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

Abstract

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.

Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species

“…However, because pervasive purifying selection is widespread among taxa, it is expected that similar selective processes would have occurred on a comparable timescale in the evolution of the taxa on which we based our clock rate priors (Meiklejohn et al, 2007;Burridge et al, 2008).…”

“…Because inclusion of codons under positive selection may bias divergence estimates, we also removed putatively selected codons from the analysed dataset. Clock rates were chosen to encompass a range of mitochondrial time-dependent rates for comparably recent (o3 million years) divergences of galaxiids and other fishes, calibrated on the basis of geologically dated changes in river drainages and isolation events (0.003-0.13 substitutions/site/ million years; Burridge et al, 2008). To account for uncertainty in clock rates, we sampled clock rates from a distribution rather than setting fixed rates.…”

Comparing Evolutionary Patterns and Variability in the Mitochondrial Control Region and Cytochrome b in Three Species of Baleen Whales

“…Yet such discrepancies may indicate that rate heterogeneity and other features of the control region in humans rapidly generate homoplasy that complicates estimates of rates. Recent studies on time dependence of molecular rates indicate that substitution rates are generally underestimated in a phylogenetic comparison of old divergences, and that comparing more recently diverged taxa provides better estimates of instantaneous substitution rates (Ho et al 2005;Ho and Larson 2006;Burridge et al 2008). For whales, fossil dates for divergences are old because the fossil record of modern species is poor.…”

Molecular clock debate: Time dependency of molecular rate estimates for mtDNA: this is not the time for wishful thinking

“…The latest example is the impressive study of fish mtDNA evolution (Burridge et al, 2008) where time-dependent rates are observed and , at least in part, due to the operation of purifying selection. However, pedigree rates do offer us an important insight to the early phase of selection (and other important evolutionary processes such as random genetic drift and bottlenecks) and this is why we must note here our disagreements with Dr Bandelt.…”