© 2007 Society of Systematic Biologists
Geological Dates and Molecular Rates: Rapid Divergence of Rivers and Their Biotas
Edited by Jack Sullivan: Associate Editor
1 Department of Zoology, University of Otago PO Box 56, Dunedin, New Zealand E-mail: jonathan.waters{at}stonebow.otago.ac.nz (J.W.)
2 Department of Geology, University of Otago PO Box 56, Dunedin, New Zealand
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Abstract |
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 Top Abstract Molecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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We highlight a novel molecular clock calibration system based on geologically dated river reversal and river capture events. Changes in drainage pattern may effect vicariant isolation of freshwater taxa, and thus provide a predictive framework for associated phylogeographic study. As a case in point, New Zealand's Pelorus and Kaituna rivers became geologically isolated from the larger Wairau River system 70 to 130 kyr BP. We conducted mitochondrial DNA phylogeographic analyses of two unrelated freshwater-limited fish taxa native to these river systems (Gobiomorphus breviceps, n = 63; Galaxias divergens, n = 95). Phylogenetic analysis of combined control region and cytochrome b sequences yielded reciprocally monophyletic clades of Pelorus-Kaituna and Wairau haplotypes for each species. Calibrated rates of molecular change based on this freshwater vicariant event are substantially faster than traditionally accepted rates for fishes but consistent with other recent inferences based on geologically young calibration points. A survey of freshwater phylogeographic literature reveals numerous examples in which the ages of recent evolutionary events may have been substantially overestimated through the use of "accepted" calibrations. We recommend that—wherever possible—biologists should start to reassess the conclusions of such studies by using more appropriate molecular calibrations derived from recent geological events.
Keywords: Biogeography; calibrations; coalescent; fish; freshwater; geomorphology; geology; molecular clock; mutation rate; palaeogeography; Pleistocene; purifying selection; refugia; time dependency; vicariance
Received August 21, 2006; Revised October 15, 2006; Accepted November 22, 2006
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Molecular Calibrations |
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TopAbstractMolecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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Geological dating underpins our knowledge of biological evolution (e.g., Keigwin, 1982; King, 2000), but evolutionary biology is yet to fully benefit from geological information. Geologically based calibrations of molecular evolution provide an important method for formulating and testing evolutionary hypotheses and for understanding timeframes of biodiversification (Rambaut and Bromham, 1998; Bromham, 2003; Bromham and Penny, 2003; Sanmartín and Ronquist, 2004). To this end, many researchers have relied upon "accepted" rates of mitochondrial DNA (mtDNA) nucleotide substitutions derived from early phylogenetic studies (calibrated using fossil data; typically 0.005 to 0.010 substitutions/site/lineage/Myr; Brown et al., 1979, 1982) and have often assumed that these are accurate and applicable across taxonomic divisions. However, some multitaxon studies have reported substantial interspecific variation in mtDNA substitution rates (Bermingham et al., 1997). In addition, recent mtDNA calibrations based on known pedigrees (Howell et al., 2003) and carbon-dated subfossil material (Lambert et al., 2002) have yielded rapid rates of change that are inconsistent with, and perhaps decoupled from, changes that become assimilated through deeper evolutionary time (Ho et al., 2005; Penny, 2005; Ho and Larson, 2006). Given the apparent incongruence between rate calibrations based on ancient versus recent timescales and among distinct taxa, it is highly desirable to undertake calibrations across a wide range of geological ages within a group of closely related taxa to help elucidate rates of molecular evolution and, specifically, to verify whether these rates change through time—the "lazy J" pattern of Ho et al. (2005) as described by Penny (2005).
Traditionally, fossil evidence has been viewed as an important means of calibrating rates of molecular change and of dating evolutionary events. The potential problems inherent in this method, however, are well documented (Bromham et al., 1999; Perez-Losada et al., 2004). First, fossil records are incomplete, have been largely eroded, and typically give only a minimum age for a particular taxon. Second, it is often difficult to establish with confidence evolutionary relationships between extant and fossil organisms.
