Variation and constraints in hybrid genome formation

Abstract

Hybridization is an important source of variation; it transfers adaptive genetic variation across species boundaries and generates new species. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve by sequencing the genomes of four island populations of the homoploid hybrid Italian sparrow Passer italiae. We report that a variety of novel and fully functional hybrid genomic combinations are likely to have arisen independently on Crete, Corsica, Sicily and Malta, with differentiation in candidate genes for beak shape and plumage colour. However, certain genomic regions are invariably inherited from the same parent species, limiting variation. These regions are over-represented on the Z chromosome and harbour candidate incompatibility loci, including DNA-repair and mitonuclear genes. These gene classes may contribute to the general reduction of introgression on sex chromosomes. This study demonstrates that hybrid genomes may vary, and identifies new candidate reproductive isolation genes.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Population structuring of the focal taxa.
Fig. 2: Local adaptation, private variation and strong selection on the Z chromosome.
Fig. 3: Parental similarity across the Z chromosome.

References

  1. 1.

    Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237 (2005).

    Article  PubMed  Google Scholar 

  2. 2.

    Abbott, R. et al. Hybridization and speciation. J. Evol. Biol. 26, 229–246 (2013).

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004).

    Article  PubMed  Google Scholar 

  4. 4.

    The Heliconius Genome Sequencing Consortium. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487, 94–98 (2012).

    Article  Google Scholar 

  5. 5.

    Rieseberg, L. H. Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301, 1211–1216 (2003).

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Sankararaman, S. et al. The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507, 354–357 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Fontaine, M. C. et al. Extensive introgression in a malaria vector species complex revealed by phylogenomics. Science 347, 1258524 (2015).

    Article  PubMed  Google Scholar 

  8. 8.

    Baack, E. J. & Rieseberg, L. H. A genomic view of introgression and hybrid speciation. Curr. Opin. Genet. Dev. 17, 513–518 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Trier, C. N., Hermansen, J. S., Sætre, G.-P. & Bailey, R. I. Evidence for mito-nuclear and sex-linked reproductive barriers between the hybrid Italian sparrow and its parent species. PLoS Genet. 10, e1004075 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Martin, S. H. et al. Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res. 23, 1817–1828 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Qvarnström, A. & Bailey, R. I. Speciation through evolution of sex-linked genes. Heredity 102, 4–15 (2008).

    Article  PubMed  Google Scholar 

  12. 12.

    Hermansen, J. S. et al. Hybrid speciation in sparrows I: phenotypic intermediacy, genetic admixture and barriers to gene flow. Mol. Ecol. 20, 3812–3822 (2011).

    Article  PubMed  Google Scholar 

  13. 13.

    Elgvin, T. O. et al. The genomic mosaicism of hybrid speciation. Sci. Adv. 3, 1–15 (2017).

    Article  Google Scholar 

  14. 14.

    Hermansen, J. S. et al. Hybrid speciation through sorting of parental incompatibilities in Italian sparrows. Mol. Ecol. 23, 5831–5842 (2014).

    Article  PubMed  Google Scholar 

  15. 15.

    Saetre, G. P. et al. Single origin of human commensalism in the house sparrow. J. Evol. Biol. 25, 788–796 (2012).

    Article  PubMed  Google Scholar 

  16. 16.

    Bache-Mathiesen, L. The Evolutionary Potential of Male Plumage Color in a Hybrid Sparrow Species. MSc thesis, University of Oslo (2015); https://www.duo.uio.no/handle/10852/45473

  17. 17.

    Meier, J. I. et al. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nat. Commun. 8, 1–11 (2017).

    Article  Google Scholar 

  18. 18.

    Burri, R. et al. Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Res. 25, 1656–1665 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Hill, W. G. & Robertson, A. The effect of linkage on limits to artificial selection. Genet. Res. 8, 269–294 (1966).

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Laine, V. N. et al. Evolutionary signals of selection on cognition from the great tit genome and methylome. Nat. Commun. 7, 1–9 (2016).

    Article  Google Scholar 

  21. 21.

    Lamichhaney, S. et al. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518, 371–375 (2015).

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Eroukhmanoff, F., Hermansen, J. S., Bailey, R. I., Sæther, S. A. & Sætre, G.-P. S. Local adaptation within a hybrid species. Heredity 111, 286–292 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Noramly, S., Freeman, A. & Morgan, B. A. Beta-catenin signaling can initiate feather bud development. Development 126, 3509–3521 (1999).

    CAS  PubMed  Google Scholar 

  24. 24.

    Guo, H. et al Wnt/beta-catenin signaling pathway activates melanocyte stem cells in vitro and in vivo. J. Dermatol. Sci. 83, 45–51 (2016).

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Mank, J. E., Nam, K. & Ellegren, H. Faster-Z evolution is predominantly due to genetic drift. Mol. Biol. Evol. 27, 661–670 (2010).

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Charlesworth, B., Coyne, J. A. & Barton, N. H. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130, 113–146 (2016).

    Article  Google Scholar 

  28. 28.

    Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B 355, 1563–1572 (2000).

    CAS  Article  Google Scholar 

  29. 29.

