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Chromosomal inversion differences correlate with range overlap in passerine birds

Nature Ecology & Evolutionvolume 1pages15261534 (2017) | Download Citation


Chromosomal inversions evolve frequently but the reasons for this remain unclear. We used cytological descriptions of 411 species of passerine birds to identify large pericentric inversion differences between species, based on the position of the centromere. Within 81 small clades comprising 284 of the species, we found 319 differences on the 9 largest autosomes combined, 56 on the Z chromosome, and 55 on the W chromosome. We also identified inversions present within 32 species. Using a new fossil-calibrated phylogeny, we examined the phylogenetic, demographic and genomic context in which these inversions have evolved. The number of inversion differences between closely related species is consistently predicted by whether the ranges of species overlap, even when time is controlled for as far as is possible. Fixation rates vary across the autosomes, but inversions are more likely to be fixed on the Z chromosome than the average autosome. Variable mutagenic input alone (estimated by chromosome size, map length, GC content or repeat density) cannot explain the differences between chromosomes in the number of inversions fixed. Together, these results support a model in which inversions increase because of their effects on recombination suppression in the face of hybridization. Other factors associated with hybridization may also contribute, including the possibility that inversions contain incompatibility alleles, making taxa less likely to collapse following secondary contact.

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  1. 1.

    Hoffmann, A. A. & Rieseberg, L. H. Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu. Rev. Ecol. Evol. Syst. 39, 21–42 (2008).

  2. 2.

    Faria, R. & Navarro, A. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 25, 660–669 (2010).

  3. 3.

    Wilson, M. A. & Makova, K. D. Genomic analyses of sex chromosome evolution. Annu. Rev. Genom. Hum. Genet. 10, 333–354 (2009).

  4. 4.

    Wright, A. E., Harrison, P. W., Montgomery, S. H., Pointer, M. A. & Mank, J. E. Independent stratum formation on the avian sex chromosomes reveals inter-chromosomal gene conversion and predominance of purifying selection on the W chromosome. Evolution 68, 3281–3295 (2014).

  5. 5.

    Kunte, K. et al. Doublesex is a mimicry supergene. Nature 507, 229–232 (2014).

  6. 6.

    Küpper, C. et al. A supergene determines highly divergent male reproductive morphs in the ruff. Nat. Genet. 48, 79–83 (2015).

  7. 7.

    Lamichhaney, S. et al. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nat. Genet. 48, 84–88 (2016).

  8. 8.

    Tuttle, E. M. et al. Divergence and functional degradation of a sex chromosome-like supergene. Curr. Biol. 26, 344–350 (2016).

  9. 9.

    Lowry, D. B. & Willis, J. H. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol. 8, e1000500 (2010).

  10. 10.

    Jones, F. C. et al. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55–61 (2012).

  11. 11.

    Rieseberg, L. H. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351–358 (2001).

  12. 12.

    Noor, M. A., Grams, K. L., Bertucci, L. A. & Reiland, J. Chromosomal inversions and the reproductive isolation of species. Proc. Natl Acad. Sci. USA 98, 12084–12088 (2001).

  13. 13.

    Brown, K. M., Burk, L. M., Henagan, L. M. & Noor, M. A. F. A test of the chromosomal rearrangement model of speciation in Drosophila pseudoobscura. Evolution 58, 1856–1860 (2004).

  14. 14.

    Ayala, D., Guerrero, R. F. & Kirkpatrick, M. Reproductive isolation and local adaptation quantified for a chromosome inversion in a malaria mosquito. Evolution 67, 946–958 (2012).

  15. 15.

    Fishman, L., Stathos, A., Beardsley, P. M., Williams, C. F. & Hill, J. P. Chromosomal rearrangements and the genetics of reproductive barriers in Mimulus (monkey flowers). Evolution 67, 2547–2560 (2013).

  16. 16.

    King, M. Species Evolution: The Role Of Chromosome Change (Cambridge Univ. Press, Cambridge, 1993).

  17. 17.

