Dimorphic Sex Chromosomes Research Articles

The evolution of huge Y chromosomes in Coccinia grandis and its sister, Coccinia schimperi.

Microscopically dimorphic sex chromosomes in plants are rare, reducing our ability to study them. One difficulty has been the paucity of cultivatable species pairs for cytogenetic, genomic and experimental work. Here, we study the newly recognized sisters Coccinia grandis and Coccinia schimperi, both with large Y chromosomes as we here show for Co. schimperi. We built genetic maps for male and female Co. grandis using a full-sibling family, inferred gene sex-linkage, and, with Co. schimperi transcriptome data, tested whether X- and Y-alleles group by species or by sex. Most sex-linked genes for which we could include outgroups grouped the X- and Y-alleles by species, but some 10% instead grouped the two species' X-alleles. There was no relationship between XY synonymous-site divergences in these genes and gene position on the non-recombining part of the X, suggesting recombination arrest shortly before or after species divergence, here dated to about 3.6 Ma. Coccinia grandis and Co. schimperi are the species pair with the most heteromorphic sex chromosomes in vascular plants (the condition in their sister remains unknown), and future work could use them to study mechanisms of Y chromosome enlargement and parallel degeneration, or to test Haldane's rule about lower hybrid fitness in the heterogametic sex. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.

Identification of the sex-determining factor in the liverwort Marchantia polymorpha reveals unique evolution of sex chromosomes in a haploid system

SummarySex determination is a central process for sexual reproduction and is often regulated by a sex determinant encoded on a sex chromosome. Rules that govern the evolution of sex chromosomes via specialization and degeneration following the evolution of a sex determinant have been well studied in diploid organisms. However, distinct predictions apply to sex chromosomes in organisms where sex is determined in the haploid phase of the life cycle: both sex chromosomes, female U and male V, are expected to maintain their gene functions, even though both are non-recombining. This is in contrast to the X-Y (or Z-W) asymmetry and Y (W) chromosome degeneration in XY (ZW) systems of diploids. Here, we provide evidence that sex chromosomes diverged early during the evolution of haploid liverworts and identify the sex determinant on the Marchantia polymorpha U chromosome. This gene, Feminizer, encodes a member of the plant-specific BASIC PENTACYSTEINE transcription factor family. It triggers female differentiation via regulation of the autosomal sex-determining locus of FEMALE GAMETOPHYTE MYB and SUPPRESSOR OF FEMINIZATION. Phylogenetic analyses of Feminizer and other sex chromosome genes indicate dimorphic sex chromosomes had already been established 430 mya in the ancestral liverwort. Feminizer also plays a role in reproductive induction that is shared with its gametolog on the V chromosome, suggesting an ancestral function, distinct from sex determination, was retained by the gametologs. This implies ancestral functions can be preserved after the acquisition of a sex determination mechanism during the evolution of a dominant haploid sex chromosome system.

Instability of the Pseudoautosomal Boundary in House Mice.

Faithful segregation of homologous chromosomes at meiosis requires pairing and recombination. In taxa with dimorphic sex chromosomes, pairing between them in the heterogametic sex is limited to a narrow interval of residual sequence homology known as the pseudoautosomal region (PAR). Failure to form the obligate crossover in the PAR is associated with male infertility in house mice (Mus musculus) and humans. Yet despite this apparent functional constraint, the boundary and organization of the PAR is highly variable in mammals, and even between subspecies of mice. Here, we estimate the genetic map in a previously documented expansion of the PAR in the M. musculus castaneus subspecies and show that the local recombination rate is 100-fold higher than the autosomal background. We identify an independent shift in the PAR boundary in the M. musculus musculus subspecies and show that it involves a complex rearrangement, but still recombines in heterozygous males. Finally, we demonstrate pervasive copy-number variation at the PAR boundary in wild populations of M. m. domesticus, M. m. musculus, and M. m. castaneus Our results suggest that the intensity of recombination activity in the PAR, coupled with relatively weak constraints on its sequence, permit the generation and maintenance of unusual levels of polymorphism in the population of unknown functional significance.

A rare exception to Haldane's rule: Are X chromosomes key to hybrid incompatibilities?

The prevalence of Haldane's rule suggests that sex chromosomes commonly have a key role in reproductive barriers and speciation. However, the majority of research on Haldane's rule has been conducted in species with conventional sex determination systems (XY and ZW) and exceptions to the rule have been understudied. Here we test the role of X-linked incompatibilities in a rare exception to Haldane's rule for female sterility in field cricket sister species (Teleogryllus oceanicus and T. commodus). Both have an XO sex determination system. Using three generations of crosses, we introgressed X chromosomes from each species onto different, mixed genomic backgrounds to test predictions about the fertility and viability of each cross type. We predicted that females with two different species X chromosomes would suffer reduced fertility and viability compared with females with two parental X chromosomes. However, we found no strong support for such X-linked incompatibilities. Our results preclude X-X incompatibilities and instead support an interchromosomal epistatic basis to hybrid female sterility. We discuss the broader implications of these findings, principally whether deviations from Haldane's rule might be more prevalent in species without dimorphic sex chromosomes.

