Advertisement

Molecular Genetics and Genomics

, Volume 291, Issue 5, pp 1955–1966 | Cite as

Evolutionary dynamics of Anolis sex chromosomes revealed by sequencing of flow sorting-derived microchromosome-specific DNA

  • Ilya G. KichiginEmail author
  • Massimo Giovannotti
  • Alex I. Makunin
  • Bee L. Ng
  • Marsel R. Kabilov
  • Alexey E. Tupikin
  • Vincenzo Caputo Barucchi
  • Andrea Splendiani
  • Paolo Ruggeri
  • Willem Rens
  • Patricia C. M. O’Brien
  • Malcolm A. Ferguson-Smith
  • Alexander S. Graphodatsky
  • Vladimir A. Trifonov
Original Article

Abstract

Squamate reptiles show a striking diversity in modes of sex determination, including both genetic (XY or ZW) and temperature-dependent sex determination systems. The genomes of only a handful of species have been sequenced, analyzed and assembled including the genome of Anolis carolinensis. Despite a high genome coverage, only macrochromosomes of A. carolinensis were assembled whereas the content of most microchromosomes remained unclear. Most of the Anolis species have homomorphic XY sex chromosome system. However, some species have large heteromorphic XY chromosomes (e.g., A. sagrei) and even multiple sex chromosomes systems (e.g. A. pogus), that were shown to be derived from fusions of the ancestral XY with microautosomes. We applied next generation sequencing of flow sorting-derived chromosome-specific DNA pools to characterize the content and composition of microchromosomes in A. carolinensis and A. sagrei. Comparative analysis of sequenced chromosome-specific DNA pools revealed that the A. sagrei XY sex chromosomes contain regions homologous to several microautosomes of A. carolinensis. We suggest that the sex chromosomes of A. sagrei are derived by fusions of the ancestral sex chromosome with three microautosomes and subsequent loss of some genetic content on the Y chromosome.

Keywords

XY sex chromosomes Sex determining (SD) genes Squamata Reptilia 

Notes

Compliance with ethical standards

Funding

The work was supported by the Budget Projects 0310-2014-0003, 0310-2014-0008, 0310-2014-0009 provided to Vladimir A. Trifonov, partly by RSF Grant No. 16-14-10009 provided to A. Graphodatsky, and by the funds provided by Ministry of Education, University and Research (Italy) (“Ricerche di citogenetica molecolare sui sistemi di determinazione del sesso nei rettili squamati, sottordine Sauria”; Grant number: PRIN2009/20093HYH97) to Vincenzo Caputo Barucchi.

Conflict of interest

The authors declare they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

438_2016_1230_MOESM1_ESM.xls (82 kb)
Supplementary material 1 (XLS 81 kb)
438_2016_1230_MOESM2_ESM.xls (74 kb)
Supplementary material 2 (XLS 74 kb)
438_2016_1230_MOESM3_ESM.docx (14 kb)
Supplementary material 3 (DOCX 13 kb)

