Poorly differentiated XX/XY sex chromosomes are widely shared across skink radiation

Abstract

Differentiated sex chromosomes are believed to be evolutionarily stable, and their emergence was suggested to lead to a remarkable increase in the diversification rate and in disparity in such groups as birds, mammals and snakes. On the other hand, poorly differentiated sex chromosomes are considered to be prone to turnovers. With around 1.700 currently known species forming c. 15% of reptile species diversity, skinks (family Scincidae) are a very diverse group of squamates known for their large ecological and morphological variability. Skinks generally have poorly differentiated and cytogenetically hardly distinguishable sex chromosomes and their sex determination was suggested to be highly variable. Here, we determined X-linked genes in the common sandfish (Scincus scincus) and demonstrate that skinks have shared the same homologous XX/XY sex chromosomes across their wide phylogenetic spectrum for at least 85 million years, approaching the age of the highly differentiated ZZ/ZW sex chromosomes of birds and advanced snakes. Skinks thus demonstrate that even poorly differentiated sex chromosomes can be evolutionarily stable and that large diversity can emerge even in groups with poorly differentiated sex chromosomes. The conservation of sex chromosomes across skinks allows us to introduce the first molecular sexing method widely applicable in this group.

Independent Evolution of Sex Chromosomes in Eublepharid Geckos, A Lineage with Environmental and Genotypic Sex Determination

“…In amniotes, sex chromosomes often seem to evolve from genomic regions with genes involved in the gonad development and differentiation [ 10 , 15 , 16 ]. The syntenic block homologous with GGA1 has been previously reported as being a part of sex chromosomes in skinks [ 19 ], also under male heterogamety. The syntenic block homologous with GGA11 was previously reported as a part of the sex chromosomes in monotremes, where it is probably not connected to sex determination but represents a later added region [ 47 ], but not in any reptile lineage.…”

“…Closer comparison of the Coleonyx elegans and the Scincus scincus [ 19 ] X-specific gene content revealed a small overlap. GGA1, GGA6 and GGA11 syntenic blocks are enriched in genes involved in gonad development and differentiation or with ectopic expression leading to sex reversals ( Table S4, in the Supplementary Materials ).…”

“…Geckos (Gekkota) are the sister group to all other squamate reptiles, except for dibamids [ 17 , 18 ] and therefore, a phylogenetically informative lineage for the reconstruction of the evolution of sex determination in amniotes. In contrast to mammals, birds and many squamate lineages such as lacertids, caenophidian snakes, iguanas, varanids and skinks (reviewed in [ 19 ]), geckos demonstrate an extensive variability in sex determination including ESD as well as male and female heterogamety [ 5 , 20 , 21 ]. It is possible that from unknown reasons geckos during their evolutionary history exhibit for an amniote lineage unusually high frequency of turnovers in sex determination systems.…”

Sex Chromosome Turnover in Bent-Toed Geckos (Cyrtodactylus)

“…These results contribute to the ever-increasing diversity of gecko sex chromosome systems. Although squamate lizards are known for a diversity of sex chromosome systems, they tend to have conserved systems within suborders or families, including scincids [ 59 ], lacertids [ 60 ], varanids [ 61 , 62 ], pleurodonts [ 63 ] (but see [ 6 , 8 ]), and caenophidian snakes [ 36 , 64 ]. In contrast, geckos regularly experience sex chromosome turnovers between families and genera, and, as demonstrated here, even within genera.…”

A 180 My-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes

“…Evolutionarily very old, conserved and homomorphic ZZ/ZW sex chromosomes are known in some ratite birds (Ratidae), dating back >130 My [27–28]. Similarly, skinks (Scincidae) share homologous, mostly poorly differentiated XX/XY sex chromosomes across a wide phylogenetic spectrum for at least 85 million years [29]. Recent findings in the teleost family Esocidae report undifferentiated sex chromosomes of similar evolutionary age (65-90 My) in teleosts [30].…”