Turtle Insights into the Evolution of the Reptilian Karyotype and the Genomic Architecture of Sex Determination

Abstract

Sex chromosome evolution remains an evolutionary puzzle despite its importance in understanding sexual development and genome evolution. The seemingly random distribution of sex-determining systems in reptiles offers a unique opportunity to study sex chromosome evolution not afforded by mammals or birds. These reptilian systems derive from multiple transitions in sex determination, some independent, some convergent, that lead to the birth and death of sex chromosomes in various lineages. Here we focus on turtles, an emerging model group with growing genomic resources. We review karyotypic changes that accompanied the evolution of chromosomal systems of genotypic sex determination (GSD) in chelonians from systems under the control of environmental temperature (TSD). These transitions gave rise to 31 GSD species identified thus far (out of 101 turtles with known sex determination), 27 with a characterized sex chromosome system (13 of those karyotypically). These sex chromosomes are varied in terms of the ancestral autosome they co-opted and thus in their homology, as well as in their size (some are macro-, some are micro-chromosomes), heterogamety (some are XX/XY, some ZZ/ZW), dimorphism (some are virtually homomorphic, some heteromorphic with larger-X, larger W, or smaller-Y), age (the oldest system could be ~195 My old and the youngest < 25 My old). Combined, all data indicate that turtles follow some tenets of classic theoretical models of sex chromosome evolution while countering others. Finally, although the study of dosage compensation and molecular divergence of turtle sex chromosomes has lagged behind research on other aspects of their evolution, this gap is rapidly decreasing with the acceleration of ongoing research and growing genomic resources in this group.

Karyotypic Evolution of Sauropsid Vertebrates Illuminated by Optical and Physical Mapping of the Painted Turtle and Slider Turtle Genomes

“…Our data expanded the physical mapping of genes involved in sexual development by detecting 20 genes out of 32 core genes in the vertebrate sex determination/differentiation cascade, including 10 genes previously reported [ 10 , 12 ]. Our findings strengthen the notion that sex chromosomes have followed independent evolutionary trajectories in distinct turtle lineages [ 43 ], as have turtle and avian sex chromosomes, and uncovered sex-linked and autosomal intra- and inter-chromosomal rearrangements. For instance, we confirmed that C. picta CPI-7 is homologous to red-eared slider ( T. scripta ) chromosome 6 [ 35 ] ( Figure 3 ), and to chicken Z chromosome ( Figure 4 B) [ 5 , 12 ], which in turn, is also homologous to the Mexican giant musk turtle ( Staurotypus triporcatus ) XY sex chromosomes [ 21 , 44 ], and to chromosome 6 of the softshell turtles Apalone spinifera and Pelodiscus sinensis [ 36 , 45 ].…”

Molecular Cytogenetic Characterization of the Sicilian Endemic Pond Turtle Emys trinacris and the Yellow-Bellied Slider Trachemys scripta scripta (Testudines, Emydidae)

“…CMA 3 staining in Emys trinacris ( Figure 3 g) showed GC content localized in the centromere and telomere in some chromosomes, in accordance with a previous report in T. s. elegans [ 53 ]. Additionally, it was previously shown that the chromosomes that carry the genes of the nucleolar organizing region (NOR) vary in the degree of heteromorphy and often correspond to the sex chromosomes in turtles [ 22 , 55 ]. Despite evidence from molecular phylogenetic studies that show differences between E. trinacris and E. orbicularis [ 13 , 56 ], our cytogenetic comparative analysis revealed similarity between the two species.…”

The Amazonian Red Side-Necked Turtle Rhinemys rufipes (Spix, 1824) (Testudines, Chelidae) Has a GSD Sex-Determining Mechanism with an Ancient XY Sex Microchromosome System

“…Interestingly, as revealed here in our study, even with ancient origin, they can also be found practically intact in recent lineages, where the X and Y of R. rufipes are undistinguished from each other, with the Y sex chromosome being identified solely by comparative genomic hybridization and recruitment of several SSR motifs. The sex chromosomes may remain undifferentiated for many reasons, for example, transitions and turnovers involving XY and ZW, evolutionary advantages promoted by the recombination between XY and/or Z and W, as well as shifts involving autosomes [ 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 , 74 , 75 , 76 , 77 , 78 , 79 , 80 , 81 , 82 , 83 , 84 , 85 , 86 , 87 , …”