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Heterogeneity in Genetic Diversity among Non-Coding Loci Fails to Fit Neutral Coalescent Models of Population History

By Jeffrey L. Peters, Trina E. Roberts, Kevin Winker and Kevin G. McCracken

Abstract

Inferring aspects of the population histories of species using coalescent analyses of non-coding nuclear DNA has grown in popularity. These inferences, such as divergence, gene flow, and changes in population size, assume that genetic data reflect simple population histories and neutral evolutionary processes. However, violating model assumptions can result in a poor fit between empirical data and the models. We sampled 22 nuclear intron sequences from at least 19 different chromosomes (a genomic transect) to test for deviations from selective neutrality in the gadwall (Anas strepera), a Holarctic duck. Nucleotide diversity among these loci varied by nearly two orders of magnitude (from 0.0004 to 0.029), and this heterogeneity could not be explained by differences in substitution rates alone. Using two different coalescent methods to infer models of population history and then simulating neutral genetic diversity under these models, we found that the observed among-locus heterogeneity in nucleotide diversity was significantly higher than expected for these simple models. Defining more complex models of population history demonstrated that a pre-divergence bottleneck was also unlikely to explain this heterogeneity. However, both selection and interspecific hybridization could account for the heterogeneity observed among loci. Regardless of the cause of the deviation, our results illustrate that violating key assumptions of coalescent models can mislead inferences of population history

