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.     

Faster evolution of Z-linked duplicate genes in chicken

It has been shown that duplicate genes on the X chromosome evolve much faster than duplicate genes on autosomes in Drosophila melanogaster.However,whether this phenomenon is general and can be applied to other species is not known.Here we examined this issue in chicken that have heterogametic females(females have ZW sex chromosome).We compared sequence divergence of duplicate genes on the Z chromosome with those on autosomes.We found that duplications on the Z chromosome indeed evolved faster than those on autosomes and show distinct patterns of molecular evolution from autosomal duplications.Examination of the expression of duplicate genes revealed an enrichment of duplications on the Z chromosome having male-biased expression and an enrichment of duplications on the autosomes having female-biased expression.These results suggest an evolutionary trend of the recruitment of duplicate genes towards reproduction-specific function.The faster evolution of duplications on Z than on the autosomes is most likely contributed by the selective forces driving the fixation of adaptive mutations on Z.Therefore,the common phenomena observed in both flies and chicken suggest that duplicate genes on sex chromosomes have distinct dynamics and are more influenced by natural selection than antosomal duplications,regardless of the kind of sex determination systems.     

X for intersection: retrotransposition both on and off the X chromosome is more frequent

As the heteromorphic sex chromosomes evolved from a pair of autosomes, the sex chromosomes became increasingly different in gene content and structure from each other and from the autosomes. Although recently there has been progress in documenting and understanding these differences, the molecular mechanisms that have fashioned some of these changes remain unclear. A new study addresses the differential distribution of retroposed genes in human and mouse genomes. Surprisingly, chromosome X is a major source and a preferred target for retrotransposition.     

Independent origin of sex chromosomes in two species of the genus Silene

Here we introduce a new model species, Silene colpophylla, that could facilitate research of sex chromosome evolution and sex-determining systems. This species is related to the well-established dioecious plant model Silene latifolia. Our results show that S. colpophylla is, similarly to S. latifolia, a male heterogametic species, but its sex chromosomes have evolved from a different pair of autosomes than in S. latifolia. The results of our phylogenetic study and mapping of homologs of S. latifolia X-linked genes indicate that the sex determination system in S. colpophylla evolved independently from that in S. latifolia. We assert that this model species pair will make it possible to study two independent patterns of sex chromosome evolution in related species.     

Evolution of heteromorphic sex chromosomes in the order Aulopiformes

The fish order Aulopiformes contains both synchronously hermaphroditic and gonochoristic species. From the cytogenetic viewpoint, few reports show that gonochoristic Aulopiformes have heteromorphic sex chromosomes. Because fish in this order give us a unique opportunity to elucidate the evolution of sex chromosomes, it is important to examine a phylogenetic relationship in Aulopiformes by both molecular evolutionary and cytogenetic methods. Thus, we conducted molecular phylogenetic and cytogenetic studies of six Aulopiform species. Our results suggested that hermaphroditic species were evolutionarily derived from gonochoristic species. It follows that the hermaphroditic species might have lost the heteromorphic sex chromosomes during evolution. Here, we suggest a possibility that heteromorphic sex chromosomes can disappear from the genome, even if they have appeared once in evolution. Taking into account Ohno's hypothesis that heteromorphic sex chromosomes might have emerged from autosomes, we propose the hypothesis that heteromorphic sex chromosomes may have undergone repeated events of appearance and disappearance during the course of fish evolution.     

Origin and evolution of mammalian sex chromosomes

Mammals present an XX/XY system of chromosomal sex determination, males being the heterogametic sex. Comparative studies of the gene content of sex chromosomes from the major groups of mammals reveal that most Y genes have X-linked homologues and that X and Y share homologous pseudoautosomal regions. These observations, together with the presence of the two homologous regions (pseudoautosomal regions) at the tips of the sex chromosomes, suggest that these chromosomes began as an ordinary pair of homologous autosomes. Birds present a ZW/ZZ system of chromosomal sex determination where females are the heterogametic sex. In this case, avian sex chromosomes are derived from different pairs of autosomes than mammals. The evolutionary pathway from the autosomal homomorphic departure to the present-day heteromorphic sex chromosomes in mammals includes suppression of X-Y recombination, differentiation of the nascent non-recombining regions, and progressive autosomal addition and attrition of the sex chromosomes. Recent results indicate that the event marking the beginning of the differentiation between the extant X and Y chromosomes occurred about 300 million years ago.     