References

  1. Alföldi J, Di Palma F, Grabherr M et al (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477:587–591CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bertolotto CEV, Rodrigues MT, Yonenaga-Yassuda Y (2001) Banding patterns, multiple sex chromosome system and localization of telomeric (TTAGGG)n sequences by FISH on two species of Polychrus (Squamata, Polychrotidae). Caryologia 54:217–226CrossRefGoogle Scholar
  3. Brinkrolf K, Rupp O, Laux H et al (2013) Chinese hamster genome sequenced from sorted chromosomes. Nat Biotechnol 31:694–695CrossRefPubMedGoogle Scholar
  4. Crawford PA, Dorn C, Sadovsky Y, Milbrandt J (1998) Nuclear receptor DAX-1 recruits nuclear receptor corepressor N-CoR to steroidogenic factor 1. Mol Cell Biol 18:2949–2956CrossRefPubMedPubMedCentralGoogle Scholar
  5. De Smet W (1981) Description of the orcein stained karyotypes of 27 lizard species (Lacertilia Reptilia) belonging to the families Iguanidae, Agamidae, Chamaeleontidae and Gekkonidae (Ascalabota). Acta Zool Pathol Antwerp 76:35–72Google Scholar
  6. Eggers S, Sinclair A (2012) Mammalian sex determination—insights from humans and mice. Chromosome Res 20:215–238CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ellegren H (2011) Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nat Rev Genet 12:157–166CrossRefPubMedGoogle Scholar
  8. Etheridge R (1960) The relationships of the anoles (Reptilia: Sauria: Iguanidae): an interpretation based on skeletal morphology. PhD Dissertation, University of MichiganGoogle Scholar
  9. Ezaz T, Graves JAM (2012) Foreword: sex and sex chromosomes—new clues from nonmodel species. Chromosome Res 20:1–5CrossRefPubMedGoogle Scholar
  10. Ezaz T, Sarre SD, O’Meally D et al (2009) Sex chromosome evolution in lizards: independent origins and rapid transitions. Cytogenet Genome Res 127:249–260CrossRefPubMedGoogle Scholar
  11. Gamble T, Geneva AJ, Glor RE, Zarkower D (2014) Anolis sex chromosomes are derived from a single ancestral pair. Evolution 68:1027–1041CrossRefPubMedGoogle Scholar
  12. Giovannotti M, Trifonov V, Paoletti A et al (2016) New insights into sex chromosome evolution in anole lizards (Reptilia, Dactyloidae). Chromosoma. doi: 10.1007/s00412-016-0585-6
  13. Gorman GC (1973) The chromosomes of the reptilia, a cytotaxonomic interpretation. Cytotaxon Vertebr Evol:349–424Google Scholar
  14. Gorman G, Atkins L (1967) The zoogeography of lesser Antillean Anolis lizards—an analysis based upon chromosomes and lactic dehydrogenases. Bull Mus Comp Zool 138:53–80Google Scholar
  15. Graves JAM (2006) Sex chromosome specialization and degeneration in mammals. Cell 124:901–914CrossRefPubMedGoogle Scholar
  16. Graves JAM (2013) How to evolve new vertebrate sex determining genes. Dev Dyn 242:354–359CrossRefPubMedGoogle Scholar
  17. Graves JAM, Peichel CL (2010) Are homologies in vertebrate sex determination due to shared ancestry or to limited options? Genome Biol 11:205CrossRefGoogle Scholar
  18. Gruetzner F, Ashley T, Rowell DM, Graves JAM (2005) How did the platypus get its sex chromosome chain? A comparison of meiotic multiples and sex chromosomes in plants and animals. Chromosoma 115:75–88CrossRefPubMedGoogle Scholar
  19. Hedges SB, Poling LL (1999) A molecular phylogeny of reptiles. Science 283:998–1001CrossRefPubMedGoogle Scholar
  20. Janzen FJ, Phillips PC (2006) Exploring the evolution of environmental sex determination, especially in reptiles. J Evol Biol 19:1775–1784CrossRefPubMedGoogle Scholar
  21. Kawagoshi T, Uno Y, Matsubara K et al (2009) The ZW micro-sex chromosomes of the chinese soft-shelled turtle (Pelodiscus sinensis, Trionychidae, Testudines) have the same origin as chicken chromosome 15. Cytogenet Genome Res 125:125–131CrossRefPubMedGoogle Scholar
  22. Kikuchi K, Hamaguchi S (2013) Novel sex-determining genes in fish and sex chromosome evolution. Dev Dyn 242:339–353CrossRefPubMedGoogle Scholar
  23. Kitano J, Peichel CL (2011) Turnover of sex chromosomes and speciation in fishes. Environ Biol Fishes 94:549–558CrossRefPubMedPubMedCentralGoogle Scholar
  24. Kitano J, Ross JA, Mori S et al (2009) A role for a neo-sex chromosome in stickleback speciation. Nature 461:1079–1083CrossRefPubMedPubMedCentralGoogle Scholar
  25. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359CrossRefPubMedPubMedCentralGoogle Scholar
  26. Losos JB (2009) Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. University of California Press, CaliforniaGoogle Scholar
  27. Makunin A, Kichigin I, Larkin D et al (2016) Contrasting origin of B chromosomes in two cervids (Siberian roe deer and grey brocket deer) unravelled by chromosome-specific DNA sequencing. BMC Genomics (in press)Google Scholar
  28. Mank JE, Vicoso B, Berlin S, Charlesworth B (2010) Effective population size and the faster-X effect: empirical results and their interpretation. Evolution 64:663–674CrossRefPubMedGoogle Scholar
