Evolutionary Strata on the Chicken Z Chromosome: Implications for Sex Chromosome Evolution

Corresponding author: Hans Ellegren, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden. E-mail hans.ellegren@ebc.uu.se

Communicating editor: N. A. JENKINS

The human X chromosome exhibits four "evolutionary strata," interpreted to represent distinct steps in the process whereby recombination became arrested between the proto X and proto Y. To test if this is a general feature of sex chromosome evolution, we studied the Z-W sex chromosomes of birds, which have female rather than male heterogamety and evolved from a different autosome pair than the mammalian X and Y. Here we analyze all five known gametologous Z-W gene pairs to investigate the "strata" hypothesis in birds. Comparisons of the rates of synonymous substitution and intronic divergence between Z and W gametologs reveal the presence of at least two evolutionary strata spread over the p and q arms of the chicken Z chromosome. A phylogenetic analysis of intronic sequence data from different avian lineages indicates that Z-W recombination ceased in the oldest stratum (on Zq; CHD1Z, HINTZ, and SPINZ) 102–170 million years ago (MYA), before the split of the Neoaves and Eoaves. However, recombination continued in the second stratum (on Zp; UBAP2Z and ATP5A1Z) until after the divergence of extant avian orders, with Z and W diverging 58–85 MYA. Our data suggest that progressive and stepwise cessation of recombination is a general feature behind sex chromosome evolution.

This article has been cited by other articles:

				K. Nam and H. Ellegren The Chicken (Gallus gallus) Z Chromosome Contains at Least Three Nonlinear Evolutionary Strata Genetics, October 1, 2008; 180(2): 1131 - 1136. [Abstract] [Full Text] [PDF]

				D. Bachtrog The Temporal Dynamics of Processes Underlying Y Chromosome Degeneration Genetics, July 1, 2008; 179(3): 1513 - 1525. [Abstract] [Full Text] [PDF]

				J. W. Thomas, M. Caceres, J. J. Lowman, C. B. Morehouse, M. E. Short, E. L. Baldwin, D. L. Maney, and C. L. Martin The Chromosomal Polymorphism Linked to Variation in Social Behavior in the White-Throated Sparrow (Zonotrichia albicollis) Is a Complex Rearrangement and Suppressor of Recombination Genetics, July 1, 2008; 179(3): 1455 - 1468. [Abstract] [Full Text] [PDF]

				T. Giraud, R. Yockteng, M. Lopez-Villavicencio, G. Refregier, and M. E. Hood Mating System of the Anther Smut Fungus Microbotryum violaceum: Selfing under Heterothallism Eukaryot. Cell, May 1, 2008; 7(5): 765 - 775. [Full Text] [PDF]

				G. Abrusan, H.-J. Krambeck, T. Junier, J. Giordano, and P. E. Warburton Biased Distributions and Decay of Long Interspersed Nuclear Elements in the Chicken Genome Genetics, January 1, 2008; 178(1): 573 - 581. [Abstract] [Full Text] [PDF]

				J. J. Smith and S. R. Voss Bird and Mammal Sex-Chromosome Orthologs Map to the Same Autosomal Region in a Salamander (Ambystoma) Genetics, September 1, 2007; 177(1): 607 - 613. [Abstract] [Full Text] [PDF]

				Z. Granevitze, S. Blum, H. Cheng, A. Vignal, M. Morisson, G. Ben-Ari, L. David, M. W. Feldman, S. Weigend, and J. Hillel Female-Specific DNA Sequences in the Chicken Genome J. Hered., May 1, 2007; 98(3): 238 - 242. [Abstract] [Full Text] [PDF]

				R. Bergero, A. Forrest, E. Kamau, and D. Charlesworth Evolutionary Strata on the X Chromosomes of the Dioecious Plant Silene latifolia: Evidence From New Sex-Linked Genes Genetics, April 1, 2007; 175(4): 1945 - 1954. [Abstract] [Full Text] [PDF]

				K. Matsubara, H. Tarui, M. Toriba, K. Yamada, C. Nishida-Umehara, K. Agata, and Y. Matsuda From the Cover: Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes PNAS, November 28, 2006; 103(48): 18190 - 18195. [Abstract] [Full Text] [PDF]

				D. A. Filatov Evolutionary History of Silene latifolia Sex Chromosomes Revealed by Genetic Mapping of Four Genes Genetics, June 1, 2005; 170(2): 975 - 979. [Abstract] [Full Text] [PDF]