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Nucleotide Diversity and Linkage Disequilibrium in Loblolly Pine

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Nucleotide Diversity and Linkage Disequilibrium in Loblolly Pine Nucleotide diversity and linkage disequilibrium in loblolly pine Garth R. Brown*, Geoffrey P. Gill*†, Robert J. Kuntz*, Charles H. Langley‡, and David B. Neale*§¶ Departments of *Environmental Horticulture and ‡Evolution and Ecology, University of California, Davis, CA 95616; and §Institute of Forest Genetics, U.S. Department of Agriculture Forest Service, Davis, CA 95616 Edited by M. T. Clegg, University of California, Irvine, CA, and approved September 8, 2004 (received for review June 14, 2004) Outbreeding species with large, stable population sizes, such as Estimating 4Ner (reviewed in refs. 4 and 5) is not as straight- widely distributed conifers, are expected to harbor relatively more forward as 4Ne␮. One approach estimates Ne and r indepen- DNA sequence polymorphism. Under the neutral theory of molec- dently (6). Ne can be estimated from diversity and interspecific ular evolution, the expected heterozygosity is a function of the divergence data but estimates of r require knowledge of the ratio product 4Ne␮, where Ne is the effective population size and ␮ is the of genetic map distance to physical map distance, of which one per-generation mutation rate, and the genomic scale of linkage or both may be inaccurate or unknown for many species. The disequilibrium is determined by 4Ner, where r is the per-generation second method estimates 4Ner directly from population DNA recombination rate between adjacent sites. These parameters samples by using moment estimators, or more recently, full- and were estimated in the long-lived, outcrossing gymnosperm loblolly composite-likelihood approaches. The composite-likelihood pine (Pinus taeda L.) from a survey of single nucleotide polymor- method of Hudson (7), which considers only a single pair of Ϸ phisms across 18 kb of DNA distributed among 19 loci from a segregating sites at a time and derives a point estimate of 4Ner ␮ common set of 32 haploid genomes. Estimates of 4Ne at silent and by multiplying all pairwise likelihoods, is computationally fast nonsynonymous sites were 0.00658 and 0.00108, respectively, and and works as well or better than other methods (7). both were statistically heterogeneous among loci. By Tajima’s D Much of the pioneering research in estimating sequence statistic, the site frequency spectrum of no locus was observed to variation and LD has arisen from large-scale sequencing surveys deviate from that predicted by neutral theory. Substantial recom- in humans (8, 9), Drosophila (10), and the angiosperm plant bination in the history of the sampled alleles was observed and species Arabidopsis (11) and maize (12). In this study, we linkage disequilibrium declined within several kilobases. The com- identified single nucleotide polymorphisms (SNPs) in Ϸ18 kb of posite likelihood estimate of 4Ner based on all two-site sample DNA distributed across 19 loci from 32 alleles of the long-lived configurations equaled 0.00175. When geological dating, an as- gymnosperm loblolly pine (Pinus taeda L.). Pertinent attributes sumed generation time (25 years), and an estimated divergence of the species include a highly outcrossed mating system with from Pinus pinaster Ait. are used, the effective population size of extensive wind dispersal of pollen (13), a 50-million-acre distri- ؋ 5 loblolly pine should be 5.6 10 . The emerging narrow range of bution in the southeastern United States (14), abundant allo- estimated silent site heterozygosities (relative to the vast range zyme and microsatellite polymorphism with only weak popula- of population sizes) for humans, Drosophila, maize, and pine tion differentiation across its range (15, 16), and a very recent parallels the paradox described earlier for allozyme polymorphism domestication history. Thus, natural, undisturbed stands of and challenges simple equilibrium models of molecular evolution. loblolly pine may be a good approximation to an idealized random mating population. In addition, the nutritive tissue of ew genetic variation within a species arises solely by the conifer seed (the megagametophyte) is maternally derived and Nprocess of mutation. A new neutral variant may be lost haploid, greatly facilitating the analysis of sequence data. This rapidly from a population at the rate of one minus its initial study was motivated not only by an interest in the underlying frequency. If the new variant is not lost, genetic, demographic, processes determining the patterns of polymorphism, but also in and evolutionary processes, in addition to random genetic drift, the hope of identifying polymorphisms that have observable determine its population frequency and its nonrandom associ- phenotypic effects. Our sampling strategy was focused primarily ation with adjacent sites (linkage disequilibrium, LD) along the on the discovery of sequence variation and estimation of ␪ in segment of DNA on which it arose. Recombination is the genic regions representative of the genome as a whole in loblolly primary genetic process that erodes LD over time. Therefore, pine. The