neo-X Chromosome Research Articles

The genome of Litomosoides sigmodontis illuminates the origins of Y chromosomes in filarial nematodes.

Heteromorphic sex chromosomes are usually thought to have originated from a pair of autosomes that acquired a sex-determining locus and subsequently stopped recombining, leading to degeneration of the sex-limited chromosome. The majority of nematode species lack heteromorphic sex chromosomes and determine sex using an X-chromosome counting mechanism, with males being hemizygous for one or more X chromosomes (XX/X0). Some filarial nematode species, including important parasites of humans, have heteromorphic XX/XY karyotypes. It has been assumed that sex is determined by a Y-linked locus in these species. However, karyotypic analyses suggested that filarial Y chromosomes are derived from the unfused homologue of an autosome involved in an X-autosome fusion event. Here, we generated a chromosome-level reference genome for Litomosoides sigmodontis, a filarial nematode with the ancestral filarial karyotype and sex determination mechanism (XX/X0). By mapping the assembled chromosomes to the rhabditid nematode ancestral linkage (or Nigon) elements, we infer that the ancestral filarial X chromosome was the product of a fusion between NigonX (the ancestrally X-linked element) and NigonD (ancestrally autosomal). In the two filarial lineages with XY systems, there have been two independent X-autosome chromosome fusion events involving different autosomal Nigon elements. In both lineages, the region shared by the neo-X and neo-Y chromosomes is within the ancestrally autosomal portion of the X, confirming that the filarial Y chromosomes are derived from the unfused homologue of the autosome. Sex determination in XY filarial nematodes therefore likely continues to operate via the ancestral X-chromosome counting mechanism, rather than via a Y-linked sex-determining locus.

High-Quality Genome Assemblies Reveal Evolutionary Dynamics of Repetitive DNA and Structural Rearrangements in the Drosophila virilis Subgroup.

High-quality genome assemblies across a range of nontraditional model organisms can accelerate the discovery of novel aspects of genome evolution. The Drosophila virilis group has several attributes that distinguish it from more highly studied species in the Drosophila genus, such as an unusual abundance of repetitive elements and extensive karyotype evolution, in addition to being an attractive model for speciation genetics. Here, we used long-read sequencing to assemble five genomes of three virilis group species and characterized sequence and structural divergence and repetitive DNA evolution. We find that our contiguous genome assemblies allow characterization of chromosomal arrangements with ease and can facilitate analysis of inversion breakpoints. We also leverage a small panel of resequenced strains to explore the genomic pattern of divergence and polymorphism in this species and show that known demographic histories largely predicts the extent of genome-wide segregating polymorphism. We further find that a neo-X chromosome in Drosophila americana displays X-like levels of nucleotide diversity. We also found that unusual repetitive elements were responsible for much of the divergence in genome composition among species. Helitron-derived tandem repeats tripled in abundance on the Y chromosome in D. americana compared to Drosophila novamexicana, accounting for most of the difference in repeat content between these sister species. Repeats with characteristics of both transposable elements and satellite DNAs expanded by 3-fold, mostly in euchromatin, in both D. americana and D. novamexicana compared to D. virilis. Our results represent a major advance in our understanding of genome biology in this emerging model clade.

On the Origin of Neo-Sex Chromosomes in the Neotropical Dragonflies Rhionaeschna bonariensis and R. planaltica (Aeshnidae, Odonata).

Odonata have holokinetic chromosomes. About 95% of species have an XX/X0 sex chromosome system, with heterogametic males. There are species with neo-XX/neo-XY sex chromosomes resulting from an X chromosome/autosome fusion. The genus Rhionaeschna includes 42 species found in the Americas. We analyzed the distribution of the nucleolar organizer region (NOR) using FISH with rDNA probes in Rhionaeschna bonariensis (n = 12 + neo-XY), R. planaltica (n = 7 + neo-XY), and Aeshna cyanea (n = 13 + X0). In R. bonariensis and A. cyanea, the NOR is located on a large pair of autosomes, which have a secondary constriction in the latter species. In R. planaltica, the NOR is located on the ancestral part of the neo-X chromosome. Meiotic analysis and FISH results in R. planaltica led to the conclusion that the neo-XY system arose by insertion of the ancestral X chromosome into an autosome. Genomic in situ hybridization, performed for the first time in Odonata, highlighted the entire neo-Y chromosome in meiosis of R. bonariensis, suggesting that it consists mainly of repetitive DNA. This feature and the terminal chiasma localization suggest an ancient origin of the neo-XY system. Our study provides new information on the origin and evolution of neo-sex chromosomes in Odonata, including new types of chromosomal rearrangements, NOR transposition, and heterochromatin accumulation.