H-Y antigen as a tool for the determination of the heterogametic sex in Amphibia

H-Y antigen was investigated in three amphibian species with different degrees of sex-chromosome differentiation: Bufo bufo, Triturus vulgaris, and Pyxicephalus adspersus. No heteromorphic sex chromosomes were found in B. bufo, but an examination of the progeny of hermaphrodites (Ponse, 1942) indicated that the female of this species was heterogametic (ZW). Sex chromosomes differing only by a very small heterochromatic region at their telomeres were found in the male of T. vulgaris (XY). Pyxicephalus adspersus revealed high differentiated ZW sex chromosomes. The results of the H-Y antigen studies on these three species indicate that H-Y antigen is expressed only in the heterogametic sex, irrespective of differences in morphological differentiation of the sex chromosomes. Therefore, H-Y antigen could be a valuable tool in determining the heterogametic sex, not only in Amphibia but possibly also in other vertebrate species that have either evolved no heteromorphic sex chromosomes or where sex-reversal experiments are not possible.     

POSITIVE SELECTION DRIVES FASTER‐Z EVOLUTION IN SILKMOTHS

Genes linked to X or Z chromosomes, which are hemizygous in the heterogametic sex, are predicted to evolve at different rates than those on autosomes. This “faster‐X effect” can arise either as a consequence of hemizygosity, which leads to more efficient selection for recessive beneficial mutations in the heterogametic sex, or as a consequence of reduced effective population size of the hemizygous chromosome, which leads to increased fixation of weakly deleterious mutations due to genetic drift. Empirical results to date suggest that, while the overall pattern across taxa is complicated, systems with male heterogamy show a faster‐X effect attributable to more efficient selection, whereas the faster‐Z effect in female‐heterogametic taxa is attributable to increased drift. To test the generality of the faster‐Z pattern seen in birds and snakes, we sequenced the genome of the lepidopteran silkmoth Bombyx huttoni. We show that silkmoths experience faster‐Z evolution, but unlike in birds and snakes, the faster‐Z effect appears to be attributable to more efficient positive selection. These results suggest that female heterogamy alone is unlikely to explain the reduced efficacy of selection on vertebrate Z chromosomes. It is likely that many factors, including differences in overall effective population size, influence Z chromosome evolution.     

Retrogenes Moved Out of the Z Chromosome in the Silkworm

Previous studies on organisms with well-differentiated X and Y chromosomes, such as Drosophila and mammals, consistently detected an excess of genes moving out of the X chromosome and gaining testis-biased expression. Several selective evolutionary mechanisms were shown to be associated with this nonrandom gene traffic, which contributed to the evolution of the X chromosome and autosomes. If selection drives gene traffic, such traffic should also exist in species with Z and W chromosomes, where the females are the heterogametic sex. However, no previous studies on gene traffic in species with female heterogamety have found any nonrandom chromosomal gene movement. Here, we report an excess of retrogenes moving out of the Z chromosome in an organism with the ZW sex determination system, Bombyx mori. In addition, we showed that those "out of Z" retrogenes tended to have ovary-biased expression, which is consistent with the pattern of non-retrogene traffic recently reported in birds and symmetrical to the retrogene movement in mammals and fruit flies out of the X chromosome evolving testis functions. These properties of gene traffic in the ZW system suggest a general role for the heterogamety of sex chromosomes in determining the chromosomal locations and the evolution of sex-biased genes.     

