Avian Species Concepts in the Light of Genomics



What is a species? This seemingly simple question has occupied the minds of numerous biologists and philosophers, resulting in the formulation of many species concepts. From a theoretical point of view, the species problem has been resolved by equating species with independently evolving lineages (i.e. the evolutionary species concept or the general lineage concept). However, the practical issues with describing and delineating species remain. The origin of species is a gradual process that typically requires thousands to millions of years, creating a grey zone of species delimitation in which taxonomy is often controversial. To account for this, an integrative taxonomy has been proposed in which different taxonomic concepts and methods are integrated in the delimitation of species. In this chapter, I argue that genomics provides another line of evidence in this pluralistic approach to species classification. Indeed, genomic data can be combined with classical species criteria, such as diagnosability, phylogeny and reproductive isolation. First, genomic data can provide an extra diagnostic feature in species delimitation. Compared to ‘old-school’ genetic markers, the use of genome-wide markers leads to a significant rise in statistical power. Second, phylogenomic analyses can resolve the evolutionary relationships within rapidly diverging or hybridizing groups of species while taking into account gene tree discordance. Third, genomic data can be used to pinpoint the genetic basis of reproductive isolation and provide a detailed description of the speciation process. All in all, the genomic era will supply avian taxonomists with a new tool box that can be applied to old concepts, leading to better informed decisions in cataloguing biodiversity.


Distinguishability General lineage concept Hybridization Integrative taxonomy Introgression Phylogenomics Reproductive isolation Speciation Species delimitation Tobias criteria 



I would like to thank Robert Kraus for giving me the opportunity to write this chapter and share my ideas on the role of genomics in avian taxonomy. These ideas are based on a chapter from my PhD thesis on hybridization in geese. I am grateful to my supervisors—Herbert Prins, Ron Ydenberg, Pim van Hooft, Sip van Wieren, Hendrik-Jan Megens and Martien Groenen—for letting me explore and develop these concepts during my PhD at Wageningen University (the Netherlands). Finally, I would like to thank two anonymous reviewers whose comments and suggestions have greatly improved this chapter.


  1. Adams DC, Berns CM, Kozak KH, Wiens JJ (2009) Are rates of species diversification correlated with rates of morphological evolution? Proc Biol Sci 276(1668):2729–2738PubMedPubMedCentralCrossRefGoogle Scholar
  2. Agapow PM, Bininda-Emonds OR, Crandall KA, Gittleman JL, Mace GM, Marshall JC, Purvis A (2004) The impact of species concept on biodiversity studies. Q Rev Biol 79(2):161–179PubMedCrossRefGoogle Scholar
  3. Alström P, Rasmussen PC, Olsson U, Sundberg P (2008) Species delimitation based on multiple criteria: the Spotted Bush Warbler Bradypterus thoracicus complex (Aves: Megaluridae). Zool J Linn Soc 154(2):291–307CrossRefGoogle Scholar
  4. Anderson E (1949) Introgressive hybridization. Wiley, New YorkCrossRefGoogle Scholar
  5. Arnold ML (2006) Evolution through genetic exchange. Oxford University Press, OxfordGoogle Scholar
  6. Ballentine B, Horton B, Brown ET, Greenberg R (2013) Divergent selection on bill morphology contributes to nonrandom mating between swamp sparrow subspecies. Anim Behav 86:467–473CrossRefGoogle Scholar
  7. Barton N, Bengtsson BO (1986) The barrier to genetic exchange between hybridising populations. Heredity 57(3):357–376PubMedCrossRefGoogle Scholar
  8. Baum DA, Donoghue MJ (1995) Choosing among alternative phylogenetic species concepts. Syst Bot 20(4):560–573CrossRefGoogle Scholar
  9. Baum DA, Shaw KL (1995) Genealogical perspectives on the species problem. Exp Mol Approach Plant Biosyst 53(289–303):123–124Google Scholar
  10. Bay RA, Ruegg K (2017) Genomic islands of divergence or opportunities for introgression? ProcBiol Sci 284(1850):20162414. CrossRefGoogle Scholar
  11. Benkman CW (1993) Adaptation to single resources and the evolution of crossbill (Loxia) diversity. Ecol Monogr 63:305–325CrossRefGoogle Scholar
  12. Benkman CW (1999) The selection mosaic and diversifying coevolution between crossbills and lodgepole pine. Am Nat 153:S75–S91PubMedCrossRefPubMedCentralGoogle Scholar