In the absence of useful fossil data, calibration of rates of molecular change often relies on correlations between genetic distance and palaeogeographic information. As it stands, however, the literature contains few geological events that can be confidently linked to specific phylogeographic breaks. Some studies have used oceanic island formation to estimate rates, such as the Hawaiian Islands (Fleischer et al., 1998; Price and Clague, 2002; Roderick and Gillespie, 1998; Gillespie and Roderick, 2002) and the Canary Islands (Thorpe et al., 1995; Gubitz et al., 2000; Brehm et al., 2003). However, island colonization represents dispersal rather than vicariance, so calibrations against island emergence may be misleading in many cases. For instance, Hawaiian Drosophila may have colonized the developing island chain 40 Mya, well before the formation of the oldest island presently inhabited (5 Mya; Beverley and Wilson, 1985; Lewin, 1985). Conversely, some island taxa may have colonized only recently, leading to potential underestimates of rates. Other rate calibrations have relied on a single geological data point, such as the rise of the Panama Isthmus 3.1 to 3.5 Mya (Vawter et al., 1980; White, 1986; Bermingham and Lessios, 1993; Lessios and Weinberg, 1994; Bermingham et al., 1997; Donaldson and Wilson, 1999; Bowen et al., 2001; Marko, 2002). Although the isthmus undoubtedly played a significant biogeographic role—perhaps a 50% increase in regional marine biodiversity (McKinney, 1998)—it gradually disrupted marine biota along a broad axis, and thus its precision as a spatiotemporal calibration point remains questionable (Knowlton and Weigt, 1998). For instance, Indo-Pacific genetic disjunctions are evident within numerous tropical marine taxa, despite the fact that the Indo-Malayan archipelago has provided only incomplete physical isolation (e.g., Chenoweth et al., 1998; Benzie, 1999a, 1999b). It therefore seems likely that Pacific and Caribbean populations of many tropical taxa diverged well before the cessation of marine connections across Panama (see Bermingham et al., 1997).
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River Capture, River Reversal |
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TopAbstractMolecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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Given the potential problems associated with traditional calibration methods outlined above, in this study we highlight a recent form of molecular calibration based on historical changes in riverine connections. River capture can be defined as the displacement of stream sections between adjacent catchments (Bishop, 1995), vicariantly isolating populations that previously inhabited the same system (Fig. 1). Similarly, flow reversal within part of a river system will result in vicariant isolation of populations on either side of the new drainage divide (Fig. 1).
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River capture and reversal represent precise spatiotemporal disruptions of linear systems (Waters et al., 2001), unlike the more gradual disruption caused by biogeographic events such as the uplift of Panama. As such, they are "sharp" vicariant events that promote genetic divergence in freshwater-limited species. River capture and reversal hypotheses are readily testable through genetic analysis of aquatic taxa that, under vicariance, are predicted to retain phylogeographic signatures of palaeodrainages. Such hypotheses are testable, with or without well-calibrated molecular clocks (Page, 1989). We have already demonstrated through genetic analysis that river capture is one of the key factors underlying the diversification of New Zealand's freshwater-limited galaxiid fishes (Waters et al., 2001, 2006; Burridge et al., 2006). Studies from many parts of the world similarly suggest that evolutionary histories of rivers often impact significantly on their associated aquatic taxa (e.g., Mayden, 1988; Musyl and Keenan, 1992; Howard and Morgan, 1993; Gollmann et al., 1997, Hurwood and Hughes, 1998; Strange, 1998; Engelbrecht et al., 2000; Kreiser et al., 2001; Poissant et al., 2005). This link between drainage history and phylogeography provides an experimental framework analogous to studies of host-parasite cospeciation, in which rivers are "hosts" and associated aquatic species effectively represent "parasites."