    Lande, R. Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement. Evolution 33, 234–251 (1979).

  18. 18.

    Hedrick, P. W. The establishment of chromosomal variants. Evolution 35, 322–332 (1981).

  19. 19.

    Walsh, J. B. Rate of accumulation of reproductive isolation by chromosome rearrangements. Am. Nat. 120, 510–532 (1982).

  20. 20.

    Lande, R. The fixation of chromosomal rearrangements in a subdivided population with local extinction and colonization. Heredity 54, 323–332 (1985).

  21. 21.

    Hooper, D. M. & Price, T. D. Rates of karyotypic evolution in Estrildid finches differ between island and continental clades. Evolution 69, 890–903 (2015).

  22. 22.

    Puig, M., Caceres, M. & Ruiz, A. Silencing of a gene adjacent to the breakpoint of a widespread Drosophila inversion by a transposon-induced antisense RNA. Proc. Natl Acad. Sci. USA 101, 9013–9018 (2004).

  23. 23.

    White, M. Chain processes in chromosomal speciation. System. Zool. 27, 285–298 (1978).

  24. 24.

    Charlesworth, D. & Charlesworth, B. Selection on recombination in clines. Genetics 91, 581–589 (1979).

  25. 25.

    Kirkpatrick, M. & Barton, N. H. Chromosome inversions, local adaptation, and speciation. Genetics 173, 419–434 (2006).

  26. 26.

    Feder, J. L., Gejji, R., Powell, T. H. Q. & Nosil, P. Adaptive chromosomal divergence driven by mixed geographic mode of evolution. Evolution 65, 2157–2170 (2011).

  27. 27.

    Dagilis, A. J. & Kirkpatrick, M. Prezygotic isolation, mating preferences, and the evolution of chromosomal inversions. Evolution 70, 1465–1472 (2016).

  28. 28.

    Ohno, S. Sex Chromosomes And Sex-Linked Genes (Springer, Berlin, Heidelberg, 1967).

  29. 29.

    Charlesworth, B. The evolution of sex chromosomes. Science 251, 1030–1033 (1991).

  30. 30.

    Del Hoyo, J., Elliott, A. & Christie, A. D. Handbook of the Birds of the World Vols 8–16 (Lynx Edicions, Barcelona, 2003–2011).

  31. 31.

    Price, T. D. et al. Niche filling slows the diversification of Himalayan songbirds. Nature 509, 222–225 (2014).

  32. 32.

    Christidis, L. Animal Cytogenetics 4: Chordata 3 B: Aves (Gebrüder Borntraeger, Stuttgart, 1990).

  33. 33.

    Price, T. Speciation in Birds (Roberts, Greenwood Village, Colorado, 2008).

  34. 34.

    Aslam, M. L. et al. A SNP based linkage map of the turkey genome reveals multiple intrachromosomal rearrangements between the turkey and chicken genomes. BMC Genomics 11, 647 (2010).

  35. 35.

    Skinner, B. M. & Griffin, D. K. Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints. Heredity 108, 37–41 (2011).

  36. 36.

    Zhang, G. et al. Comparative genomics reveals insights into avian genome evolution and adaptation. Science 346, 1311–1320 (2014).

  37. 37.

    Kawakami, T. 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. 23, 4035–4058 (2014).

  38. 38.

    Singhal, S. et al. Stable recombination hotspots in birds. Science 350, 928–932 (2015).

  39. 39.

    Knief, U. et al. Fitness consequences of polymorphic inversions in the zebra finch genome. Genome Biol. 17, 199 (2016).

  40. 40.

    Claramunt, S. & Cracraft, J. A new time tree reveals Earth historys imprint on the evolution of modern birds. Sci. Adv. 1, e1501005 (2015).

  41. 41.

    Hudson, E. J. & Price, T. D. Pervasive reinforcement and the role of sexual selection in biological speciation. J. Hered. 105, 821–833 (2014).

  42. 42.

