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 earliest findings were obtained in genetic studies of carnivores (Wayne et al. 1991), humans (Howell et al. 2003) and birds (Garc ıa-Moreno 2004). Subsequent large-scale, data-rich analyses of mitochondrial DNA have revealed time-dependent biases in rate estimates from a broad cross section of taxa (Fig. 1), including insects (Papadopoulou et al. 2010; Ho & Lo 2013), primates and birds (Ho et al. 2005; Subramanian et al. 2009), fish (Genner et al. 2007; Burridge et al. 2008) and amniotes (Molak & Ho 2015). A number of investigations of mitochondrial genome evolution within species have yielded evidence of timedependent rate estimates. "
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    ABSTRACT: We are writing in response to a recent critique by Emerson & Hickerson (2015), who challenge the evidence of a time-dependent bias in molecular rate estimates. This bias takes the form of a negative relationship between inferred evolutionary rates and the ages of the calibrations on which these estimates are based. Here, we present a summary of the evidence obtained from a broad range of taxa that supports a time-dependent bias in rate estimates, with a consideration of the potential causes of these observed trends. We also describe recent progress in improving the reliability of evolutionary rate estimation and respond to the concerns raised by Emerson & Hickerson (2015) about the validity of rates estimated from time-structured sequence data. In doing so, we hope to dispel some misconceptions and to highlight several research directions that will improve our understanding of time-dependent biases in rate estimates.
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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. "
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    ABSTRACT: Population histories depend on the interplay between exogeneous and endogeneous factors. In marine species, phylogeographic and demographic patterns are often shaped by sea level fluctuations, water currents and dispersal ability. Using mitochondrial control region sequences (n = 120), we infer phylogeographic structure and historic population size changes of a common littoral fish species, the black-faced blenny Tripterygion delaisi (Perciformes, Blennioidei, Tripterygiidae) from the north-eastern Adriatic Sea. We find that Adriatic T. delaisi are differentiated from conspecific populations in the remaining Mediterranean, but display little phylogeographic structure within the Adriatic basin. The pattern is consistent with passive dispersal of planktonic larvae along cyclonic currents within the Adriatic Sea, but limited active dispersal of adults. Demographic reconstructions are consistent with recent population expansion, probably triggered by rising sea levels after the last glacial maximum (LGM). Placing the onset of population growth between the LGM and the warming of surface waters (18 000–13 000 years BP) and employing a novel expansion dating approach, we inferred a substitution rate of 2.61–3.61% per site per MY. Our study is one of only few existing investigations of the genetic structure of animals within the Adriatic basin and is the first to provide an estimate for mitochondrial control region substitution rates in blennioid fishes.
    Full-text · Article · Oct 2015 · Journal of Zoological Systematics and Evolutionary Research
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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.
    Full-text · Article · Mar 2015 · PeerJ
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