Gene-Level,but Not Chromosome-Wide,Divergence between a Very Young House Fly Proto-Y Chromosome and Its Homologous Proto-X Chromosome

X and Y chromosomes are usually derived from a pair of homologous autosomes, which then diverge from each other over time. Although Y-specific features have been characterized in sex chromosomes of various ages, the earliest stages of Y chromosome evolution remain elusive. In particular, we do not know whether early stages of Y chromosome evolution consist of changes to individual genes or happen via chromosome-scale divergence from the X. To address this question, we quantified divergence between young proto-X and proto-Y chromosomes in the house fly, Musca domestica. We compared proto-sex chromosome sequence and gene expression between genotypic (XY) and sex-reversed (XX) males. We find evidence for sequence divergence between genes on the proto-X and proto-Y, including five genes with mitochondrial functions. There is also an excess of genes with divergent expression between the proto-X and proto-Y, but the number of genes is small. This suggests that individual proto-Y genes, but not the entire proto-Y chromosome, have diverged from the proto-X. We identified one gene, encoding an axonemal dynein assembly factor (which functions in sperm motility), that has higher expression in XY males than XX males because of a disproportionate contribution of the proto-Y allele to gene expression. The upregulation of the proto-Y allele may be favored in males because of this gene’s function in spermatogenesis. The evolutionary divergence between proto-X and proto-Y copies of this gene, as well as the mitochondrial genes, is consistent with selection in males affecting the evolution of individual genes during early Y chromosome evolution.     

Deep ancestry of mammalian X chromosome revealed by comparison with the basal tetrapod Xenopus tropicalis

ABSTRACT: BACKGROUND: The X and Y sex chromosomes are conspicuous features of placental mammal genomes. Mammalian sex chromosomes arose from an ordinary pair of autosomes after the proto-Y acquired a male-determining gene and degenerated due to suppression of X-Y recombination. Analysis of earlier steps in X chromosome evolution has been hampered by the long interval between the origins of teleost and amniote lineages as well as scarcity of X chromosome orthologs in incomplete avian genome assemblies. RESULTS: This study clarifies the genesis and remodelling of the X chromosome by using a combination of sequence analysis, meiotic map information, and cytogenetic localization to compare amniote genome organization with that of the amphibian Xenopus tropicalis. Nearly all orthologs of human X genes localize to X. tropicalis chromosomes 2 and 8, consistent with an ancestral X-conserved region and a single X-added region precursor. This finding contradicts a previous hypothesis of three evolutionary strata in this region. Homologies between human, opossum, chicken and frog chromosomes suggest a single X-added region predecessor in therian mammals, corresponding to opossum chromosomes 4 and 7. A more ancient X-added ancestral region, currently extant as a major part of chicken chromosome 1, is likely to have been present in the progenitor of synapsids and sauropsids. Analysis of X chromosome gene content emphasizes conservation of single protein coding genes and the role of tandem arrays in formation of novel genes. CONCLUSIONS: Chromosomal regions orthologous to Therian X chromosomes have been located in the genome of the frog X. tropicalis. These ancestral components experienced a series of fusion and breakage events to give rise to avian autosomes and mammalian sex chromosomes. The early branching tetrapod X. tropicalis' simple diploid genome and robust synteny to amniotes greatly enhances studies of vertebrate chromosome evolution.     

Recombination is suppressed and variability reduced in a nascent Y chromosome

Several hypotheses have been elaborated to account for the evolutionary decay commonly observed in full-fledged Y chromosomes. Enhanced drift, background selection and selective sweeps, which are expected to result from reduced recombination, may all share responsibilities in the initial decay of proto-Y chromosomes, but little empirical information has been gathered so far. Here we take advantage of three markers that amplify on both of the morphologically undifferentiated sex chromosomes of the European tree frog (Hyla arborea) to show that recombination is suppressed in males (the heterogametic sex) but not in females. Accordingly, genetic variability is reduced on the Y, but in a way that can be accounted for by merely the number of chromosome copies per breeding pair, without the need to invoke background selection or selective sweeps.     

