Examining the role of effective population size on mitochondrial and multilocus divergence time discordance in a songbird.

Brian Tilston Smith,John Klicka,Jose Castresana

doi:10.1371/journal.pone.0055161

Abstract

Estimates of speciation times are subject to a number of potential errors. One source of bias is that effective population size (Ne) has been shown to influence substitution rates. This issue is of particular interest for phylogeographic studies because population sizes can vary dramatically among genetically structured populations across species’ ranges. In this study, we used multilocus data to examine temporal phylogeographic patterns in a widespread North American songbird, the Northern Cardinal (Cardinalis cardinalis). Species tree estimation indicated that the phylogeographic structure of C. cardinalis was comprised of four well-supported mainland lineages with large population sizes (large Ne) and two island lineages comprised of much smaller populations (small Ne). We inferred speciation times from mtDNA and multilocus data and found there was discordance between events that represented island-mainland divergences, whereas both estimates were similar for divergences among mainland lineages. We performed coalescent simulations and found that the difference in speciation times could be attributed to stochasticity for a recently diverged island lineage. However, the magnitude of the change between speciation times estimated from mtDNA and multilocus data of an older island lineage was substantially greater than predicted by coalescent simulations. For this divergence, we found the discordance in time estimates was due to a substantial increase in the mtDNA substitution rate in the small island population. These findings indicate that in phylogeographic studies the relative tempo of evolution between mtDNA and nuclear DNA can become highly discordant in small populations.

Highlights

Reconstructing the phylogeographic history of species is reliant on having accurate estimates of speciation times
A growing body of literature has shown that effective population size may influence a species substitution rate, but it is unclear whether accelerated substitution rates are attributed to populations being large or small
We found that small populations are subject to both, stochastic effects that give the appearance of a rate increase and actual elevated substitution rates

Summary

Introduction

Reconstructing the phylogeographic history of species is reliant on having accurate estimates of speciation times. Studies have shown substitution rates can vary among closely related species or even within species that have different Ne [8] This issue is of particular interest for phylogeographic studies because population sizes in species can vary dramatically across their ranges. The nearly neutral model of evolution predicts that slightly deleterious mutations will become fixed at a higher rate in small populations [10] In larger populations, these slightly deleterious mutations are presumed to be removed by purifying selection. These DNA substitutions result in either a change in the amino acid (nonsynonymous change) that is subject to selection or a redundant change in the codon sequence (synonymous change) that presumably does not affect fitness. One approach that attempts to explain the variation observed in amino acid changes is the estimation of the nonsynonymous/ synonymous substitution rate ratio (dN/dS) between lineages with different sized Ne

Methods

Results

Discussion

Conclusion