RESUMEN

How consistent are the evolutionary trajectories of sex chromosomes shortly after they form? Insights into the evolution of recombination, differentiation, and degeneration can be provided by comparing closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and its sister species, the Japan Sea stickleback (G. nipponicus), have been well characterized. Little is known, however, about the sex chromosomes of their congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees to obtain experimentally phased whole genome sequences from blackspotted stickleback X and Y chromosomes. Using multispecies gene trees and analysis of shared duplications, we demonstrate that Chromosome 19 is the ancestral sex chromosome and that its oldest stratum evolved in the common ancestor of the genus. After the blackspotted lineage diverged, its sex chromosomes experienced independent and more extensive recombination suppression, greater X-Y differentiation, and a much higher rate of Y degeneration than the other two species. These patterns may result from a smaller effective population size in the blackspotted stickleback. A recent fusion between the ancestral blackspotted stickleback Y chromosome and Chromosome 12, which produced a neo-X and neo-Y, may have been favored by the very small size of the recombining region on the ancestral sex chromosome. We identify six strata on the ancestral and neo-sex chromosomes where recombination between the X and Y ceased at different times. These results confirm that sex chromosomes can evolve large differences within and between species over short evolutionary timescales.

Asunto(s)

RESUMEN

Sex chromosomes are a peculiar constituent of the genome because the evolutionary forces that fix the primary sex-determining gene cause genic degeneration and accumulation of junk DNA in the heterogametic partner. One of the most spectacular phenomena in sex chromosome evolution is the occurrence of neo-Y chromosomes, which lead to X1X2Y sex-determining systems. Such neo-sex chromosomes are critical for understanding the processes of sex chromosome evolution because they rejuvenate their total gene content. We assembled the male and female genomes at the chromosome level of the spotted knifejaw (Oplegnathus punctatus), which has a cytogenetically recognized neo-Y chromosome. The full assembly and annotation of all three sex chromosomes allowed us to reconstruct their evolutionary history. Contrary to other neo-Y chromosomes, the fusion to X2 is quite ancient, estimated at 48 Ma. Despite its old age and being even older in the X1 homologous region which carries a huge inversion that occurred as early as 55-48 Ma, genetic degeneration of the neo-Y appears to be only moderate. Transcriptomic analysis showed that sex chromosomes harbor 87 genes, which may serve important functions in the testis. The accumulation of such male-beneficial genes, a large inversion on the X1 homologous region and fusion to X2 appear to be the main drivers of neo-Y evolution in the spotted knifejaw. The availability of high-quality assemblies of the neo-Y and both X chromosomes make this fish an ideal model for a better understanding of the variability of sex determination mechanisms and of sex chromosome evolution.

Asunto(s)

RESUMEN

BACKGROUND: Although Tokudaia muenninki has multiple extra copies of the Sry gene on the Y chromosome, loss of function of these sequences is indicated. To examine the Sry gene function for sex determining in T. muenninki, we screened a BAC library and identified a clone (SRY26) containing complete SRY coding and promoter sequences. RESULTS: SRY26 showed high identity to mouse and rat SRY. In an in vitro reporter gene assay, SRY26 was unable to activate testis-specific enhancer of Sox9. Four lines of BAC transgenic mice carrying SRY26 were generated. Although the embryonic gonads of XX transgenic mice displayed sufficient expression levels of SRY26 mRNA, these mice exhibited normal female phenotypes in the external and internal genitalia, and up-regulation of Sox9 was not observed. Expression of the SRY26 protein was confirmed in primate-derived COS7 cells transfected with a SRY26 expression vector. However, the SRY26 protein was not expressed in the gonads of BAC transgenic mice. CONCLUSIONS: Overall, these results support a previous study demonstrated a long Q-rich domain plays essential roles in protein stabilization in mice. Therefore, the original aim of this study, to examine the function of the Sry gene of this species, was not achieved by creating TG mice.

Asunto(s)

RESUMEN

The mountain pine beetle (Dendroctonus ponderosae) is an insect native to western North America; however, its geographical range has recently expanded north in BC and east into Alberta. To understand the population structure in the areas of expansion, 16 gene-linked microsatellites were screened and compared to neutral microsatellites using outlier analyses of Fst and Fct values. One sex-linked gene, inhibitor of apoptosis (IAP), showed a strong signature of positive selection for neo-X alleles and was analyzed for evidence of adaptive variation. Alleles of IAP were sequenced, and differences between the neo-X and neo-Y alleles were consistent with neutral evolution suggesting that the neo-Y allele may not be under functional constraints. Neo-Y alleles were amplified from gDNA, but not effectively from cDNA, suggesting that there was little IAP expression from neo-Y alleles. There were no differences in overall IAP expression between males and females with the common northern neo-X allele suggesting that the neo-X allele in males compensates for the reduced expression of neo-Y alleles. However, males lacking the most common northern neo-X allele thought to be selected for in northern populations had reduced overall IAP expression in early October-at a time when beetles are preparing for overwintering. This suggests that the most common allele may have more rapid upregulation. The reduced function of neo-Y alleles of IAP suggested by both sequence differences and lower levels of expression may foster a highly selective environment for neo-X alleles such as the common northern allele with more efficient upregulation.