Contrasting patterns of molecular evolution of the genes on the new and old sex chromosomes of Drosophila miranda

In organisms with chromosomal sex determination, sex is determined by a set of dimorphic sex chromosomes that are thought to have evolved from a set of originally homologous chromosomes. The chromosome inherited only through the heterogametic sex (the Y chromosome in the case of male heterogamety) often exhibits loss of genetic activity for most of the genes carried on its homolog and is hence referred to as degenerate. The process by which the proto-Y chromosome loses its genetic activity has long been the subject of much speculation. We present a DNA sequence variation analysis of marker genes on the evolving sex chromosomes (neo-sex chromosomes) of Drosophila miranda. Due to its relatively recent origin, the neo-Y chromosome of this species is presumed to be still experiencing the forces responsible for the loss of its genetic activity. Indeed, several previous studies have confirmed the presence of some active loci on this chromosome. The genes on the neo-Y chromosome surveyed in the current study show generally lower levels of variation compared with their counterparts on the neo-X chromosome or an X-linked gene. This is in accord with a reduced effective population size of the neo-Y chromosome. Interestingly, the rate of replacement nucleotide substitutions for the neo-Y linked genes is significantly higher than that for the neo-X linked genes. This is not expected under a model where the faster evolution of the X chromosome is postulated to be the main force driving the degeneration of the Y chromosome.     

Reduced levels of microsatellite variability on the neo-Y chromosome of Drosophila miranda

BACKGROUND: In many species, sex is determined by a system involving X and Y chromosomes, the latter having lost much of their genetic activity. Sex chromosomes have evolved independently many times, and several different mechanisms responsible for the degeneration of the Y chromosome have been proposed. Here, we have taken advantage of the secondary sex chromosome pair in Drosophila miranda to test for the effects of evolutionary forces involved in the early stages of Y-chromosome degeneration. Because of a fusion of one of the autosomes to the Y chromosome, a neo-Y chromosome and a neo-X chromosome have been formed, resulting in the transmission of formerly autosomal genes in association with the sex chromosomes. RESULTS: We found a 25-fold lower level of variation at microsatellites located on the neo-Y chromosome compared with homologous loci on the neo-X chromosome, or with autosomal and X-linked microsatellites. Sequence analyses of the region flanking the microsatellites suggested that the neo-sex chromosomes originated about 1 million years ago. CONCLUSIONS: Variability of the neo-Y chromosome of D. miranda is substantially reduced below expectations at mutation-drift equilibrium. Such a reduction is predicted by theories of the degeneration of the Y chromosome. Another possibility is that there is little or no mutation at microsatellite loci on a non-recombining chromosome such as the neo-Y, but this seems inconsistent with other data.     

A dynamic view of sex chromosome evolution

Sex chromosomes are derived from ordinary autosomes. The X chromosome is thought to maintain most of its ancestral genes over evolutionary time, whereas its Y counterpart degenerates, owing to its lack of recombination. Genomic analyses of young sex chromosome pairs support this view and have shed light on the evolutionary processes underlying loss of gene function on the Y. Studies of ancestral sex chromosomes, however, have also revealed that the process of sex chromosome evolution can be more dynamic than traditionally appreciated. In particular, ancient Y-chromosomes are characterized not only by a loss of genes relative to the X but also by recurrent gains of individual genes or genomic regions, and they often accumulate genes beneficial to males. Furthermore, X chromosomes are not passive players in this evolutionary process but respond both to their sex-biased transmission and to Y-chromosome degeneration, through feminization and the evolution of dosage compensation.     

植物性染色体进化及性别决定基因研究进展

植物性染色体起源于1对常染色体, 其在不同雌雄异株植物中多次起源并独立演变, 是研究性染色体起源和进化机制的理想材料。过去的研究在一定程度上阐明了植物性染色体的起源和演化动力; 且性染色体遗传退化、性别决定基因以及剂量补偿效应正逐渐成为研究的热点。近年来, 关于植物性染色体进化及性别决定基因的研究取得了一些重要进展。该文综述了植物性染色体的起源、进化、遗传退化、剂量补偿效应以及性别决定基因等, 并对植物性染色体进化研究发展趋势进行了展望。     

Evolution of Sex Determination and Sex Chromosomes: A Novel Alternative Paradigm

Sex chromosomes can differ between species as a result of evolutionary turnover, a process that can be driven by evolution of the sex determination pathway. Canonical models of sex chromosome turnover hypothesize that a new master sex determining gene causes an autosome to become a sex chromosome or an XY chromosome pair to switch to a ZW pair (or vice versa). Here, a novel paradigm for the evolution of sex determination and sex chromosomes is presented, in which there is an evolutionary transition in the master sex determiner, but the X chromosome remains unchanged. There are three documented examples of the novel paradigm, and it is hypothesized that a similar process could happen in a ZW sex chromosome system. Three other taxa are also identified where the novel paradigm may have occurred, and how it could be distinguished from canonical trajectories in these and additional taxa is also described.     

