Abstract

The caenophidian (assigned also as “advanced”) snakes are traditionally viewed as a group of reptiles with a limited karyotypic variation and stable ZZ/ZW sex chromosomes. The W chromosomes of the caenophidian snakes are heterochromatic, and pioneering studies demonstrated that they are rich in repetitive elements. However, a comparative study of the evolutionary dynamics of the repetitive content of the W chromosome across the whole lineage is missing. Using molecular-cytogenetic techniques, we explored the distribution of four repetitive motifs (microsatellites GATA, GACA, AG and telomeric-like sequences), which are frequently accumulated in differentiated sex chromosomes in vertebrates, in the genomes of 13 species of the caenophidian snakes covering a wide phylogenetic spectrum of the lineage. The results demonstrate a striking variability in the morphology and the repetitive content of the W chromosomes even between closely-related species, which is in contrast to the homology and long-term stability of the gene content of the caenophidian Z chromosome. We uncovered that the tested microsatellite motifs are accumulated on the degenerated, heterochromatic W chromosomes in all tested species of the caenophidian snakes with the exception of the Javan file snake representing a basal clade. On the other hand, the presence of the accumulation of the telomeric-like sequences on the caenophidian W chromosome is evolutionary much less stable. Moreover, we demonstrated that large accumulations of telomeric-like motifs on the W chromosome contribute to sexual differences in the number of copies of the telomeric and telomeric-like repeats estimated by quantitative PCR, which might be confusing and incorrectly interpreted as sexual differences in telomere length.

Highlights

  • Snakes represent around one third of all current species of squamate reptiles

  • It was speculated that the enormous difference in the diversification rates between non-caenophidian and caenophidian snakes can be attributed to the differences in the degree of differentiation of sex chromosomes [4]

  • We suggested that in snake evolution, the formation of the sex-specific heterochromatin preceded the emergence of GATA accumulations on the W chromosome, which would question the role of the banded krait minor-satellite DNA (Bkm) repeats in the origin of sex-specific heterochromatin even in snakes

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Summary

Introduction

Snakes represent around one third of all current species of squamate reptiles. The reasons for their unusual evolutionary success are not known. Not all snake groups are diversified; nearly 90% of snake species 3000 out of 3400) belong to the group Caenophidia (advanced snakes), to their subclade Colubroidea [1]. The key to understanding the evolutionary success of snakes is in uncovering the processes responsible for the superradiation of caenophidian/colubroid snakes in the last 80 million years (dating follows [2]). The colonization of new areas and the evolution of advanced venom-delivery systems were suggested to be responsible for the large diversity of caenophidian and colubroid snakes [3]. It was speculated that the enormous difference in the diversification rates between non-caenophidian and caenophidian snakes can be attributed to the differences in the degree of differentiation of sex chromosomes [4]

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