Chromosome-Level Genome Assembly Reveals Dynamic Sex Chromosomes in Neotropical Leaf-Litter Geckos (Sphaerodactylidae:Sphaerodactylus)

Abstract

Sex determination is a critical element of successful vertebrate development, suggesting that sex chromosome systems might be evolutionarily stable across lineages. For example, mammals and birds have maintained conserved sex chromosome systems over long evolutionary time periods. Other vertebrates, in contrast, have undergone frequent sex chromosome transitions, which is even more amazing considering we still know comparatively little across large swaths of their respective phylogenies. One reptile group in particular, the gecko lizards (infraorder Gekkota), show an exceptional lability with regard to sex chromosome transitions and may possess the majority of transitions within squamates (lizards and snakes). However, detailed genomic and cytogenetic information about sex chromosomes is lacking for most gecko species, leaving large gaps in our understanding of the evolutionary processes at play. To address this, we assembled a chromosome-level genome for a gecko (Sphaerodactylidae: Sphaerodactylus) and used this assembly to search for sex chromosomes among six closely related 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 a new XY) within the genus. Interestingly, we confirmed two different linkage groups as XY sex chromosome systems that were previously unknown to act as sex chromosomes in tetrapods (syntenic with Gallus chromosome 3 and Gallus chromosomes 18/30/33), further highlighting a unique and fascinating trend that most linkage groups have the potential to act as sex chromosomes in squamates.

Chromosome-Level Genome Assembly of the Cape Cliff Lizard (Hemicordylus capensis)

“…To investigate synteny between H. capensis and other squamates, we used GENESPACE v0.9.3 ( Lovell et al 2022 ) with OrthoFinder v2.5.4 ( Emms and Kelly 2019 ) in “default” mode and the genome annotations and protein sequences of S. townsendi ( Pinto et al 2022 ) and P. platyrhinos ( Koochekian et al 2022 ).…”

A lizard is never late: squamate genomics as a recent catalyst for understanding sex chromosome and microchromosome evolution

“…(2) Trends in data generation and assembly Regardless of sequencing methodology implemented, most empiricists have become aware that the quality of sample collection and preparation can "make or break" a genome assembly experiment. This includes every stage of sample preparation up to its conversion from bases to bytes, including, but not limited to: tissue selection, dissection, storage, extraction, library prep, sequencing, and assembly (Dahn et al 2022;Pinto et al 2022Pinto et al & 2023. Many squamate species are rare/hard to collect, have a limited distribution (Meiri et al 2018), and lack material in museum collections adequate for long-read sequencing or chromatic-contact sequencing (HiC).…”

“…obs. )), squamate DNA appears to remain remarkably stable throughout this process, which provides some relief for field collection and sub-optimal tissue conditions-preferring blood or liver tissue when available (Dahn et al 2022;Pinto et al 2022Pinto et al & 2023. These factors prime squamates to benefit from recent advances in sequencing technologylike long, accurate sequencing readsthat have opened new doors in genome assembly.…”

“…These factors prime squamates to benefit from recent advances in sequencing technology – like long, accurate sequencing reads – that have opened new doors in genome assembly. Just as the publication of the first human reference genome at the turn of the century signaled the beginnings of the “genomics age”, the recent publication of the complete human telomere-to-telomere (T2T) genome assembly has signaled a ‘rebirth’ of the genomics age, where now all model systems can be subject to high-quality reference genomes for relatively low cost, including squamates (Nurk et al 2022; Pinto et al 2022, 2023; Rhie et al 2021; Sun et al 2021). The recent advances in genome assembly capability has largely been driven by third generation sequencing technologies, including Pacific Biosciences (PacBio) and Oxford Nanopore Technologies (ONT) platforms (e.g.…”

ZZ/ZW Sex Chromosomes in the Madagascar Girdled Lizard, Zonosaurus madagascariensis (Squamata: Gerrhosauridae)

“…An emerging pattern is that some lineages such as birds, caenophidian snakes, iguanas, lacertids, mammals and monitors have stable, differentiated sex chromosomes for a long evolutionary time [7][8][9][10][11][12]. On the other hand, some reptilian lineages exhibit variability in sex determination, which can be attributed to their old age and quite ancient transitions in sex determination [13] or to relatively frequent turnovers of sex chromosomes [14,15]. Recently, the attention has been directed to one of the last highly diversified clades among squamate reptiles which has been understudied in this regard: the scincoidean lizards.…”