estimation of ␳ requires that considerably larger two key parameters in simple population genetic models that segments of contiguous DNA be sequenced. Based on Hudson’s govern the amount and distribution of intraspecific sequence (7) assertion that the estimate of ␳ with the lowest variance is variation are the population mutation parameter, ␪ ϭ 4Ne␮, and ␳ ϭ obtained for sites a known distance apart (in base pairs), when the population recombination parameter, 4Ner, where Ne is ␳ Ϸ ␮ bp multiplied by distance is 5, the relatively short sequences the effective population size, is the per-generation, per-base obtained in this study are not sufficient to provide reliable pair mutation rate, and r is the per-generation recombination locus-specific estimates of ␳. Instead, a genome-wide estimate of rate between adjacent sites. ␳ ␮ was obtained from the two-site sample configurations pooled Estimates of 4Ne can be readily calculated from DNA across loci. sequences obtained from population samples, even with rela- tively small data sets. Watterson’s estimate of 4Ne␮ as ␪W (1) is based on the number of polymorphic sites in a sample of This paper was submitted directly (Track II) to the PNAS office. sequences drawn at random from a population. A second Abbreviations: LD, linkage disequilibrium; SNP, single nucleotide polymorphism; indel, estimate of 4Ne␮ is nucleotide diversity, or ␲ (2), which is the insertion͞deletion. average number of pairwise nucleotide differences between Data deposition: The sequences reported in this paper have been deposited in the GenBank sequences in a sample. ␲ depends on both the number of database (accession nos. AY648063–AY648094, AY670330–AY670645, AY752403– AY752466, and AY764393–AY764928). polymorphic sites and their frequency, whereas ␪W is indepen- dent of frequencies. Tajima (3) developed a test statistic, D,to †Present address: Vialactia Biosciences, Auckland 1031, New Zealand. ¶ compare ␲ and ␪W and to infer selection and demographic events To whom correspondence should be addressed. E-mail: [email protected]. PLANT BIOLOGY by a skew in the site frequency spectra. © 2004 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0404231101 PNAS ͉ October 19, 2004 ͉ vol. 101 ͉ no. 42 ͉ 15255–15260 Downloaded by guest on September 29, 2021 Materials and Methods Several descriptors of the amount of LD in the sample were Plant Material. The breeding of loblolly pine began only in the mid obtained. The number of haplotypes and the minimum number 1950s with mass selection of well adapted individuals from of historical recombination events, RM, inferred from the four- undisturbed natural stands. These individuals are conserved to gamete test (20) were determined by using DNASP. The descrip- this day as first-generation breeding material by grafting. The tive statistic of LD, r2 (21), and its significance, determined by a sample of 32 genotypes includes 14 first-generation selections one-tailed Fisher’s exact test, were calculated by using TASSEL archived in the 1950s by the North Carolina State University (www.maizegenetics.net͞bioinformatics͞tasselindex.htm). The Industry Cooperative Tree Improvement Program and 18 indi- average decay of LD with distance was modeled similarly to viduals resulting from controlled crossing of the mass selections previous research in maize (22). Under a standard Wright– (second-generation breeding material). It was presumed that the Fisher model, the expected value of r2, E(r2), is equal to 1͞(1 ϩ first-generation breeding material is unrelated. The second- 4Ner) (21). It has been shown (23) that, with a low mutation rate generation material introduced a slight bias, which should have and adjustment for sample size (n), this expectation is minimal impact because of the expected high levels of heterozy- 10 ϩ C ͑3 ϩ C͒͑12 ϩ 12 C ϩ C2͒ gosity and meiotic segregation, by the erroneous inclusion of two E͑r2͒ ϭ ͫ ͬͫ1 ϩ ͬ, pairs of half sibs. The geographic distribution of the sample ͑2 ϩ C͒͑11 ϩ C͒ n͑2 ϩ C͒͑11 ϩ C͒ encompasses most of the natural range of loblolly pine with the [1] exception of Florida; the origins of the first-generation selections or the two parents of the second-generation selections are where C ϭ ␳ ϭ 4Ner. A least squares fit of the C parameter in included in Table 4, which is published as supporting information this equation was obtained by the general algorithm described in on the PNAS web site. Weyerhaeuser (Federal Way, WA) ref. 24 implemented in KALEIDAGRAPH software (version 3.6.4, provided seeds from each individual, and, after seed germina- Syngergy, Reading, PA). tion, haploid DNA was extracted from the excised megagameto- The composite-likelihood method of (7) was used to estimate phyte by using the Plant DNeasy kit (Qiagen, Valencia, CA). 4Ner as described in ref. 25, but with haploid sample configu- ration probabilities. Frisse et al. (25) distinguished between PCR and DNA Sequencing. Sequencing of alleles was performed 4Nerbp (ϭ ␳), where rbp is the per-generation crossing-over rate directly by using haploid megagametophyte DNA. Sequence between adjacent sites, and 4Nere, where re is the ‘‘effective’’ data were obtained for 19 loci in most of the 32 samples.
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