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. 2024 Feb 20;121(8):e2319696121.
doi: 10.1073/pnas.2319696121. Epub 2024 Feb 12.

Genomes, fossils, and the concurrent rise of modern birds and flowering plants in the Late Cretaceous

Shaoyuan Wu  1 , Frank E Rheindt  2 , Jin Zhang  3 , Jiajia Wang  1 , Lei Zhang  1 , Cheng Quan  4 , Zhiheng Li  5 , Min Wang  5 , Feixiang Wu  5 , Yanhua Qu  6 , Scott V Edwards  7 , Zhonghe Zhou  5 , Liang Liu  8
Affiliations

Genomes, fossils, and the concurrent rise of modern birds and flowering plants in the Late Cretaceous

Shaoyuan Wu et al. Proc Natl Acad Sci U S A. .

Abstract

The phylogeny and divergence timing of the Neoavian radiation remain controversial despite recent progress. We analyzed the genomes of 124 species across all Neoavian orders, using data from 25,460 loci spanning four DNA classes, including 5,756 coding sequences, 12,449 conserved nonexonic elements, 4,871 introns, and 2,384 intergenic segments. We conducted a comprehensive sensitivity analysis to account for the heterogeneity across different DNA classes, leading to an optimal tree of Neoaves with high resolution. This phylogeny features a novel Neoavian dichotomy comprising two monophyletic clades: a previously recognized Telluraves (land birds) and a newly circumscribed Aquaterraves (waterbirds and relatives). Molecular dating analyses with 20 fossil calibrations indicate that the diversification of modern birds began in the Late Cretaceous and underwent a constant and steady radiation across the KPg boundary, concurrent with the rise of angiosperms as well as other major Cenozoic animal groups including placental and multituberculate mammals. The KPg catastrophe had a limited impact on avian evolution compared to the Paleocene-Eocene Thermal Maximum, which triggered a rapid diversification of seabirds. Our findings suggest that the evolution of modern birds followed a slow process of gradualism rather than a rapid process of punctuated equilibrium, with limited interruption by the KPg catastrophe. This study places bird evolution into a new context within vertebrates, with ramifications for the evolution of the Earth's biota.

Keywords: Neoavian phylogeny; gradualism; modern bird divergence; molecular clock; punctuated evolution.

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Conflict of interest statement

Competing interests statement:The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Effects of the four individual DNA classes on species tree inference. (A) Comparison of the number of significantly discordant nodes for trees estimated using NJst and RAxML methods across all six pairwise combinations of DNA classes. The significance of differences between NJst and RAxML trees was examined using a binomial test. Note that the number of significantly discordant nodes (bootstrap support >= 80%) for trees built using RAxML is significantly greater than for trees built using NJst. (B) Consistency of the four DNA classes with the multispecies coalescent model. The concordant ratio indicates the proportion of gene tree heterogeneity that can be explained by the multispecies coalescent model. (C) Compatibility of maximum likelihood gene trees built from the four DNA classes. The discordant ratio indicates the proportion of significantly discordant majority triplets across all pairwise comparisons among DNA classes. Abbreviation: Inter, intergenic.
Fig. 2.
Fig. 2.
Phylogenetic relationships of modern birds. The time-calibrated tree of 124 avian species was constructed using the coalescence-based method NJst from a combination of maximum likelihood gene trees of CDS, intron, and intergenic segments after removing 30% outliers. Numbers on nodes indicate bootstrap support values, with numbers >90% not shown. Background shading indicates the Late Cretaceous era.
Fig. 3.
Fig. 3.
Interordinal diversification of modern birds and placental mammals from the Late Cretaceous to the Paleogene. Note that both crown Aves and placental mammals underwent a constant and steady differentiation across the KPg boundary, without apparent interruption by the KPg mass extinction event. The green background indicates the increase of taxonomic diversity of flowering plants. The data on placental mammal and angiosperm diversity are based on Liu et al. (25) and Condamine et al. (26), respectively.
Fig. 4.
Fig. 4.
Diversity changes in modern birds, placental mammals, multituberculate mammals, marine ray-finned fishes, holometabolous insects (butterflies, bees, ants, etc.), and flowering plants from the Cretaceous to the present time. The panel on the Upper Right shows the correlation coefficients of diversity changes between angiosperms and each of the five animal groups: a) crown Aves, b) placental mammals, c) multituberculates, d) marine ray-finned fishes, and e) holometabolous insects. The curve of average global temperature represents a proxy for climatic changes during the Cretaceous and Cenozoic. Note that among the six taxonomic groups analyzed in the figure, the KPg extinction event only had a noticeable negative impact on the biodiversity of ray-finned fishes, but not on the other five groups. The diversity curves of placental mammals, multituberculates, ray-finned fishes, holometabolous insects, and angiosperms were plotted based on data extracted from Liu et al. (25), Wilson et al. (35), Guinot and Cavin (36), Nicholson et al. (37), and Condamine et al. (26), respectively. The curve of global temperature changes was plotted based on data extracted from Condamine et al. (26).
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