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.
References
[1]
Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V. Darwin's abominable mystery: Insights from a supertree of the angiosperms. Proc Natl Acad Sci USA. 2004;101(7):1904–9. pmid:14766971 doi: 10.1073/pnas.0308127100
[2]
Alfaro ME, Santini F, Brock C, Alamillo H, Dornburg A, Rabosky DL, et al. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc Natl Acad Sci USA. 2009;106(32):13410–4. doi: 10.1073/pnas.0811087106. pmid:19633192
[3]
Jetz W, Thomas G, Joy J, Hartmann K, Mooers A. The global diversity of birds in space and time. Nature. 2012;491(7424):444–8. doi: 10.1038/nature11631. pmid:23123857
[4]
Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. Whole genome analyses resolve the early branches in the tree of life of modern birds. Science. 2014;346(6215):1320–31. doi: 10.1126/science.1253451. pmid:25504713
[5]
Oliver JC. Microevolutionary processes generate phylogenomic discordance at ancient divergences. Evolution. 2013;67(6):1823–30. doi: 10.1111/evo.12047. pmid:23730773
[6]
Avise JC, Robinson TJ. Hemiplasy: a new term in the lexicon of phylogenetics. Syst Biol. 2008;57(3):503–7. doi: 10.1080/10635150802164587. pmid:18570042
[7]
Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, et al. Insights into hominid evolution from the gorilla genome sequence. Nature. 2012;483(7388):169–75. doi: 10.1038/nature10842. pmid:22398555
[8]
Ray DA, Xing J, Salem A-H, Batzer MA. SINEs of a nearly perfect character. Syst Biol. 2006;55(6):928–35. pmid:17345674 doi: 10.1080/10635150600865419
[9]
Han K-L, Braun EL, Kimball RT, Reddy S, Bowie RCK, Braun MJ, et al. Are transposable element insertions homoplasy free?: an examination using the avian tree of life. Syst Biol. 2011;60(3):375–86. doi: 10.1093/sysbio/syq100. pmid:21303823
[10]
Suh A, Paus M, Kiefmann M, Churakov G, Franke FA, Brosius J, et al. Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nat Commun. 2011;2:443. doi: 10.1038/ncomms1448. pmid:21863010
[11]
Takahashi K, Terai Y, Nishida M, Okada N. Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in lake Tanganyika as revealed by analysis of the insertion of retroposons. Mol Biol Evol. 2001;18(11):2057–66. pmid:11606702 doi: 10.1093/oxfordjournals.molbev.a003747
[12]
Hallstr？m BM, Janke A. Mammalian evolution may not be strictly bifurcating. Mol Biol Evol. 2010;27(12):2804–16. doi: 10.1093/molbev/msq166. pmid:20591845
[13]
Nishihara H, Maruyama S, Okada N. Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proc Natl Acad Sci USA. 2009;106(13):5235–40. doi: 10.1073/pnas.0809297106. pmid:19286970
[14]
Hormozdiari F, Konkel MK, Prado-Martinez J, Chiatante G, Herraez IH, Walker JA, et al. Rates and patterns of great ape retrotransposition. Proc Natl Acad Sci USA. 2013;110(33):13457–62. doi: 10.1073/pnas.1310914110. pmid:23884656
[15]
