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

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

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

Alexander Suh et al. PLoS Biol..

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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Phylogenetic tree of rare genomic changes reveals varying degree of incomplete lineage sorting across Neoaves diversification.
(A) The main whole-genome sequence tree from Jarvis et al. [4] mapped with our 2,118 retrotransposon markers (745 incongruent markers; tree length = 5,579; consistency index = 0.40; retention index = 0.64). (B) The same markers mapped on the single MPRE tree (S2 Data) resulting from analysis of their 2,118 presence/absence patterns (720 incongruent markers; tree length = 5,377; consistency index = 0.41; retention index = 0.66) under Felsenstein’s polymorphism parsimony [16]. Black branches indicate topological concordances between the MPRE tree and the main Jarvis et al. tree [4], and discordances are limited to the deepest neoavian internodes (grey dashed branches) and the conflicting position of the mousebird (grey branches). The amount of ILS-free, conflict-free insertion events (blue bold numbers) was identified for each internode, and numbers within doughnut plots indicate counts of ILS-affected RE insertion events leading to the persistence of insertion polymorphisms across two (green), three (orange), or more (red parts of doughnut plots) speciation events. (C–E) Schematic illustration of the different genealogical fates of segregating presence (colored lines) or absence (black lines) alleles following RE insertion (colored circles) in an exemplary five-taxon species tree. We show one respective example for the different degrees of gene tree–species tree conflict that can be caused by incomplete lineage sorting (ILS) across two (C), three (D), or more than three (E) successive speciation events. Incongruence of RE presence/absence patterns (dashed boxes) is illustrated with REs as colored ovals, target site duplications as white squares, and orthologous genomic flanks as black lines. The bird paintings were generated by Jon Fjeldså (used with permission).
Fig 2
Fig 2. Comparison of RE marker support for the possible positions of mousebirds within core landbirds.
The seven alternative groupings are shown in descending order of support and include the mousebird topology of (A), our MPRE tree and the genome-level UCE tree of [4], (C) the Hackett et al. tree [18], (D) the main Jarvis et al. tree [4], (E) two limited retrotransposon studies [10,23], and (G) the main McCormack et al. tree [20]. Blue bold numbers indicate the amount of RE insertion events that are conflict-free with each of the seven alternatives, respectively. Higher-level taxon names are shown for well-supported monophyla, such as the eagles/New World vulture clade (Accipitrimorphae [4]), the passerine/parrot/falcon/seriema clade (Australaves [25]), and the woodpecker/bee-eater/hornbill/trogon/cuckoo-roller clade (Coraciimorphae [4], sensu stricto without mousebird). The bird paintings were generated by Jon Fjeldså (used with permission).
Fig 3
Fig 3. Dynamics of incomplete lineage sorting and RE insertion rates across the dated main Jarvis et al. tree [4].
Per-branch levels of ILS (A) and RE insertion rates (B) vary considerably across the diversification of Neoaves. We derived these values from mapping our 2,118 RE markers on the main Jarvis et al. tree [4] (Fig 1A). For each branch, percentages of ILS were calculated by dividing the amount of ILS-affected markers by the total amount of markers (S2 Table). The latter value was then divided by the respective branch length to estimate the RE insertion rate per MY (S2 Table). Notably, branch length and degree of ILS correlate negatively (S2 Table) (C), but there is no correlation between branch length and RE insertion rate (S2 Table) (D) or between degree of ILS and RE insertion rate (S2 Table) (E). Orange dots denote those branches that are incongruent between the main Jarvis et al. tree [4] and our MPRE tree (cf. Fig 1A and 1B).
Fig 4
Fig 4. Phylogenetic network of rare genomic changes reveals three adaptive radiations of Neoaves with varying complexity of genealogical incongruences.
(A) Neighbor-net [31] analysis of 2,118 RE presence/absence patterns suggests that Neoaves diversification may be more accurately visualized as a largely bifurcating tree with highly reticulate structures at the base of the core landbird radiation and across most of the initial super-radiation. Within the latter, red-brown reticulations highlight bifurcate relationships (cf. Fig 1A and 1B) with limited conflict if stretched boxes are longer than they are wide. In contrast, the core waterbird radiation exhibits limited conflict and appears fully bifurcating (cf. Fig 1A and 1B). (B–D) Distribution of frequencies of RE markers without and with ILS (i.e., persistence across ≥two speciation events) for each of the three adaptive radiations (S3 Table). (B) Core waterbird radiation with 18% total ILS, mostly across two speciation events. (C) Core landbird radiation with 27% total ILS, most of which led to weak or moderate conflict via ILS across two to three speciation events. (D) The initial super-radiation exhibits 73% total ILS, almost exclusively with strong discordances caused by persistence of ILS across five or more speciation events.
Fig 5
Fig 5. Genomic location of rare genomic changes reveals prevalence of incomplete lineage sorting across all chromosomes.
(A) Distribution of RE markers across the chromosomes of the zebra finch genome plotted against per-marker count of speciation events during which respective ILS persisted (S1 Table). Locations of intronic markers are indicated in dark colors, while putatively intergenic markers are denoted in light colors. (B–D) Supernetworks [31] illustrate the complex reticulations of topology conflicts between compared trees. These conflicts exhibit highly similar distributions (cf. Fig 4A) in supernetwork comparisons between the MPRE tree (Fig 1B, S2 Data) and a tree based on 114 Z-chromosomal REs (S2 Data) (B), between the MPRE tree and a tree based on 140 REs from microchromosomes (i.e., all chromosomes smaller than 20 Mb; S2 Data) (C), and among seven different genome-level sequence analyses from Jarvis et al. [4] (D). Colors of reticulations correspond to the coloration used in Fig 4 for discerning the three adaptive radiations of Neoaves. See Supporting Information (S3 and S4 Figs) for species labels and details on the trees compared in supernetworks.
Fig 6
Fig 6. Longer ILS duration of a biallelic polymorphism leads to an exponential increase of hemiplasy.
(A) Illustration of all the RE presence/absence patterns that are theoretically possible after ILS across two to four speciation events (extension of the examples shown in Fig 1C–1E). This permitted us to calculate the amounts of possible character distributions that are incongruent or congruent with the species tree under the observed durations of ILS across up to 17 speciation events (S5 Table). Note that conflict-free patterns parsimoniously correspond to ILS across one or fewer speciation events. (B) The amount of species tree-congruent patterns increases linearly (2n) with ILS duration. (C) The amount of hemiplasy (i.e., species tree-incongruent patterns) increases exponentially (2n– 2n) with ILS duration. (D) The probability for the occurrence of hemiplasy in a biallelic polymorphism reaches 50% after ILS across three speciation events and 99% after ILS across eleven speciation events (S5 Table).
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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.

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