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Heterogeneity in genetic diversity among non-coding loci fails to fit neutral coalescent models of population history.

Peters JL, Roberts TE, Winker K, McCracken KG - PLoS ONE (2012)

Bottom Line: However, violating model assumptions can result in a poor fit between empirical data and the models.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Wright State University, Dayton, Ohio, United States of America. jeffrey.peters@wright.edu

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.

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Two-island model results.Mean and 95% HPDs of estimates of the five parameters from the two-island model of population divergence. Gray shading indicates the joint estimates obtained by multiplying the posteriors among loci. Loci are ranked by nucleotide diversity from low to high.
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pone-0031972-g005: Two-island model results.Mean and 95% HPDs of estimates of the five parameters from the two-island model of population divergence. Gray shading indicates the joint estimates obtained by multiplying the posteriors among loci. Loci are ranked by nucleotide diversity from low to high.

Mentions: The two-island model of population divergence suggested high heterogeneity in Θ among the 22 loci, even after controlling for heterogeneous substitution rates (including uncertainty in μR; Fig. 5). The 95% highest posterior distributions (HPDs) did not overlap for 35 pairs of loci for ΘOW, but overlapped between all pairs for ΘNW. Calculating joint estimates of Θ resulted in a narrow range of values that were consistent with the observed genetic diversity at all loci for both OW (Θ = 0.0092, 95% HPD = 0.0077–0.011) and NW (Θ = 0.0042, 95% HPD = 0.0028–0.0052) populations (Fig. 5). Regardless, 17 loci and the joint estimates supported higher effective population sizes for OW gadwalls relative to NW gadwalls. Estimates of M among loci were less heterogeneous, with 7 and 6 pairs of loci having non-overlapping 95% HPDs for MOW and MNW, respectively (Fig. 5). Joint estimates of M suggested higher gene flow (forward in time) into North America (MNW = 1480, 95% = 1050–1850) than into Eurasia (MOW = 1010, 95% CI = 660–1340). Recombination rates also varied significantly among loci, with higher-diversity loci tending to have higher recombination rates, although low-diversity loci contained little information regarding recombination (Fig. 5).


Heterogeneity in genetic diversity among non-coding loci fails to fit neutral coalescent models of population history.

Peters JL, Roberts TE, Winker K, McCracken KG - PLoS ONE (2012)

Two-island model results.Mean and 95% HPDs of estimates of the five parameters from the two-island model of population divergence. Gray shading indicates the joint estimates obtained by multiplying the posteriors among loci. Loci are ranked by nucleotide diversity from low to high.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3285185&req=5

pone-0031972-g005: Two-island model results.Mean and 95% HPDs of estimates of the five parameters from the two-island model of population divergence. Gray shading indicates the joint estimates obtained by multiplying the posteriors among loci. Loci are ranked by nucleotide diversity from low to high.
Mentions: The two-island model of population divergence suggested high heterogeneity in Θ among the 22 loci, even after controlling for heterogeneous substitution rates (including uncertainty in μR; Fig. 5). The 95% highest posterior distributions (HPDs) did not overlap for 35 pairs of loci for ΘOW, but overlapped between all pairs for ΘNW. Calculating joint estimates of Θ resulted in a narrow range of values that were consistent with the observed genetic diversity at all loci for both OW (Θ = 0.0092, 95% HPD = 0.0077–0.011) and NW (Θ = 0.0042, 95% HPD = 0.0028–0.0052) populations (Fig. 5). Regardless, 17 loci and the joint estimates supported higher effective population sizes for OW gadwalls relative to NW gadwalls. Estimates of M among loci were less heterogeneous, with 7 and 6 pairs of loci having non-overlapping 95% HPDs for MOW and MNW, respectively (Fig. 5). Joint estimates of M suggested higher gene flow (forward in time) into North America (MNW = 1480, 95% = 1050–1850) than into Eurasia (MOW = 1010, 95% CI = 660–1340). Recombination rates also varied significantly among loci, with higher-diversity loci tending to have higher recombination rates, although low-diversity loci contained little information regarding recombination (Fig. 5).

Bottom Line: However, violating model assumptions can result in a poor fit between empirical data and the models.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Wright State University, Dayton, Ohio, United States of America. jeffrey.peters@wright.edu

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.

Show MeSH