Chromosome banding in amphibia

The distribution of constitutive heterochromatin on the chromosomes of Triturus a. alpestris, T. v. vulgaris and T. h. helveticus (Amphibia, Urodela) was investigated. Sex-specific chromosomes were determined in the karyotypes of T. a. alpestris (chromosomes 4) and T. v. vulgaris (chromosomes 5). The male animals have one heteromorphic chromosome pair, of which only one homologue displays heterochromatic telomeres in the long arms; the telomeres of the other homologue are euchromatic. This chromosome pair is always homomorphic and without telomeric heterochromatin in the female animals. There is a highly reduced crossing-over frequency between the heteromorphic chromosome arms in the male meiosis of T. a. alpestris; in T. v. vulgaris no crossing-over at all occurs between the heteromorphic chromosome arms. No heteromorphisms between the homologues exist on the corresponding lampbrush chromosomes of the female meiosis. In T. h. helveticus no sex-specific heteromorphism of the constitutive heterochromatin could be determined. The male animals of this species, however, already possess a chromosome pair with a greatly reduced frequency of chiasma-formation in the long arms. The C-band patterns and the pairing configurations of the sex-specific chromosomes in the male meiosis indicate an XX/XY-type of sex-determination for the three species. A revision of the literature about experimental interspecies hybridizations, gonadic structure of haploid and polyploid animals, and sex-linked genes yielded further evidence in favor of male heterogamety. The results moreover suggest that the heterochromatinization of the Y-chromosome was the primary step in the evolution of the sex chromosomes.     

Sex Determination in the Fly Megaselia Scalaris, a Model System for Primary Steps of Sex Chromosome Evolution

The fly Megaselia scalaris Loew possesses three homomorphic chromosome pairs; 2 is the sex chromosome pair in two wild-type laboratory stocks of different geographic origin (designated ``original' sex chromosome pair in this paper). The primary male-determining function moves at a very low rate to other chromosomes, thereby creating new Y chromosomes. Random amplified polymorphic DNA markers obtained by polymerase chain reaction with single decamer primers and a few available phenotypic markers were used in testcrosses to localize the sex-determining loci and to define the new sex chromosomes. Four cases are presented in which the primary male-determining function had been transferred from the original Y chromosome to a new locus either on one of the autosomes or on the original X chromosome, presumably by transposition. In these cases, the sex-determining function had moved to a different locus without an obvious cotransfer of other Y chromosome markers. Thus, with Megaselia we are afforded an experimental system to study the otherwise hypothetical primary stages of sex chromosome evolution. An initial molecular differentiation is apparent even in the new sex chromosomes. Molecular differences between the original X and Y chromosomes illustrate a slightly more advanced stage of sex chromosome evolution.     

Gender in plants: sex chromosomes are emerging from the fog

Although most plants have flowers with both male and female sex organs, there are several thousands of plant species where male or female flowers form on different individuals. Surprisingly, the presence of well-established sex chromosomes in these dioecious plants is rare. The best-described example is white campion, for which large sex chromosomes have been identified and mapped partially. A recent study presented a comprehensive genetic and physical mapping of the genome of dioecious papaya. It revealed a short male specific region on the Y chromosome (MSY) that does not recombine with the X chromosome, providing strong evidence that the sex chromosomes originated from a regular pair of autosomes. The primitive papaya Y chromosome thus represents an early event in sex chromosome evolution. In this article, we review the current status of plant sex-chromosome research and discuss the advantages of different dioecious models.     

A new look at the evolution of avian sex chromosomes

Birds have a ubiquitous, female heterogametic, ZW sex chromosome system. The current model suggests that the Z chromosome and its degraded partner, the W chromosome, evolved from an ancestral pair of autosomes independently from the mammalian XY male heteromorphic sex chromosomes--which are similar in size, but not gene content (Graves, 1995; Fridolfsson et al., 1998). Furthermore the degradation of the W has been proposed to be progressive, with the basal clade of birds (the ratites) possessing virtually homomorphic sex chromosomes and the more recently derived birds (the carinates) possessing highly heteromorphic sex chromosomes (Ohno, 1967; Solari, 1993). Recent findings have suggested an alternative to independent evolution of bird and mammal chromosomes, in which an XY system took over directly from an ancestral ZW system. Here we examine recent research into avian sex chromosomes and offer alternative suggestions as to their evolution.     