The Chromosomal Distribution of Sex-Biased MicroRNAs in Drosophila is Nonadaptive.

Genes are often differentially expressed between males and females. In Drosophila melanogaster, the analysis of sex-biased microRNAs (short noncoding regulatory molecules) has revealed striking differences with protein-coding genes. Mainly, the X chromosome is enriched in male-biased microRNA genes, although it is depleted of male-biased protein-coding genes. The paucity of male-biased genes in the X chromosome is generally explained by an evolutionary process called demasculinization. I suggest that the excess of male-biased microRNAs in the X chromosome is due to high rates of de novo emergence of microRNAs (mostly in other neighboring microRNAs), a tendency of novel microRNAs in the X chromosome to be expressed in testis, and to a lack of a demasculinization process. To test this hypothesis, I analyzed the expression profile of microRNAs in males, females, and gonads in D. pseudoobscura, in which an autosome translocated into the X chromosome effectively becoming part of a sex chromosome (neo-X). I found that the pattern of sex-biased expression is generally conserved between D. melanogaster and D. pseudoobscura. Also, orthologous microRNAs in both species conserve their chromosomal location, indicating that there is no evidence of demasculinization or other interchromosomal movement of microRNAs. Drosophila pseudoobscura-specific microRNAs in the neo-X chromosome tend to be male-biased and particularly expressed in testis. In summary, the apparent paradox resulting from male-biased protein-coding genes depleted in the X chromosome and an enrichment in male-biased microRNAs is consistent with different evolutionary dynamics between coding genes and short RNAs.

Effects of the neo-X chromosome on genomic signatures of hybridization in Rumex hastatulus.

Natural hybrid zones provide opportunities for studies of the evolution of reproductive isolation in wild populations. Although recent investigations have found that the formation of neo-sex chromosomes is associated with reproductive isolation, the mechanisms remain unclear in most cases. Here, we assess the contemporary structure of gene flow in the contact zone between largely allopatric cytotypes of the dioecious plant Rumex hastatulus, a species with evidence of sex chromosome turn-over. Males to the west of the Mississippi river, USA, have an X and a single Y chromosome, whereas populations to the east of the river have undergone a chromosomal rearrangement giving rise to a larger X and two Y chromosomes. Using reduced-representation sequencing, we provide evidence that hybrids form readily and survive multiple backcross generations in the field, demonstrating the potential for ongoing gene flow between the cytotypes. Cline analysis of each chromosome separately captured no signals of difference in cline shape between chromosomes. However, principal component regression revealed a significant increase in the contribution of individual SNPs to inter-cytotype differentiation on the neo-X chromosome, but no correlation with recombination rate. Cline analysis revealed that the only SNPs with significantly steeper clines than the genome average were located on the neo-X. Our data are consistent with a role for neo-sex chromosomes in reproductive isolation between R.hastatulus cytotypes. Our investigation highlights the importance of studying plant hybrid zones for understanding the evolution of sex chromosomes.

The emergence of a new sex-system (XX/XY1Y2) suggests a species complex in the “monotypic” rodent Oecomys auyantepui (Rodentia, Sigmodontinae)

X-autosome translocation (XY1Y2) has been reported in distinct groups of vertebrates suggesting that the rise of a multiple sex system within a species may act as a reproductive barrier and lead to speciation. The viability of this system has been linked with repetitive sequences located between sex and autosomal portions of the translocation. Herein, we investigate Oecomys auyantepui, using chromosome banding and Fluorescence In Situ Hybridization with telomeric and Hylaeamys megacephalus whole-chromosome probes, and phylogenetic reconstruction using mtDNA and nuDNA sequences. We describe an amended karyotype for O. auyantepui (2n = 64♀65♂/FNa = 84) and report for the first time a multiple sex system (XX/XY1Y2) in Oryzomyini rodents. Molecular data recovered O. auyantepui as a monophyletic taxon with high support and cytogenetic data indicate that O. auyantepui may exist in two lineages recognized by distinct sex systems. The Neo-X exhibits repetitive sequences located between sex and autosomal portions, which would act as a boundary between these two segments. The G-banding comparisons of the Neo-X chromosomes of other Sigmodontinae taxa revealed a similar banding pattern, suggesting that the autosomal segment in the Neo-X can be shared among the Sigmodontinae lineages with a XY1Y2 sex system.

