The Staurotypus Turtles and Aves Share the Same Origin of Sex Chromosomes but Evolved Different Types of Heterogametic Sex Determination

Abstract

Reptiles have a wide diversity of sex-determining mechanisms and types of sex chromosomes. Turtles exhibit temperature-dependent sex determination and genotypic sex determination, with male heterogametic (XX/XY) and female heterogametic (ZZ/ZW) sex chromosomes. Identification of sex chromosomes in many turtle species and their comparative genomic analysis are of great significance to understand the evolutionary processes of sex determination and sex chromosome differentiation in Testudines. The Mexican giant musk turtle (Staurotypus triporcatus, Kinosternidae, Testudines) and the giant musk turtle (Staurotypus salvinii) have heteromorphic XY sex chromosomes with a low degree of morphological differentiation; however, their origin and linkage group are still unknown. Cross-species chromosome painting with chromosome-specific DNA from Chinese soft-shelled turtle (Pelodiscus sinensis) revealed that the X and Y chromosomes of S. triporcatus have homology with P. sinensis chromosome 6, which corresponds to the chicken Z chromosome. We cloned cDNA fragments of S. triporcatus homologs of 16 chicken Z-linked genes and mapped them to S. triporcatus and S. salvinii chromosomes using fluorescence in situ hybridization. Sixteen genes were localized to the X and Y long arms in the same order in both species. The orders were also almost the same as those of the ostrich (Struthio camelus) Z chromosome, which retains the primitive state of the avian ancestral Z chromosome. These results strongly suggest that the X and Y chromosomes of Staurotypus turtles are at a very early stage of sex chromosome differentiation, and that these chromosomes and the avian ZW chromosomes share the same origin. Nonetheless, the turtles and birds acquired different systems of heterogametic sex determination during their evolution.

Mammalian X homolog acts as sex chromosome in lacertid lizards

“…Such situation was previously reported among the sex chromosomes of Staurotypus turtles (XY; Kawagoshi et al, 2014) Rens et al, 2007). It was suggested that thanks to their gene content, particularly due to the inclusion of genes related to gonad differentiation, some chromosomes are more likely than others to start functioning as sex chromosomes (O'Meally et al, 2012).…”

“…As far as we know, sex chromosomes of lacertids are not homologous with those of other sauropsid lineages with known gene content, such as advanced snakes (Matsubara et al, 2006;Vicoso et al, 2013), iguanas (see, for example, Alföldi et al, 2011;Rovatsos et al, 2014a-c), geckos (Kawai et al, 2009), turtles (see, for example, Kawagoshi et al, 2012Kawagoshi et al, , 2014 and birds (see, for example, Zhou et al, 2014). The lacertid Z chromosome partially shares gene content with the ancestral therian X, and thus we assume that these sex chromosome systems probably evolved from the same ancestral chromosome (syntenic block).…”

“…In any case, more robust testing of the hypotheses of the ancestral sex determination and on the evolution of sex-determining mechanisms in amniotes is largely precluded by our very limited knowledge about the homology of sex chromosomes and sex-determining genes among particular groups. The homology of sex chromosomes can be inferred from the knowledge of the gene content of sex chromosomes; however, it has been identified in only a few amniote lineages such as viviparous mammals (see, for example, Kohn et al, 2004) and monotremes (see, for example, Rens et al, 2007), birds (see, for example, Zhou et al, 2014), several turtle species (see, for example, Kawagoshi et al, 2012Kawagoshi et al, , 2014, advanced snakes (Matsubara et al, 2006;Vicoso et al, 2013;Rovatsos et al, 2015), iguanas (see, for example, Alföldi et al, 2011;Rovatsos et al, 2014a-c), a gecko (Kawai et al, 2009) and recently also a lacertid lizard (Srikulnath et al, 2014).…”

Cytogenetic Insights into the Evolution of Chromosomes and Sex Determination Reveal Striking Homology of Turtle Sex Chromosomes to Amphibian Autosomes

“…Also, because genomes may retain inactive copies of the NOR after translocations have occurred, silver staining reveals only a partial view of NOR's evolutionary history. Thus, we also used 18S rDNA FISH (18S-NOR) as previously applied to a few turtle taxa [Kawai et al, 2007;Cleiton and Giuliano-Caetano, 2008;Badenhorst et al, 2013Badenhorst et al, , 2015Kawagoshi et al, 2014] to detect potentially inactive NOR copies that may have passed undetected in some of the turtles previously examined using AgNOR or scNOR techniques. Our 18S FISH data of the 13 target taxa includes the first reports of 18S-NORs for 7 of them (GIN, CSE, SOD, CIN, EMA, COB, and PSU) ( table 1 ).…”

“…Of these 10 cases, 3 involved microchromosomes and 7 macrochromosomes. Relatively little is known about the molecular content of turtle sex chromosomes, although information is increasing [Kawagoshi et al, 2009[Kawagoshi et al, , 2012[Kawagoshi et al, , 2014Montiel et al 2016]. Molecular cytogenetic data from comparative genome hybridization (CGH) has been used to identify the extent of the male-or female-limited region of the turtle sex chromosomes [Ezaz et al, 2006;Kawai et al, 2007;Martinez et al, 2008;Badenhorst et al, 2013;Montiel et al, 2016] where recombination should be reduced or absent.…”