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. 2015 Dec 11;1(11):e1501005.
doi: 10.1126/sciadv.1501005. eCollection 2015 Dec.

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

Santiago Claramunt  1 , Joel Cracraft  1
Affiliations

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

Santiago Claramunt et al. Sci Adv. .

Abstract

Determining the timing of diversification of modern birds has been difficult. We combined DNA sequences of clock-like genes for most avian families with 130 fossil birds to generate a new time tree for Neornithes and investigated their biogeographic and diversification dynamics. We found that the most recent common ancestor of modern birds inhabited South America around 95 million years ago, but it was not until the Cretaceous-Paleogene transition (66 million years ago) that Neornithes began to diversify rapidly around the world. Birds used two main dispersion routes: reaching the Old World through North America, and reaching Australia and Zealandia through Antarctica. Net diversification rates increased during periods of global cooling, suggesting that fragmentation of tropical biomes stimulated speciation. Thus, we found pervasive evidence that avian evolution has been influenced by plate tectonics and environmental change, two basic features of Earth's dynamics.

Keywords: K-Pg mass extinction; avian evolution; divergence times; diversification rates; global biogeography.

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Figures

Fig. 1
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 t1…tn (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
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
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
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).
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