  29. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12CrossRefGoogle Scholar
  30. Matsubara K, Tarui H, Toriba M (2006) Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci 103:18190–18195. doi: 10.1073/pnas.0605274103 CrossRefPubMedPubMedCentralGoogle Scholar
  31. McKenna A, Hanna M, Banks E et al (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303CrossRefPubMedPubMedCentralGoogle Scholar
  32. Nicholson K, Crother B, Guyer C, Savage J (2012) It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa 3477:1–108Google Scholar
  33. O’Meally D, Ezaz T, Georges A et al (2012) Are some chromosomes particularly good at sex? Insights from amniotes. Chromosome Res 20:7–19CrossRefPubMedGoogle Scholar
  34. Poe S (2013) 1986 Redux: new genera of anoles (Squamata: Dactyloidae) are unwarranted. Zootaxa 3626(2):295–299CrossRefPubMedGoogle Scholar
  35. Presgraves DC (2008) Sex chromosomes and speciation in Drosophila. Trends Genet 24:336–343CrossRefPubMedPubMedCentralGoogle Scholar
  36. Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842CrossRefPubMedPubMedCentralGoogle Scholar
  37. Quinn AE, Georges A, Sarre SD et al (2007) Temperature sex reversal implies sex gene dosage in a reptile. Science 316:411CrossRefPubMedGoogle Scholar
  38. Quinn AE, Sarre SD, Ezaz T et al (2011) Evolutionary transitions between mechanisms of sex determination in vertebrates. Biol Lett 7:443–448CrossRefPubMedPubMedCentralGoogle Scholar
  39. Qvarnström A, Bailey RI (2008) Speciation through evolution of sex-linked genes. Heredity 102:4–15CrossRefPubMedGoogle Scholar
  40. Rovatsos M, Altmanová M, Pokorná M, Kratochvíl L (2014a) Conserved sex chromosomes across adaptively radiated anolis lizards. Evolution 68:2079–2085CrossRefPubMedGoogle Scholar
  41. Rovatsos M, Pokorná M, Altmanová M, Kratochvíl L (2014b) Cretaceous park of sex determination: sex chromosomes are conserved across iguanas. Biol Lett 10:20131093CrossRefPubMedPubMedCentralGoogle Scholar
  42. Sarre SD, Ezaz T, Georges A (2011) Transitions between sex-determining systems in reptiles and amphibians. Annu Rev Genom Hum Genet 12:391–406CrossRefGoogle Scholar
  43. Smith CA, Roeszler KN, Ohnesorg T et al (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267–271CrossRefPubMedGoogle Scholar
  44. Solari AJ, Rahn MI (2005) Fine structure and meiotic behaviour of the male multiple sex chromosomes in the genus Alouatta. Cytogenet Genome Res 108:262–267CrossRefPubMedGoogle Scholar
  45. Swain A, Lovell-Badge R (1999) Mammalian sex determination: a molecular drama. Genes Dev 13:755–767CrossRefPubMedGoogle Scholar
  46. Telenius H, Carter NP, Bebb CE et al (1992) Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer. Genomics 13:718–725CrossRefPubMedGoogle Scholar
  47. Veyrunes F, Waters PD, Miethke P et al (2008) Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res 18:965–973CrossRefPubMedPubMedCentralGoogle Scholar
  48. Vicoso B, Bachtrog D (2013) Reversal of an ancient sex chromosome to an autosome in Drosophila. Nature 499:332–335CrossRefPubMedPubMedCentralGoogle Scholar
  49. Webster TP, Hall WP, Williams EE (1972) Fission in the evolution of a lizard karyotype. Science 177:611–613CrossRefPubMedGoogle Scholar
  50. Yang F, Trifonov V, Ng BL et al (2009) generation of paint probes by flow-sorted and microdissected chromosomes. In: Liehr T (ed) Fluorescence in situ hybridization (FISH)—application guide. Springer, Berlin, pp 35–52CrossRefGoogle Scholar
  51. Zatloukalová P, Hřibová E, Kubaláková M et al (2011) Integration of genetic and physical maps of the chickpea (Cicer arietinum L.) genome using flow-sorted chromosomes. Chromosome Res 19:729–739CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ilya G. Kichigin
    • 1
    Email author
  • Massimo Giovannotti
    • 2
  • Alex I. Makunin
    • 1
  • Bee L. Ng
    • 3
  • Marsel R. Kabilov
    • 4
  • Alexey E. Tupikin
    • 4
  • Vincenzo Caputo Barucchi
    • 2
    • 5
  • Andrea Splendiani
    • 2
  • Paolo Ruggeri
    • 2
  • Willem Rens
    • 6
  • Patricia C. M. O’Brien
    • 6
  • Malcolm A. Ferguson-Smith
    • 6
  • Alexander S. Graphodatsky
    • 1
    • 7
  • Vladimir A. Trifonov
    • 1
    • 7
  1. 1.Institute of Molecular and Cellular Biology SB RASNovosibirskRussia
  2. 2.Dipartimento di Scienze della Vita e dell’AmbienteUniversità Politecnica delle MarcheAnconaItaly
  3. 3.Cytometry Core FacilityThe Wellcome Trust Sanger InstituteCambridgeUK
  4. 4.Institute of Chemical Biology and Fundamental Medicine SB RASNovosibirskRussia
  5. 5.Consiglio Nazionale delle RicercheIstituto di Scienze Marine Sezione Pesca MarittimaAnconaItaly
  6. 6.Cambridge Resource Centre for Comparative Genomics, Department of Veterinary MedicineUniversity of CambridgeCambridgeUK
  7. 7.Novosibirsk State UniversityNovosibirskRussia

Personalised recommendations