    Poelstra, J. W., Vijay, N., Hoeppner, M. P. & Wolf, J. B. W. Transcriptomics of colour patterning and coloration shifts in crows. Mol. Ecol. 24, 4617–4628 (2015).

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Tomarev, S. I. & Nakaya, N. Olfactomedin domain-containing proteins: possible mechanisms of action and functions in normal development and pathology. Mol. Neurobiol. 40, 122–138 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    David, W. M., Mitchell, D. L. & Walter, R. B. DNA repair in hybrid fish of the genus Xiphophorus. Comp. Biochem. Physiol. C. 138, 301–309 (2004).

    Google Scholar 

  32. 32.

    Greig, D., Travisano, M., Louis, E. J. & Borts, R. H. A role for the mismatch repair system during incipient speciation in Saccharomyces. J. Evol. Biol. 16, 429–437 (2003).

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Schumer, M. & Brandvain, Y. Determining epistatic selection in admixed populations. Mol. Ecol. 25, 2577–2591 (2016).

    Article  PubMed  Google Scholar 

  34. 34.

    Barton, N. H. The role of hybridization in evolution. Mol. Ecol. 10, 551–568 (2001).

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    McKenna, A. et al The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Van der Auwera, G. A. et al. From FastQ data to high-confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr. Protoc. Bioinforma. 11, 1–33 (2013).

    Google Scholar 

  39. 39.

    Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: Analysis of Next Generation Sequencing Data. BMC Bioinforma. 15, 356 (2014).

    Article  Google Scholar 

  41. 41.

    Fumagalli, M., Vieira, F. G., Linderoth, T. & Nielsen, R. ngsTools: methods for population genetics analyses from next-generation sequencing data. Bioinformatics 30, 1486–1487 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Fumagalli, M. et al. Quantifying population genetic differentiation from next-generation sequencing data. Genetics 195, 979–992 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Martin, S. H., Davey, J. W. & Jiggins, C. D. Evaluating the use of ABBA–BABA statistics to locate introgressed loci. Mol. Biol. Evol. 32, 244–257 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Zamani, N. et al. Unsupervised genome-wide recognition of local relationship patterns. BMC Genom. 14, 1–11 (2013).

    Article  Google Scholar 

  47. 47.

    Bouckaert, R. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    O’Connell, J. et al. A general approach for haplotype phasing across the full spectrum of relatedness. PLoS Genet. 10, e1004234 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Bruen, T. C., Philippe, H. & Bryant, D. A simple and robust statistical test for detecting the presence of recombination. Genetics 172, 2665–2681 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Yule, U. G. A mathematical theory of evolution, based on the conclusions of Dr. J. C. Willis, F.R.S. Phil. Trans. R. Soc. Lond. B 213, 21–87 (1925).

    Article  Google Scholar 

  52. 52.

    Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710–722 (2010).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239–2252 (2011).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Matschiner, M. Fitchi: haplotype genealogy graphs based on the Fitch algorithm. Bioinformatics 32, 1250–1252 (2016).

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Burri, R. et al. Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Res. 25, 1656–1665 (2015).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Beissbarth, T. & Speed, T. P. GOstat: find statistically overrepresented gene ontologies within a group of genes. Bioinformatics 20, 1464–1465 (2004).

    CAS  Article  PubMed  Google Scholar 

  57. 57.

    Smith, A. C., Blackshaw, J. A. & Robinson, A. J. MitoMiner: a data warehouse for mitochondrial proteomics data. Nucleic Acids Res. 40, D1160–D1167 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Benjamini, Y. Simultaneous and selective inference: current successes and future challenges. Biom. J. 52, 708–721 (2010).

    Article  PubMed  Google Scholar 

  59. 59.

    Pfeifer, B., Wittelsbürger, U., Ramos-Onsins, S. E. & Lercher, M. J. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol. Biol. Evol. 31, 1929–1936 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank M. Tesaker and BirdLife Malta for help with field work, L. Piñeiro and L. Bache-Mathiesen for providing morphological data, and A. Nilsson for comments on the manuscript. This work was funded by a Swedish Research Council post doctoral grant and a Wenner-Gren Fellowship to A.R. and a Norwegian Science Foundation grant to G-P.S. and A.R.

Author information

Affiliations

Authors

Contributions

A.R. conceived the study, carried out field work and laboratory work, designed analyses, analysed data and wrote the manuscript. C.N.T. helped design analyses, and provided scripts, F.E. carried out field work and the gene ontology analyses, J.S.H. carried out field work and the final touches in figure preparation, M.M. performed the BEAST and Saguaro analyses and M.R. performed the recombination rate analyses and principal component analysis. T.O.E. provided the house sparrow reference genome, and G.P.S. identified the study system, designed the sampling strategy and carried out field work. All co-authors commented on the manuscript.

Corresponding author

Correspondence to Anna Runemark.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figures 1–10, Supplementary Tables 1–23

Life Sciences Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Runemark, A., Trier, C.N., Eroukhmanoff, F. et al. Variation and constraints in hybrid genome formation. Nat Ecol Evol 2, 549–556 (2018). https://doi.org/10.1038/s41559-017-0437-7

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing