Evolutionary Insights of the ZW Sex Chromosomes in Snakes: A New Chapter Added by the Amazonian Puffing Snakes of the Genus Spilotes

Abstract

Amazonian puffing snakes (Spilotes; Colubridae) are snakes widely distributed in the Neotropical region. However, chromosomal data are scarce in this group and, when available, are only limited to karyotype description using conventional staining. In this paper, we focused on the process of karyotype evolution and trends for sex chromosomes in two Amazonian Puffer Snakes (S. pulllatus and S. sulphureus). We performed an extensive karyotype characterization using conventional and molecular cytogenetic approaches. The karyotype of S. sulphureus (presented here for the first time) exhibits a 2n = 36, similar to that previously described in S. pullatus. Both species have highly differentiated ZZ/ZW sex chromosomes, where the W chromosome is highly heterochromatic in S. pullatus but euchromatic in S. sulphureus. Both W chromosomes are homologous between these species as revealed by cross-species comparative genomic hybridization, even with heterogeneous distributions of several repetitive sequences across their genomes, including on the Z and on the W chromosomes. Our study provides evidence that W chromosomes in these two species have shared ancestry.

Landscape of snake’ sex chromosomes evolution spanning 85 MYR reveals ancestry of sequences despite distinct evolutionary trajectories

“…In addition, two different classes of sequences, the PBI-MspI and EQU-BamHI-4 ( EQU-BamHI-4 being putatively reported as sex-linked 27 , 35 ) have been identified on the 4th homomorphic pair of Boa constrictor females, therefore, being identified as the sex pair in these studies 34 , 35 . Similarly, in most of the pit vipers, rattlesnakes and colubrids, the 4th chromosomal pair also represent the sex chromosomes 24 , 25 , 36 – 38 , even when homomorphic, as already identified through accumulation of Bkm repeats in some species 39 , 40 , suggesting a conserved trend for sex chromosome evolution in Snakes.…”

“…Among non-avian reptiles, the majority of the snakes karyotyped so far exhibit a ZZ/ZW sex chromosome system, with different stages of evolutionary degeneration or amplification of W chromosomes 23 – 25 . However, undifferentiated sex chromosomes (and more recently unique Y sex-linked markers, suggesting an XY male heterogametic system) have also been reported in some genera such as in Python and Boa 26 .…”

“…The gene content of both the Z and the W chromosomes are thought to be relatively conserved in snakes 24 , 27 , 28 . Still, the high variability of W chromosome (regarding morphology and/or gene content) in major clades suggests a remarkable role of repetitive sequences accumulation in their architecture and evolution 24 , 25 , 29 . Unlike the W, the Z chromosomes are thought to be more stable among Serpentes lineages, and non-drastic shifts in morphology have been reported in different snake clades 23 – 25 , 30 .…”

Interstitial Telomeric Repeats Are Rare in Turtles

“…Cytogenetic studies have detected ITRs in numerous species across vertebrate lineages, including mammals, fishes, birds, non-avian reptiles and amphibians [3,[27][28][29][30][39][40][41][42][43][44][45][46]. In non-avian reptiles, distribution of telomeric sequences have been extensively studied in squamates, i.e., lizards and snakes, where ITRs were detected in approximately 100 species, despite the generally conserved chromosome morphology in this group [28,45,[47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63][64]. It was proposed that intrachromosomal rearrangements might have a crucial role in the formation of ITRs in squamate reptiles [28,63].…”

Revisiting the Karyotype Evolution of Neotropical Boid Snakes: A Puzzle Mediated by Chromosomal Fissions

“…Most of the Serpentes lineages have 2n = 36 chromosomes (16 macro + 20 microchromosomes), which is considered a plesiomorphic feature for the suborder [ 25 , 26 , 27 , 28 ]. However, Boidae differs from other families by presenting the greatest chromosomal diversity among the Booidea families, with 2n ranging from 36 to 44 chromosomes, including an undifferentiated XY sex chromosome system [ 24 , 25 , 29 ].…”