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

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 supersex 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.

Genome Complexity Reduction High-Throughput Genome Sequencing of Green Iguana (Iguana iguana) Reveal a Paradigm Shift in Understanding Sex-Chromosomal Linkages on Homomorphic X and Y Sex Chromosomes

“…Using comparative gene mapping (i.e., chromosome mapping by means of a cytogenetic technique) and whole-genome sequencing, genomic convergence has been detected in which unrelated sex chromosomes share syntenies across distantly related taxa (Voss et al, 2001;Matsuda et al, 2005;Matsubara et al, 2006Matsubara et al, , 2012Matsubara et al, , 2019Srikulnath et al, 2009aSrikulnath et al, ,b, 2013Srikulnath et al, , 2014Srikulnath et al, , 2015Alföldi et al, 2011;Pokorná et al, 2011;Ezaz et al, 2013Ezaz et al, , 2017Young et al, 2013;Gamble et al, 2017;Augstenová et al, 2018;Singchat et al, 2018Singchat et al, , 2020aIannucci et al, 2019;Lind et al, 2019;Ahmad et al, 2020). The ACAXspecific region contains genomic content orthologous to genes on GGA15 (Alföldi et al, 2011), which is homologous to the Z chromosome of the Chinese softshell turtle (Pelodiscus sinensis) and the spiny softshell turtle (Apalone spinifera) (Kawagoshi et al, 2009(Kawagoshi et al, , 2014.…”

“…The ACAXspecific region contains genomic content orthologous to genes on GGA15 (Alföldi et al, 2011), which is homologous to the Z chromosome of the Chinese softshell turtle (Pelodiscus sinensis) and the spiny softshell turtle (Apalone spinifera) (Kawagoshi et al, 2009(Kawagoshi et al, , 2014. This result led to the prediction of a hypothetical larger ancestral amniote super-sex chromosome with overlaps of partial linkage homology among sex chromosomes of amniotes, whereby multiple translocations have then resulted in the appearance of various sex chromosomes in amniotes (Ezaz et al, 2017;Singchat et al, 2018Singchat et al, , 2020aMatsubara et al, 2019;Srikulnath et al, 2019;Ahmad et al, 2020). In the present study, six out of 29 SNP/PA loci that were perfectly sexlinked with phenotypic sex assignment showed partial homology with a number of amniote sex chromosomes (GGA5, GGA18, GGA27, GGA28, and GGAZ) (International Chicken Genome Sequencing Consortium, 2004) (Supplementary Figure S4).…”

“…Interestingly, the cohybridization signals of the same sex-chromosomal linkage homology are also observed for different chromosomes, as seen in cDNA and bacterial artificial chromosome (BAC) chromosomal maps (Matsuda et al, 2005;Matsubara et al, 2006Matsubara et al, , 2012Matsubara et al, , 2019Srikulnath et al, 2009aSrikulnath et al, ,b, 2013Srikulnath et al, , 2014Srikulnath et al, , 2015Uno et al, 2012;Singchat et al, 2018Singchat et al, , 2020a. Patterns of FISH signals for the same BACs on multiple different chromosome pairs might result from the presence of common genomic elements (O'Meally et al, 2010;Ezaz et al, 2017;Singchat et al, 2018Singchat et al, , 2020aMatsubara et al, 2019). These findings suggest the possibility that chromosomal rearrangement, such as fission or translocation, might have occurred in an ancestral amniote super-sex chromosome, which has been evolutionarily conserved after divergence ∼320 million years ago (MYA) (Hedges and Vidal, 2009).…”

“…Comparison of genomewide single-nucleotide polymorphisms (SNPs) between males and females of the Siamese cobra revealed female-specific loci that also show partial homology with a variety of amniote sex chromosomes, including the ACA X-linked region as GGA15 (Laopichienpong et al, 2020), supporting the hypothesis that the Siamese cobra W sex chromosome is derived from a larger ancestral amniote super-sex chromosome. Interestingly, the cohybridization signals of the same sex-chromosomal linkage homology are also observed for different chromosomes, as seen in cDNA and bacterial artificial chromosome (BAC) chromosomal maps (Matsuda et al, 2005;Matsubara et al, 2006Matsubara et al, , 2012Matsubara et al, , 2019Srikulnath et al, 2009aSrikulnath et al, ,b, 2013Srikulnath et al, , 2014Srikulnath et al, , 2015Uno et al, 2012;Singchat et al, 2018Singchat et al, , 2020a. Patterns of FISH signals for the same BACs on multiple different chromosome pairs might result from the presence of common genomic elements (O'Meally et al, 2010;Ezaz et al, 2017;Singchat et al, 2018Singchat et al, , 2020aMatsubara et al, 2019).…”

“…Genome sequence analyses and cross-species chromosome mapping have, however, detected genomic convergence in which unrelated sex chromosomes share linkage homologies across distantly related lineages. This might involve genomic regions orthologous to squamate chromosome 2 (SR2) and snake W sex chromosomes (Matsubara et al, 2006(Matsubara et al, , 2012(Matsubara et al, , 2019Srikulnath et al, 2009aSrikulnath et al, ,b, 2013Srikulnath et al, , 2014Srikulnath et al, , 2015Alföldi et al, 2011;Pokorná et al, 2011;Uno et al, 2012;Matsuda et al, 2015;Ezaz et al, 2017;Singchat et al, 2018Singchat et al, , 2020a. Comparison of genomewide single-nucleotide polymorphisms (SNPs) between males and females of the Siamese cobra revealed female-specific loci that also show partial homology with a variety of amniote sex chromosomes, including the ACA X-linked region as GGA15 (Laopichienpong et al, 2020), supporting the hypothesis that the Siamese cobra W sex chromosome is derived from a larger ancestral amniote super-sex chromosome.…”