  13. Benkman CW (2003) Divergent selection drives the adaptive radiation of crossbills. Evolution 57:1176–1181PubMedCrossRefPubMedCentralGoogle Scholar
  14. Berlocher SH, Feder JL (2002) Sympatric speciation in phytophagous insects: moving beyond controversy? Annu Rev Entomol 47:773–815PubMedCrossRefPubMedCentralGoogle Scholar
  15. Bolnick DI, Fitzpatrick BM (2007) Sympatric speciation: models and empirical evidence. Annu Rev Ecol Evol Syst 38:459–487CrossRefGoogle Scholar
  16. Braun EL, Cracraft J, Houde P (2019) Resolving the avian tree of life from top to bottom: the promise and potential boundaries of the phylogenomic era. In: Kraus RHS (ed) Avian genomics in ecology and evolution. Springer, ChamGoogle Scholar
  17. Brown WL (1957) Centrifugal speciation. Q Rev Biol 32(3):247–277CrossRefGoogle Scholar
  18. Brumfield RT, Liu L, Lum DE, Edwards SV (2008) Comparison of species tree methods for reconstructing the phylogeny of bearded manakins (Aves: Pipridae, Manacus) from multilocus sequence data. Syst Biol 57(5):719–731PubMedCrossRefPubMedCentralGoogle Scholar
  19. Bush GL (1975) Modes of animal speciation. Annu Rev Ecol Syst 6:339–364CrossRefGoogle Scholar
  20. Butlin RK, Galindo J, Grahame JW (2008) Review. Sympatric, parapatric or allopatric: the most important way to classify speciation? Philos Trans R Soc Lond B Biol Sci 363(1506):2997–3007PubMedPubMedCentralCrossRefGoogle Scholar
  21. Campbell CR, Poelstra JW, Yoder AD (2018) What is speciation genomics? The roles of ecology, gene flow, and genomic architecture in the formation of species. Biol J Linn Soc 124(4):561–583CrossRefGoogle Scholar
  22. Caro LM, Caycedo-Rosales PC, Bowie RCK, Slabbekoorn H, Cadena CD (2013) Ecological speciation along an elevational gradient in a tropical passerine bird? J Evol Biol 26:357–374PubMedCrossRefGoogle Scholar
  23. Cook OF (1906) Factors of species-formation. Science 23(587):506–507PubMedCrossRefPubMedCentralGoogle Scholar
  24. Cooney CR, Tobias JA, Weir JT, Botero CA, Seddon N (2017) Sexual selection, speciation and constraints on geographical range overlap in birds. Ecol Lett 20:863–871PubMedCrossRefPubMedCentralGoogle Scholar
  25. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MAGoogle Scholar
  26. Cracraft J (1983) Species concepts and speciation analysis. In: Johnston RF (ed) Current ornithology. Plenum Press, New York, pp 159–187CrossRefGoogle Scholar
  27. Cruickshank TE, Hahn MW (2014) Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow. Mol Ecol 23(13):3133–3157PubMedCrossRefGoogle Scholar
  28. Darwin C (1859) The origin of species by means of natural selection: the preservation of favoured races in the struggle for life. Murray, LondonGoogle Scholar
  29. Davalos LM, Cirranello AL, Geisler JH, Simmons NB (2012) Understanding phylogenetic incongruence: lessons from phyllostomid bats. Biol Rev 87(4):991–1024PubMedCrossRefPubMedCentralGoogle Scholar
  30. Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85(3):407–415CrossRefGoogle Scholar
  31. De Queiroz K (1998) The general lineage concept of species: species criteria, and the process of speciation. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 57–75Google Scholar
  32. De Queiroz K (1999) The general lineage concept of species and the defining properties of the species category. In: Wilson RA (ed) Species: new interdisciplinary essays. MIT Press, Cambridge, MAGoogle Scholar
  33. De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56(6):879–886PubMedCrossRefPubMedCentralGoogle Scholar
  34. de Queiroz K, Donoghue MJ (1988) Phylogenetic systematics and the species problem. Cladistics 4(4):317–338CrossRefGoogle Scholar
  35. Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24(6):332–340PubMedCrossRefPubMedCentralGoogle Scholar
  36. Degnan JH, Salter LA (2005) Gene tree distributions under the coalescent process. Evolution 59(1):24–37PubMedCrossRefPubMedCentralGoogle Scholar
  37. Delmore KE, Hubner S, Kane NC, Schuster R, Andrew RL, Camara F, Guigo R, Irwin DE (2015) Genomic analysis of a migratory divide reveals candidate genes for migration and implicates selective sweeps in generating islands of differentiation. Mol Ecol 24(8):1873–1888PubMedCrossRefGoogle Scholar
  38. DeSalle R, Egan MG, Siddall M (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philos Trans R Soc Lond B Biol Sci 360(1462):1905–1916PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dhami KK, Joseph L, Roshier DA, Peters JL (2016) Recent speciation and elevated Z-chromosome differentiation between sexually monochromatic and dichromatic species of Australian teals. J Avian Biol 47(1):92–102CrossRefGoogle Scholar