RESUMEN

In most phylogenetic lineages, the evolution of sex chromosomes is accompanied by their heteromorphization and degradation of one of them. The neo-sex chromosomes are useful model for studying early stages of these processes. Recently two lineages of the neo-sex chromosomes on different stages of heteromorphization was discovered in Pamphagidae family. The neo-sex chromosome heteromorphization was analyzed by generation of DNA probes derived from the neo-Xs and neo-Ys followed with chromosome painting in nineteen species of Pamphagidae family. The homologous regions of the neo-sex chromosomes were determined in closely related species with the painting procedure and image analysis with application of the Visualization of the Specific Signal in Silico software package. Results of these analyses and distribution of C-positive regions in the neo-sex chromosomes revealed details of the heteromorphization of the neo-sex chromosomes in species from both phylogenetic lineages of Pamphagidae grasshoppers. The hypothetical mechanism of the neo-Y degradation was suggested. It includes expansion of different repeats from the proximal neo-Y chromosome region by inversions, spreading them towards distal region. Amplification of these repeats leads to formation of C-positive regions and elimination of the C-negative regions located between them.

RESUMEN

X chromosome inactivation (XCI) is an essential mechanism to compensate gene dosage in mammals. Here, we show that XCI has evolved differently in two species of the genus Tokudaia. The Amami spiny rat, Tokudaia osimensis, has a single X chromosome in males and females (XO/XO). By contrast, the Okinawa spiny rat, Tokudaia muenninki, has XX/XY sex chromosomes like most mammals, although the X chromosome has acquired a neo-X region by fusion with an autosome. BAC clones containing the XIST gene, which produces the long non-coding RNA XIST required for XCI, were obtained by screening of T. osimensis and T. muenninki BAC libraries. Each clone was mapped to the homologous region of the X inactivation center in the X chromosome of the two species by BAC-FISH. XIST RNAs were expressed in T. muenninki females, whereas no expression was observed in T. osimensis. The sequence of the XIST RNA was compared with that of mouse, showing that the XIST gene is highly conserved in T. muenninki. XIST RNAs were localized to the ancestral X region (Xq), to the heterochromatic region (pericentromeric region), and partially to the neo-X region (Xp). The hybridization pattern correlated with LINE-1 accumulation in Xq but not in Xp. Dosage of genes located on the neo-X chromosome was not compensated, suggesting that the neo-X region is in an early state of XCI. By contrast, many mutations were observed in the XIST gene of T. osimensis, indicating its loss of function in the XO/XO species.

Asunto(s)

RESUMEN

BACKGROUND: Neo-XY sex chromosome determination is a rare event in short horned grasshoppers, but it appears with unusual frequency in the Pamphagidae family. The neo-Y chromosomes found in several species appear to have undergone heterochromatinization and degradation, but this subject needs to be analyzed in other Pamphagidae species. We perform here karyotyping and molecular cytogenetic analyses in 12 Pamphagidae species from the center of biodiversity of this group in the previously-unstudied Anatolian plateau. RESULTS: The basal karyotype for the Pamphagidae family, consisting of 18 acrocentric autosomes and an acrocentric X chromosome (2n♂ = 19, X0; 2n♀ = 20, XX), was found only in G. adaliae. The karyotype of all other studied species consisted of 16 acrocentric autosomes and a neo-XY sex chromosome system (2n♂♀ = 18, neo-XX♀/neo-XY♂). Two different types of neo-Y chromosomes were found. One of them was typical for three species of the Glyphotmethis genus, and showed a neo-Y chromosome being similar in size to the XR arm of the neo-X, with the addition of two small subproximal interstitial C-blocks. The second type of the neo-Y chromosome was smaller and more heterochromatinized than the XR arm, and was typical for all Nocarodeini species studied. The chromosome distribution of C-positive regions and clusters of ribosomal DNA (rDNA) and telomeric repeats yielded additional information on evolution of these neo-XY systems. CONCLUSION: Most Pamphagidae species in the Anatolian region were found to have neo-XY sex chromosome systems, belonging to two different evolutionary lineages, marked by independent X-autosome fusion events occurred within the Trinchinae and Pamphaginae subfamilies. The high density of species carrying neo-XY systems in the Anatolian region, and the different evolutionary stage for the two lineages found, one being older than the other, indicates that this region has a long history of neo-XY sex chromosome formation.