Tectonically active landscapes with well-characterized geomorphologies provide ideal systems for the study of palaeohydrology and its biological effects. New Zealand's active Alpine Fault has profoundly impacted regional topography and drainage patterns (Koons, 1995). Specifically, southwest movement of the Pacific Plate relative to the Australian Plate has caused progressive contraction across the eastern South Island, resulting in the growth of mountain ranges and intervening basins over the last 5 Myr. River drainage systems have evolved progressively with time, some valleys becoming "pinched off," whereas others have eroded through intervening drainage divides into new catchments (Craw et al., 1999; Waters et al., 2001). Glaciations of mountains during the Quaternary yielded large volumes of sediment that locally choked valleys and caused river capture (Burridge et al., 2006); associated sea level fluctuations also contributed to changes in drainage geometry.
In the current study we demonstrate the potential for molecular change rate calibrations based on geologically dated alterations in river drainage geometry. Central New Zealand's Pelorus River drained southwards through the Kaituna Valley into the Wairau River system until Kaituna reversal severed this connection in the late Quaternary (Fig 2; Mortimer and Wopereis, 1998). Kaituna River reversal occurred between ca. 70 and 130 kyr BP, after deposition of river terraces associated with regional glaciation (Oxygen Isotope Stage 6, 128 to 186 kyr BP; Begg and Johnston, 2000) and before terrace top sedimentation at ca. 70 kyr BP (optically stimulated luminescence dating; Craw and Waters, 2007). The Pelorus and Kaituna rivers, by contrast, remained confluent until sea levels reached that of their junction (ca. 7 kyr BP). Under vicariance, we predict that freshwater-limited taxa will exhibit phylogeographic relationships consistent with this drainage history (Fig. 3). Phylogeographic analyses of the only freshwater-limited fishes native to all three of these rivers (Galaxias divergens (Galaxiidae); Gobiomorphus breviceps (Eleotridae)) are used to calibrate rates of mtDNA change. The broadscale phylogeography of these taxa has already been described elsewhere (Smith et al., 2005; Burridge et al., 2006; Waters et al., 2006). For the sake of clarity, in the current study we include only samples from the major rivers involved here (Pelorus, Kaituna, Wairau) and exclude populations from additional nearby rivers that have had Holocene connections to the Pelorus-Kaituna (e.g., Keneperu Head Stream) or Wairau (e.g., Robin Hood Bay Stream) systems. In each case, these now isolated populations are genetically very closely related to their "parent" systems (see Burridge et al., 2006; Waters et al., 2006).
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Materials and Methods |
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TopAbstractMolecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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Data Collection
Samples of Galaxias divergens (n = 95) and Gobiomorphus breviceps (n = 63) were obtained from the Pelorus, Kaituna, and Wairau catchments (Appendix 1; Fig. 4). Specimens were collected with pole-nets or electrofishing apparatus and stored on dry ice or placed in 95% ethanol. The number of individuals sequenced per species ranged from 23 to 31 in the Pelorus, 15 to 20 in the Kaituna, and 25 to 39 in the Wairau, and the number of sampling localities per species per catchment ranged from 5 to 8 in the Pelorus, 5 to 6 in the Kaituna, and 8 to 16 in the Wairau. All phylogenetic analyses were rooted with outgroup sequences sourced from northwestern South Island populations (Motueka and Buller rivers; sequences from Smith et al., 2005; Waters et al., 2006).
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Protocols for total DNA extraction, amplification, and sequencing of mitochondrial control region (CR) of galaxiids are described in Waters and Wallis (2001a). Amplification of Gobiomorphus breviceps CR employed the protocol of Smith et al. (2003, 2005), yielding sequences of 385 bp. The complete cytochrome b (cyt b) gene of both species was amplified with primers cytb-Glu and cytb-Thr (Waters and Wallis, 2001b), and sequencing was performed with the former primer, yielding 768 bp for G. divergens and 900 bp for G. breviceps. DNA sequencing was performed using the ABI Prism Big-Dye kit (Applied Biosystems).