Degnan JH, Rosenberg NA. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol. 2009;24(6):332–40. doi: 10.1016/j.tree.2009.01.009. pmid:19307040
[16]
Felsenstein J. Alternative methods of phylogenetic inference and their interrelationship. Syst Biol. 1979;28(1):49–62. doi: 10.1093/sysbio/28.1.49
[17]
Ericson PGP, Anderson CL, Britton T, Elzanowski A, Johansson US, K？llersj？ M, et al. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett. 2006;2(4):543–7. pmid:17148284 doi: 10.1098/rsbl.2006.0523
[18]
Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, et al. A phylogenomic study of birds reveals their evolutionary history. Science. 2008;320(5884):1763–8. doi: 10.1126/science.1157704. pmid:18583609
[19]
Kimball RT, Wang N, Heimer-McGinn V, Ferguson C, Braun EL. Identifying localized biases in large datasets: A case study using the avian tree of life. Mol Phylogenet Evol. 2013;69(3):1021–32. doi: 10.1016/j.ympev.2013.05.029. pmid:23791948
[20]
McCormack JE, Harvey MG, Faircloth BC, Crawford NG, Glenn TC, Brumfield RT. A phylogeny of birds based on over 1,500 loci collected by target enrichment and high-throughput sequencing. PLoS ONE. 2013;8(1):e54848. doi: 10.1371/journal.pone.0054848. pmid:23382987
[21]
Yuri T, Kimball RT, Harshman J, Bowie RCK, Braun MJ, Chojnowski JL, et al. Parsimony and model-based analyses of indels in avian nuclear genes reveal congruent and incongruent phylogenetic signals. Biology. 2013;2:419–44. doi: 10.3390/biology2010419. pmid:24832669
[22]
Churakov G, Sadasivuni MK, Rosenbloom KR, Huchon D, Brosius J, Schmitz J. Rodent evolution: back to the root. Mol Biol Evol. 2010;27(6):1315–26. doi: 10.1093/molbev/msq019. pmid:20100942
[23]
Matzke A, Churakov G, Berkes P, Arms EM, Kelsey D, Brosius J, et al. Retroposon insertion patterns of neoavian birds: strong evidence for an extensive incomplete lineage sorting era. Mol Biol Evol. 2012;29(6):1497–501. doi: 10.1093/molbev/msr319. pmid:22319163
[24]
Wang N, Braun EL, Kimball RT. Testing hypotheses about the sister group of the Passeriformes using an independent 30-locus dataset. Mol Biol Evol. 2012;29(2):737–50. doi: 10.1093/molbev/msr230. pmid:21940640
[25]
Ericson PGP. Evolution of terrestrial birds in three continents: biogeography and parallel radiations. J Biogeogr. 2012;39(5):813–24. doi: 10.1111/j.1365-2699.2011.02650.x.
[26]
Mayr G. The origins of crown group birds: molecules and fossils. Palaeontology. 2014;57(2):231–42. doi: 10.1111/pala.12103
[27]
Brown JW, van Tuinen M. Evolving perceptions on the antiquity of the modern avian tree. In: Dyke G, Kaiser G, editors. Living Dinosaurs: The Evolutionary History of Modern Birds. Chichester: John Wiley & Sons, Ltd; 2011. p. 306–24.
[28]
van Tuinen M. Advanced birds (Neoaves). In: Hedges SB, Kumar S, editors. The timetree of life. New York: Oxford University Press; 2009. p. 419–22.