虫草蝙蝠蛾的有丝分裂染色体特性

本文首次报道虫草蝠蛾(鳞翅目,蝙蝠蛾科,蝠蛾属)的有丝分裂染色体核型。应用醋酸分离和热干燥技术,研究了云南的两种虫草蝠蛾Hepialus zhayuensis Chu et Wang和Hepialus sp.的有丝分裂染色体,它们的染色体数目为2n=64。在有丝分裂的早中期染色体上清晰地呈现出散漫着丝粒。然而,分裂中期和较晚的中期阶段,每条染色体都具显著的初级着丝粒(即主缢痕)。它们的雄性中期核型中都有一对典型的异形性染色体,X染色体着色稍淡,且都具中或亚中着丝粒;Y染色体比X染色体长,染色很深。 在雄性的分裂间期细胞中,观察到异固缩性染色质体,此异固缩体是Y染色体。     

Parallel divergence and degradation of the avian W sex chromosome

Sex chromosomes are ubiquitous in birds but our understanding of how they originated and evolved has remained incomplete. Recent work by Tsuda et al. on tinamou and ratite birds suggests that, although all bird sex chromosomes evolved from the same pair of autosomes, the Z and W sex chromosomes have diverged from one another several times independently. This parallel evolution of the avian W presents a means for comparison in studies of sex chromosome evolution, which could help us understand more about the general forces that shape the development of all types of sex chromosome.     

Genetics of sex determination in flowering plants

Most flowering plant species are hermaphroditic, but a small number of species in most plant families are unisexual (i.e., an individ-ual will produce only male or female gametes). Because species with unisexual flowers have evolved repeatedly from hermaphroditic progenitors, the mechanisms controlling sex determination in flowering plants are extremely diverse. Sex is most strongly determined by genotype in all species but the mechanisms range from a single controlling locus to sex chromosomes bearing several linked locirequired for sex determination. Plant hormones also influence sex expression with variable effects from species to species. Here, we review the genetic control of sex determination from a number of plant species to illustrate the variety of extant mechanisms. We emphasize species that are now used as models to investigate the molecular biology of sex determination. We also present our own investigations of the structure of plant sex chromosomes of white campion (Silene latifolia - Melan-drium album). The cytogenetic basis of sex determination in white campion is similar to mammals in that it has a male-specific Y-chromosome that carries dominant male determining genes. If one copy of this chromosome is in the genome, the plant is male. Otherwise it is female. Like mammalian Y-chromosomes, the white campion Y-chromosome is rich in repetitive DNA. We isolated repetitive sequences from microdissected Y-chromosomes of white campion to study the distribution of homologous repeated sequences on the Y-chromosome and the other chromosomes. We found the Y to be especially rich in repetitive sequences that were generally dispersed over all the white campion chromosomes. Despite its repetitive character, the Y-chromosome is mainly euchromatic. This may be due to the relatively recent evolution of the white campion sex chromosomes compared to the sex chromosomes of animals. © 1994 Wiley-Liss, Inc.     

Sequence differentiation associated with an inversion on the neo-X chromosome of Drosophila americana

Sex chromosomes originate from pairs of autosomes that acquire controlling genes in the sex-determining cascade. Universal mechanisms apparently influence the evolution of sex chromosomes, because this chromosomal pair is characteristically heteromorphic in a broad range of organisms. To examine the pattern of initial differentiation between sex chromosomes, sequence analyses were performed on a pair of newly formed sex chromosomes in Drosophila americana. This species has neo-sex chromosomes as a result of a centromeric fusion between the X chromosome and an autosome. Sequences were analyzed from the Alcohol dehydrogenase (Adh), big brain (bib), and timeless (tim) gene regions, which represent separate positions along this pair of neo-sex chromosomes. In the northwestern range of the species, the bib and Adh regions exhibit significant sequence differentiation for neo-X chromosomes relative to neo-Y chromosomes from the same geographic region and other chromosomal populations of D. americana. Furthermore, a nucleotide site defining a common haplotype in bib is shown to be associated with a paracentric inversion [In(4)ab] on the neo-X chromosome, and this inversion suppresses recombination between neo-X and neo-Y chromosomes. These observations are consistent with the inversion acting as a recombination modifier that suppresses exchange between these neo-sex chromosomes, as predicted by models of sex chromosome evolution.     

