition, we hypothesize that the soil seed bank plays an important role in the maintenance of the large genetic diversity in the SI species (in particular L. peruvianum).W HETHER diversity levels in the genomes of animals and plants are shaped mainly by neutral processes or selection is a recurrent theme in population genetics. In many organisms, genes in regions of low recombination exhibit reduced levels of DNA polymorphism, while divergence among species remains relatively unaffected. These observations may be explained by genetic hitchhiking, involving advantageous mutations sweeping through a population (Maynard Smith and Haigh 1974) and/or by background selection eliminating unconditionally deleterious mutations (Charlesworth et al. 1993(Charlesworth et al. , 1995. Depending on the effective recombination rate in the regions subjected to either of the above processes and on the strength of natural selection, linked neutral variation is reduced under both selection scenarios, while interspecific divergence is not influenced.A positive correlation between DNA diversity and recombination rate has been found in many organisms, both animals (Aguadé et al. 1989;Stephan and Langley 1989;Begun and Aquadro 1992;Nachman 1997;Nachman et al. 1998) and plants (Dvorak et al. 1998;Kraft et al. 1998;Stephan and Langley 1998). Such patterns were usually attributed to the action of natural selection. However, neutral explanations for an observed positive correlation between recombination and diversity have also been proposed, when, in addition to intraspecific variation, divergence also scaled with recombination rate (e.g., Wang et al. 1997;Hellmann et al. 2003).Among plants, maize (Zea mays ssp. m...

Fitness effects of derived deleterious mutations in four closely related wild tomato species with spatial structure

“…These loci are single-copy complementary DNA markers originally mapped by Tanksley et al (1992) in genomic regions with different recombination rates (Stephan and Langley, 1998). The gene products putatively perform key housekeeping functions, and thus purifying selection is suggested to drive their evolution (Supplementary Table S2; Roselius et al, 2005). Genomic DNA was extracted from silica-dried tomato leaves using the DNeasy Plant Mini Kit (Qiagen GmbH, Hilden, Germany).…”

“…The new sequences for S. habrochaites and S. arcanum have been deposited in GenBank under accession numbers GU950656-GU951412. In addition, this study also analyzes our previously published sequences sampled from each of four populations in both S. peruvianum and S. chilense, as well as outgroup sequences from tomato relatives (Baudry et al, 2001;Roselius et al, 2005;Arunyawat et al, 2007). We also included one previously sequenced sample of S. habrochaites, which was obtained from the Tomato Genetics Resource Center at UC Davis (http://tgrc.ucdavis.edu; accession LA1775, 'Ancash', see Supplementary Table S1 and Städler et al, 2005).…”

The heterogeneous levels of linkage disequilibrium in white spruce genes and comparative analysis with other conifers

“…The p a /p s ratio is another parameter indicative of selection with values 41 generally suggestive of positive selection (Roselius et al, 2005;Caldwell and Michelmore, 2009). In our data set, the average p a /p s ratio was 0.21 (in line with the average Ka/Ks ratio of 0.17 for 3374 contigs from expressed sequence tag (EST) sequences assembly, Pavy et al (2006)), indicating generally strong purifying selection.…”

“…These wide ranges of nucleotide diversity among nuclear plant genes have been accounted for by different mutation rates, selection and demographic effects (Roselius et al, 2005).…”

Genetic hitchhiking versus background selection: the controversy and its implications

“…population genetics that uses molecular data such as RFLP, microsatellite or DNA sequence data). Since the phenomenon of reduced variation in regions of restricted recombination has also been found in organisms other than Drosophila (for instance, in humans (Nachman et al 1998;Hellmann et al 2003) and several plant species such as wild tomatoes (Stephan & Langley 1998;Roselius et al 2005)), it has provoked extensive modelling and analysis efforts. The development of methods for distinguishing BGS and hitchhiking was a major activity in those years (until about 2000).…”