Asunto(s)

RESUMEN

Although previous cytogenetic analysis of Pamphagidae grasshoppers pointed to considerable karyotype uniformity among most of the species in the family, our study of species from Armenia has discovered other, previously unknown karyotypes, differing from the standard for Pamphagidae mainly in having unusual sets of sex chromosomes. Asiotmethis turritus (Fischer von Waldheim, 1833), Paranocaracris rubripes (Fischer von Waldheim, 1846), and Nocaracris cyanipes (Fischer von Waldheim, 1846) were found to have the karyotype 2n♂=16+neo-XY and 2n♀=16+neo-XX, the neo-X chromosome being the result of centromeric fusion of an ancient acrocentric X chromosome and a large acrocentric autosome. The karyotype of Paranothrotes opacus (Brunner von Wattenwyl, 1882) was found to be 2n♂=14+X1X2Y and 2n♀=14+X1X1X2X2., the result of an additional chromosome rearrangement involving translocation of the neo-Y and another large autosome. Furthermore, evolution of the sex chromosomes in these species has involved different variants of heterochromatinization and miniaturization of the neo-Y. The karyotype of Eremopeza festiva (Saussure, 1884), in turn, appeared to have the standard sex determination system described earlier for Pamphagidae grasshoppers, 2n♂=18+X0 and 2n♀=18+XX, but all the chromosomes of this species were found to have small second C-positive arms. Using fluorescent in situ hybridization (FISH) with 18S rDNA and telomeric (TTAGG)n DNA repeats to yield new data on the structural organization of chromosomes in the species studied, we found that for most of them, clusters of repeats homologous to 18S rDNA localize on two, three or four pairs of autosomes and on the X. In Eremopeza festiva, however, FISH with labelled 18S rDNA painted C-positive regions of all autosomes and the X chromosome; clusters of telomeric repeats localized primarily on the ends of the chromosome arms. Overall, we conclude that the different stages of neo-Y degradation revealed in the Pamphagidae species studied make the family a very promising and useful model for studying sex chromosome evolution.

RESUMEN

The scuttle fly, Megaselia scalaris, is often cited as a model in which to study early sex chromosome evolution because of its homomorphic sex chromosomes, low but measurable molecular differentiation between sex chromosomes, and occasional transposition of the male-determining element to different chromosomes in laboratory cultures. Counterintuitively, natural isolates consistently show sex linkage to the second chromosome. Frequent natural transposition of the male-determining element should lead to the loss of male specificity of any nontransposed material on the previous sex-linked chromosome pair. Using next-generation sequencing data from a newly obtained natural isolate of M. scalaris, we show that even highly conservative estimates for the size of the male-specific genome are likely too large to be contained within a transposable element. This result strongly suggests that transposition of the male-determining region either is extremely rare or has not persisted recently in natural populations, allowing for differentiation of the sex chromosomes of this species.

Asunto(s)

RESUMEN

Entelegyne spiders rarely show fusions yielding neo-Y chromosomes, which M. J. D. White attributed to a constraint in spiders, namely their proximal chiasma localization acting to upset meiotic segregation in males with fusions. Of the 75 taxa of Habronattus and outgroups studied, 47 have X1 X2 0 sex chromosomes in males, 10 have X1 X2 Y, 15 have X1 X2 X3 Y, 2 have X0, and one has both X1 X2 0 and X1 X2 X3 Y. Chromosome numbers and behavior suggest neo-Ys formed by an autosome-X fusion to make X1 X2 Y, with a second fusion to an autosome to make X1 X2 X3 Y. Phylogeny shows at least 8-15 gains (or possibly some losses) of neo-Y (i.e., X-autosome fusions), a remarkable number for such a small clade. In contrast to the many X-autosome fusions, at most one autosome-autosome fusion is indicated. Origins of neo-Y are correlated significantly with distal localization of chiasmata, supporting White's hypothesis that evolution of neo-Y systems is facilitated by looser pairing (distal chiasmata) at meiosis. However, an alternative (or contributing) explanation for the correlation is that X-autosome fusions were selected to permit isolation of male-favored alleles to the neo-Y chromosome, aided by distal chiasmata limiting recombination. This intralocus sexual conflict hypothesis could explain both the many X-autosome fusions, and the stunning complexity of male Habronattus courtship displays.

Asunto(s)