Phylogeny Reconstruction
Phylogenetic relationships among mtDNA sequences were reconstructed via maximum parsimony, maximum likelihood, and Bayesian analyses. Parsimony and likelihood analyses were performed by PAUP*4.0b10 (Swofford, 2003) using the heuristic search algorithm with 10 replicates of random sequence addition. Gaps were treated as missing data. Maximum likelihood analyses were performed under a single substitution model across all sites (G. divergens = TrN+
; G. breviceps = TrN+I+), as selected from a set of 56 hierarchically nested candidates using ModelTest 3.7 and the likelihood-ratio test (Posada and Crandall, 1998). Bootstrap analyses (Felsenstein, 1985) employed 10 heuristic searches for each of 5000 bootstrap replicates under parsimony and one heuristic search for each of 370 bootstrap replicates under maximum likelihood.
Bayesian analysis was performed using MrBayes 3.1.2 (Ronquist and Huelsenbeck, 2003), with separate substitution models for CR and cyt b as determined via ModelTest (cyt b = TrN+; G. divergens CR = HKY+I+; G. breviceps CR = F81+). Model parameters were derived from the default prior distributions, and were unlinked among partitions (CR, cyt b). A variable rate prior was employed among partitions. Duplicate Monte Carlo Markov chain searches were performed, each with four chains of 107 generations, and trees were sampled every 102 generations. Three of the chains were heated according to "Temp = 0.1" to improve mixing. Attainment of asymptotes (stationarity) for LnL and nucleotide substitution model parameters was achieved within the first 105 generations. Convergence of runs was indicated by an average standard deviation of split frequencies between duplicate runs of less than 0.01; starting values were 0.13 and 0.11 for G. divergens and G. breviceps, respectively, values less than 0.01 were attained within the first 0.5 x 106 generations, and final values were 
0.002. Consequently, the first 104 trees sampled (106 generations) were discarded as burn-in prior to the calculation of a consensus topology and bipartition posterior probabilities.
Rate Calibration
Rates of molecular change were calibrated via three strategies. Firstly, clock-like evolution of DNA sequences among populations was assessed via a likelihood-ratio test (Felsenstein, 1988). We restricted our analysis to the Pelorus, Kaituna, and Wairau populations, plus a single outgroup individual (from the Motueka), thereby ignoring any non-clock-like evolution among outgroup taxa. The appropriate nucleotide substitution models for the analysis of these reduced data sets were TrN+ for G. divergens and TrN+I+ for G. breviceps (cyt b + CR). Given significant deviation from clock-like evolution, we adopted Sanderson's (2002) penalized likelihood (PL) method—a semiparametric approach—to account for intraspecific rate heterogeneity across each data set. Specifically, rates of molecular change associated with the geologically constrained node (Pelorus-Kaituna versus Wairau, 70 to 130 kyr BP) were estimated using the truncated Newton (TN) algorithm, incorporating an additive penalty function implemented in the software r8s 1.71 (Sanderson, 2003). Optimal "smoothing" parameters for each species were determined empirically using the cross-validation procedure recommended by Sanderson (2003). Calculations were repeated multiple times to assess sensitivity to variation in the smoothing parameter. However, this approach offers no correction for genetic distance that already existed at the time populations were physically isolated.
Net sequence distances between sister clades were calculated as 
= dij– 0.5(di + dj), where d is the maximum genetic distance between haplotypes located in either clade i or j, under the appropriate model of nucleotide substitution based on Wairau, Pelorus, and Kaituna haplotypes (G. divergens cyt b + CR, CR and G. breviceps CR = TrN+; G. divergens cyt b = HKY+I+ ; G. breviceps cyt b + CR = TrN+I+; G. breviceps CR = F81). Net sequence distance offers compensation for genetic diversity already present in the ancestral population at the time of vicariance, assuming that it is approximated by contemporary intra-population distances.