X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes.

The sequence diversity of natural and laboratory populations of Brugia pahangi and Brugia malayi was assessed with Illumina resequencing followed by mapping in order to identify single nucleotide variants and insertions/deletions. In natural and laboratory Brugia populations, there is a lack of sequence diversity on chromosome X relative to the autosomes (πX/πA = 0.2), which is lower than the expected (πX/πA = 0.75). A reduction in diversity is also observed in other filarial nematodes with neo-X chromosome fusions in the genera Onchocerca and Wuchereria, but not those without neo-X chromosome fusions in the genera Loa and Dirofilaria. In the species with neo-X chromosome fusions, chromosome X is abnormally large, containing a third of the genetic material such that a sizable portion of the genome is lacking sequence diversity. Such profound differences in genetic diversity can be consequential, having been associated with drug resistance and adaptability, with the potential to affect filarial eradication.

Chromosome-level genome assembly reveals genomic architecture of northern range expansion in the mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae).

Genome sequencing methods and assembly tools have improved dramatically since the 2013 publication of draft genome assemblies for the mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae). We conducted proximity ligation library sequencing and scaffolding to improve contiguity, and then used linkage mapping and recent bioinformatic tools for correction and further improvement. The new assemblies have dramatically improved contiguity and gaps compared to the originals: N50values increased 26- to 36-fold, and the number of gaps were reduced by half. Ninety per cent of the content of the assemblies is now contained in 12 and 11scaffolds for the female and male assemblies, respectively. Based on linkage mapping information, the 12largest scaffolds in both assemblies represent all 11 autosomal chromosomes and the neo-X chromosome. These assemblies now have nearly chromosome-sized scaffolds and will be instrumental for studying genomic architecture, chromosome evolution, population genomics, functional genomics, and adaptation in this and other pest insects. We also identified regions in two chromosomes, including the ancestral-X portion of the neo-X chromosome, with elevated differentiation between northern and southern Canadian populations.

Epigenetics drive the evolution of sex chromosomes in animals and plants.

We review how epigenetics affect sex chromosome evolution in animals and plants. In a few species, sex is determined epigenetically through the action of Y-encoded small RNAs. Epigenetics is also responsible for changing the sex of individuals through time, even in species that carry sex chromosomes, and could favour species adaptation through breeding system plasticity. The Y chromosome accumulates repeats that become epigenetically silenced which leads to an epigenetic conflict with the expression of Y genes and could accelerate Y degeneration. Y heterochromatin can be lost through ageing, which activates transposable elements and lowers male longevity. Y chromosome degeneration has led to the evolution of meiotic sex chromosome inactivation in eutherians (placentals) and marsupials, and dosage compensation mechanisms in animals and plants. X-inactivation convergently evolved in eutherians and marsupials via two independently evolved non-coding RNAs. In Drosophila, male X upregulation by the male specific lethal (MSL) complex can spread to neo-X chromosomes through the transposition of transposable elements that carry an MSL-binding motif. We discuss similarities and possible differences between plants and animals and suggest future directions for this dynamic field of research. This article is part of the theme issue 'How does epigenetics influence the course of evolution?'

