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

RESEARCH ARTICLE The Dynamics of Incomplete Lineage Sorting across the Ancient Adaptive Radiation of Neoavian Birds Alexander Suh*, Linnéa Smeds, Hans Ellegren Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, Uppsala, Sweden a11111 * Abstract OPEN ACCESS Citation: Suh A, Smeds L, Ellegren H (2015) The Dynamics of Incomplete Lineage Sorting across the Ancient Adaptive Radiation of Neoavian Birds. PLoS Biol 13(8): e1002224. doi:10.1371/journal. pbio.1002224 Academic Editor: David Penny, Massey University, NEW ZEALAND Received: February 2, 2015 Accepted: July 10, 2015 Published: August 18, 2015 Copyright: © 2015 Suh et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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 superradiations, 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. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: 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 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. PLOS Biology | DOI:10.1371/journal.pbio.1002224 August 18, 2015 1 / 18 Incomplete Lineage Sorting and the Radiation of Birds design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Abbreviations: ILS, incomplete lineage sorting; KPg, Cretaceous-Paleogene; LTR, long terminal repeat element; MPRE, most parsimonious RE; MY, million years; MYA, million years ago; Ne, effective population size; RE, retrotransposed element; UCE, ultraconserved element. 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. 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]. Among the latter, birds are one of the most speciose groups with a total of >10,500 recognized species that are proposed to be the result of mostly recent accelerations of diversification rates [3]. Nevertheless, 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 <15 million years (MY) [4]. Simulations suggest that the distribution of neoavian internode lengths causes a very high probability of gene tree–species tree incongruences [5], i.e., hemiplasy derived from incomplete lineage sorting (ILS) [6]. ILS denotes the persistence of ancestral polymorphisms across multiple successive speciation events and is followed by stochastic allele fixation in each descendant lineage, potentially making phylogenetic inference at the level of individual loci problematic. Past studies on the extent of ILS during speciation have been restricted to recent divergences because homoplasy needs to be low. For example, divergences among great apes show that ~30% of the gorilla genome exhibits nucleotide substitution patterns incongruent with the human/chimpanzee/gorilla species tree [7]. In contrast, the characteristics of ILS remain to be explored in adaptive radiations. As virtually homoplasy-free phylogenetic rare genomic changes [8,9], retrotransposed elements (REs) exhibit conflicting phylogenetic signals only when their insertions occurred on short internodes; they can thus be used to localize and quantify ILS even on very deep timescales [8,10–13]. Results and Discussion We analyzed ~130,000 long terminal repeat (LTR) retrotransposons in th (...truncated)