Impact of Repetitive DNA Elements on Snake Genome Biology and Evolution

Abstract

The distinctive biology and unique evolutionary features of snakes make them fascinating model systems to elucidate how genomes evolve and how variation at the genomic level is interlinked with phenotypic-level evolution. Similar to other eukaryotic genomes, large proportions of snake genomes contain repetitive DNA, including transposable elements (TEs) and satellite repeats. The importance of repetitive DNA and its structural and functional role in the snake genome, remain unclear. This review highlights the major types of repeats and their proportions in snake genomes, reflecting the high diversity and composition of snake repeats. We present snakes as an emerging and important model system for the study of repetitive DNA under the impact of sex and microchromosome evolution. We assemble evidence to show that certain repetitive elements in snakes are transcriptionally active and demonstrate highly dynamic lineage-specific patterns as repeat sequences. We hypothesize that particular TEs can trigger different genomic mechanisms that might contribute to driving adaptive evolution in snakes. Finally, we review emerging approaches that may be used to study the expression of repetitive elements in complex genomes, such as snakes. The specific aspects presented here will stimulate further discussion on the role of genomic repeats in shaping snake evolution.

Remnant of Unrelated Amniote Sex Chromosomal Linkage Sharing on the Same Chromosome in House Gecko Lizards, Providing a Better Understanding of the Ancestral Super-Sex Chromosome

“…Based on the comparative genomics in the gecko lizards [ 22 , 23 ], HPL1 is likely homologous to chromosome 3 of Schlegel’s Japanese gecko ( Gekko japonicus , Schlegel, 1836) [ 92 ]. These observations of hybridization patterns of all BACs mapped on HPL lead us to support previous reports of shared unrelated partial sex chromosomal linkages that were also observed in the gecko lizard and a large ancestral super-sex chromosome that correlated between SR2 and snake W sex chromosomes [ 8 , 9 , 10 , 24 , 48 , 50 , 51 , 52 ]. Common genomic elements such as repetitive sequences might result in hybridizing the same BACs onto multiple different chromosome pairs, suggesting the contribution of transitions to sex chromosomes across amniotes.…”

“…Based on the comparative genomics in the gecko lizards [22,23], HPL1 is likely homologous to chromosome 3 of Schlegel's Japanese gecko (Gekko japonicus, Schlegel, 1836) [92]. These observations of hybridization patterns of all BACs mapped on HPL lead us to support previous reports of shared unrelated partial sex chromosomal linkages that were also observed in the gecko lizard and a large ancestral super-sex chromosome that correlated between SR2 and snake W sex chromosomes [8][9][10]24,48,[50][51][52].…”

“…Dynamics of their SDSs and karyotypic patterns lead us to propose that an extensive process of genomic reorganization has occurred in this lineage compared with other squamate reptiles [ 23 , 24 , 39 , 94 , 95 ]. When considering sex chromosomal linkage homologies and an ancestral amniote super-sex chromosome, SR2 and snake W sex chromosomes share partial sex chromosomal linkage homologies with sex-related elements or common genomic regions of other amniotes [ 8 , 9 , 10 , 24 , 48 , 50 , 51 , 52 ]. The stochastic occurrence of chromosomal rearrangements in the gecko lizard lineage is, thus, appropriate to test the current direction of an ancestral super-sex chromosome, as distinct from other squamate reptiles.…”

“…Contrary to the trap, the frequent turnover of SDSs, which are distributed in many gecko lizards, most amphibians and many fish species, can inhibit differentiation when newly derived sex chromosomes have not had time to degenerate [ 112 , 113 , 114 , 115 , 116 , 117 , 118 , 119 , 120 , 121 ]. An alternative explanation is that some amniote chromosomes may have evolved repeatedly into sex chromosomes [ 8 , 9 , 10 , 24 , 48 , 49 , 50 , 51 , 52 ]. Certain genome sections might tend to be recruited to function as sex chromosomes more often than other parts due to their content of genes or genomic elements involved in gonad differentiation.…”

“…Thus, they are an excellent group for testing general hypotheses on sex determination and sex chromosome evolution. Interestingly, partial sex chromosomal linkage homologies have also been found between chromosomes in different amniote lineages, while unrelated sex chromosomes share linkage homologies across distantly related groups, such as the Hokou gecko ( Gekko hokouensis , Pope, 1928) and chicken ( Gallus gallus , Linnaeus, 1758) [ 8 , 9 , 10 , 21 , 24 , 48 , 49 , 50 , 51 , 52 , 53 , 54 ]. Currently, squamate reptile chromosome 2 (SR2) and snake W sex chromosomes are hypothesized to share partial sex chromosomal linkage homologies with sex-related elements or common genomic regions, such as repeats, supporting the concept that the two chromosomes were associated with a larger ancestral amniote super-sex chromosome before multiple fissions into different lineages [ 8 , 9 , 10 , 24 , 48 , 49 , 50 , 51 , 52 , 55 , 56 ].…”