Coalescent simulations under the four-parameter isolation model (Wakeley and Hey, 1997) were also employed to accommodate differences in the time since the most recent common ancestor of contemporary haplotypes and the physical isolation of populatons. Using the IM software (Hey and Nielsen 2006), genealogical topologies were simulated and updated along a Monte Carlo Markov chain during which the four model parameters (divergence time, ancestral, and two contemporary population sizes) were recorded. Nucleotide substitution was assumed to follow the HKY model—that most similar to those selected by ModelTest that is implemented by IM. Upper bounds of parameter priors were set such that posterior distributions were fully contained within them. Consequently, posterior modes could be taken as maximum-likelihood parameter estimates, with the 90% highest posterior density (HPD) providing credibility intervals (Nielsen and Wakeley, 2001). An initial Monte Carlo Markov chain was commenced with a burn-in period of 105 generations, after which parameter trendline plots were examined for the attainment of stationarity (i.e., absence of consistent increase or decrease) and parameter values were subsequently recorded every 10 generations. Independence of samples collected along a chain was assessed via their autocorrelation statistics, and runs were continued until the effective sample size (ESS) exceeded 1000 for all parameters (typically > 5 x 106 generations). An independent run was conducted with a different random number seed to assess convergence upon the true stationary distribution. Estimates of the divergence time parameter (t) were converted into mutation rate (u)—based on geologically derived estimates of generations elapsed since Wairau and Pelorus-Kaituna river isolation (t)—using the relationship t = tu (Hey and Nielsen, 2004). We employed female generation times of 1 and 2 years for G. divergens and G. breviceps, respectively, which may be conservative for a proportion of females of each species (2 and 3 years, respectively; Hopkins, 1971; Staples, 1975; McDowall, 2000; Hamilton and Poulin, 2001), and hence lead to slight underestimates of molecular rate.
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Results |
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TopAbstractMolecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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Variation within and among Catchments
All unique DNA sequences new to this study are available on GenBank (accession numbers EF140909 [GenBank] to EF140979 [GenBank] ; see also previously published sequences DQ380252 [GenBank] to DQ380331 [GenBank] , DQ461150 [GenBank] to DQ461614 [GenBank] ), and data matrices and associated trees are available from TreeBASE (submissions SN3151 to SN13294, SN3151 to SN13295). In the Wairau, Galaxias divergens yielded 16 haplotypes and Gobiomorphus breviceps 5 haplotypes (combined across cyt b and CR); for Kaituna, 4 and 5 haplotypes were found, respectively, and 15 and 6 from the Pelorus River. No haplotypes were shared across drainages.
Phylogeographic Relationships
Results from maximum likelihood, maximum parsimony, and Bayesian analyses yielded concordant topologies with respect to the composition of major clades, and similar levels of topological support in most cases (Fig. 5). For each species, Pelorus, Kaituna, and Wairau haplotypes represented a well-supported monophyletic assemblage relative to outgroup haplotypes from the Motueka and Buller river systems (1.00 Bayesian bipartition probability [pP], > 96% parsimony and likelihood bootstrap support; Fig. 5). Wairau River haplotypes of each species were monophyletic and received high support (> 0.97 pP, > 85% bootstrap) with the exception of G. divergens under maximum likelihood (41%; Fig. 5). Kaituna and Pelorus haplotypes clustered together with high support for G. divergens (1.00 pP, > 97% bootstrap) and moderate support for G. breviceps (0.88 pP, 60% bootstrap; Fig. 5). The Kaituna and Pelorus haplotypes, however, were not reciprocally monophyletic, although there was moderate support (0.94 pP, 65 to 66% bootstrap) for the monophyly of Kaituna Galaxias divergens haplotypes. High-frequency "private" haplotypes detected within each of the Kaituna and Pelorus systems are consistent with substantial population genetic divergence between these recently (7 kyr BP) isolated systems. Phylogeographic structuring within drainages was absent for both species, with the exception of an isolated G. divergens clade associated with a headwater site within the Pelorus system (site PM; Fig. 4, Fig. 5).