Molecular and evolutionary analysis of a plant Y chromosome.

Plants have evolved a great diversity of sex determination systems. Among these, the XY system, also found in mammals, is one of the most exciting since it gives the opportunity to compare the evolution of sex chromosomes in two different kingdoms. Whereas genetic and molecular mechanisms controlling sex determination in drosophila and mammals, have been well studied, very little is known about such processes in plants. White campion (Silene latifolia) is an example of plant with X and Y chromosomes. What is the origin of the X and Y chromosomes? How did they evolve from a pair of autosomes? In our laboratory, we have isolated the first active genes located on a plant Y chromosome. We are using them as markers to trace the origin and evolution of sex chromosomes in the Silene genus.     

Microdissection and painting of the Y chromosome in spinach (Spinacia oleracea)

Spinach has long been used as a model for genetic and physiological studies of sex determination and expression. Although trisomic analysis from a cross between diploid and triploid plants identified the XY chromosome as the largest chromosome, no direct evidence has been provided to support this at the molecular level. In this study, the largest chromosomes of spinach from mitotic metaphase spreads were microdissected using glass needles. Degenerate oligonucleotide primed polymerase chain reaction was used to amplify the dissected chromosomes. The amplified products from the Y chromosome were identified using the male-specific marker T11A. For the first time, the largest spinach chromosome was confirmed to be a sex chromosome at the molecular level. PCR products from the isolated chromosomes were used in an in situ probe mixture for painting the Y chromosome. The fluorescence signals were mainly distributed on all chromosomes and four pair of weaker punctate fluorescence signal sites were observed on the terminal region of two pair of autosomes. These findings provide a foundation for the study of sex chromosome evolution in spinach.     

转座子在植物XY性染色体起源与演化过程中的作用

XY性染色体决定系统是决定植物性别的主要方式,但是对于其起源与演化机制却知之甚少。目前认为,携带控制雌蕊或雄蕊发育基因的一对常染色体由于某种未知原因的突变形成早期的neo-Y或neo-X性染色体,随着演化的进行,早期XY性染色体之间的重组逐渐受到抑制,非重组区域扩展最终形成异型的性染色体。研究发现,重复序列的累积以及DNA甲基化等因素都可能参与了XY性染色体的异染色质化、重组抑制及Y染色体体积增大过程。转座子作为一种基因组中含量最高的重复序列在性染色体演化中扮演了重要的角色,包括性染色体演化的起始激发,以及导致性染色体局部表观遗传修饰使其发生异染色质化扩展和重组抑制。文章综述了转座子在植物性染色体上的累积及其与性染色体异染色质化之间的关系,并简要分析了转座子在性染色体演化过程中的作用。     

Multicolor FISH mapping of the dioecious model plant,<Emphasis Type="Italic"> Silene latifolia</Emphasis>

Silene latifolia is a key plant model in the study of sex determination and sex chromosome evolution. Current studies have been based on genetic mapping of the sequences linked to sex chromosomes with analysis of their characters and relative positions on the X and Y chromosomes. Until recently, very few DNA sequences have been physically mapped to the sex chromosomes of S. latifolia. We have carried out multicolor fluorescent in situ hybridization (FISH) analysis of S. latifolia chromosomes based on the presence and intensity of FISH signals on individual chromosomes. We have generated new markers by constructing and screening a sample bacterial artificial chromosome (BAC) library for appropriate FISH probes. Five newly isolated BAC clones yielded discrete signals on the chromosomes: two were specific for one autosome pair and three hybridized preferentially to the sex chromosomes. We present the FISH hybridization patterns of these five BAC inserts together with previously described repetitive sequences (X-43.1, 25S rDNA and 5S rDNA) and use them to analyze the S. latifolia karyotype. The autosomes of S. latifolia are difficult to distinguish based on their relative arm lengths. Using one BAC insert and the three repetitive sequences, we have constructed a standard FISH karyotype that can be used to distinguish all autosome pairs. We also analyze the hybridization patterns of these sequences on the sex chromosomes and discuss the utility of the karyotype mapping strategy presented to study sex chromosome evolution and Y chromosome degeneration.Communicated by J.S. Heslop-Harrison