  40. Dieckmann U, Tautz D, Doebeli M, Metz JA (2004) Epilogue. In: Dieckmann U, Doebeli M, Metz JA, Tautz D (eds) Adaptive speciation. Cambridge University Press, Cambridge, pp 380–394CrossRefGoogle Scholar
  41. Donegan TM (2018) What is a species? A new universal method to measure differentiation and assess the taxonomic rank of allopatric populations, using continuous variables. Zookeys 757:1–67CrossRefGoogle Scholar
  42. Ellegren H, Smeds L, Burri R, Olason PI, Backström N, Kawakami T, Kunstner A, Makinen H, Nadachowska-Brzyska K, Qvarnström A, Uebbing S, Wolf JBW (2012) The genomic landscape of species divergence in Ficedula flycatchers. Nature 491(7426):756–760PubMedCrossRefGoogle Scholar
  43. Feder JL, Chilcote CA, Bush GL (1988) Genetic differentiation between sympatric host races of the apple maggot fly Rhagoletis pomonella. Nature 336(6194):61–64CrossRefGoogle Scholar
  44. Feder JL, Roethele FB, Filchak K, Niedbalski J, Romero-Severson J (2003) Evidence for inversion polymorphism related to sympatric host race formation in the apple maggot fly, Rhagoletis pomonella. Genetics 163(3):939–953PubMedPubMedCentralGoogle Scholar
  45. Fitzpatrick BM (2004) Rates of evolution of hybrid inviability in birds and mammals. Evolution 58(8):1865–1870PubMedCrossRefPubMedCentralGoogle Scholar
  46. Fitzpatrick BM, Fordyce JA, Gavrilets S (2008) What, if anything, is sympatric speciation? J Evol Biol 21(6):1452–1459PubMedCrossRefPubMedCentralGoogle Scholar
  47. Friesen VL, Smith AL, Gó Mez-Díaz E, Bolton M, Furness RW, Gonzá Lez-Solís J, Monteiro LR, Futuyma DJ (2007) Sympatric speciation by allochrony in a seabird. Proc Natl Acad Sci USA 104:18589–18594PubMedCrossRefGoogle Scholar
  48. Fuchs J, Pons JM, Liu L, Ericson PGP, Couloux A, Pasquet E (2013) A multi-locus phylogeny suggests an ancient hybridization event between Campephilus and melanerpine woodpeckers (Ayes: Picidae). Mol Phylogenet Evol 67(3):578–588PubMedCrossRefGoogle Scholar
  49. Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton University Press, Princeton, NJGoogle Scholar
  50. Gohli J, Leder EH, Garcia-Del-Rey E, Johannessen LE, Johnsen A, Laskemoen T, Popp M, Lifjeld JT (2015) The evolutionary history of Afrocanarian blue tits inferred from genomewide SNPs. Mol Ecol 24(1):180–191PubMedCrossRefPubMedCentralGoogle Scholar
  51. Haasl RJ, Payseur BA (2016) Fifteen years of genomewide scans for selection: trends, lessons and unaddressed genetic sources of complication. Mol Ecol 25(1):5–23PubMedCrossRefGoogle Scholar
  52. Harr B (2006) Genomic islands of differentiation between house mouse subspecies. Genome Res 16(6):730–737PubMedPubMedCentralCrossRefGoogle Scholar
  53. Harrison RG (1998) Linking evolutionary pattern and process. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 19–31Google Scholar
  54. Harrison RG (2012) The language of speciation. Evolution 66(12):3643–3657PubMedCrossRefGoogle Scholar
  55. Hebert PD, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2(10):e312PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hendry AP, Bolnick DI, Berner D, Peichel CL (2009) Along the speciation continuum in sticklebacks. J Fish Biol 75(8):2000–2036PubMedCrossRefGoogle Scholar
  57. Hey J (2006) On the failure of modern species concepts. Trends Ecol Evol 21(8):447–450PubMedCrossRefPubMedCentralGoogle Scholar
  58. Hooper DM, Price TD (2015) Rates of karyotypic evolution in Estrildid finches differ between island and continental clades. Evolution 69(4):890–903PubMedCrossRefGoogle Scholar
  59. Huang H, Rabosky DL (2014) Sexual selection and diversification: reexamining the correlation between dichromatism and speciation rate in birds. Am Nat 184:E101–E114PubMedCrossRefPubMedCentralGoogle Scholar
  60. Irwin DE, Irwin JH, Smith TB (2011) Genetic variation and seasonal migratory connectivity in Wilson’s warblers (Wilsonia pusilla): species-level differences in nuclear DNA between western and eastern populations. Mol Ecol 20(15):3102–3115PubMedCrossRefGoogle Scholar
  61. Isaac NJ, Mallet J, Mace GM (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19(9):464–469PubMedCrossRefGoogle Scholar
  62. Isler ML, Isler PR, Whitney BM (1998) Use of vocalizations to establish species limits in antbirds (Passeriformes; Thamnophilidae). Auk 115:557–590Google Scholar
  63. Jacobsen F, Omland KE (2012) Extensive introgressive hybridization within the northern oriole group (Genus Icterus) revealed by three-species isolation with migration analysis. Ecol Evol 2(10):2413–2429PubMedPubMedCentralCrossRefGoogle Scholar
  64. Jarvis ED (2016) Perspectives from the avian phylogenomics project: questions that can be answered with sequencing all genomes of a vertebrate class. Annu Rev Anim Biosci 4:45–59PubMedCrossRefGoogle Scholar
