Abstract

The diversification of neoavian birds is one of the most rapid adaptive radiations of extant organisms. Recent whole-genome sequence analyses have much improved the resolution of the neoavian radiation and suggest concurrence with the Cretaceous-Paleogene (K-Pg) boundary, yet the causes of the remaining genome-level irresolvabilities appear unclear. Here we show that genome-level analyses of 2,118 retrotransposon presence/absence markers converge at a largely consistent Neoaves phylogeny and detect a highly differential temporal prevalence of incomplete lineage sorting (ILS), i.e., the persistence of ancestral genetic variation as polymorphisms during speciation events. We found that ILS-derived incongruences are spread over the genome and involve 35% and 34% of the analyzed loci on the autosomes and the Z chromosome, respectively. Surprisingly, Neoaves diversification comprises three adaptive radiations, an initial near-K-Pg super-radiation with highly discordant phylogenetic signals from near-simultaneous speciation events, followed by two post-K-Pg radiations of core landbirds and core waterbirds with much less pronounced ILS. We provide evidence that, given the extreme level of up to 100% ILS per branch in super-radiations, particularly rapid speciation events may neither resemble a fully bifurcating tree nor are they resolvable as such. As a consequence, their complex demographic history is more accurately represented as local networks within a species tree.

Highlights

  • The rich biodiversity of many organismal groups is the result of bursts of rapid species diversifications, with extreme examples in angiosperms [1] and vertebrates [2]

  • We analyzed ~130,000 long terminal repeat (LTR) retrotransposons in the 48 recently sequenced bird genomes [4] and obtained 2,118 presence/absence patterns of insertions that occurred within the neoavian radiation and are distributed genome-wide (S1 Table, S1 Fig, S1 Data)

  • We conclude that Neoaves diversification is more complex than can be shown in fully bifurcating trees and exhibits a dynamic picture of incomplete lineage sorting (ILS)

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Summary

Introduction

The rich biodiversity of many organismal groups is the result of bursts of rapid species diversifications, with extreme examples in angiosperms [1] and vertebrates [2]. The deep roots of 95% of these species lie within the ancient adaptive radiation of Neoaves, comprising all contemporary avian lineages except Palaeognathae (ratites and tinamous) and the Galloanserae (chicken and ducks). This massive radiation exhibits the highest known diversification rate among deep vertebrate radiations [2], coincides with the Cretaceous-Paleogene (K-Pg) boundary, and gave rise to 36 extant bird lineages within

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