Skip to main content
Log in

Diverse stages of sex-chromosome differentiation in tinamid birds: evidence from crossover analysis in Eudromia elegans and Crypturellus tataupa

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

All extant birds share the same sex-chromosome system: ZZ males and ZW females with striking differences in the stages of sex-chromosome differentiation between the primitive palaeognathus ratites and the large majority of avian species grouped within neognaths. Evolutionarily close to ratites is the neotropical order Tinamiformes that has been scarcely explored regarding their ZW pair morphology and constitution. Tinamous, when compared to ratites, constitute a large group among Palaeognathae, therefore, exploring the extent of homology between the Z and W chromosomes in this group might reveal key features on the evolution of the avian sex chromosomes. We mapped MLH1 foci that are crossover markers on pachytene bivalents to determine the size and localization of the homologous region shared by the Z and W chromosomes in two tinamous: Eudromia elegans and Crypturellus tataupa. We found that the homologous (pseudoautosomal) region differ significantly in size between these two species. They both have a single recombination event on the long arm of the acrocentric Z and W chromosomes. However, in E. elegans the pseudoautosomal region occupies one-fourth of the W chromosome, while in C. tataupa it is restricted to the tip of the long arm of the W. The W chromosomes in these two species differ in their heterochromatin content: in E. elegans it shows a terminal euchromatic segment and in C. tataupa is completely heterochromatic. These results show that tinamous have ZW pairs with more diversified stages of differentiation compared to ratites. Finally, the idea that the avian proto-sex chromosomes started to diverge from the end of the long arm towards the centromere of an acrocentric pair is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ansari HA, Takagi N, Sasaki M (1988) Morphological differentiation of sex chromosomes in three species of ratite birds. Cytogenet Cell Genet 47:185–188

    Article  Google Scholar 

  • Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24:94–102

    Article  PubMed  Google Scholar 

  • Calderón PL, Pigozzi MI (2006) Mlh1-focus mapping in birds shows equal recombination between sexes and diversity of crossover patterns. Chromosome Res 14:605–612

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Garnero A, Ledesma M, Gunski RJ (2006) Alta homeologia cariotípica na família Tinamidae (Aves: Tinamiformes). Rev Bras Ornitol 14:53–58

    Google Scholar 

  • Harshman J, Braun EL, Braun MJ, Huddleston CJ, Bowie RC, Chojnowski JL, Hackett SJ, Han KL, Kimball RT, Marks BD, Miglia KJ, Moore WS, Reddy S, Sheldon FH, Steadman DW, Steppan SJ, Witt CC, Yuri T (2008) Phylogenomic evidence for multiple losses of flight in ratite birds. Proc Natl Acad Sci 105:13462–13467

    Article  PubMed  CAS  Google Scholar 

  • Huxley TH (1867) On the classification of birds; and on the taxonomic value of the modifications of certain of the cranial bones observable in that class. Proc Zool Soc Lond 145:415–472

    Google Scholar 

  • Janes DE, Ezaz T, Graves JAM, Edwards SV (2009) Recombination and nucleotide diversity in the sex chromosomal pseudoautosomal region of the emu, Dromaius novaehollandiae. J Hered 100:125–136

    Article  PubMed  CAS  Google Scholar 

  • Lawson Handley L-J, Ceplitis H, Ellegren H (2004) Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution. Genetics 167:367–376

    Article  CAS  Google Scholar 

  • Livezey BC, Zusi RL (2007) Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zool J Linn Soc 149:1–95

    Article  PubMed  Google Scholar 

  • Mank JE, Ellegren H (2007) Parallel divergence and degradation of the avian W sex chromosome. Trends Ecol Evol 22:389–391

    Article  PubMed  Google Scholar 

  • Nam K, Ellegren H (2008) The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata. Genetics 180:1131–1136

    Article  PubMed  CAS  Google Scholar 

  • Nishida-Umehara C, Fujiwara A, Ogawa A, Mizuno S, Abe S, Yoshida MC (1999) Differentiation of Z and W chromosomes revealed by replication banding and FISH mapping of sexchromosome-linked DNA markers in the cassowary (Aves, Ratitae). Chromosome Res 7:635–640