The Staurotypus Turtles and Aves Share the Same Origin of Sex Chromosomes but Evolved Different Types of Heterogametic Sex Determination

Reptiles have a wide diversity of sex-determining mechanisms and types of sex chromosomes. Turtles exhibit temperature-dependent sex determination and genotypic sex determination, with male heterogametic (XX/XY) and female heterogametic (ZZ/ZW) sex chromosomes. Identification of sex chromosomes in many turtle species and their comparative genomic analysis are of great significance to understand the evolutionary processes of sex determination and sex chromosome differentiation in Testudines. The Mexican giant musk turtle (Staurotypus triporcatus, Kinosternidae, Testudines) and the giant musk turtle (Staurotypus salvinii) have heteromorphic XY sex chromosomes with a low degree of morphological differentiation; however, their origin and linkage group are still unknown. Cross-species chromosome painting with chromosome-specific DNA from Chinese soft-shelled turtle (Pelodiscus sinensis) revealed that the X and Y chromosomes of S. triporcatus have homology with P. sinensis chromosome 6, which corresponds to the chicken Z chromosome. We cloned cDNA fragments of S. triporcatus homologs of 16 chicken Z-linked genes and mapped them to S. triporcatus and S. salvinii chromosomes using fluorescence in situ hybridization. Sixteen genes were localized to the X and Y long arms in the same order in both species. The orders were also almost the same as those of the ostrich (Struthio camelus) Z chromosome, which retains the primitive state of the avian ancestral Z chromosome. These results strongly suggest that the X and Y chromosomes of Staurotypus turtles are at a very early stage of sex chromosome differentiation, and that these chromosomes and the avian ZW chromosomes share the same origin. Nonetheless, the turtles and birds acquired different systems of heterogametic sex determination during their evolution.     

THE EFFECTS OF SELECTION AND GENETIC DRIFT ON THE GENOMIC DISTRIBUTION OF SEXUALLY ANTAGONISTIC ALLELES

Sexual antagonism (SA) occurs when an allele that is beneficial to one sex, is detrimental to the other. This conflict can result in balancing, directional, or disruptive selection acting on SA alleles. A body of theory predicts the conditions under which sexually antagonistic mutants will invade and be maintained in stable polymorphism under balancing selection. There remains, however, considerable debate over the distribution of SA genetic variation across autosomes and sex chromosomes, with contradictory evidence coming from data and theory. In this article, we investigate how the interplay between selection and genetic drift will affect the genomic distribution of sexually antagonistic alleles. The effective population sizes can differ between the autosomes and the sex chromosomes due to a number of ecological factors and, consequently, the distribution of SA genetic variation in genomes. In general, we predict the interplay of SA selection and genetic drift should lead to the accumulation of SA alleles on the X in male heterogametic (XY) species and, on the autosomes in female heterogametic (ZW) species, especially when sexual competition is strong among males.     

ZW,XY, and yet ZW: Sex chromosome evolution in snakes even more complicated

Snakes are historically important in the formulation of several central concepts on the evolution of sex chromosomes. For over 50 years, it was believed that all snakes shared the same ZZ/ZW sex chromosomes, which are homomorphic and poorly differentiated in “basal” snakes such as pythons and boas, while heteromorphic and well differentiated in “advanced” (caenophidian) snakes. Recent molecular studies revealed that differentiated sex chromosomes are indeed shared among all families of caenophidian snakes, but that boas and pythons evolved likely independently male heterogamety (XX/XY sex chromosomes). The historical report of heteromorphic ZZ/ZW sex chromosomes in a boid snake was previously regarded as ambiguous. In the current study, we document heteromorphic ZZ/ZW sex chromosomes in a boid snake. A comparative approach suggests that these heteromorphic sex chromosomes evolved very recently and that they are poorly differentiated at the sequence level. Interestingly, two snake lineages with confirmed male heterogamety possess homomorphic sex chromosomes, but heteromorphic sex chromosomes are present in both snake lineages with female heterogamety. We point out that this phenomenon is more common across squamates. The presence of female heterogamety in non‐caenophidian snakes indicates that the evolution of sex chromosomes in this lineage is much more complex than previously thought, making snakes an even better model system for the evolution of sex chromosomes.     