  65. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, Suh A, Weber CC, da Fonseca RR, Li JW, Zhang F, Li H, Zhou L, Narula N, Liu L, Ganapathy G, Boussau B, Bayzid MS, Zavidovych V, Subramanian S, Gabaldon T, Capella-Gutierrez S, Huerta-Cepas J, Rekepalli B, Munch K, Schierup M, Lindow B, Warren WC, Ray D, Green RE, Bruford MW, Zhan XJ, Dixon A, Li SB, Li N, Huang YH, Derryberry EP, Bertelsen MF, Sheldon FH, Brumfield RT, Mello CV, Lovell PV, Wirthlin M, Schneider MPC, Prosdocimi F, Samaniego JA, Velazquez AMV, Alfaro-Nunez A, Campos PF, Petersen B, Sicheritz-Ponten T, Pas A, Bailey T, Scofield P, Bunce M, Lambert DM, Zhou Q, Perelman P, Driskell AC, Shapiro B, Xiong ZJ, Zeng YL, Liu SP, Li ZY, Liu BH, Wu K, Xiao J, Yinqi X, Zheng QM, Zhang Y, Yang HM, Wang J, Smeds L, Rheindt FE, Braun M, Fjeldsa J, Orlando L, Barker FK, Jonsson KA, Johnson W, Koepfli KP, O’Brien S, Haussler D, Ryder OA, Rahbek C, Willerslev E, Graves GR, Glenn TC, McCormack J, Burt D, Ellegren H, Alstrom P, Edwards SV, Stamatakis A, Mindell DP, Cracraft J, Braun EL, Warnow T, Jun W, Gilbert MTP, Zhang GJ (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346(6215):1320–1331PubMedPubMedCentralCrossRefGoogle Scholar
  66. Johns GC, Avise JC (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Mol Biol Evol 15(11):1481–1490PubMedCrossRefGoogle Scholar
  67. Kawakami T, Smeds L, Backstrom N, Husby A, Qvarnstrom A, Mugal CF, Olason P, Ellegren H (2014) 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 23(16):4035–4058PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kimura M, Clegg SM, Lovette IJ, Holder KR, Girman DJ, Mila B, Wade P, Smith TB (2002) Phylogeographical approaches to assessing demographic connectivity between breeding and overwintering regions in a nearctic-neotropical warbler (Wilsonia pusilla). Mol Ecol 11(9):1605–1616PubMedCrossRefGoogle Scholar
  69. Kirkpatrick M, Ravigne V (2002) Speciation by natural and sexual selection: models and experiments. Am Nat 159:S22–S35PubMedCrossRefGoogle Scholar
  70. Kirschel AN, Slabbekoorn H, Blumstein DT, Cohen RE, de Kort SR, Buermann W, Smith TB (2011) Testing alternative hypotheses for evolutionary diversification in an African songbird: rainforest refugia versus ecological gradients. Evolution 65(11):3162–3174PubMedCrossRefPubMedCentralGoogle Scholar
  71. Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Philos Trans R Soc Lond B Biol Sci 361(1475):1929–1940PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kraus RHS, Wink M (2015) Avian genomics: fledging into the wild! J Ornithol 156(4):1–15CrossRefGoogle Scholar
  73. Kraus RHS, Kerstens HH, van Hooft P, Megens HJ, Elmberg J, Tsvey A, Sartakov D, Soloviev SA, Crooijmans RPMA, Groenen MAM, Ydenberg RC, Prins HHT (2012) Widespread horizontal genomic exchange does not erode species barriers among sympatric ducks. BMC Evol Biol 12(1):45PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kulikova IV, Drovetski SV, Gibson DD, Harrigan RJ, Rohwer S, Sorenson MD, Winker K, Zhuravlev YN, McCracken KG (2005) Phylogeography of the Mallard (Anas platyrhynchos): hybridization, dispersal, and lineage sorting contribute to complex geographic structure. Auk 122(3):949–965CrossRefGoogle Scholar
  75. Lackey AC, Boughman JW (2017) Evolution of reproductive isolation in stickleback fish. Evolution 71(2):357–372PubMedCrossRefGoogle Scholar
  76. Lovette IJ (2004) Mitochondrial dating and mixed-support for the “2% rule” in birds. Auk 121(1):1–6Google Scholar
  77. Luckow M (1995) Species concepts – assumptions, methods, and applications. Syst Bot 20(4):589–605CrossRefGoogle Scholar
  78. Maddison WP (1997) Gene trees in species trees. Syst Biol 46(3):523–536CrossRefGoogle Scholar
  79. Mallet J (1995) A species definition for the modern synthesis. Trends Ecol Evol 10(7):294–299PubMedCrossRefGoogle Scholar
  80. Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20(5):229–237PubMedCrossRefGoogle Scholar
  81. Mason NA, Taylor SA (2015) Differentially expressed genes match bill morphology and plumage despite largely undifferentiated genomes in a Holarctic songbird. Mol Ecol 24(12):3009–3025PubMedCrossRefGoogle Scholar
  82. Mayden RL (1997) A hierarchy of species concepts: the denouement in the saga of the species problem. In: Claridge MF, Dawah HA, Wilson MR (eds) Species: the units of diversity. Chapman and Hall, London, pp 381–423Google Scholar
  83. Mayden RL (1999) Consilience and a hierarchy of species concepts: advances toward closure on the species puzzle. J Nematol 31(2):95–116PubMedPubMedCentralGoogle Scholar