Karyotypes diversity in some Iranian Pamphagidae grasshoppers (Orthoptera, Acridoidea, Pamphagidae): new insights on the evolution of the neo-XY sex chromosomes

For the first time, cytogenetic features of grasshoppers from Iran have been studied. In this paper we conducted a comparative cytogenetic analysis of six species from the family Pamphagidae. The species studied belong to subfamilies Thrinchinae Stål, 1876 (Eremopeza bicoloripes (Moritz, 1928), E. saussurei (Uvarov, 1918)) and Pamphaginae (Saxetania paramonovi (Dirsh, 1927), Tropidauchen escalerai Bolívar, 1912, Tropidauchen sp., and Paranothrotes citimus Mistshenko, 1951). We report information about the chromosome number and morphology, C-banding patterns, and localization of ribosomal DNA clusters and telomeric (TTAGG)n repeats. Among these species, only S. paramonovi had an ancestral Pamphagidae karyotype (2n=18+X0♂; FN=19♂). The karyotypes of the remaining species differed from the ancestral karyotypes. The karyotypes of E. bicoloripes and E. saussurei, despite having the same chromosome number (2n=18+X0♂) had certain biarmed chromosomes (FN=20♂ and FN=34♂ respectively). The karyotypes of T. escalerai and Tropidauchen sp. consisted of eight pairs of acrocentric autosomes, one submetacentric neo-X chromosome and one acrocentric neo-Y chromosome in males (2n=16+neo-X neo-Y♂). The karyotype of P. citimus consisted of seven pairs of acrocentric autosomes, submetacentric the neo-X1 and neo-Y and acrocentric the neo-X2 chromosomes (2n=14+neo-X1 neo-X2 neo-Y♂). Comparative analysis of the localization and size of C-positive regions, the position of ribosomal clusters and the telomeric DNA motif in the chromosomes of the species studied, revealed early unknown features of their karyotype evolution. The data obtained has allowed us to hypothesize that the origin and early phase of evolution of the neo-Xneo-Y♂ sex chromosome in the subfamily Pamphaginae, are linked to the Iranian highlands.

Complex Evolutionary History of the Y Chromosome in Flies of the Drosophila obscura Species Group.

The Drosophila obscura species group shows dramatic variation in karyotype, including transitions among sex chromosomes. Members of the affinis and pseudoobscura subgroups contain a neo-X chromosome (a fusion of the X with an autosome), and ancestral Y genes have become autosomal in species harboring the neo-X. Detailed analysis of species in the pseudoobscura subgroup revealed that ancestral Y genes became autosomal through a translocation to the small dot chromosome. Here, we show that the Y-dot translocation is restricted to the pseudoobscura subgroup, and translocation of ancestral Y genes in the affinis subgroup likely followed a different route. We find that most ancestral Y genes have translocated to unique autosomal or X-linked locations in different taxa of the affinis subgroup, and we propose a dynamic model of sex chromosome formation and turnover in the obscura species group. Our results suggest that Y genes can find unique paths to escape unfavorable genomic environments that form after sex chromosome–autosome fusions.

Chromosome-Level Assembly of Drosophila bifasciata Reveals Important Karyotypic Transition of the X Chromosome

The Drosophila obscura species group is one of the most studied clades of Drosophila and harbors multiple distinct karyotypes. Here we present a de novo genome assembly and annotation of D. bifasciata, a species which represents an important subgroup for which no high-quality chromosome-level genome assembly currently exists. We combined long-read sequencing (Nanopore) and Hi-C scaffolding to achieve a highly contiguous genome assembly approximately 193 Mb in size, with repetitive elements constituting 30.1% of the total length. Drosophila bifasciata harbors four large metacentric chromosomes and the small dot, and our assembly contains each chromosome in a single scaffold, including the highly repetitive pericentromeres, which were largely composed of Jockey and Gypsy transposable elements. We annotated a total of 12,821 protein-coding genes and comparisons of synteny with D. athabasca orthologs show that the large metacentric pericentromeric regions of multiple chromosomes are conserved between these species. Importantly, Muller A (X chromosome) was found to be metacentric in D. bifasciata and the pericentromeric region appears homologous to the pericentromeric region of the fused Muller A-AD (XL and XR) of pseudoobscura/affinis subgroup species. Our finding suggests a metacentric ancestral X fused to a telocentric Muller D and created the large neo-X (Muller A-AD) chromosome ∼15 MYA. We also confirm the fusion of Muller C and D in D. bifasciata and show that it likely involved a centromere-centromere fusion.

