The origin and differentiation process of X and Y chromosomes of the black marsh turtle (Siebenrockiella crassicollis, Geoemydidae, Testudines)

Abstract

The black marsh turtle (Siebenrockiella crassicollis) has morphologically differentiated X and Y sex chromosomes. To elucidate the origin and evolutionary process of S. crassicollis X and Y chromosomes, we performed cross-species chromosome painting with chromosome-specific DNA from Chinese soft-shelled turtle (Pelodiscus sinensis) and chromosome mapping of the sex-linked genes of S. crassicollis using FISH. The X and Y chromosomes of S. crassicollis were hybridized with DNA probe of P. sinensis chromosome 5, which is homologous to chicken chromosome 5. S. crassicollis homologues of 14 chicken chromosome 5-linked genes were all localized to the X long arm, whereas two genes were mapped to the Y short arm and the other 12 genes were localized to the Y long arm in the same order as the X chromosome. This result suggests that extensive linkage homology has been retained between chicken chromosome 5 and S. crassicollis X and Y chromosomes and that S. crassicollis X and Y chromosomes are at an early stage of sex chromosome differentiation. Comparison of the locations of two site-specific repetitive DNA sequences on the X and Y chromosomes demonstrated that the centromere shift was the result of centromere repositioning, not of pericentric inversion.

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

“…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.…”

“…Further, XTR4 carries Wt1 , another important regulator of gonadal formation and putative master TSD gene in Chrysemys [Valenzuela, 2008]. Moreover, the evolution of turtle sex chromosome systems in all these cases involved chromosomal inversions, and in all but Trionychid turtles, these inversions encompassed Dmrt1 or Wt1 [Kawagoshi et al, 2009[Kawagoshi et al, , 2012[Kawagoshi et al, , 2014Montiel et al, 2016]. The evolutionary origin of the Pangshura smithii ZZ/ZW system [Sharma et al, 1975] in the same turtle family Geoemy didae as Siebenrockiella , as well as the origin of the sex chromosomes of chelid turtles ( Emydura , Chelodina , and Acanthochelys radiolata ), remains unknown.…”

Mammalian X homolog acts as sex chromosome in lacertid lizards

“…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).…”

Extraordinary Diversity in the Origins of Sex Chromosomes in Anurans Inferred from Comparative Gene Mapping

“…Current information on the genetic linkage of sex chromosomal genes in nonavian reptiles and fish indicates multiple origins of sex chromosomes in these organisms [Kawai et al, 2007[Kawai et al, , 2009; Kawagoshi et al, 2009Kawagoshi et al, , 2012Kawagoshi et al, , 2014Charlesworth and Mank, 2010;Kikuchi and Hamaguchi, 2013]. According to phylogenetic analyses, it was once thought that female heterogamety was the ancestral state of sex determination in anurans, and maleheterogametic sex determination has been acquired independently several times as a result of mutations in autosomal genes involved in male sex determination [Hillis and Green, 1990].…”