XX/XY sex chromosomes in a blind lizard (Dibamidae): Towards understanding the evolution of sex determination in squamates

Abstract

The reconstruction of the evolutionary history of sex determination in squamate reptiles (lizards and snakes) is complicated by missing data in many lineages, erroneous reports, and often questionable inferences on state homology. Therefore, despite the large effort, the reconstruction of the ancestral sex determination in squamate reptiles is still controversial. With the hope to shed light on this problem, we aspired to identify the sex chromosome gene content in Dibamus deharvengi, the representative of the family Dibamidae, the putative sister clade to all other squamates. Our analyses revealed XX/XY sex‐determination system in D. deharvengi: the X chromosome contains genes with homologues scattered across chicken chromosomes 8, 12, 13, 18, 30, and 33, and the Y chromosome seems to largely degenerate. To the best of our knowledge, this combination has never been reported to form sex chromosomes in any amniote lineage. It suggests that the sex chromosomes can represent an apomorphy of a clade including D. deharvengi. Our findings cover an important gap in the knowledge of sex determination in reptiles and further support multiple independent origins of sex chromosomes in this group.

Sex chromosome evolution: The remarkable diversity in the evolutionary rates and mechanisms

“…For instance, in this special issue: Using a combination of short‐read and long‐read sequencing, Evans et al (2022) and Duhamel et al (2022) perform a chromosome‐scale genome assembly in the Marsabit clawed frog and anther‐smut fungi, respectively. These approaches allow the study of intra‐specific variation of sex chromosome divergence in the frog and reveal independent chromosomal rearrangement in the mating‐type chromosomes of the fungi. With short‐read WGS and the help of existing reference genomes, Sigeman et al (2022) investigate the translocation nature of a novel neo‐sex chromosome in Sylvivoidea songbirds, whilst Rovatsos et al (2022) reveal a XX/XY sex determination system in a blind lizard and further identified a novel combination of homologous genes using the chicken X chromosome as reference. With short‐read whole‐genome pooled sequencing, Ansai et al (2022) and Jeffries et al (2022) investigate the sex‐determining regions and sex chromosome turnover across closely related fish taxa. With RAD‐seq, Keating et al (2022) and Meuser et al (2022) perform analysis in multiple individuals per sex to investigate possible sex‐determining regions and infer sex chromosome turnovers. …”

“…Their results suggest frequent turnovers in this lineage as well. Rovatsos et al (2022) set out to provide insights into the phylogeny and the ancestral state of sex determination in squamate reptiles, which is still unresolved (reviewed by Kratochvíl, Gamble, et al, 2021). They identify a XX/XY sex chromosome system in a blind lizard, a member of a potential sister lineage to all other squamates, by comparative gene coverage analysis of a male and a female genome.…”

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

“…some linkage groups are more likely to be recruited as a sex chromosome than others (Kratochvíl et al 2021). However, the pattern was weak and the discovery of additional linkage groups acting as sex chromosomes in geckos and dibamids requires a reevaluation (Pensabene et al 2023; Pinto et al 2022; Rovatsos et al 2022). Additionally, inferences that all taxa within a clade share an ancestral sex chromosome, i.e.…”

“…Fortunately, recent advances in DNA sequencing technologies have allowed us to sample more broadly and ask finer-scale questions about how sex chromosomes originate, degenerate, and turnover (e.g. Acosta et al 2019; Gamble et al 2015; 2017; 2018; Keating et al 2020; Kostmann et al 2021; Nielsen et al 2018; 2019; 2020; Pinto et al 2022; Rovatsos et al 2019b; 2022); so the intertwined nature of developing squamate genomics and sex chromosome evolution presents great promise for future work in identifying and characterizing sex chromosome linkage groups across squamates.…”