Snake W Sex Chromosome: The Shadow of Ancestral Amniote Super-Sex Chromosome

Heteromorphic sex chromosomes, particularly the ZZ/ZW sex chromosome system of birds and some reptiles, undergo evolutionary dynamics distinct from those of autosomes. The W sex chromosome is a unique karyological member of this heteromorphic pair, which has been extensively studied in snakes to explore the origin, evolution, and genetic diversity of amniote sex chromosomes. The snake W sex chromosome offers a fascinating model system to elucidate ancestral trajectories that have resulted in genetic divergence of amniote sex chromosomes. Although the principal mechanism driving evolution of the amniote sex chromosome remains obscure, an emerging hypothesis, supported by studies of W sex chromosomes of squamate reptiles and snakes, suggests that sex chromosomes share varied genomic blocks across several amniote lineages. This implies the possible split of an ancestral super-sex chromosome via chromosomal rearrangements. We review the major findings pertaining to sex chromosomal profiles in amniotes and discuss the evolution of an ancestral super-sex chromosome by collating recent evidence sourced mainly from the snake W sex chromosome analysis. We highlight the role of repeat-mediated sex chromosome conformation and present a genomic landscape of snake Z and W chromosomes, which reveals the relative abundance of major repeats, and identifies the expansion of certain transposable elements. The latest revolution in chromosomics, i.e., complete telomere-to-telomere assembly, offers mechanistic insights into the evolutionary origin of sex chromosomes

Data from: Evolutionary dynamics of the gametologous CTNNB1 gene on the Z and W chromosomes of snakes

Snakes exhibit genotypic sex determination with female heterogamety (ZZ males and ZW females), and the state of sex chromosome differentiation also varies among lineages. To investigate the evolutionary history of homologous genes located in the non-recombining region of differentiated sex chromosomes in snakes, partial sequences of the gametologous CTNNB1 gene were analyzed for 12 species belonging to henophid (Cylindrophiidae, Xenopeltidae, and Pythonidae) and caenophid snakes (Viperidae, Elapidae, and Colubridae). Nonsynonymous/synonymous substitution ratios (Ka/Ks) in coding sequences were low (Ka/Ks < 1) between CTNNB1Z and CTNNB1W, suggesting that these two genes may have similar functional properties. However, frequencies of intron sequence substitutions and insertion-deletions were higher in CTNNB1Z than CTNNB1W, suggesting that Z-linked sequences evolved faster than W-linked sequences. Molecular phylogeny based on both intron and exon sequences showed the presence of two major clades: (1) Z-linked sequences of Caenophidia, and (2) W-linked sequences of Caenophidia clustered with Z-linked sequences of Henophidia, which suggests that the sequence divergence between CTNNB1Z and CTNNB1W in Caenophidia may have occurred by the cessation of recombination after the split from Henophidia

Table_S6

Nucleotide sequence divergence (Kz) in intron10 and intron 11 of male-derived CTNNB1Z sequences among eight snake species (below diagonal), and female-derived CTNNB1Z sequences (above diagonal). Standard errors are indicated for all values. Table is also available in PDF format in the "Supplementary file" PD

Data from: Evolutionary dynamics of the gametologous CTNNB1 gene on the Z and W chromosomes of snakes

Snakes exhibit genotypic sex determination with female heterogamety (ZZ males and ZW females), and the state of sex chromosome differentiation also varies among lineages. To investigate the evolutionary history of homologous genes located in the non-recombining region of differentiated sex chromosomes in snakes, partial sequences of the gametologous CTNNB1 gene were analyzed for 12 species belonging to henophid (Cylindrophiidae, Xenopeltidae, and Pythonidae) and caenophid snakes (Viperidae, Elapidae, and Colubridae). Nonsynonymous/synonymous substitution ratios (Ka/Ks) in coding sequences were low (Ka/Ks < 1) between CTNNB1Z and CTNNB1W, suggesting that these two genes may have similar functional properties. However, frequencies of intron sequence substitutions and insertion-deletions were higher in CTNNB1Z than CTNNB1W, suggesting that Z-linked sequences evolved faster than W-linked sequences. Molecular phylogeny based on both intron and exon sequences showed the presence of two major clades: (1) Z-linked sequences of Caenophidia, and (2) W-linked sequences of Caenophidia clustered with Z-linked sequences of Henophidia, which suggests that the sequence divergence between CTNNB1Z and CTNNB1W in Caenophidia may have occurred by the cessation of recombination after the split from Henophidia

Table_S3

Frequencies of synonymous and nonsynonymous substitutions in the exon11 of male-derived CTNNB1Z sequences among eight snake species. Ks values are shown above the diagonal, and Ka values are shown below the diagonal. Standard errors are indicated in all values. Table is also available in PDF format in the "Supplementary file" PD

Snakes in this study

Snake samples (figure/species) used in this study

Table_S4

Frequencies of synonymous and nonsynonymous substitutions in the exon 11 of female-derived CTNNB1Z sequences among eight snake species. Ks values are shown above the diagonal, and Ka values are shown below the diagonal. Standard errors are indicated in all values. Table is also available in PDF format in the "Supplementary file" PD

Table_S5

Frequencies of nonsynonymous/synonymous substitution ratios (Ka/Ks) in exon 11 of the CTNNB1 gene among eight snake species. The CTNNB1W gene is shown above the diagonal with the CTNNB1Z gene below the diagonal. Table is also available in PDF format in the "Supplementary file" PD

Supplementary file

Supplementary file includes supplementary figures and tables, which are relevant to publication. Please note that the supplementary tables included in this PDF are also uploaded separately, as .xlsx files

Table_S2

Pair-wise comparison of amino acid sequence identities (%) of CTNNB1W among eight snake species. Table is also available in PDF format in the "Supplementary file" PD