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Rate Calibrations
Comparable levels of genetic distance were observed between Wairau and Pelorus-Kaituna populations across both mitochondrial regions, and across both species. Net sequence distances were similar across regions (cyt b, CR) and species (Fig. 5); combined region corrected distances were 0.0138 and 0.0140 subs./site in G. divergens and G. breviceps, respectively. Calibration of these distances against the geologically determined age of the Kaituna River reversal (70 to 130 kyr BP) yielded lineage-specific rates of 0.053 to 0.100 substitutions/site/lineage/Myr for the combined regions.
Likelihood scores for G. divergens and G. breviceps topologies for Wairau, Pelorus, and Kaituna haplotypes, with a single Motueka outgroup, were significantly different depending on whether or not a molecular clock was enforced (G. divergens 
342 = 86.07, P = 0.000; G. breviceps 152 = 48.17, P = 0.000). Consequently, we adopted Sanderson's (2002) penalized likelihood (PL) method to estimate rates. Estimates across the combined mtDNA regions for the smoothed topologies were 0.116 or 0.061 substitutions/site/lineage/Myr for G. divergens and 0.073 or 0.038 substitutions/site/lineage/Myr for G. breviceps, depending on whether the age of Pelorus-Kaituna and Wairau isolation was constrained at 70 or 130 kyr BP, respectively.
Independent Monte Carlo Markov chain runs yielded convergent marginal posterior probability distributions for each parameter, with distinct peaks and zero-probability tails contained within the prior distribution (e.g., Fig. 6). Divergence time (t) marginal posterior probabilities for combined fragments were represented by peaks at 8.84 and 8.59 (independent runs) for G. divergens (HPD 4.86 to 16.05 and 4.04 to 13.26) and 4.13 and 3.95 (independent runs) for G. breviceps (HPD 1.73 to 8.23 and 1.67 to 8.19). Assuming population isolation 130 kyr BP—the upper limit based on geological reconstructions—values of t correspond to 0.053 and 0.052 mutations/site/lineage/Myr for G. divergens (independent runs, HDP 0.024 to 0.080 and 0.024 to 0.080 mutations/site/lineage/Myr), and 0.025 and 0.023 mutations/site/lineage/Myr for G. breviceps (independent runs, HDP 0.010 to 0.049 and 0.010 to 0.049 mutations/site/lineage/Myr). Faster rates are derived when assuming population isolation 70 kyr BP—the lower limit based on geological reconstructions (Table 1).
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Although our analyses excluded some populations that have recently been isolated from those analyzed here, inclusion of such populations (Keneperu Head Stream, Robin Hood Bay Stream, Clarence River) had little impact on the inferred rates (data not shown).
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Discussion |
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TopAbstractMolecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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To make reliable vicariant biogeographic inferences, it is necessary to assess geological and biological data independently (Bishop, 1995; Waters and Craw, 2006). The congruent pattern detected here from phylogeographic analysis of two independent fish taxa—and from drainage history established independently using geological data—strongly support a vicariant (causal) relationship between river palaeohydrology and fish cladogenesis. This correlation between geology and genetics provides a clear basis for calibrating rates of molecular change based on geological dates.
The mtDNA rate calibrations obtained here (0.023 to 0.116 changes/site/lineage/Myr; Table 1) are several times more rapid than traditionally accepted rates for vertebrate mtDNA (e.g., Brown et al., 1979, 1982) and, more specifically, for fish mtDNA. Molecular clock studies of fishes based on Tertiary calibration points typically yield between 0.006 and 0.007 substitutions/site/lineage/Myr for mitochondrial protein coding genes (McKay et al., 1996; Bermingham et al., 1997; Zardoya and Doadrio, 1999; Machordom and Doadrio, 2001; Sivasundar et al., 2001; Dowling et al., 2002; Doadrio and Domínguez, 2004), and between 0.007 and 0.018 substitutions/site/lineage/Myr for noncoding regions (Shedlock et al., 1992; Stepien and Faber, 1998; Donaldson and Wilson, 1999).