  84. Mayr E (1969) Principles of systematic zoology. McGraw-Hill, New YorkGoogle Scholar
  85. Mayr E (1982) The growth of biological thought: diversity, evolution, and inheritance. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  86. Mayr E, Ashlock PD (1991) Principles of systematic zoology. McGraw-Hill, New YorkGoogle Scholar
  87. Meier-Kolthoff JP, Auch AF, Klenk HP, Goker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60PubMedPubMedCentralCrossRefGoogle Scholar
  88. Meiri S, Mace GM (2007) New taxonomy and the origin of species. PLoS Biol 5(7):e194PubMedPubMedCentralCrossRefGoogle Scholar
  89. Meise W (1928) Die Verbreitung der Aaskrähe (Formenkreis Corvus corone L.). DornblüthGoogle Scholar
  90. Michel AP, Sim S, Powell THQ, Taylor MS, Nosil P, Feder JL (2010) Widespread genomic divergence during sympatric speciation. Proc Natl Acad Sci USA 107(21):9724–9729PubMedCrossRefPubMedCentralGoogle Scholar
  91. Monteiro LR, Furness RW (1998) Speciation through temporal segregation of Madeiran storm petrel (Oceanodroma castro) populations in the Azores? Philos Trans R Soc Lond B Biol Sci 353:945–953PubMedCentralCrossRefPubMedGoogle Scholar
  92. Morrow EH, Pitcher TE, Arnqvist G (2003) No evidence that sexual selection is an “engine of speciation” in birds. Ecol Lett 6:228–234CrossRefGoogle Scholar
  93. Nadeau NJ, Whibley A, Jones RT, Davey JW, Dasmahapatra KK, Baxter SW, Quail MA, Joron M, Ffrench-Constant RH, Blaxter ML, Mallet J, Jiggins CD (2012) Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philos Trans R Soc Lond B Biol Sci 367(1587):343–353PubMedPubMedCentralCrossRefGoogle Scholar
  94. Naomi SI (2011) On the integrated frameworks of species concepts: Mayden’s hierarchy of species concepts and de Queiroz’s unified concept of species. J Zool Syst Evol Res 49(3):177–184CrossRefGoogle Scholar
  95. Nater A, Burri R, Kawakami T, Smeds L, Ellegren H (2015) Resolving evolutionary relationships in closely related species with whole-genome sequencing data. Syst Biol 64(6):1000–1017PubMedPubMedCentralCrossRefGoogle Scholar
  96. Nixon KC, Wheeler QD (1990) An amplification of the phylogenetic species concept. Cladistics 6(3):211–223CrossRefGoogle Scholar
  97. Noor MAF, Bennett SM (2009) Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species. Heredity 103(6):439–444PubMedPubMedCentralCrossRefGoogle Scholar
  98. Noor MAF, Grams KL, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci USA 98(21):12084–12088PubMedCrossRefPubMedCentralGoogle Scholar
  99. Nosil P (2012) Ecological speciation. Oxford University Press, OxfordCrossRefGoogle Scholar
  100. Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18(3):375–402PubMedCrossRefGoogle Scholar
  101. Oswald JA, Harvey MG, Remsen RC, Foxworth DU, Cardiff SW, Dittmann DL, Megna LC, Carling MD, Brumfield RT (2016) Willet be one species or two? A genomic view of the evolutionary history of Tringa semipalmata. Auk 133(4):593–614CrossRefGoogle Scholar
  102. Ottenburghs J, Ydenberg RC, Van Hooft P, Van Wieren SE, Prins HHT (2015) The Avian Hybrids Project: gathering the scientific literature on avian hybridization. Ibis 157(4):892–894CrossRefGoogle Scholar
  103. Ottenburghs J, Megens HJ, Kraus RH, Madsen O, van Hooft P, van Wieren SE, Crooijmans RP, Ydenberg RC, Groenen MA, Prins HH (2016a) A tree of geese: a phylogenomic perspective on the evolutionary history of True Geese. Mol Phylogenet Evol 101:303–313PubMedCrossRefPubMedCentralGoogle Scholar
  104. Ottenburghs J, van Hooft P, Van Wieren SE, Ydenberg RC, Prins HHT (2016b) Birds in a bush: toward an avian phylogenetic network. Auk 133:577–582CrossRefGoogle Scholar
  105. Ottenburghs J, Kraus RHS, van Hooft P, Van Wieren SE, Ydenberg RC, Prins HHT (2017) Avian introgression in the genomic era. Avian Res 8:30CrossRefGoogle Scholar
  106. Oyler-McCance SJ, Cornman RS, Jones KL, Fike JA (2015) Genomic single-nucleotide polymorphisms confirm that Gunnison and Greater Sage-grouse are genetically well differentiated and that the Bi-State population is distinct. Condor 117(2):217–227CrossRefGoogle Scholar
  107. Oyler-McCance SJ, Oh KP, Langin KM, Aldridge CL (2016) A field ornithologist’s guide to genomics: practical considerations for ecology and conservation. Auk 133(4):626–648CrossRefGoogle Scholar
  108. Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7:16PubMedPubMedCentralCrossRefGoogle Scholar
  109. Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5(5):568–583PubMedPubMedCentralGoogle Scholar