    Article  PubMed  CAS  Google Scholar 

  • Ogawa A, Murata K, Mizuno S (1998) The location of Z- and W-linked marker genes and sequence on the homomorphic sex chromosomes of the ostrich and the emu. Proc Natl Acad Sci USA 95:4415–4418

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI (1999) Origin and evolution of the sex chromosomes in birds. Biocell 23:79–95

    PubMed  CAS  Google Scholar 

  • Pigozzi MI (2001) Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Cell Genet 95:129–133

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI (2007) Localization of single-copy sequences on chicken synaptonemal complex spreads using fluorescence in situ hybridization (FISH). Cytogenet Genome Res 119:105–112

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI (2008) Relationship between physical and genetic distances along the zebra finch Z chromosome. Chromosome Res 16:839–849

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (1997) Extreme axial equalization and wide distribution of recombination nodules in the primitive ZW pair of Rhea americana (Aves, Ratitae). Chromosome Res 5:421–428

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (1999) The ZW pairs of two paleognath birds from two orders show transitional stages of sex chromosome differentiation. Chromosome Res 7:541–551

    Article  PubMed  CAS  Google Scholar 

  • Pigozzi MI, Solari AJ (2005) Meiotic recombination in the ZW pair of a tinamid bird shows a differential pattern compared with neognaths. Genome 48:286–290

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Enderle E, Schindler D, Schemp W (1989) Chromosome banding and DNA replication patterns in bird karyotypes. Cytogenet Cell Genet 52:139–146

    Article  PubMed  CAS  Google Scholar 

  • Shetty S, Griffin DK, Graves JAM (1999) Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res 7:289–295

    Article  PubMed  CAS  Google Scholar 

  • Shetty S, Kirby P, Zarkower D, Graves JAM (2002) DMRT1 in a ratite bird: evidence for a role in sex determination and discovery of a putative regulatory element. Cytogenet Genome Res 99:245–251

    Article  PubMed  CAS  Google Scholar 

  • Sibley CG, Monroe BL Jr (1991) Distribution and taxonomy of birds of the world. Yale University Press, New Haven

    Google Scholar 

  • Solari AJ (1993) Sex chromosomes and sex determination in vertebrates. CRC Press, Boca Raton

    Google Scholar 

  • Solovei I, Gaginskaya ER, Hutchison N, MacGregor H (1993) Avian sex chromosomes in the lampbrush form: the ZW bivalents from six species of birds. Chromosome Res 1:153–166

    Article  PubMed  CAS  Google Scholar 

  • Takagi N, Itoh M, Sasaki M (1972) Chromosome studies in four species of Ratitae (Aves). Chromosoma 36:281–291

    Article  PubMed  CAS  Google Scholar 

  • Tsuda Y, Nishida-Umehara C, Ishijima J, Yamada K, Matsuda Y (2007) Comparison of the Z and W sex chromosomal architectures in elegant crested tinamou (Eudromia elegans) and ostrich (Struthio camelus) and the process of sex chromosome differentiation in palaeognathous birds. Chromosoma 116:159–173

    Article  PubMed  Google Scholar 

  • van Tuinen TM, Sibley CG, Hedges SB (2000) The early history of modern birds inferred from DNA sequences of nuclear and mitochondrial ribosomal genes. Mol Biol Evol 17:451–457

    PubMed  Google Scholar 

Download references

Acknowledgments

I am grateful to Julio Contreras and Yolanda Davies for their expertise in taxonomic identification of eggs and birds in the wild. This work was supported by grants from the University of Buenos Aires (UBACyT 429) and CONICET (PIP 124) to MIP.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María Inés Pigozzi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pigozzi, M.I. Diverse stages of sex-chromosome differentiation in tinamid birds: evidence from crossover analysis in Eudromia elegans and Crypturellus tataupa . Genetica 139, 771–777 (2011). https://doi.org/10.1007/s10709-011-9581-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-011-9581-1

Keywords

Navigation