Topics: Research Article
Publisher: Public Library of Science
OAI identifier: oai:pubmedcentral.nih.gov:3285185
Provided by: PubMed Central
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    1. (2006). A ˚kesson S
    2. (2007). A new approach to estimate parameters of speciation models with application to apes.
    3. (2001). A new statistical method for haplotype reconstruction from population data.
    4. (2008). A phylogenomic study of birds reveals their evolutionary history.
    5. (2004). A physical map of the chicken genome.
    6. (1987). A test of neutral molecular evolution based on nucleotide data.
    7. (2009). A welltested set of primers to amplify regions spread across the avian genome.
    8. (2005). Adaptive evolution of non-coding
    9. (2005). Arlequin (version 3.0): An integrated software package for population genetics data analysis.
    10. (1991). Avian CD4 and CD8 interact with a cellular tyrosine protein kinase homologous to mammalian p56lck.
    11. (2005). Bayesian coalescent inference of past population dynamics from molecular sequences.
    12. (2010). Bayesian inference of species trees from multilocus data.
    13. (2006). Challenges of detecting directional selection after a bottleneck: Lessons from Sorghum bicolor.
    14. (1998). Chicken CD4, CD8ab, and CD8aa T Cell co-receptor molecules.
    15. (2005). Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes.
    16. (2005). Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species.
    17. (2006). Contrasting patterns of sequence divergence and base composition between Drosophila introns and intergenic regions.
    18. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing.
    19. (2000). Detecting bottlenecks and selective sweeps from DNA sequence polymorphism.
    20. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.
    21. (2001). Did the Pleistocene glaciations promote divergence? Tests of explicit refugial models in montane grasshoppers.
    22. (1973). Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms.
    23. (2008). Divergence across Australia’s Carpentarian barrier: Statistical phylogeography of the red-backed fairy wren (Malurus melanocephalus).
    24. (2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods.
    25. (2008). Duplication and accelerated evolution of growth hormone gene in passerine birds.
    26. (2003). Fedorov A
    27. (1997). Fluctuating population size and the ratio of effective to census population size.
    28. (2011). Gene flow and hybridization between numerically imbalanced populations of two duck species in the Falkland Islands.
    29. (2009). Gene flow and species delimitation.
    30. (2009). Gene flow in the face of countervailing selection: Adaptation to highaltitude hypoxia in the beta A hemoglobin subunit of yellow-billed pintails in the Andes.
    31. (1990). Gene genealogies and the coalescent process.
    32. (2002). Genealogical trees, coalescent theory and the analysis of genetic polymorphisms.
    33. (2002). Generating samples under a Wright-Fisher neutral model of genetic variation.
    34. (2000). Genetic drift in an infinite population: The pseudohitchhiking model.
    35. (2004). Heterogeneous patterns of variation among multiple human X-Linked loci.
    36. (2010). How robust are ‘‘Isolation with Migration’’ analyses to violations of the IM model? A simulation study.
    37. (2005). Hybridization as an invasion of the genome.
    38. (1960). Hybridization in the Anatidae and its taxonomic implications.
    39. (2002). Hybridization patterns and the evolution of reproductive isolation in ducks.
    40. (2000). Inference of population structure using multilocus genotype data.
    41. (2008). Integrating phylogenetic and population genetic analyses of multiple loci to test species divergence hypotheses in Passerina buntings.
    42. (2011). Interpreting the estimated timing of migration events between hybridizing species.
    43. (2005). Is homoplasy or lineage sorting the source of incongruent mtDNA and nuclear gene trees in the stiff-tailed ducks (Nomonyx-Oxyura)?
    44. (2010). Isolation with migration models for more than two populations.
    45. (2006). LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters.
    46. (2009). Learning about modes of speciation by computational approaches.
    47. (2007). Looking for Darwin in all the wrong places: The misguided quest for positive selection at the nucleotide sequence level.
    48. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
    49. (2008). Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris—Large effective population sizes and rates of long-term gene flow.
    50. (2003). More taxa, more characters: The hoatzin problem is still unresolved.
    51. (2007). Multi-locus phylogeography of the dusky dolphin (Lagenorhynchus obscurus): Passive dispersal via the west-wind drift or response to prey species and climate change?
    52. (2004). Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis.
    53. (2005). Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations.
    54. (2011). Multilocus phylogeography and population structure of common eiders breeding in North America and Scandinavia.
    55. (2008). Multilocus phylogeography of a Holarctic duck: Colonization of North America from Eurasia by gadwall (Anas strepera).
    56. (2007). Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between gadwall and falcated duck (Anas spp.).
    57. (2010). Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera).
    58. (2005). On the number of New World founders: A population genetic portrait of the peopling of the Americas.
    59. (2004). Parallel radiations in the primary clades of birds.
    60. (2004). Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila.
    61. (2008). Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata.
    62. (2000). Perspective: Gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies.
    63. (2005). Phylogenetics of wigeons and allies (Anatidae: Anas): The importance of sampling multiple loci and multiple individuals.
    64. (2006). Population size does not influence mitochondrial genetic diversity in animals.
    65. (2007). Population structure and mitochondrial polyphyly in North American gadwalls (Anas strepera).
    66. (2008). Positive and negative selection on noncoding DNA in Drosophila simulans.
    67. (1994). Posterior predictive P-values.
    68. (2007). Purifying selection maintains highly conserved noncoding sequences in Drosophila.
    69. (2006). Rambaut A
    70. (2007). Recombination and linkage disequilibrium in Arabidopsis thaliana.
    71. (2007). Recombination-filtered genomic datasets by information maximization.
    72. (1999). Roehl A
    73. (2006). Selection, recombination and demographic history in Drosophila miranda.
    74. (2010). Seqphase: A web tool for interconverting phase input/output files and fasta sequence alignments.
    75. (2009). Signatures of high-altitude adaptation in the major hemoglobin of five species of Andean dabbling ducks.
    76. (2003). Signatures of natural selection in the human genome.
    77. (1938). Size of population and breeding structure in relation to evolution.
    78. (2010). Speciation in the European rabbit (Oryctolagus cuniculus): Islands of differentiation on the X chromosome and autosomes.
    79. (1989). Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism.
    80. (2009). Statistical Phylogeography.
    81. (2009). Team
    82. (1989). The biologic roles of CD2, CD4, and CD8 in T-cell Activation.
    83. (2009). The chicken gene nomenclature committee report.
    84. (1982). The coalescent.
    85. (1989). The effect of change in population size on DNA polymorphism.
    86. (2006). The evolution of spliceosomal introns: Patterns, puzzles and progress.
    87. (1974). The hitch-hiking effect of a favourable gene.
    88. (2008). The impact of natural selection on the genome: Emerging patterns in Drosophila and Arabidopsis.
    89. (2004). The incomplete natural history of mitochondria.
    90. (1983). The neutral theory of molecular evolution. Cambridge:
    91. (2007). The variance of coalescent time estimates from DNA sequences.
    92. (2000). When did the human population size start increasing?

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