    Noor, M. A. F. How often does sympatry affect sexual isolation in Drosophila? Am. Nat. 149, 1156–1163 (1997).

  43. 43.

    McCarthy, E. M. Handbook of Avian Hybrids of the World (Oxford Univ. Press, Oxford, 2006).

  44. 44.

    Payseur, B. A. & Rieseberg, L. H. A genomic perspective on hybridization and speciation. Mol. Ecol. 25, 2337–2360 (2016).

  45. 45.

    Weir, J. T. & Price, T. D. Limits to speciation inferred from times to secondary sympatry and ages of hybridizing species along a latitudinal gradient. Am. Nat. 177, 462–469 (2011).

  46. 46.

    Price, T. D. & Bouvier, M. M. The evolution of F1 postzygotic incompatibilities in birds. Evolution 56, 2083–2089 (2002).

  47. 47.

    Navarro, A. & Barton, N. H. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57, 447–459 (2003).

  48. 48.

    Turelli, M. & Orr, H. A. Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154, 1663–1679 (2000).

  49. 49.

    Coyne, J. A. & Orr, H. A. Patterns of speciation in Drosophila. Evolution 43, 362–381 (1989).

  50. 50.

    Lande, R. Models of speciation by sexual selection on polygenic traits. Proc. Natl Acad. Sci. USA 78, 3721–3725 (1981).

  51. 51.

    Levan, A., Fredga, K. & Sandberg, A. A. Nomenclature for centromeric position on chromosomes. Hereditas 52, 201–220 (1964).

  52. 52.

    Krasikova, A., Daks, A., Zlotina, A. & Gaginskaya, E. Polymorphic heterochromatic segments in Japanese quail microchromosomes. Cytogenet. Genome Res. 126, 148–155 (2009).

  53. 53.

    Zlotina, A. et al. Centromere positions in chicken and Japanese quail chromosomes: de novo centromere formation versus pericentric inversions. Chromosome Res. 20, 1017–1032 (2012).

  54. 54.

    Rutkowska, J., Lagisz, M. & Nakagawa, S. The long and the short of avian W chromosomes: no evidence for gradual W shortening. Biol. Lett. 8, 636–638 (2012).

  55. 55.

    Marshall, O. J., Chueh, A. C., Wong, L. H. & Choo, K. H. A. Neocentromeres: new insights into centromere structure, disease development, and karyotype evolution. Am. J. Hum. Genet. 82, 261–282 (2008).

  56. 56.

    Ellegren, H. The evolutionary genomics of birds. Annu. Rev. Ecol. Evol. Syst. 44, 239–259 (2013).

  57. 57.

    Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

  58. 58.

    Posada, D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256 (2008).

  59. 59.

    Maddison, W. P. & Maddison, D. R. Mesquite: a modular system for evolutionary analysis. v. 2.75. (2011);

  60. 60.

    Pebesma, E. J. & Bivand, R. S. sp: classes and methods for spatial data. R package v. 0.9-44. (2016).

  61. 61.

    Schnute, J. T., Boers, N., Haigh, R. & Couture-Beil, A. PBSmapping: PBS Mapping 2.59. R package version. (2015);

  62. 62.

    Dunning, J. B. Handbook of Avian Body Masses (CRC, Boca Raton, Florida 1993).

  63. 63.

    Nevo, E., Beiles, A. & Ben-Shlomo, R. The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In Evolutionary Dynamics of Genetic Diversity. Lecture Notes in Biomathematics Vol. 53 (ed. Mani, G. S.) 13–213 (Springer, Berlin, Heidelberg, 1984).

  64. 64.

    Cole, C. T. Genetic variation in rare and common plants. Annu. Rev. Ecol. Evol. Syst. 34, 213–237 (2003).

  65. 65.

    Leffler, E. M. et al. Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol. 10, e1001388 (2012).

  66. 66.

    White, E. P., Ernest, S. K. M., Kerkhoff, A. J. & Enquist, B. J. Relationships between body size and abundance in ecology. Trends Ecol. Evol. 22, 323–330 (2007).

