Research ArticleEVOLUTIONARY ECOLOGY

A new time tree reveals Earth history’s imprint on the evolution of modern birds

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Science Advances  11 Dec 2015:
Vol. 1, no. 11, e1501005
DOI: 10.1126/sciadv.1501005
  • Fig. 1 Example of the method used for generating clade age priors from the fossil record.

    (A) The fossil Wieslochia weissi from the Oligocene of Germany shows an apomorphy of the suborder Tyranni: a well-developed tuberculum ligamenti collateralis ventralis. Therefore, Wieslochia sets an absolute minimum age for the time of origin (stem age) of the Tyranni, which is the same as the crown age of Eupasseres. The oldest fossil of the suborder Passeri would also set a minimum age for Eupasseres, but it is younger than Wieslochia. Note that fossils that only show an apomorphy of Eupasseres may be in the stem branch; for this reason, they are not informative regarding the minimum age of crown Eupasseres. (B) The first record of Eupasseres (Tyranni or Passeri) in other continents completes a set of fossil occurrences of ages t1tn (see data set 1 for details). (C) This set of ages does not depart significantly from a uniform distribution (Kolmogorov-Smirnov test, D = 0.25, P = 0.7). Therefore, the likelihood function for the upper bound (θ) of a uniform distribution [1/(θ)n for θ > tn] is used to generate a distribution for the true age of Eupasseres. (D) However, the oldest fossil does not have a precise age estimate but was assigned to a geological time interval that spans several million years (the same is true for other fossils in the set, but their ages do not influence the likelihood). Therefore, pseudosamples of tn are generated by sampling uniformly from the time interval to which the oldest fossil was assigned and used for generating multiple distributions of clade age. (E) Averaging these pseudoreplicated distributions results in a final distribution, which is then modeled with a standard probability density function that mimics its shape: a log-normal distribution, a log mean of 1.7, and a log SD of 0.8. This standard distribution is used as clade age prior in Bayesian divergence time estimation.

  • Fig. 2 Time trees of modern birds from Bayesian divergence time estimation using fossil calibrations.

    Maximum clade credibility (MCC) trees from a Bayesian divergence time estimation using calibration priors inferred from the fossil record. (A) MCC tree from the analysis of 124,196 bases from the first and second codon positions of 1156 clock-like genes from Jarvis et al. (3) and 10 calibration priors. (B) MCC tree from the analysis of 4092 bases of the recombination-activating genes for 230 species and 24 calibration priors. Black diamonds are calibration nodes, black dots are clades that were constrained to match relationships supported by recent multilocus and genomic analyses (3, 28), red density distributions are clade age prior probabilities derived empirically from a quantitative analysis of the fossil record of clades, and blue bars represent 95% highest posterior densities for node age from the posterior distribution. Median ages are indicated for large clades mentioned in the text (blue dots).

  • Fig. 3 Time tree of modern birds with reconstruction of ancestral geographic regions.

    Fitch parsimony optimizations of ancestral geographic regions are shown at the nodes. Multiple regions at a node represent alternative, equally parsimonious optimizations. The tree is the maximum clade credibility tree of a Bayesian analysis of recombination-activating genes for 230 species and 24 calibration priors and with the addition a posteriori of 25 fossil taxa that represent Holarctic distributions for clades now restricted to the tropics. Distributions at the tips are those of the clades they represent. Schematic representations of global paleogeography at the K-Pg transition, the middle Eocene, and the middle Miocene are shown together with major postulated interregional connections as inferred from paleogeographic evidence and biogeographic analysis. Higher-level taxa are indicated on the right (see fig. S2 for species names).

  • Fig. 4 Diversification rates through time for modern birds and major events in Earth history during the Late Cretaceous and the Cenozoic.

    (A) Red: Net lineage diversification rate (speciation-extinction) estimated for 5-Ma intervals using birth-death shifts models (120) (lines are medians of 500 estimates from a sample of the posterior distribution of trees from the Bayesian time-tree analysis; light boxes around medians are interquartile ranges). Blue: Deep-ocean temperatures estimated from a global compilation of benthic foraminifera oxygen isotope data (124) represented by a local regression smoother and associated 95% confidence intervals. Major tectonic and meteorite events are also indicated. (B) Relative extinction rate (extinction/speciation) (lines are medians, and light boxes around medians are interquartile ranges from 500 estimates from the tree posterior).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/1/11/e1501005/DC1

    Text

    Fig. S1. Probability density distributions for the age of the most recent common ancestor (crown age) of 24 avian clades in the RAG data set inferred from the distribution of fossil occurrences.

    Fig. S2. Biogeographic ancestral area reconstruction using Fitch parsimony optimization.

    Fig. S3. Alternative biogeographic ancestral area reconstructions.

    Fig. S4. Diversification through time of modern birds and Earth history events.

    Fig. S5. Effect of the tree prior on Bayesian divergence time estimation.

    Table S1. Probability distributions of clade age from fossil occurrences, used as calibration priors in Bayesian divergence time analysis in BEAST 2.

    Table S2. Reconstructions of the taxonomic composition of Late Cretaceous–Cenozoic global avifaunas.

    Table S3. Environmental birth-death models of the associations between diversification rates and global temperature in modern birds.

    Table S4. Birth-death shift models representing associations between Earth history events and diversification rates in modern birds.

    Data set 1. Fossils used for calibration.

    Data set 2. Biogeographic and richness information.

    References (126185)

  • Supplementary Materials

    This PDF file includes:

    • Text
    • Fig. S1. Probability density distributions for the age of the most recent common ancestor (crown age) of 24 avian clades in the RAG data set inferred from the distribution of fossil occurrences.
    • Fig. S2. Biogeographic ancestral area reconstruction using Fitch parsimony optimization.
    • Fig. S3. Alternative biogeographic ancestral area reconstructions.
    • Fig. S4. Diversification through time of modern birds and Earth history events.
    • Fig. S5. Effect of the tree prior on Bayesian divergence time estimation.
    • Table S1. Probability distributions of clade age from fossil occurrences, used as calibration priors in Bayesian divergence time analysis in BEAST 2.
    • Table S2. Reconstructions of the taxonomic composition of Late Cretaceous–Cenozoic global avifaunas.
    • Table S3. Environmental birth-death models of the associations between diversification rates and global temperature in modern birds.
    • Table S4. Birth-death shift models representing associations between Earth history events and diversification rates in modern birds.
    • References (126–186)

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    Other Supplementary Material for this manuscript includes the following:

    • Data set 1 (Microsoft Excel format). Fossils used for calibration.
    • Data set 2 (Microsoft Excel format). Biogeographic and richness information.

    Files in this Data Supplement:

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