  110. Parchman T, Benkman C, Britch S (2006) Patterns of genetic variation in the adaptive radiation of New World crossbills (Aves: Loxia). Mol Ecol 15:1873–1887PubMedCrossRefGoogle Scholar
  111. Paterson HEH (1993) Evolution and the recognition concept of species: collected writings. Johns Hopkins University Press, Baltimore, MDGoogle Scholar
  112. Paulay G (1985) Adaptive radiation on an isolated oceanic island – the Cryptorhynchinae (Curculionidae) of Rapa revisited. Biol J Linn Soc 26(2):95–187CrossRefGoogle Scholar
  113. Paxton KL, Yau M, Moore FR, Irwin DE (2013) Differential migratory timing of western populations of Wilson’s warbler (Cardellina Pusilla) revealed by mitochondrial DNA and stable isotopes. Auk 130(4):689–698CrossRefGoogle Scholar
  114. Payseur BA (2016) Genetic links between recombination and speciation. PLoS Genet 12(6):e1006066PubMedPubMedCentralCrossRefGoogle Scholar
  115. Phillimore AB, Orme CDL, Thomas GH, Blackburn TM, Bennett PM, Gaston KJ, Owens IPF (2008) Sympatric speciation in birds is rare: insights from range data and simulations. Am Nat 171:646–657PubMedCrossRefGoogle Scholar
  116. Pinho C, Hey J (2010) Divergence with gene flow: models and data. Annu Rev Ecol Evol Syst 41(41):215–230CrossRefGoogle Scholar
  117. Podos J, Dybboe R, Jensen MO (2013) Ecological speciation in Darwin’s finches: parsing the effects of magic traits. Curr Zool 59:8–19CrossRefGoogle Scholar
  118. Poelstra JW, Vijay N, Bossu CM, Lantz H, Ryll B, Muller I, Baglione V, Unneberg P, Wikelski M, Grabherr MG, Wolf JBW (2014) The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344(6190):1410–1414PubMedCrossRefGoogle Scholar
  119. Presgraves DC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11(3):175–180PubMedCrossRefGoogle Scholar
  120. Price T (2008) Speciation in birds. Roberts and Company, Greenwood Village, COGoogle Scholar
  121. Ravinet M, Faria R, Butlin RK, Galindo J, Bierne N, Rafajlović M, Noor MAF, Mehlig B, Westram AM (2017) Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. J Evol Biol 30:1450–1477PubMedCrossRefGoogle Scholar
  122. Rheindt FE, Edwards SV (2011) Genetic introgression: an integral but neglected component of speciation in birds. Auk 128(4):620–632CrossRefGoogle Scholar
  123. Rheindt FE, Christidis L, Norman JA (2009) Genetic introgression, incomplete lineage sorting and faulty taxonomy create multiple cases of polyphyly in a montane clade of tyrant-flycatchers (Elaenia, Tyrannidae). Zool Scr 38(2):143–153CrossRefGoogle Scholar
  124. Ribeiro ÂM, Lloyd P, Bowie RCK (2011) A tight balance between natural selection and gene flow in a southern African arid-zone endemic bird. Evolution 65:3499–3514PubMedCrossRefPubMedCentralGoogle Scholar
  125. Richards RA (2010) The species problem: a philosophical analysis. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  126. Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16(7):351–358PubMedCrossRefPubMedCentralGoogle Scholar
  127. Rokas A, Williams BL, King N, Carroll SB (2003) Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425(6960):798–804PubMedCrossRefPubMedCentralGoogle Scholar
  128. Roux C, Fraïsse C, Romiguier J, Anciaux Y, Galtier N, Bierne N (2016) Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biol 14(2):e2000234PubMedPubMedCentralCrossRefGoogle Scholar
  129. Ruegg K, Anderson EC, Boone J, Pouls J, Smith TB (2014a) A role for migration-linked genes and genomic islands in divergence of a songbird. Mol Ecol 23(19):4757–4769PubMedCrossRefPubMedCentralGoogle Scholar
  130. Ruegg KC, Anderson EC, Paxton KL, Apkenas V, Lao S, Siegel RB, DeSante DF, Moore F, Smith TB (2014b) Mapping migration in a songbird using high-resolution genetic markers. Mol Ecol 23(23):5726–5739PubMedCrossRefGoogle Scholar
  131. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8(3):336–352CrossRefGoogle Scholar
  132. Ryan P, Bloomer P, Moloney C, Grant T, Delport W (2007) Ecological speciation in South Atlantic island finches. Science 315(5817):1420–1423PubMedCrossRefGoogle Scholar
  133. Sangster G (2009) Increasing numbers of bird species result from taxonomic progress, not taxonomic inflation. Proc Biol Sci 276(1670):3185–3191PubMedPubMedCentralCrossRefGoogle Scholar
  134. Sangster G (2014) The application of species criteria in avian taxonomy and its implications for the debate over species concepts. Biol Rev 89(1):199–214PubMedCrossRefGoogle Scholar
