The first chromosome-level gecko genome reveals dynamic sex chromosomes in Neotropical leaf-litter geckos (Sphaerodactylidae:Sphaerodactylus)

Abstract

Sex chromosomes have evolved many times across eukaryotes, indicating both their importance and their evolutionary flexibility. Some vertebrate groups, such as mammals and birds, have maintained a single, conserved sex chromosome system across long evolutionary time periods. By contrast, many reptiles, amphibians, and fish have undergone frequent sex chromosome transitions, most of which remain to be catalogued. Among reptiles, gecko lizards (infraorder Gekkota) have shown an exceptional lability with regard to sex chromosome transitions and may possess the majority of transitions within squamates (lizards and snakes). However—across geckos—information about sex chromosome linkage is expressly lacking, leaving large gaps in our understanding of the evolutionary processes at play in this system. To address this gap, we assembled the first chromosome-level genome for a gecko and use this linkage information to survey six Sphaerodactylus species using a variety of genomic data, including whole-genome re-sequencing, RADseq, and RNAseq. Previous work has identified XY systems in two species of Sphaerodactylus geckos. We expand upon that work to identify between two and four sex chromosome cis-transitions (XY to XY) within the genus. Interestingly, we confirmed two linkage groups as XY sex chromosome systems that were previously unknown to act as sex chromosomes in tetrapods (syntenic with Gallus 3 and Gallus 18/30/33). We highlight the increasing evidence that most (if not all) linkage groups will likely be identified as a sex chromosome in future studies given thorough enough sampling.

It’s a Trap?! Escape from an ancient, ancestral sex chromosome system and implication ofFoxl2as the putative primary sex determining gene in a lizard (Anguimorpha; Shinisauridae)

“…Of note, however, at present it is difficult to assess the precise genomic coordinates and gene content of the SDR due to the chimeric nature of the reference genome assembly. To our knowledge, this is the first demonstration in a tetrapod of the syntenic region of chicken chromosome 9 being recruited in a sex determining role (Kratochvíl et al 2021), lending further support to the idea that all chromosomes will likely be recruited into a sex determining role given thorough enough phylogenetic sampling (Graves and Peichel, 2010;Hodgkin, 2002;O'Meally et al 2012;Pinto et al 2022).…”

“…homomorphic sex chromosomes). Other methods must be employed, such as advanced cytogenetic techniques or high-throughput DNA sequencing technologies, to identify sex chromosome systems in these taxa (Gamble and Zarkower, 2014;Gamble et al 2017;Pinto et al 2022).…”

“…In other words, testing this hypothesis is contingent upon having sufficient data necessary to identify a transition away from a sex chromosome system which typically requires a reference genome to coordinate linkage groups (which are rare in squamates; , genome-scale data from both sexes (e.g. Vicoso et al 2013;Gamble et al 2015;Pinto et al 2022), and a robust phylogenetic hypothesis to establish relationships within the focal taxa (Nielsen et al 2019). Thus, the burden of proof is higher for identifying escapes from these putative "evolutionary traps," which may be partially responsible for the dearth of examples.…”

Incomplete dosage balance and dosage compensation in the ZZ/ZW Gila monster (Heloderma suspectum) revealed byde novogenome assembly

“…Third, outside of pseudoautosomal regions, females should not have any heterozygous sites because they possess a single Z. Instead, we suggest that this is due to reads from the female W chromosomes mismapping to the Z (Pinto et al, 2022;Schield et al, 2019;Webster et al, 2019) because there is no W chromosome in the assembly. To explore this further, we called variants in the RNAseq data and observed similar heterozygous rates in males and females (Supplemental Table S5).…”

Identification of a cis‐sex chromosome transition in banded geckos (Coleonyx, Eublepharidae, Gekkota)

“…This result was especially interesting as the sex chromosomes of C. brevis are not homologous to the XX/XY sex chromosomes of C. elegans and C. mitratus . Such novel sex chromosome diversity is becoming commonplace amongst geckos, as every recent study seems to identify a new sex‐determination system (Keating et al, 2020, 2021; Pinto et al, In press; Pokorná et al, 2014; Augstenová et al, 2021; Gamble, et al, 2015; Rovatsos, et al, 2016; Rovatsos et al, 2021; Pensabene et al, 2020; Nielsen, et al, 2019). These frequent turnovers should make geckos a priority for future studies in order to uncover additional diversity and utilize this fascinating group of lizards as a model for studying sex chromosome evolution.…”