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Cited by 239Evolution and Paleontology StudiesPaleontology and Evolutionary BiologyPlant Diversity and Evolution

The DOI matches its Crossref record; 114 of the 117 references it cites were found in a registry or an index.

Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages

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Brown, Joseph W, Rest, Joshua S, García-Moreno, Jaime, Sorenson, Michael D, Mindell, David P·2008·BMC Biology
DOI 10.1186/1741-7007-6-6PMC PMC2267772
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Abstract

BACKGROUND: Determining an absolute timescale for avian evolutionary history has proven contentious. The two sources of information available, paleontological data and inference from extant molecular genetic sequences (colloquially, 'rocks' and 'clocks'), have appeared irreconcilable; the fossil record supports a Cenozoic origin for most modern lineages, whereas molecular genetic estimates suggest that these same lineages originated deep within the Cretaceous and survived the K-Pg (Cretaceous-Paleogene; formerly Cretaceous-Tertiary or K-T) mass-extinction event. These two sources of data therefore appear to support fundamentally different models of avian evolution. The paradox has been speculated to reflect deficiencies in the fossil record, unrecognized biases in the treatment of genetic data or both. Here we attempt to explore uncertainty and limit bias entering into molecular divergence time estimates through: (i) improved taxon (n = 135) and character (n = 4594 bp mtDNA) sampling; (ii) inclusion of multiple cladistically tested internal fossil calibration points (n = 18); (iii) correction for lineage-specific rate heterogeneity using a variety of methods (n = 5); (iv) accommodation of uncertainty in tree topology; and (v) testing for possible effects of episodic evolution. RESULTS: The various 'relaxed clock' methods all indicate that the major (basal) lineages of modern birds originated deep within the Cretaceous, although temporal intraordinal diversification patterns differ across methods. We find that topological uncertainty had a systematic but minor influence on date estimates for the origins of major clades, and Bayesian analyses assuming fixed topologies deliver similar results to analyses with unconstrained topologies. We also find that, contrary to expectation, rates of substitution are not autocorrelated across the tree in an ancestor-descendent fashion. Finally, we find no signature of episodic molecular evolution related to either speciation events or the K-Pg boundary that could systematically mislead inferences from genetic data. CONCLUSION: The 'rock-clock' gap has been interpreted by some to be a result of the vagaries of molecular genetic divergence time estimates. However, despite measures to explore different forms of uncertainty in several key parameters, we fail to reconcile molecular genetic divergence time estimates with dates taken from the fossil record; instead, we find strong support for an ancient origin of modern bird lineages, with many extant orders and families arising in the mid-Cretaceous, consistent with previous molecular estimates. Although there is ample room for improvement on both sides of the 'rock-clock' divide (e.g. accounting for 'ghost' lineages in the fossil record and developing more realistic models of rate evolution for molecular genetic sequences), the consistent and conspicuous disagreement between these two sources of data more likely reflects a genuine difference between estimated ages of (i) stem-group origins and (ii) crown-group morphological diversifications, respectively. Further progress on this problem will benefit from greater communication between paleontologists and molecular phylogeneticists in accounting for error in avian lineage age estimates.

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Crossref · 10.1186/1741-7007-6-6