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.     

The origin and evolution of vertebrate sex chromosomes and dosage compensation

In mammals, birds, snakes and many lizards and fish, sex is determined genetically (either male XY heterogamy or female ZW heterogamy), whereas in alligators, and in many reptiles and turtles, the temperature at which eggs are incubated determines sex. Evidently, different sex-determining systems (and sex chromosome pairs) have evolved independently in different vertebrate lineages. Homology shared by Xs and Ys (and Zs and Ws) within species demonstrates that differentiated sex chromosomes were once homologous, and that the sex-specific non-recombining Y (or W) was progressively degraded. Consequently, genes are left in single copy in the heterogametic sex, which results in an imbalance of the dosage of genes on the sex chromosomes between the sexes, and also relative to the autosomes. Dosage compensation has evolved in diverse species to compensate for these dose differences, with the stringency of compensation apparently differing greatly between lineages, perhaps reflecting the concentration of genes on the original autosome pair that required dosage compensation. We discuss the organization and evolution of amniote sex chromosomes, and hypothesize that dosage insensitivity might predispose an autosome to evolving function as a sex chromosome.     

ANOLIS SEX CHROMOSOMES ARE DERIVED FROM A SINGLE ANCESTRAL PAIR

To explain the frequency and distribution of heteromorphic sex chromosomes in the lizard genus Anolis, we compared the relative roles of sex chromosome conservation versus turnover of sex‐determining mechanisms. We used model‐based comparative methods to reconstruct karyotype evolution and the presence of heteromorphic sex chromosomes onto a newly generated Anolis phylogeny. We found that heteromorphic sex chromosomes evolved multiple times in the genus. Fluorescent in situ hybridization (FISH) of repetitive DNA showed variable rates of Y chromosome degeneration among Anolis species and identified previously undetected, homomorphic sex chromosomes in two species. We confirmed homology of sex chromosomes in the genus by performing FISH of an X‐linked bacterial artificial chromosome (BAC) and quantitative PCR of X‐linked genes in multiple Anolis species sampled across the phylogeny. Taken together, these results are consistent with long‐term conservation of sex chromosomes in the group. Our results pave the way to address additional questions related to Anolis sex chromosome evolution and describe a conceptual framework that can be used to evaluate the origins and evolution of heteromorphic sex chromosomes in other clades.     

两栖动物性染色体的多样性及其 进化机制的研究进展

两栖动物性别决定类型和性染色体具有多样性的特点。在已发现异形性染色体两栖动物中,大部分物种Y或W染色体大于其对应的X或Z染色体,少数物种具有高度分化的Y或W染色体。同时两栖动物类群内基因组大小差异大,性染色体间分子水平上也存在差异。高频转换、偶然重组和染色体重排可能是两栖动物性染色体进化过程中的关键机制。本综述通过对两栖动物性染色体进化的深入探讨,揭示其遗传性别决定的机理,有助于对两栖动物性别人工调控的进一步探索。     

Holozygosity for sex-linked genes in males of the termiteIncisitermes schwarzi

The termite Incisitermes schwarzi has multiple sex chromosomes that have arisen by repeated translocations between autosomes and previously existing sex chromosomes. Two sex-linked allozyme loci--Acp-1 and Est-3--are holozygous, not hemizygous, in males (the heterogametic sex). Both loci show less than 1% crossing-over between X and Y chromosomes, and alleles of both are in marked disequilibrium with respect to X vs Y linkage. The two loci assort independently in female meiosis, indicating that they lie on different sex chromosomes. But they are tightly linked in male meiosis because of nonrandom assortment of the multiple X and Y chromosomes in males of this species. The findings of holozygosity and strong linkage disequilibrium suggest that differential selection in the two sexes at or near these loci may be responsible for the establishment of the translocations in this species. The existence of active Y-linked alleles also suggests that the translocations may have occurred recently.