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.
Highlights
DNA polymorphisms provide an invaluable means to study the influence of historical processes that shape genetic diversity, such as divergence times, gene flow, and fluctuations in population sizes
An Old World (OW) population occurs from Spain to Japan, and a New World (NW) population occurs from Alaska to the east coast of North America
Genetic evidence suggests that population structure within continents is limited to a few peripheral populations that differ from the remaining populations in mitochondrial DNA haplotype frequencies [10,38], but that nuclear DNA is consistent with a single panmictic population within each continent [10]
Summary
DNA polymorphisms provide an invaluable means to study the influence of historical processes that shape genetic diversity, such as divergence times, gene flow, and fluctuations in population sizes. Coalescent methods incorporate the stochastic variance of genetic processes by estimating parameters from many genealogies consistent with the data, and provide a framework for testing competing hypotheses while accounting for uncertainty (i.e., confidence intervals) in parameter estimates [3,4]. A multilocus approach has been motivated by two fundamental problems with single-locus studies: the stochasticity of mutation and genetic drift creates variable signatures in DNA even when different loci experienced identical population histories [3,13,14], and single-locus studies do not adequately address the possibility that selection, not population history, has generated patterns in DNA [15,16,17]. Drift, and selection operate independently on unlinked loci, applying coalescent methods to multiple loci can strengthen inferences of population history
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