  135. Scally A, Dutheil JY, Hillier LW, Jordan GE, Goodhead I, Herrero J, Hobolth A, Lappalainen T, Mailund T, Marques-Bonet T, McCarthy S, Montgomery SH, Schwalie PC, Tang YA, Ward MC, Xue Y, Yngvadottir B, Alkan C, Andersen LN, Ayub Q, Ball EV, Beal K, Bradley BJ, Chen Y, Clee CM, Fitzgerald S, Graves TA, Gu Y, Heath P, Heger A, Karakoc E, Kolb-Kokocinski A, Laird GK, Lunter G, Meader S, Mort M, Mullikin JC, Munch K, O’Connor TD, Phillips AD, Prado-Martinez J, Rogers AS, Sajjadian S, Schmidt D, Shaw K, Simpson JT, Stenson PD, Turner DJ, Vigilant L, Vilella AJ, Whitener W, Zhu B, Cooper DN, de Jong P, Dermitzakis ET, Eichler EE, Flicek P, Goldman N, Mundy NI, Ning Z, Odom DT, Ponting CP, Quail MA, Ryder OA, Searle SM, Warren WC, Wilson RK, Schierup MH, Rogers J, Tyler-Smith C, Durbin R (2012) Insights into hominid evolution from the gorilla genome sequence. Nature 483(7388):169–175PubMedPubMedCentralCrossRefGoogle Scholar
  136. Schroeder MA (2008) Variation in Greater Sage-grouse morphology by region and population. Washington Department of Fish and Wildlife, Bridgeport, WAGoogle Scholar
  137. Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19(4):198–207PubMedCrossRefGoogle Scholar
  138. Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455(7213):620–U623PubMedCrossRefGoogle Scholar
  139. Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA, Peichel CL, Saetre GP, C. Bank, Brannstrom A, Brelsford A, Clarkson CS, Eroukhmanoff F, Feder JL, Fischer MC, Foote AD, Franchini P, Jiggins CD, Jones FC, Lindholm AK, Lucek K, Maan ME, Marques DA, Martin SH, Matthews B, Meier JI, Most M, Nachman MW, Nonaka E, Rennison DJ, Schwarzer J, Watson ET, Westram AM, Widmer A (2014) Genomics and the origin of species. Nat Rev Genet 15(3):176–192PubMedCrossRefPubMedCentralGoogle Scholar
  140. Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: “magic” but not rare? Trends Ecol Evol 26:389–397PubMedCrossRefGoogle Scholar
  141. Shaffer HB, Thomson RC (2007) Delimiting species in recent radiations. Syst Biol 56(6):896–906PubMedCrossRefGoogle Scholar
  142. Shields GF (1982) Comparative avian cytogenetics – a review. Condor 84(1):45–58CrossRefGoogle Scholar
  143. Singhal S, Leffler EM, Sannareddy K, Turner I, Venn O, Hooper DM, Strand AI, Li Q, Raney B, Balakrishnan CN, Griffith SC, McVean G, Przeworski M (2015) Stable recombination hotspots in birds. Science 350(6263):928–932PubMedPubMedCentralCrossRefGoogle Scholar
  144. Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annu Rev Ecol Evol Syst 35:199–227CrossRefGoogle Scholar
  145. Smith HM (1965) More evolutionary terms. Syst Biol 14(1):57–58Google Scholar
  146. Smith JW, Benkman CW (2007) A coevolutionary arms race causes ecological speciation in crossbills. Am Nat 169:455–465PubMedCrossRefGoogle Scholar
  147. Smith T, Wayne R, Girman D, Bruford M (1997) A role for ecotones in generating rainforest biodiversity. Science 276(5320):1855–1857CrossRefGoogle Scholar
  148. Smith TB, Calsbeek R, Wayne RK, Holder KH, Pires D, Bardeleben C (2005) Testing alternative mechanisms of evolutionary divergence in an African rain forest passerine bird. J Evol Biol 18:257–268PubMedCrossRefGoogle Scholar
  149. Smith T, Thomassen H, Freedman A, Sehgal R, Buermann W, Saatchi S, Pollinger J, Mila B, Pires D, Wayne G (2011) Patterns of divergence in the olive sunbird Cyanomitra olivacea (Aves: Nectariniidae) across the African rainforest-savanna ecotone. Biol J Linn Soc 103:821–835CrossRefGoogle Scholar
  150. Smith JW, Sjoberg SM, Mueller MC, Benkman CW (2012) Assortative flocking in crossbills and implications for ecological speciation. Proc Biol Sci 279:4223–4229PubMedPubMedCentralCrossRefGoogle Scholar
  151. Sokal RR, Sneath PHA (1963) Principles of numerical taxonomy. Freeman, San Francisco, CAGoogle Scholar
  152. Sonsthagen SA, Wilson RE, Chesser RT, Pons JM, Crochet PA, Driskell A, Dove C (2016) Recurrent hybridization and recent origin obscure phylogenetic relationships within the ‘white-headed’ gull (Larus sp.) complex. Mol Phylogenet Evol 103:41–54PubMedCrossRefGoogle Scholar
  153. Sorenson MD, Sefc KM, Payne RB (2003) Speciation by host switch in brood parasitic indigobirds. Nature 424(6951):928–931PubMedCrossRefGoogle Scholar
  154. 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):e1002224PubMedPubMedCentralCrossRefGoogle Scholar
  155. Taylor RS, Friesen VL (2017) The role of allochrony in speciation. Mol Ecol 26:3330–3342PubMedCrossRefPubMedCentralGoogle Scholar
  156. Taylor SE, Young JR (2006) A comparative behavioral study of three Greater Sage-grouse populations. Wilson J Ornithol 118(1):36–41CrossRefGoogle Scholar
  157. Taylor RS, Bailie A, Gulavita P, Birt T, Aarvak T, Anker-Nilssen T, Barton DC, Lindquist K, Bedolla-Guzmán Y, Quillfeldt P, Friesen VL (2018) Sympatric population divergence within a highly pelagic seabird species complex (Hydrobates spp.). J Avian Biol 49(1).