Pease JB, Hahn MW. More accurate phylogenies inferred from low-recombination regions in the presence of incomplete lineage sorting. Evolution. 2013;67(8):2376–84. doi: 10.1111/evo.12118. pmid:23888858
[31]
Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23(2):254–67. pmid:16221896
[32]
Ellegren H. Evolutionary stasis: the stable chromosomes of birds. Trends Ecol Evol. 2010;25(5):283–91. doi: 10.1016/j.tree.2009.12.004. pmid:20363047
[33]
Ellegren H. The evolutionary genomics of birds. Annu Rev Ecol Evol Syst. 2013;44(1):239–59. doi: 10.1146/annurev-ecolsys-110411-160327
[34]
Hillier LW, Miller W, Birney E, Warren W, Hardison RC, Ponting CP, et al. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432(7018):695–716. pmid:15592404
[35]
Aslam M, Bastiaansen J, Crooijmans R, Vereijken A, Megens H-J, Groenen M. A SNP based linkage map of the turkey genome reveals multiple intrachromosomal rearrangements between the turkey and chicken genomes. BMC Genomics. 2010;11(1):647. doi: 10.1186/1471-2164-11-647
[36]
Backstr？m N, Forstmeier W, Schielzeth H, Mellenius H, Nam K, Bolund E, et al. The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res. 2010;20(4):485–95. doi: 10.1101/gr.101410.109. pmid:20357052
[37]
Kawakami T, Smeds L, Backstr？m N, Husby A, Qvarnstr？m A, Mugal CF, et al. A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution. Mol Ecol. 2014;23(16):4035–58. doi: 10.1111/mec.12810. pmid:24863701
[38]
Rosenberg NA. Discordance of species trees with their most likely gene trees: a unifying principle. Mol Biol Evol. 2013;30(12):2709–13. doi: 10.1093/molbev/mst160. pmid:24030555
[39]
Salichos L, Rokas A. Inferring ancient divergences requires genes with strong phylogenetic signals. Nature. 2013;497(7449):327–31. doi: 10.1038/nature12130. pmid:23657258
[40]
Slatkin M, Pollack JL. Subdivision in an ancestral species creates asymmetry in gene trees. Mol Biol Evol. 2008;25(10):2241–6. doi: 10.1093/molbev/msn172. pmid:18689871
[41]
Hoelzer GA, Meinick DJ. Patterns of speciation and limits to phylogenetic resolution. Trends Ecol Evol. 1994;9(3):104–7. doi: 10.1016/0169-5347(94)90207-0. pmid:21236789
[42]
Longrich NR, Tokaryk T, Field DJ. Mass extinction of birds at the Cretaceous–Paleogene (K–Pg) boundary. Proc Natl Acad Sci USA. 2011;108(37):15253–7. doi: 10.1073/pnas.1110395108. pmid:21914849
[43]
O'Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, et al. The placental mammal ancestor and the post–K-Pg radiation of placentals. Science. 2013;339(6120):662–7. doi: 10.1126/science.1229237. pmid:23393258
[44]
Wolf YI, Rogozin IB, Grishin NV, Koonin EV. Genome trees and the tree of life. Trends Genet. 2002;18(9):472–9. pmid:12175808 doi: 10.1016/s0168-9525(02)02744-0
[45]
Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science. 2014;346(6215):1311–20. doi: 10.1126/science.1251385. pmid:25504712
[46]
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110(1–4):462–7. pmid:16093699 doi: 10.1159/000084979
[47]
Suh A, Kriegs JO, Brosius J, Schmitz J. Retroposon insertions and the chronology of avian sex chromosome evolution. Mol Biol Evol. 2011;28:2993–7. doi: 10.1093/molbev/msr147. pmid:21633113
[48]
Smit A, Hubley R, Green P. RepeatMasker Open-3.3.0. . 1996–2010.
Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008;9:286–98. doi: 10.1093/bib/bbn013. pmid:18372315
[51]
Suh A, Kriegs JO, Donnellan S, Brosius J, Schmitz J. A universal method for the study of CR1 retroposons in non-model bird genomes. Mol Biol Evol. 2012;29:2899–903. pmid:22522308 doi: 10.1093/molbev/mss124
[52]
Suh A, Churakov G, Ramakodi MP, Platt RN II, Jurka J, Kojima KK, et al. Multiple lineages of ancient CR1 retroposons shaped the early genome evolution of amniotes. Genome Biol Evol. 2015;7(1):205–17. doi: 10.1093/gbe/evu256
[53]
Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. Phylogenomic analyses data of the Avian Phylogenomics Project. GigaSci. 2015;4:4. doi: 10.1186/s13742-014-0038-1
[54]
Crooks GE, Hon G, Chandonia J-M, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188–90. pmid:15173120 doi: 10.1101/gr.849004
[55]
Schneider TD, Stephens RM. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 1990;18(20):6097–100. pmid:2172928 doi: 10.1093/nar/18.20.6097
