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

Abstract

The majority of lizards classified in the superfamily Iguanoidea have an XX/XY sexdetermination system in which sex-chromosomal linkage shows homology with chicken (Gallus gallus) chromosome 15 (GGA15). However, the genomics of sex chromosomes remain largely unexplored owing to the presence of homomorphic sex chromosomes in majority of the species. Recent advances in high-throughput genome complexity reduction sequencing provide an effective approach to the identification of sexspecific loci with both single-nucleotide polymorphisms (SNPs) and restriction fragment presence/absence (PA), and a better understanding of sex chromosome dynamics in Iguanoidea. In this study, we applied Diversity Arrays Technology (DArTseq TM) in 29 phenotypic sex assignments (14 males and 15 females) of green iguana (Iguana iguana). We confirmed a male heterogametic (XX/XY) sex determination mode in this species, identifying 29 perfectly sex-linked SNP/PA loci and 164 moderately sex-linked SNP/PA loci, providing evidence probably indicative of XY recombination. Three loci from among the perfectly sex-linked SNP/PA loci showed partial homology with several amniote sex chromosomal linkages. The results support the hypothesis of an ancestral super-sex chromosome with overlaps of partial sex-chromosomal linkages. However, only one locus among the moderately sex-linked loci showed homology with GGA15, which suggests that the specific region homologous to GGA15 was located outside the non-recombination region but in close proximity to this region of the sex chromosome

Snake W Sex Chromosome: The Shadow of Ancestral Amniote Super-Sex Chromosome

“…The molecular machinery of the sex determination pathway is observed across ESD amniote lineages, which concurs with independent co-option of the same epigenetic process [59]. Interestingly, recent comparative genomic analyses indicate that the majority of the squamate reptile chromosome 2 (SR2) and the snake W sex chromosomes share partial sex chromosomal linkage homologies with sex-related elements of other amniotes, despite their apparent diversity of sex-determining mechanisms [18,25,27,28,[30][31][32]58]. Hypothetically, the SR2 and snake W sex chromosomes may have been part of a larger ancestral amniote super-sex chromosome with a GSD system that subsequently split into many sex chromosomes across several amniote lineages by multiple chromosomal rearrangements such as fission [27,28,30].…”

“…Sex chromosomes evolved independently multiple times within amniotes and remained notably stable after their emergence in mammals, birds, and many lineages of reptiles [16][17][18]56,57]. This scenario is supported by evidence of the same linkage homology blocks that perform the role of sex chromosomes in several amniote lineages, or by unrelated sex chromosomes sharing partial linkage homologies across distantly related groups [18,25,27,28,[30][31][32]58]. This was probably caused by multiple random selections from a limited number of linkage homologies, or a stronger tendency for a linkage homology to be co-opted owing to its gene content, particularly as a result of enrichment of the genes involved in gonad differentiation, and the possibility of homologous sex-determining systems [7].…”

“…Cessation of recombination triggers structural changes, predominantly on the Y or W sex chromosomes, including accumulation of deleterious mutations, degradation of gene content, accumulation of repeats, heterochromatinization, and changes in gene expression [20][21][22][23][24][25][26][27][28][29][30][31][32]. Deleterious mutations might accumulate in the nonrecombining region through Muller's ratchet or genetic drift, causing Y or W genes to lose their function or disappear altogether [33].…”

An Investigation of ZZ/ZW and XX/XY Sex Determination Systems in North African Catfish (Clarias gariepinus, Burchell, 1822)

“…Although transposable elements can be dispersed on many chromosomes or even throughout the entire genome, large amplification of the elements are often found on sex chromosomes in many organisms ( Ahmad et al, 2020 ; Koomgun et al, 2020 ; Laopichienpong et al, 2020 ; Yoshido et al, 2020 ). The presence of accumulated TEs leads to the establishment of heterochromatin, and possibly also to TE recombination between non-homologous copies.…”

“…This suggests that the XX/XY sex determination system might co-exist with ZZ/ZW system in the same individuals of C. gariepinus. Genomic convergence has been detected by comparative cytogenetics studies in which unrelated sex chromosomes share sex chromosomal linkage homologies across distantly related species (Srikulnath et al, 2014(Srikulnath et al, , 2015Ahmad et al, 2020;Koomgun et al, 2020;Laopichienpong et al, 2020;Singchat et al, 2020a,b). We found that a male-linked locus under the 70:30 criterion shared partial homology with ADD3 which is localized on GGA6, which is further orthologous to sex chromosomes of sand lizard (Lacerta agilis).…”