The Dynamics of Incomplete Lineage Sorting across the Ancient Adaptive Radiation of Neoavian Birds

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.

Abstract

A study of ancient genetic variation reveals genomic evidence for near-simultaneous speciation at the base of Neoaves (a group containing most modern birds), which temporally coincides with the mass extinction of nonavian dinosaurs and archaic birds.

Author Summary

The rise of modern birds began after the mass extinction of nonavian dinosaurs and archaic birds at the Cretaceous-Paleogene (K-Pg) boundary, about 66 million years ago. This coincides with the super-rapid adaptive radiation of Neoaves (a group that contains most modern birds), which has been difficult to resolve even with whole genome sequences. We reconstructed the genealogical fates of thousands of rare genomic changes (insertions of selfish mobile elements called retrotransposons), a third of which were found to be affected by a phenomenon known as incomplete lineage sorting (ILS), namely a persistence of polymorphisms across multiple successive speciation events. Astoundingly, we found that near the K-Pg boundary, speciation events were accompanied by extreme levels of ILS, suggesting a near-simultaneous, star-like diversification process that appears plausible in the context of instantaneous niche availability that must have followed the K-Pg mass extinction. Our genome-scale results provide a population genomic explanation as to why some species radiations may be more complex than a fully bifurcating tree of life. We suggest that, under such circumstances, ILS bears witness to the biological limitation of phylogenetic resolution.