Identification of two independent X-autosome translocations in closely related mammalian (Proechimys) species

Multiple sex chromosome systems have been described for several mammalian orders, with different species from the same genus sharing the same system (e.g., X1X2Y or XY1Y2). This is important because the translocated autosome may be influenced by the evolution of the recipient sex chromosome, and this may be related to speciation. It is often thought that the translocation of an autosome to a sex chromosome may share a common origin among phylogenetically related species. However, the neo-X chromosomes of Proechimys goeldii (2n = 24♀, 25♂/NFa = 42) and Proechimys gr. goeldii (2n = 16♀, 17♂/NFa = 14) have distinct sizes and morphologies that have made it difficult to determine whether they have the same or different origins. This study investigates the origins of the XY1Y2 sex chromosome determination system in P. goeldii (PGO) and P. gr. goeldii (PGG) and elucidates the chromosomal rearrangements in this low-diploid-number group of Proechimys species. Toward this end, we produced whole-chromosome probes for P. roberti (PRO; 2n = 30♂/NFa = 54) and P. goeldii (2n = 25♂/NFa = 42) and used them in comparative chromosomal mapping. Our analysis reveals that multiple translocations and inversions are responsible for the karyotype diversity of these species, with only three whole-chromosomes conserved between PRO and PGO and eight between PGO and PGG. Our data indicate that multiple sex chromosome systems have originated twice in Proechimys. As small populations are prone to the fixation of chromosomal rearrangements, we speculate that biological features of Rodentia contribute to this fixation. We also highlight the potential of these rodents as a model for studying sex chromosome evolution.

Gene-by-Gene or Localized Dosage Compensation on the Neo-X Chromosome in Drosophila miranda.

Many organisms have a global mechanism for dosage compensation (DC) operating along the entire male X chromosome, which equalizes gene expression on the male X with that on the two Xs in females and/or on autosomes. At the initial stage of sex chromosome evolution, however, gene-by-gene (or localized) DC may also be necessary because the degeneration of Y-linked genes occurs independently at different times. We therefore tested whether the up-regulation of X-linked genes depends on the status of their Y-linked homologs, using the young sex chromosomes, neo-X and neo-Y, in Drosophila miranda. In support of the presence of gene-by-gene DC, the extent of up-regulation in males was indeed higher for neo-X-linked genes with pseudogenized neo-Y-linked homologs than for neo-X-linked genes with functional neo-Y-linked homologs. Further molecular evolutionary analysis also supports the idea that many individual neo-X-linked genes first acquired the potential for up-regulation, which then enabled the pseudogenization of neo-Y-linked homologs, without serious deleterious effects on male fitness.

Uncovering the evolutionary history of neo-XY sex chromosomes in the grasshopper Ronderosia bergii (Orthoptera, Melanoplinae) through satellite DNA analysis

BackgroundNeo-sex chromosome systems arose independently multiple times in evolution, presenting the remarkable characteristic of repetitive DNAs accumulation. Among grasshoppers, occurrence of neo-XY was repeatedly noticed in Melanoplinae. Here we analyzed the most abundant tandem repeats of R. bergii (2n = 22, neo-XY♂) using deep Illumina sequencing and graph-based clustering in order to address the neo-sex chromosomes evolution.ResultsThe analyses revealed ten families of satDNAs comprising about ~1% of the male genome, which occupied mainly C-positive regions of autosomes. Regarding the sex chromosomes, satDNAs were recorded within centromeric or interstitial regions of the neo-X chromosome and four satDNAs occurred in the neo-Y, two of them being exclusive (Rber248 and Rber299). Using a combination of probes we uncovered five well-defined cytological variants for neo-Y, originated by multiple paracentric inversions and satDNA amplification, besides fragmented neo-Y. These neo-Y variants were distinct in frequency between embryos and adult males.ConclusionsThe genomic data together with cytogenetic mapping enabled us to better understand the neo-sex chromosome dynamics in grasshoppers, reinforcing differentiation of neo-X and neo-Y and revealing the occurrence of multiple additional rearrangements involved in the neo-Y evolution of R. bergii. We discussed the possible causes that led to differences in frequency for the neo-Y variants between embryos and adults. Finally we hypothesize about the role of DNA satellites in R. bergii as well as putative historical events involved in the evolution of the R. bergii neo-XY.

