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

Abstract

: 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.

Keywords: chromosomal rearrangements; evolution; genome; next-generation sequencing; repeat elements; sex determination.

Figure 1

Schematic diagram of different phases in ZW sex chromosome evolution. We propose a hypothetical evolutionary model to illustrate the origin and evolution of ZW sex chromosomes. First, owing to strong selection of an evolutionary hotspot region, an ancestral autosomal pair undergoes mutation to become a sex determination region, and transformation into homomorphic proto-sex chromosomes. This is followed by heteromorphic differentiation resulting in formation of a proto-W chromosome with cessation of recombination and gain of female beneficial sequences for fitness and adaptation. The proto-W chromosome subsequently undergoes structural changes, such as rearrangements, gene degradation, repeat accumulations, and heterochromatinization, to form a neo-ZW chromosome system with limited differentiation. In some cases, during this stage turnover cycles might convert the partially differentiated heteromorphic sex chromosomes into homomorphic sex chromosomes, as in certain snake species, such as Ptyas species. To achieve full heteromorphy the neo-ZW chromosomes escape this evolutionary trap, and the young W chromosome undergoes severe degeneration with lineage-specific sequence variation and evolves into a mature and stable sex chromosome.

Figure 2

Gene ontology (GO) enrichment of annotated genes on the W chromosome of Indian cobra. Clustering heatmap plot with log₁₀ (p-value) from functional enrichment tests and information content (IC). A higher log₁₀ (p-value) represents a more enriched function. The results show that W chromosomes carry an enriched set of genes associated with development, histone deacetylation, signaling, and transport.

Figure 3

Comparative genomic characterization of repeated DNA contents between the W and Z sex chromosomes. Repeat landscape of (a) W and (b) Z sex chromosomes. Histogram plots show the degree of sequence divergence of each transposable element (TE) derived from its consensus (X-axis) in relation to the percentage of its copies in the total genetic contents of the chromosome (Y-axis). Peaks represent waves of insertion (black arrows) of elements into the sex chromosome. Older insertions of TEs are shown as a peak wave on the right side (K-value > 25) of the plot, whereas younger elements are depicted on the left side (K-value < 25). Different colors show distinct element types, as described on the right. A higher abundance of LTRs (green) of the Z sex chromosome landscape as indicated by a green arrow, is evident. The Y-axis percentage difference and a recent wave of expansion on the Z chromosome are evident. (c) Comparative analysis of Z and W localized repeat contents. Each column represents the copy number percentage stacked for the repeated element. Different proportions for Z and W sex chromosomes are indicated in blue and red, respectively. Elements with higher proportions (in blue) show expansion; those TEs present exclusively on Z chromosomes, and absent on W chromosomes are highlighted in blue text on the X-axis.

Figure 4

(a) Phylogeny of 108 snake species, with available data for karyotypes and genome size, belonging to the families Boidae, Viperidae, Elapidae, and Colubridae. (b) Boxplots show the distribution of chromosome number and genome size (C-value) for the four families. Each dot represents the species as given in the phylogeny. The phylogenetic tree was sourced from TimeTree databases (http://www.timetree.org) [202] and shows each species with information on chromosome number (2n) and genome size variation. Data were sourced from the Animal Genome Size Database (http://www.genomesize.com) [203].