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Figures

Figure 1 Different ways that fossil and molecular data date lineages. Time intervals defined by the horizontal dashed lines and vertical arrows pertain to age estimates for the divergence between hypothetical lineages X and Y. Even with a complete fossil record and perfect molecular clock a discrepancy is expected between fossil (FA) and molecular (MA) age estimates. As diagnostic morphological characters generally evolve (TMorphology) after species divergence (TSpecies), the fossil record will always underestimate (by δDiagnostic character) the true speciation time. Genetic data, on the other hand, will overestimate speciation time (by δCoalescence), as polymorphisms present during species divergence will coalesce some time in the past (TGene; related to the ancestral species effective population size). The genuine difference between molecular and morphological divergence times will thus be δTrue MA-FA. With a less complete fossil record, the oldest known fossil is unlikely to temporally correspond precisely to the origination of a diagnostic character delimiting X and Y, further decreasing FA by δOldest fossil. Under the more realistic scenario of lineage-specific rate heterogeneity and limited taxon/character sampling, errors associated with molecular methods (δClock error) may result in overestimation or underestimation of the true speciation time, although underestimates are bounded by the fossil constraint (δFossil error). The observed discrepancy in age estimates, δRealized MA-FA, may be considerably larger than expectations (δTrue MA-FA).
Figure 1 Different ways that fossil and molecular data date lineages. Time intervals defined by the horizontal dashed lines and vertical arrows pertain to age estimates for the divergence between hypothetical lineages X and Y. Even with a complete fossil record and perfect molecular clock a discrepancy is expected between fossil (FA) and molecular (MA) age estimates. As diagnostic morphological characters generally evolve (TMorphology) after species divergence (TSpecies), the fossil record will always underestimate (by δDiagnostic character) the true speciation time. Genetic data, on the other hand, will overestimate speciation time (by δCoalescence), as polymorphisms present during species divergence will coalesce some time in the past (TGene; related to the ancestral species effective population size). The genuine difference between molecular and morphological divergence times will thus be δTrue MA-FA. With a less complete fossil record, the oldest known fossil is unlikely to temporally correspond precisely to the origination of a diagnostic character delimiting X and Y, further decreasing FA by δOldest fossil. Under the more realistic scenario of lineage-specific rate heterogeneity and limited taxon/character sampling, errors associated with molecular methods (δClock error) may result in overestimation or underestimation of the true speciation time, although underestimates are bounded by the fossil constraint (δFossil error). The observed discrepancy in age estimates, δRealized MA-FA, may be considerably larger than expectations (δTrue MA-FA).CC BY · PubMed Central
Figure 2 Alternative tree topologies. TConsensus (left) represents a conservative consensus estimate of avian familial relationships [53] (AICc = 421460.9166). TOptimal (right) is our optimal topology derived from a partitioned model maximum likelihood search in RAxML (AICc = 414160.2536). Some topological constraints were implemented in this search (see additional file 1). Solid circles and numbers indicate the placement of calibration points (see Table 5 for ages). Letters denote nodes whose age estimates are provided in Table 3.
Figure 2 Alternative tree topologies. TConsensus (left) represents a conservative consensus estimate of avian familial relationships [53] (AICc = 421460.9166). TOptimal (right) is our optimal topology derived from a partitioned model maximum likelihood search in RAxML (AICc = 414160.2536). Some topological constraints were implemented in this search (see additional file 1). Solid circles and numbers indicate the placement of calibration points (see Table 5 for ages). Letters denote nodes whose age estimates are provided in Table 3.CC BY · PubMed Central
Figure 3 Comparative timing of divergences for avian orders and families based on four different 'relaxed clock' methods. Chronograms based on the optimal mtDNA tree reconstruction (TOptimal) using r8s (top left), Dating5 (bottom left), PATHd8 (top right) and Multidivtime (bottom right); see methods for explanation of differences between analytical approaches. For legibility, error bars are removed and trees are pruned to the family level. Filled circles denote major clades: orange, Paleognathae; purple, Neognathae; blue, Galloanserae; green, Neoaves; red, Passeriformes. Time is given in millions of years before present. The vertical dashed lines indicate the K-Pg boundary. r8s, Dating5 and Multidivtime reconstructions support Cretaceous origin and diversification. PATHd8 alone supports Cretaceous origin but Tertiary diversification.
Figure 3 Comparative timing of divergences for avian orders and families based on four different 'relaxed clock' methods. Chronograms based on the optimal mtDNA tree reconstruction (TOptimal) using r8s (top left), Dating5 (bottom left), PATHd8 (top right) and Multidivtime (bottom right); see methods for explanation of differences between analytical approaches. For legibility, error bars are removed and trees are pruned to the family level. Filled circles denote major clades: orange, Paleognathae; purple, Neognathae; blue, Galloanserae; green, Neoaves; red, Passeriformes. Time is given in millions of years before present. The vertical dashed lines indicate the K-Pg boundary. r8s, Dating5 and Multidivtime reconstructions support Cretaceous origin and diversification. PATHd8 alone supports Cretaceous origin but Tertiary diversification.CC BY · PubMed Central
Figure 4 A timeline for early avian evolution. Maximum clade credibility (MCC) chronogram inferred using the non-autocorrelated model of rate evolution in BEAST while allowing topology to vary (TFlexible). Time is given in millions of years before present. The vertical dashed line indicates the K-Pg boundary. Error bars (blue and green) represent 95% posterior credibility intervals and are only given for nodes that were present on more than 50% of the posterior sampled trees. An unambiguous ancient diversification is indicated by 37 credibility intervals restricted to the Cretaceous (green bars).
Figure 4 A timeline for early avian evolution. Maximum clade credibility (MCC) chronogram inferred using the non-autocorrelated model of rate evolution in BEAST while allowing topology to vary (TFlexible). Time is given in millions of years before present. The vertical dashed line indicates the K-Pg boundary. Error bars (blue and green) represent 95% posterior credibility intervals and are only given for nodes that were present on more than 50% of the posterior sampled trees. An unambiguous ancient diversification is indicated by 37 credibility intervals restricted to the Cretaceous (green bars).CC BY · PubMed Central
Figure 5 Estimated rates of molecular evolution over time, in assessment of possible episodic evolution. Standardized inferred rate of sequence evolution (per data partition) is plotted against inferred age for internal nodes on the optimal mtDNA tree reconstruction (TOptimal) using Multidivtime. Time is given in millions of years before present. No support is shown for an accelerated rate accompanying initial avian diversification or following the K-Pg boundary (vertical dashed line).
Figure 5 Estimated rates of molecular evolution over time, in assessment of possible episodic evolution. Standardized inferred rate of sequence evolution (per data partition) is plotted against inferred age for internal nodes on the optimal mtDNA tree reconstruction (TOptimal) using Multidivtime. Time is given in millions of years before present. No support is shown for an accelerated rate accompanying initial avian diversification or following the K-Pg boundary (vertical dashed line).CC BY · PubMed Central
Figure 6 Information content. Posterior 95% credibility interval width is plotted against posterior mean divergence time using the results from Multidivtime on TOptimal. Here R2 indicates the amount of information present in the data matrix and the regression coefficient is an estimate of the expected uncertainty that is independent of sequence length.
Figure 6 Information content. Posterior 95% credibility interval width is plotted against posterior mean divergence time using the results from Multidivtime on TOptimal. Here R2 indicates the amount of information present in the data matrix and the regression coefficient is an estimate of the expected uncertainty that is independent of sequence length.CC BY · PubMed Central

