Nucleotide diversity and linkage disequilibrium in loblolly pine

doi:10.1073/pnas.0404231101

Nucleotide diversity and linkage disequilibrium in loblolly pine

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)

Abstract

Outbreeding species with large, stable population sizes, such as widely distributed conifers, are expected to harbor relatively more DNA sequence polymorphism. Under the neutral theory of molecular evolution, the expected heterozygosity is a function of the product 4N _eμ, where N _e is the effective population size and μ is the per-generation mutation rate, and the genomic scale of linkage disequilibrium is determined by 4N _e r, where r is the per-generation recombination rate between adjacent sites. These parameters were estimated in the long-lived, outcrossing gymnosperm loblolly pine (Pinus taeda L.) from a survey of single nucleotide polymorphisms across ≈18 kb of DNA distributed among 19 loci from a common set of 32 haploid genomes. Estimates of 4N _eμ at silent and nonsynonymous sites were 0.00658 and 0.00108, respectively, and both were statistically heterogeneous among loci. By Tajima's D statistic, the site frequency spectrum of no locus was observed to deviate from that predicted by neutral theory. Substantial recombination in the history of the sampled alleles was observed and linkage disequilibrium declined within several kilobases. The composite likelihood estimate of 4N _e r based on all two-site sample configurations equaled 0.00175. When geological dating, an assumed generation time (25 years), and an estimated divergence from Pinus pinaster Ait. are used, the effective population size of loblolly pine should be 5.6 × 10⁵. The emerging narrow range of estimated silent site heterozygosities (relative to the vast range of population sizes) for humans, Drosophila, maize, and pine parallels the paradox described earlier for allozyme polymorphism and challenges simple equilibrium models of molecular evolution.

Footnotes

↵ ¶ To whom correspondence should be addressed. E-mail: dbneale{at}ucdavis.edu.
↵ † Present address: Vialactia Biosciences, Auckland 1031, New Zealand.
This paper was submitted directly (Track II) to the PNAS office.
Abbreviations: LD, linkage disequilibrium; SNP, single nucleotide polymorphism; indel, insertion/deletion.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AY648063-AY648094, AY670330-AY670645, AY752403-AY752466, and AY764393-AY764928).