Abstract

Mitochondrial sequence data is often used to reconstruct the demographic history of Pleistocene populations in an effort to understand how species have responded to past climate change events. However, departures from neutral equilibrium conditions can confound evolutionary inference in species with structured populations or those that have experienced periods of population expansion or decline. Selection can affect patterns of mitochondrial DNA variation and variable mutation rates among mitochondrial genes can compromise inferences drawn from single markers. We investigated the contribution of these factors to patterns of mitochondrial variation and estimates of time to most recent common ancestor (TMRCA) for two clades in a co-operatively breeding avian species, the white-browed babbler Pomatostomus superciliosus. Both the protein-coding ND3 gene and hypervariable domain I control region sequences showed departures from neutral expectations within the superciliosus clade, and a two-fold difference in TMRCA estimates. Bayesian phylogenetic analysis provided evidence of departure from a strict clock model of molecular evolution in domain I, leading to an over-estimation of TMRCA for the superciliosus clade at this marker. Our results suggest mitochondrial studies that attempt to reconstruct Pleistocene demographic histories should rigorously evaluate data for departures from neutral equilibrium expectations, including variation in evolutionary rates across multiple markers. Failure to do so can lead to serious errors in the estimation of evolutionary parameters and subsequent demographic inferences concerning the role of climate as a driver of evolutionary change. These effects may be especially pronounced in species with complex social structures occupying heterogeneous environments. We propose that environmentally driven differences in social structure may explain observed differences in evolutionary rate of domain I sequences, resulting from longer than expected retention times for matriarchal lineages in the superciliosus clade.

Highlights

  • The use of mitochondrial DNA as a marker for studying the demographic and evolutionary history of natural populations is widely established [1]

  • As population size expansion leads to changes in the frequency distribution of haplotypes we calculated Strobeck’s S statistic [42] and R2 [43]

  • Strobeck’s S statistic provides the probability of observing a sample that has the same or fewer haplotypes than h whereas R2 contrasts the number of singletons and the mean number of differences amongst haplotypes

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Summary

Introduction

The use of mitochondrial DNA (mtDNA) as a marker for studying the demographic and evolutionary history of natural populations is widely established [1]. Numerous studies have demonstrated that the mitochondrial genome shows departures from neutral equilibrium expectations due to the effect of selection (mutation-drift disequilibrium) or population processes (migration-drift disequilibrium). Failure to account for non-equilibrium conditions can lead to serious errors in the estimation of demographic parameters such as changes in effective population size and the timing of expansion or bottleneck events. Selection for adaptive mutations may vary in the effect they have on populations of different sizes [4], leading to a weak or unpredictable relationship between mtDNA diversity and population size [5]. In species with sexbiased dispersal, for example, rare alleles can become fixed within philopatric social groups [6], increasing the amount of betweengroup variation leading to an effective population size greater than the number of breeding adults [7]

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