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

PLoS Biol. 2015 Aug 18;13(8):e1002224. doi: 10.1371/journal.pbio.1002224. eCollection 2015 Aug.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Birds / classification
  • Birds / genetics*
  • Evolution, Molecular*
  • Genetic Speciation*
  • Genetic Variation*
  • Genome
  • Hybridization, Genetic
  • Phylogeny*

Grant support

This work was supported by an Advanced Investigator Grant (NEXTGENMOLECOL) from the European Research Council, a Wallenberg Scholar Award from the Knut and Alice Wallenberg Foundation and grants from the Swedish Research Council (2007-8731 and 2010-5650) to HE. Computations were performed on resources provided by the Swedish National Infrastructure for Computing (SNIC) through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under Project b2012135. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.