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

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.

SUBMITTER: Peters JL

PROVIDER: S-EPMC3285185 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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

Peters Jeffrey L JL Roberts Trina E TE Winker Kevin K McCracken Kevin G KG

PloS one 20120222 2

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 genomi ...[more]

PMID: 22384117

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Project description:The establishment and spread of aquatic invasive species are ecologically and economically harmful and a source of conservation concern internationally. Processes of species invasion have traditionally been inferred from observational data of species presence/absence and relative abundance. However, genetic-based approaches can provide valuable sources of inference. Restriction site-associated DNA sequencing was used to identify and genotype single nucleotide polymorphism (SNP) loci for Round Gobies (Neogobius melanostomus) (N = 440) from 18 sampling locations in the Great Lakes and in three Michigan, USA, drainages (Flint, Au Sable, and Cheboygan River basins). Sampled rivers differed in size, accessibility, and physical characteristics including man-made dispersal barriers. Population levels of genetic diversity and interpopulation variance in SNP allele frequency were used in coalescence-based approximate Bayesian computation (ABC) to statistically compare models representing competing hypotheses regarding source population, postcolonization dispersal, and demographic history in the Great Lakes and inland waters. Results indicate different patterns of colonization across the three drainages. In the Flint River, models indicate a strong population bottleneck (<3% of contemporary effective population size) and a single founding event from Saginaw Bay led to the colonization of inland river segments. In the Au Sable River, analyses could not distinguish potential source populations, but supported models indicated multiple introductions from one source population. In the Cheboygan River, supported models indicated that colonization likely proceeded from east (Lake Huron source) to west among inland locales sampled in the system. Despite the recent occupancy of Great Lakes and inland habitats, large numbers of loci analyzed in an ABC framework enable statistically supported identification of source populations and reconstruction of the direction of inland spread and demographic history following establishment. Information from analyses can direct management actions to limit the spread of invasive species from identified sources and most probable vectors into additional inland aquatic habitats.

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Project description:BackgroundAccurate modelling of substitution processes in protein-coding sequences is often hampered by the computational burdens associated with full codon models. Lately, codon partition models have been proposed as a viable alternative, mimicking the substitution behaviour of codon models at a low computational cost. Such codon partition models however impose independent evolution of the different codon positions, which is overly restrictive from a biological point of view. Given that empirical research has provided indications of context-dependent substitution patterns at four-fold degenerate sites, we take those indications into account in this paper.ResultsWe present so-called context-dependent codon partition models to assess previous empirical claims that the evolution of four-fold degenerate sites is strongly dependent on the composition of its two flanking bases. To this end, we have estimated and compared various existing independent models, codon models, codon partition models and context-dependent codon partition models for the atpB and rbcL genes of the chloroplast genome, which are frequently used in plant systematics. Such context-dependent codon partition models employ a full dependency scheme for four-fold degenerate sites, whilst maintaining the independence assumption for the first and second codon positions.ConclusionsWe show that, both in the atpB and rbcL alignments of a collection of land plants, these context-dependent codon partition models significantly improve model fit over existing codon partition models. Using Bayes factors based on thermodynamic integration, we show that in both datasets the same context-dependent codon partition model yields the largest increase in model fit compared to an independent evolutionary model. Context-dependent codon partition models hence perform closer to codon models, which remain the best performing models at a drastically increased computational cost, compared to codon partition models, but remain computationally interesting alternatives to codon models. Finally, we observe that the substitution patterns in both datasets are drastically different, leading to the conclusion that combined analysis of these two genes using a single model may not be advisable from a context-dependent point of view.

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

Publications

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

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