Although it has recently been demonstrated that mass-specific metabolic rate explains much of the difference in substitution rate among taxa (Gillooly et al. 2005), the key determinants of body size and thermal habit do not differ appreciably between the species studied herein and several of the fish taxa for which slower rates have been recovered (e.g., temperate cyprinids: Dowling et al. 2002; Doadrio and Domínguez 2004). The misspecification of substitution models can impact on the calculation of distances (Yang et al., 1994; Gaut and Lewis, 1995) and associated rates, as can the application of calibrations to distances derived under different models (e.g., the implementation of "percent sequence divergence" calibrations without reference to underlying models; Lovette, 2004)—a problem rarely acknowledged. However, model misspecification cannot explain the elevated rates reported here as they are observed even when using uncorrected distances (Fig. 5). We also note that the IM software returned elevated rates despite the inability to accommodate heterogeneity in substitution rates among sites.
Discrepancies between rates generated here and the majority of those reported for fishes (see above) are consistent with the hypothesized "time dependency of molecular rates," where faster divergence rates are observed from calibrations based on younger versus older events (Ho et al., 2005; Penny, 2005; Ho and Larson, 2006). This hypothesis is based on the expectation that higher numbers of mutations contribute to branch lengths (i.e., divergence) at pedigree or shallow phylogenetic levels than at deeper phylogenetic levels, where the actions of purifying selection and drift will have precluded some mutations from contributing to branch lengths (Parsons et al., 1997; Hasegawa et al., 1998; Ballard and Whitlock, 2004; Ho et al., 2005; Penny, 2005; Burridge et al., 2006; Kivisild et al., 2006; MacEachern et al., 2006). Under this hypothesis, the same underlying mutation rate can result in distinct divergence rates across different temporal scales.
Rate estimates from the current study were obtained by calibration against a geological event (70 to 130 kyr BP) much younger than those used in the fish studies listed above (> 3 Mya). Interestingly, the few fish studies that have calibrated against events less than 1 Mya yielded divergence rates similar to those generated here. Studies of cichlids have returned CR rates of 0.032 to 0.044 mutations/site/lineage/Myr for the 0.57 to 1.00 Mya origin of Lake Malawi utaka and mbuna lineages (Sturmbauer et al., 2001) and 0.029 to 0.035 substitutions/site/lineage/Myr for the < 23 kyr BP origin of Lake Apoyo Amphilophus (Barluenga and Meyer, 2004). Likewise, Burridge et al. (2006) reported CR and cyt b rates of 0.032 to 0.133 substitutions/site/Myr for populations of two independent galaxiid species that were each vicariantly isolated by a 10–20 kyr BP river capture event in central New Zealand. Consequently, the elevated rates for Galaxias and Gobiomorphus probably reflect the young ages of the associated calibration points, and may be inappropriate for dating divergences at deeper phylogenetic levels (Hasegawa et al., 1998; Ho et al., 2005; Burridge et al., 2006; Ho and Larson, 2006).
Together with the study of Burridge et al. (2006), the current analysis represents the first case in which dated river capture or reversal events have been used to calibrate DNA evolution. This may seem surprising, as river capture is by no means a rare phenomenon for freshwater taxa (e.g., see Kozak et al., 2006; Burridge et al., 2007). Some previous studies have simply "played it safe," favoring dates derived from accepted calibrations rather than employing the geological data at hand (Waters et al., 2001). For instance, the application of traditionally accepted mtDNA substitution rates suggests that speciation of a lacustrine fish species (Galaxias auratus) from its riverine ancestor (Galaxias truttaceus; corrected mtDNA divergence 0.019 substitutions/site) substantially predated the formation of the lake where the speciation event presumably occurred (Ovenden et al., 1993; Waters et al., 2000). However, the Galaxias rates from our current study would yield lineage ages more consistent with that of the lake.