  67. 67.

    Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010).

  68. 68.

    Grafen, A. The phylogenetic regression. Phil. Trans. R. Soc. Lond. B–Biol. Sci. 326, 119–157 (1989).

  69. 69.

    Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & Team, R. C. nlme: Linear and nonlinear mixed effects models. R package v. 3.1-117. (2014);

  70. 70.

    Bartoń, K. MuMIn: multi-model inference. R package v. 1.5 (2013).

  71. 71.

    Martin, P. R., Montgomerie, R. & Lougheed, S. C. Color patterns of closely related bird species are more divergent at intermediate levels of breeding range sympatry. Am. Nat. 185, 443–451 (2015).

  72. 72.

    Baudat, F. & de Massy, B. Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosome Res. 15, 565–577 (2007).

  73. 73.

    De Massy, B. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu. Rev. Genet. 47, 563–599 (2013).

  74. 74.

    Ellegren, H. & Fridolfsson, A. K. Male-driven evolution of DNA sequences in birds. Nat. Genet. 17, 182–184 (1997).

  75. 75.

    Axelsson, E., Smith, N., Sundstrom, H., Berlin, S. & Ellegren, H. Male-biased mutation rate and divergence in autosomal, Z-linked and W-linked introns of chicken and turkey. Mol. Biol. Evol. 21, 1538–1547 (2004).

  76. 76.

    Smit, A. F., Hubley, R. & Green, P. RepeatMasker Open-3.0. (2010);

  77. 77.

    Warren, W. C. et al. The genome of a songbird. Nature 464, 757–762 (2010).

  78. 78.

    Backstrom, N. et al. The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res. 20, 485–495 (2010).

  79. 79.

    Poelstra, J. W. et al. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344, 1410–1414 (2014).

  80. 80.

    Dumont, B. L. & Payseur, B. A. Evolution of the genomic rate of recombination in mammals. Evolution 62, 276–294 (2008).

  81. 81.

    Dumont, B. L. & Payseur, B. A. Evolution of the genomic recombination rate in Murid rodents. Genetics 187, 643–657 (2011).

  82. 82.

    Smukowski, C. S. & Noor, M. A. F. Recombination rate variation in closely related species. Heredity 107, 496–508 (2011).

  83. 83.

    Yu, G., Smith, D. K., Zhu, H., Guan, Y. & Lam, T. T. Y. ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol. Evol.  8, 28–36 (2017).

  84. 84.

    Jenks, G. F. The data model concept in statistical mapping. Int. Yearbook Cartogr. 7, 186–190 (1967).

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We thank N. S. Bulatova, B. S. W. Chang, E. J. de Lucca, G. Semenov, P. Tang, I. M. Ventura, Y. Wu and the University of Chicago Library for their help in accessing cytological studies not available online; S. G. Dubay, K. Supriya and A. E. White for their assistance with statistical analyses and figure aesthetics; and A. Hipp, R. Hudson, M. Kronforst and M. Przeworski for their comments on the manuscript. Tissue materials for species without data on GenBank generously came from the Kansas University Biodiversity Institute and Natural History Museum (KU), the Field Museum of Natural History (FMNH) and the Australian National Wildlife Collection (ANWC). A. E. Johnson provided original artwork of the Chloris greenfinches used in Fig. 1.

Author information


  1. Committee on Evolutionary Biology, University of Chicago, Chicago, IL, 60637, USA

    • Daniel M. Hooper
    •  & Trevor D. Price
  2. Department of Ecology and Evolution, University of Chicago, Chicago, IL, 60637, USA

    • Trevor D. Price


  1. Search for Daniel M. Hooper in:

  2. Search for Trevor D. Price in:


D.M.H. collected the data, ran the analyses and wrote the manuscript, all with input from T.D.P. Supported in part by an NSF Doctoral Dissertation Improvement Grant (DDIG1601323) to T.D.P. and D.M.H.

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The authors declare no competing financial interests.

Corresponding author

Correspondence to Daniel M. Hooper.

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