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Show all 117 references

Research works printed but not linked: 4

  1. Easteal S: Molecular evidence for the early divergence of placental mammals. BioEssays. 1999, 21: 1052-1058. 10.1002/(SICI)1521-1878(199912)22:1<1052::AID-BIES9>3.0.CO;2-6. · DOI
  2. Swofford DL: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) 4 (beta 10). 2003, Sunderland, MA: Sinauer Associates
  3. Britton T, Anderson CL, Jaquet D, Lundqvist S, Bremer K: PATHd8 – a new method for estimating divergence times in large phylogenetic trees without a molecular clock. 2006, [ http://www.math.su.se/PATHd8 ]
  4. Cutler DJ: Dating5. 2000

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Metadata

Authors
Brown, J. W., Rest, J. S., García-Moreno, J., Sorenson, M. D., & Mindell, D. P.
Affiliations
  • University of Michigan (US)
  • University of Chicago (US)
  • Boston University (US)
Corresponding author
Brown, Joseph W
ORCID
Venue
BMC Biology
Publisher
Springer Science and Business Media LLC
Published
2008-01-28
Volume
6
Issue
1
Pages
6-6
ISSN
1741-7007 (ISSN-L)
DOI
10.1186/1741-7007-6-6
PMC
PMC2267772
OpenAlex
W2099180789
Cited by
236
References
117
Citations by year
2026: 1 · 2025: 4 · 2024: 7 · 2023: 2 · 2022: 4 · 2021: 5 · 2020: 5 · 2019: 5 · 2018: 7 · 2017: 5 · 2016: 15 · 2015: 31 · 2014: 29 · 2013: 24 · 2012: 20
FWCI
18.01
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Deep Blue (University of Michigan) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • OpenBU (Boston University) (submittedVersion, cc-by)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Evolutionary Biology
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant Diversity and Evolution
Keywords
avian evolution, mitochondrial DNA, K-Pg mass extinction, fossil calibration, relaxed molecular clock, topological uncertainty, avian phylogeny, Cenozoic diversification, fossil record bias
MeSH terms
Animals, Bayes Theorem, Birds, DNA, Mitochondrial, Fossils, Phylogeny, Genetic Variation, Evolution, Molecular, Genetic Speciation

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