Unique XCI evolution in Tokudaia: initial XCI of the neo-X chromosome in Tokudaia muenninki and function loss of XIST in Tokudaia osimensis.

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.

Accelerated pseudogenization on the neo-X chromosome in Drosophila miranda.

Y chromosomes often degenerate via the accumulation of pseudogenes and transposable elements. By contrast, little is known about X-chromosome degeneration. Here we compare the pseudogenization process between genes on the neo-sex chromosomes in Drosophila miranda and their autosomal orthologues in closely related species. The pseudogenization rate on the neo-X is much lower than the rate on the neo-Y, but appears to be higher than the rate on the orthologous autosome in D. pseudoobscura. Genes under less functional constraint and/or genes with male-biased expression tend to become pseudogenes on the neo-X, indicating the accumulation of slightly deleterious mutations and the feminization of the neo-X. We also find a weak trend that the genes with female-benefit/male-detriment effects identified in D. melanogaster are pseudogenized on the neo-X, implying the masculinization of the neo-X. These observations suggest that both X and Y chromosomes can degenerate due to a complex suite of evolutionary forces.

Extremely low nucleotide diversity in the X-linked region of papaya caused by a strong selective sweep.

BackgroundThe papaya Y-linked region showed clear population structure, resulting in the detection of the ancestral male population that domesticated hermaphrodite papayas were selected from. The same populations were used to study nucleotide diversity and population structure in the X-linked region.ResultsDiversity is very low for all genes in the X-linked region in the wild dioecious population, with nucleotide diversity π syn = 0.00017, tenfold lower than the autosomal region (π syn = 0.0017) and 12-fold lower than the Y-linked region (π syn = 0.0021). Analysis of the X-linked sequences shows an undivided population, suggesting a geographically wide diversity-reducing event, whereas two subpopulations were observed in the autosomes separating gynodioecy and dioecy and three subpopulations in the Y-linked region separating three male populations. The extremely low diversity in the papaya X-linked region was probably caused by a recent, strong selective sweep before domestication, involving either the spread of a recessive mutation in an X-linked gene that is beneficial to males or a partially dominant mutation that benefitted females or both sexes. Nucleotide diversity in the domesticated X samples is about half that in the wild Xs, probably due to the bottleneck when hermaphrodites were selected during domestication.ConclusionsThe extreme low nucleotide diversity in the papaya X-linked region is much greater than observed in humans, great apes, and the neo-X chromosome of Drosophila miranda, which show the expected pattern of Y-linked genes < X-linked genes < autosomal genes; papaya shows an unprecedented pattern of X-linked genes < autosomal genes < Y-linked genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-1095-9) contains supplementary material, which is available to authorized users.

Sex chromosome diversity in Armenian toad grasshoppers (Orthoptera, Acridoidea, Pamphagidae).

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.

Ancient Male Recombination Shaped Genetic Diversity of Neo-Y Chromosome in Drosophila albomicans.

Researchers studying Y chromosome evolution have drawn attention to neo-Y chromosomes in Drosophila species due to their resembling the initial stage of Y chromosome evolution. In the studies of neo-Y chromosome of Drosophila miranda, the extremely low genetic diversity observed suggested various modes of natural selection acting on the nonrecombining genome. However, alternative possibility may come from its peculiar origin from a single chromosomal fusion event with male achiasmy, which potentially caused and maintained the low genetic diversity of the neo-Y chromosome. Here, we report a real case where a neo-Y chromosome is in transition from an autosome to a typical Y chromosome. The neo-Y chromosome of Drosophila albomicans harbored a rich genetic diversity comparable to its gametologous neo-X chromosome and an autosome in the same genome. Analyzing sequence variations in 53 genes and measuring recombination rates between pairs of loci by cross experiments, we elucidated the evolutionary scenario of the neo-Y chromosome of D. albomicans having high genetic diversity without assuming selective force, i.e., it originated from a single chromosomal fusion event, experienced meiotic recombination during the initial stage of evolution and diverged from neo-X chromosome by the suppression of recombination tens or a few hundreds of thousand years ago. Consequently, the observed high genetic diversity on the neo-Y chromosome suggested a strong effect of meiotic recombination to introduce genetic variations into the newly arisen sex chromosome.