Accommodating Heterogenous Rates of Evolution in Molecular Divergence Dating Methods: An Example Using Intercontinental Dispersal of Plestiodon (Eumeces) Lizards

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Abstract
Identifying and dating historical biological events is a fundamental goal of evolutionary biology, and recent analytical advances permit the modeling of factors known to affect both the accuracy and the precision of molecular date estimates. As the use of multilocus data sets becomes increasingly routine, it becomes more important to evaluate the potentially confounding effects of rate heterogeneity both within (e.g., codon positions) and among loci when estimating divergence times. Here, using Plestiodon lizards as a test case, we examine the effects of accommodating rate heterogeneity among data partitions on divergence time estimation. Plestiodon inhabits both East Asia and North America, yet both the geographic origin of the genus and timing of dispersal between the continents have been debated. For each of the eight independently evolving loci and a combined data set, we conduct single model and partitioned analyses. We found that extreme saturation has obscured the underlying rate of evolution in the mitochondrial DNA (mtDNA), resulting in severe underestimation of the rate in this locus. As a result, the age of the crown Plestiodon clade was overestimated by 15-17 Myr by the unpartitioned analysis of the combined loci data. However, the application of partition-specific models to the combined data resulted in ages that were fully congruent with those inferred by the individual nuclear loci. Although partitioning improved divergence date estimates of the mtDNA-only analysis, the ages were nonetheless overestimated, thus indicating an inadequacy of our current models to capture the complex nature of mtDNA evolution in over large time scales. Finally, the statistically incongruent age distributions inferred by the partitioned and unpartitioned analyses of the combined data support mutually exclusive hypotheses of the timing of intercontinental dispersal of Plestiodon from Asia to North America. Analyses that best capture the rate of evolution in the combined data set infer that this exchange occurred via Beringia ∼18.0-30 Ma.