  158. Templeton AR (1981) Mechanisms of speciation – a population genetic approach. Annu Rev Ecol Syst 12:23–48CrossRefGoogle Scholar
  159. Templeton AR (1989) The meaning of species and speciation: a genetic perspective. In: Ereshefsky M (ed) The units of evolution: essays on the nature of species. MIT Press, Cambridge, pp 159–183Google Scholar
  160. Tobias JA, Seddon N, Spottiswoode CN, Pilgrim JD, Fishpool LDC, Collar NJ (2010) Quantitative criteria for species delimitation. Ibis 152:724–746CrossRefGoogle Scholar
  161. Toews DPL, Campagna L, Taylor SA, Balakrishnan CN, Baldassarre DT, Deane-Coe PE, Harvey MG, Hooper DM, Irwin DE, Judy CD, Mason NA, McCormack JE, McCracken KG, Oliveros CH, Safran RJ, Scordato ESC, Stryjewski KF, Tigano A, Uy JAC, Winger BM (2016) Genomic approaches to understanding population divergence and speciation in birds. Auk 133(1):13–30CrossRefGoogle Scholar
  162. Turner TL, Hahn MW (2010) Genomic islands of speciation or genomic islands and speciation? Mol Ecol 19(5):848–850PubMedCrossRefGoogle Scholar
  163. Turner TL, Hahn MW, Nuzhdin SV (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biol 3(9):1572–1578CrossRefGoogle Scholar
  164. Van Valen L (1976) Ecological species, multispecies, and oaks. Taxon 25:233–239CrossRefGoogle Scholar
  165. Vignal A, Eöry L (2019) Avian genomics in animal breeding and the end of the model organism. In: Kraus RHS (ed) Avian genomics in ecology and evolution. Springer, ChamGoogle Scholar
  166. Volker M, Backstrom N, Skinner BM, Langley EJ, Bunzey SK, Ellegren H, Griffin DK (2010) Copy number variation, chromosome rearrangement, and their association with recombination during avian evolution. Genome Res 20(4):503–511PubMedPubMedCentralCrossRefGoogle Scholar
  167. Wakeley J (2009) Coalescent theory: an introduction. Roberts and Company, Greenwood Village, COGoogle Scholar
  168. Wallace SJ, Morris-Pocock JA, González-Solís J, Quillfeldt P, Friesen VL (2017) A phylogenetic test of sympatric speciation in the Hydrobatinae (Aves: Procellariiformes). Mol Phylogenet Evol 107:39–47PubMedCrossRefPubMedCentralGoogle Scholar
  169. White MJD (1969) Chromosomal rearrangements and speciation in animals. Annu Rev Genet 3(1):75–98CrossRefGoogle Scholar
  170. Wiens JJ, Servedio MR (2000) Species delimitation in systematics: inferring diagnostic differences between species. Proc Biol Sci 267(1444):631–636PubMedPubMedCentralCrossRefGoogle Scholar
  171. Wiley EO, Mayden RL (2000) The evolutionary species concept. In: Wheeler QD, Meier R (eds) Species concepts and phylogenetic theory: a debate. Columbia University Press, New YorkGoogle Scholar
  172. Will KW, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 54(5):844–851PubMedCrossRefPubMedCentralGoogle Scholar
  173. Wink M (2019) A historical perspective of avian genomics. In: Kraus RHS (ed) Avian genomics in ecology and evolution. Springer, ChamGoogle Scholar
  174. Wolf JBW, Ellegren H (2017) Making sense of genomic islands of differentiation in light of speciation. Nat Rev Genet 18:87–100PubMedCrossRefPubMedCentralGoogle Scholar
  175. Wu C-I, Ting C-T (2004) Genes and speciation. Nat Rev Genet 5(2):114–122PubMedCrossRefPubMedCentralGoogle Scholar
  176. Zhen Y, Harrigan RJ, Ruegg KC, Anderson EC, Ng TC, Lao S, Lohmueller KE, Smith TB (2017) Genomic divergence across ecological gradients in the Central African rainforest songbird (Andropadus virens). Mol Ecol 26:4966–4977PubMedCrossRefPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Evolutionary BiologyUppsala UniversityUppsalaSweden

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