Geological Dates and Molecular Rates: Fish DNA Sheds Light on Time Dependency

Department of Zoology, University of Otago, Dunedin, New Zealand.
Molecular Biology and Evolution (Impact Factor: 9.11). 05/2008; 25(4):624-33. DOI: 10.1093/molbev/msm271
Source: PubMed


Knowledge of DNA evolution is central to our understanding of biological history, but how fast does DNA change? Previously, pedigree and ancient DNA studies--focusing on evolution in the short term--have yielded molecular rate estimates substantially faster than those based on deeper phylogenies. It has recently been suggested that short-term, elevated molecular rates decay exponentially over 1-2 Myr to long-term, phylogenetic rates, termed "time dependency of molecular rates." This transition has potential to confound molecular inferences of demographic parameters and dating of many important evolutionary events. Here, we employ a novel approach--geologically dated changes in river drainages and isolation of fish populations--to document rates of mitochondrial DNA change over a range of temporal scales. This method utilizes precise spatiotemporal disruptions of linear freshwater systems and hence avoids many of the limitations associated with typical DNA calibration methods involving fossil data or island formation. Studies of freshwater-limited fishes across the South Island of New Zealand have revealed that genetic relationships reflect past, rather than present, drainage connections. Here, we use this link between drainage geology and genetics to calibrate rates of molecular evolution across nine events ranging in age from 0.007 Myr (Holocene) to 5.0 Myr (Pliocene). Molecular rates of change in galaxiid fishes from calibration points younger than 200 kyr were faster than those based on older calibration points. This study provides conclusive evidence of time dependency in molecular rates as it is based on a robust calibration system that was applied to closely related taxa, and analyzed using a consistent and rigorous methodology. The time dependency observed here appears short-lived relative to previous suggestions (1-2 Myr), which has bearing on the accuracy of molecular inferences drawn from processes operating within the Quaternary and mechanisms invoked to explain the decay of rates with time.

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Available from: Jon Waters, Feb 03, 2014
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    • "The internally calibrated estimates obtained in the present study are likely an improvement over values borrowed from distant species. Due to the time dependency of molecular rates (Burridge et al. 2008; Peterson and Masel 2009; Ho et al. 2011; but see Emerson and Hickerson 2015), the very recent calibration points used in our dating restrict the applicability of our substitution rate estimates to analyses of recent evolution, in the scales of tens and perhaps hundreds of thousands of years. "
    Journal of Zoological Systematics and Evolutionary Research 10/2015; 53(4):291-299. DOI:10.1111/jzs.12110 · 1.68 Impact Factor
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    • "We observed this pattern across the entire timescale that was analysed, beyond at least 10 6 years in non-coding markers and 10 7 years in coding markers (Table 1 and Table S4). This is in contrast with previous estimates of the temporal depth of time-dependence, which has been variously estimated at a few hundred years (Richards M in Gibbons, 1998), around 50 kyr (Henn et al., 2009), 200 kyr (Burridge et al., 2008), or 1–2 Myr (Ho et al., 2005; Papadopoulou, Anastasiou & Vogler, 2010). However, our finding of a prolonged decay in molecular rate estimates is consistent with recent evidence from a large-scale analysis of substitution rates in viruses, which revealed a time-dependent bias in rate estimates across a temporal scale spanning 10 orders of magnitude (Duchêne, Holmes & Ho, 2014). "
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    ABSTRACT: Evolutionary timescales can be estimated from genetic data using the molecular clock, often calibrated by fossil or geological evidence. However, estimates of molecular rates in mitochondrial DNA appear to scale negatively with the age of the clock calibration. Although such a pattern has been observed in a limited range of data sets, it has not been studied on a large scale in metazoans. In addition, there is uncertainty over the temporal extent of the time-dependent pattern in rate estimates. Here we present a meta-analysis of 239 rate estimates from metazoans, representing a range of timescales and taxonomic groups. We found evidence of time-dependent rates in both coding and non-coding mitochondrial markers, in every group of animals that we studied. The negative relationship between the estimated rate and time persisted across a much wider range of calibration times than previously suggested. This indicates that, over long time frames, purifying selection gives way to muta-tional saturation as the main driver of time-dependent biases in rate estimates. The results of our study stress the importance of accounting for time-dependent biases in estimating mitochondrial rates regardless of the timescale over which they are inferred.
    PeerJ 03/2015; 3(3). DOI:10.7717/peerj.821 · 2.11 Impact Factor
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    • "However, especially in the case of large ancestral population sizes, a bias in rate estimation arises when one assumes a time of divergence between sister populations and then equates this time with the TMRCA between samples collected from the two sister populations. Unfortunately, the expected difference in splitting times between gene trees and species/population trees as well as the large stochastic variance in coalescent gene tree divergence times are often both ignored in these studies (but see Burridge et al. 2008). This oversight results in a strong upward bias in rate estimates as the assumed calibration time approaches zero (Charlesworth 2010), and the apparent mutation rate is expected to approach infinity as the geologically calibrated time of divergence approaches zero (Tuffley et al. 2012) (Fig. 3). "
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    ABSTRACT: There is increasing momentum surrounding the hypothesis that rates of molecular evolution between individuals within contemporary populations are high, and that these rates decrease as a function of time, perhaps over several millions of years, before reaching stationarity. The implications of this are powerful, potentially reshaping our view of how climate history impacts upon both species distribution patterns and the geographic structuring of genetic variation within species. However, our assessment of the hypothesis reveals a lack of theoretical support and empirical evidence for hypothesized magnitudes of time-dependent rates of molecular evolution, with much of the apparent rate changes coming from artefacts and biases inherent in the methods of rate estimation. Our assessment also reveals a problem with how serial sampling is implemented for mutation rate estimation using ancient DNA samples, rendering published estimates unreliable.This article is protected by copyright. All rights reserved.
    Molecular Ecology 01/2015; 24(4). DOI:10.1111/mec.13070 · 6.49 Impact Factor
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