Consequence of Paradigm Shift with Repeat Landscapes in Reptiles: Powerful Facilitators of Chromosomal Rearrangements for Diversity and Evolution

Abstract

Reptiles are notable for the extensive genomic diversity and species richness among amniote classes, but there is nevertheless a need for detailed genome-scale studies. Although the monophyletic amniotes have recently been a focus of attention through an increasing number of genome sequencing projects, the abundant repetitive portion of the genome, termed the “repeatome”, remains poorly understood across different lineages. Consisting predominantly of transposable elements or mobile and satellite sequences, these repeat elements are considered crucial in causing chromosomal rearrangements that lead to genomic diversity and evolution. Here, we propose major repeat landscapes in representative reptilian species, highlighting their evolutionary dynamics and role in mediating chromosomal rearrangements. Distinct karyotype variability, which is typically a conspicuous feature of reptile genomes, is discussed, with a particular focus on rearrangements correlated with evolutionary reorganization of micro- and macrochromosomes and sex chromosomes. The exceptional karyotype variation and extreme genomic diversity of reptiles are used to test several hypotheses concerning genomic structure, function, and evolution.

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

“…Comparative chromosome maps between squamate reptiles and birds using cross-species BAC FISH mapping revealed that GGA5 (CH261-161B22, BAC clone) and GGAZ (CH261-129A16, BAC clone) are mapped on different pairs of green iguana microchromosomes, whereas GGA5 (CH261-161B22, BAC clone) is homologous to the long arm of the W sex chromosome of N. kaouthia, Notechis scutatus and Daboia russelii, and chromosome 1 of Varanus salvator macromaculatus, and corresponds to squamate chromosome 2 (SR2) (Srikulnath et al, 2013;Singchat et al, 2018Singchat et al, , 2020a. These results thus strongly support the hypothesis of an ancestral amniote super-sex chromosome that might have involved genomic regions orthologous to SR2 and the snake W sex chromosome (Ezaz et al, 2017;Singchat et al, 2018Singchat et al, , 2020aMatsubara et al, 2019;Ahmad et al, 2020). By contrast, we did not detect any evidence of loci in the nonrecombination region homologous to GGA15; however, only one of 961 SNP/PA loci retained with the filtering criterion 90:10 male:female as moderately sex-linked loci was homologous to GGA15.…”

“…This finding suggests that the specific region containing genetic constituents homologous to GGA15 tends to be located outside the non-recombination region but in close proximity to the non-recombination region of the sex chromosomes in green iguana. The location of GGA15 might therefore be more distant from the putative sex-determination locus in green iguana, differing from the previous hypothesis (Lambert et al, 2016;Rodrigues et al, 2018;Sopniewski et al, 2019;Ahmad et al, 2020). This becomes 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).…”

“…It is possible that multiple independent diversification events in the analyzed region among green iguana individuals in the present study (i.e., intraspecific polymorphism) were associated with inversion of the ancestral sex-determination locus or translocation of the analyzed green iguana X-specific genes to the recombination region, as found in the one locus corresponding to GGA15. An additional possibility is the hypothesis of an ancestral super-sex chromosome as revealed by several segments involving sex-chromosomal linkages in several amniote species (Ezaz et al, 2017;Singchat et al, 2018Singchat et al, , 2020aMatsubara et al, 2019;Ahmad et al, 2020). The results of genome-wide SNP analysis, as is possible using DArTseq TM technology, provide a large number of sex-specific SNP/PA loci at perfectly and moderately sexlinked loci for identification of sex determination and sex-linked markers, although the method can only be applied to a small group of closely related species (Sopniewski et al, 2019).…”