Partial Amniote Sex Chromosomal Linkage Homologies Shared on Snake W Sex Chromosomes Support the Ancestral Super-Sex Chromosome Evolution in Amniotes.

Worapong Singchat,Rebecca E O'Connor,Prateep Duengkae,Syed Farhan Ahmad,Darren K Griffin,Narongrit Muangmai,Kornsorn Srikulnath,Surin Peyachoknagul,Siwapech Sillapaprayoon

doi:10.3389/fgene.2020.00948

Abstract

Squamate reptile chromosome 2 (SR2) is thought to be an important remnant of an ancestral amniote super-sex chromosome, but a recent study showed that the Siamese cobra W sex chromosome is also a part of this larger ancestral chromosome. To confirm the existence of an ancestral amniote super-sex chromosome and understand the mechanisms of amniote sex chromosome evolution, chromosome maps of two snake species [Russell’s viper: Daboia russelii (DRU) and the common tiger snake: Notechis scutatus (NSC)] were constructed using bacterial artificial chromosomes (BACs) derived from chicken and zebra finch libraries containing amniote sex chromosomal linkages. Sixteen BACs were mapped on the W sex chromosome of DRU and/or NSC, suggesting that these BACs contained a common genomic region shared with the W sex chromosome of these snakes. Two of the sixteen BACs were co-localized to DRU2 and NSC2, corresponding to SR2. Prediction of genomic content from all BACs mapped on snake W sex chromosomes revealed a large proportion of long interspersed nuclear element (LINE) and short interspersed nuclear element (SINE) retrotransposons. These results led us to predict that amplification of LINE and SINE may have occurred on snake W chromosomes during evolution. Genome compartmentalization, such as transposon amplification, might be the key factor influencing chromosome structure and differentiation. Multiple sequence alignments of all BACs mapped on snake W sex chromosomes did not reveal common sequences. Our findings indicate that the SR2 and snake W sex chromosomes may have been part of a larger ancestral amniote super-sex chromosome, and support the view of sex chromosome evolution as a colorful myriad of situations and trajectories in which many diverse processes are in action.

Highlights

Observations suggest that the common ancestor of snakes and birds lived about 260 million years ago, with gross chromosome morphology diverging soon after (Smith and Sinclair, 2004; Vallender and Lahn, 2006)
We examined more than 20 DAPI-stained metaphase spreads for one female Russell’s viper (DRU) and one female Tiger
Chicken and zebra finch bacterial artificial chromosomes (BACs) located on GGA1, GGA2p, GGA4p, GGA5, GGA6, GGA9, GGA13, GGA15, GGA17, GGA23, GGA27, GGA28, and GGAZ were mapped to Daboia russelii (DRU) and Notechis scutatus (NSC) (9 chicken BACs and 10 zebra finch BACs) (Figures 2,3 and Table 1)

Summary

Introduction

Observations suggest that the common ancestor of snakes and birds lived about 260 million years ago, with gross chromosome morphology diverging soon after (Smith and Sinclair, 2004; Vallender and Lahn, 2006). To understand the phenomenon of unrelated sex chromosomal linkages, those of snakes, a number of molecular resources for comparative genomic analyses have been developed for the Siamese cobra (Naja kaouthia) These include sex-linked markers, a bacterial artificial chromosome (BAC) chromosome map, and genome-wide single nucleotide polymorphic analysis (Singchat et al, 2018, 2020; Laopichienpong et al, submitted data). These findings suggest that in addition to squamate reptile chromosome 2 (SR2), the Siamese cobra W sex chromosomes share partial sex chromosomal linkage homologies with sex-related elements of other amniotes, despite their apparent diversity of sex determining mechanisms (Ezaz et al, 2017; Singchat et al, 2018, 2020; Matsubara et al, 2019; Ahmad et al, 2020)

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Results

Conclusion