A number of molecular genetic analyses have tested for Pleistocene divergence between fish populations thought to have been vicariantly isolated by glacial processes. In some cases, these studies employed "accepted" calibrations and concluded that population isolation predates the Pleistocene. For instance, Strange and Burr (1997) used a calibration of 0.01 substitutions/site/lineage/Myr to "test the hypothesis that Pleistocene vicariance was the primary mode of cladogenesis and speciation" using five distinct freshwater fish genera from the North American highlands (Ozark versus Appalachian mtDNA haplotypes). Contrary to expectations, three of the five clades (Erimystax, Odontopholis, Litocara) yielded pre-Pleistocene divergence estimates. Similarly, Burridge (2000) concluded that, in three independent comparisons, divergence of temperate Australian marine fishes predated a Pleistocene vicariant barrier (Bassian Isthmus) thought to have promoted their speciation. In the above examples, application of faster calibrations such as those detected in our current study would have yielded divergence time estimates consistent with documented geological history.
Several recent mtDNA phylogeographical studies of Northern Hemisphere freshwater fishes have used accepted or slow calibrations to test hypotheses of postglacial colonization. In many cases, such studies have failed to verify the predicted recolonization scenarios. Culling et al. (2006), for example, used a slow calibration (0.0042 substitutions/site/lineage/Myr; Perdices and Doadrio, 2001) and tentatively concluded (a posteriori) that Cobitis taenia survived the most recent glaciation in Western Europe, "an area which had been thought of as unsuitable for habitation and reproduction due to the presence of the Scandinavian ice sheet." Similarly, Gum et al. (2005) used the "commonly employed" 0.01 substitutions/site/lineage/Myr and argued that northern versus central European Thymallus diverged "approximately 150,000 BP ... clearly predating the late Pleistocene glaciations," and that Central lineages "did not contribute to the recent colonization of the N or NE European region after the Last Glacial Maximum." We argue that the application of these slow calibrations led to systematic overestimation of divergence timings (e.g., Holocene divergences assigned to previous interglacial phases), and that the invoked northern European refugia never existed. In another recent study, Weiss et al. (2000) also employed 0.01 substitutions/site/lineage/Myr and rejected the post-Pleistocene recolonization of northern Europe by Atlantic coast populations of Salmo trutta. They concluded that Portuguese haplotypes "may have diverged from other Atlantic clade haplotypes at least 200,000 years ago ... long before the last glacial maximum." Finally, Kontula and Väinölä (2003) employed 0.002 to 0.006 substitutions/site/lineage/Myr to test for "a relatively recent, Wisconsinian origin of the deepwater sculpin" (Myoxocephalus thompsoni), but concluded that invasion of the North American Arctic "took place several glaciation cycles ago." Presumably reflecting the use of an unrealistically slow calibration, their analysis did "not suffice to comment on the late-glacial dispersal directions." In all of the above studies, the application of faster rates would have yielded results more consistent with postglacial colonization, as might have been predicted at the outset of each study (e.g., Audzijonyte and Väinölä, 2006).
We suggest that, when evidence for vicariance is compelling, biologists should make some attempt to establish associated molecular calibrations. For instance, a recent molecular study by Mateos (2005) argued that a single vicariant event—mediated by volcanism—isolated fish populations in western Mexico, in much the same way that the Panama Isthmus isolated marine taxa (Bermingham et al., 1997). In this case, the age of vicariance was simply estimated on the basis of molecular data (3 to 6 Mya). We advocate that geological ages should be employed, wherever possible, to facilitate more accurate genetic dating of important evolutionary events.
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Acknowledgments |
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TopAbstractMolecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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Richard Allibone, Shan Crow, and Kim Garrett assisted with the collection of specimens. Peter Smith provided outgroup sequences for Gobiomorphus. This research was funded by Marsden contract UOO0404 (Royal Society of New Zealand) and a University of Otago Research Grant.
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References |
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TopAbstractMolecular CalibrationsRiver Capture, River ReversalMaterials and MethodsResultsDiscussionAcknowledgmentsReferences |
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