Genomics of the hop pseudo-autosomal regions

Hop is one of the few dioecious plants with dimorphic sex chromosomes. Because the entire Cannabaceae family is dioecious, hop and other members of this family are thought to have a relatively older sex chromosomal system than other plant species. Hop cones are only produced in female hops with or without fertilization. This has lead to most genomic research being directed toward female plants. The work we present provides genomic resources surrounding male plants. We have produced a draft genome for the male hop line USDA 21422M using a novel genome assembly method. In addition, we identified a 1.3 Mb set of scaffolds, which appear to be the male specific region based upon specificity with male hop accessions. This set includes a smaller high confidence total length 18 Kb set of scaffolds, which are supported by over 500 individuals, including the USDA world collection of hop varieties and two mapping populations, with genotyping by sequencing. We also have identified a portion of the Teamaker × 21422M linkage map to be associated with the pseudo-autosomal region (PAR). Within the genomic scaffolds, we identified a set of genes that are sex-linked and likely located in the PAR.

How Many Non-coding RNAs Does It Take to Compensate Male/Female Genetic Imbalance?

Genetic sex determination in mammals relies on dimorphic sex chromosomes that confer phenotypic/physiologic differences between males and females. In this heterogametic system, X and Y chromosomes diverged from an ancestral pair of autosomes, creating a genetic disequilibrium between XX females and XY males. Dosage compensation mechanisms alleviate intrinsic gene dosage imbalance, leading to equal expression levels of most X-linked genes in the two sexes. In therian mammals, this is achieved through inactivation of one of the two X chromosomes in females. Failure to undergo X-chromosome inactivation (XCI) results in developmental arrest and death. Although fundamental for survival, a surprising loose conservation in the mechanisms to achieve XCI during development in therian lineage has been, and continues, to be uncovered. XCI involves the concerted action of non-coding RNAs (ncRNAs), including the well-known Xist RNA, and has thus become a classical paradigm to study the mode of action of this particular class of transcripts. In this chapter, we will describe the processes coping with sex chromosome genetic imbalance and how ncRNAs underlie dosage compensation mechanisms and influence male-female differences in mammals. Moreover, we will discuss how ncRNAs have been tinkered with during therian evolution to adapt XCI mechanistic to species-specific constraints.

The evolution of sex chromosomes in organisms with separate haploid sexes.

The evolution of dimorphic sex chromosomes is driven largely by the evolution of reduced recombination and the subsequent accumulation of deleterious mutations. Although these processes are increasingly well understood in diploid organisms, the evolution of dimorphic sex chromosomes in haploid organisms (U/V) has been virtually unstudied theoretically. We analyze a model to investigate the evolution of linkage between fitness loci and the sex-determining region in U/V species. In a second step, we test how prone nonrecombining regions are to degeneration due to accumulation of deleterious mutations. Our modeling predicts that the decay of recombination on the sex chromosomes and the addition of strata via fusions will be just as much a part of the evolution of haploid sex chromosomes as in diploid sex chromosome systems. Reduced recombination is broadly favored, as long as there is some fitness difference between haploid males and females. The degeneration of the sex-determining region due to the accumulation of deleterious mutations is expected to be slower in haploid organisms because of the absence of masking. Nevertheless, balancing selection often drives greater differentiation between the U/V sex chromosomes than in X/Y and Z/W systems. We summarize empirical evidence for haploid sex chromosome evolution and discuss our predictions in light of these findings.

Polygenic sex determination system in zebrafish.

BackgroundDespite the popularity of zebrafish as a research model, its sex determination (SD) mechanism is still unknown. Most cytogenetic studies failed to find dimorphic sex chromosomes and no primary sex determining switch has been identified even though the assembly of zebrafish genome sequence is near to completion and a high resolution genetic map is available. Recent publications suggest that environmental factors within the natural range have minimal impact on sex ratios of zebrafish populations. The primary aim of this study is to find out more about how sex is determined in zebrafish.Methodology/Principal FindingsUsing classical breeding experiments, we found that sex ratios across families were wide ranging (4.8% to 97.3% males). On the other hand, repeated single pair crossings produced broods of very similar sex ratios, indicating that parental genotypes have a role in the sex ratio of the offspring. Variation among family sex ratios was reduced after selection for breeding pairs with predominantly male or female offspring, another indication that zebrafish sex is regulated genetically. Further examinations by a PCR-based “blind assay" and array comparative genomic hybridization both failed to find universal sex-linked differences between the male and female genomes. Together with the ability to increase the sex bias of lines by selective breeding, these data suggest that zebrafish is unlikely to utilize a chromosomal sex determination (CSD) system.Conclusions/SignificanceTaken together, our study suggests that zebrafish sex is genetically determined with limited, secondary influences from the environment. As we have not found any sign for CSD in the species, we propose that the zebrafish has a polygenic sex determination system.

Turnover of sex chromosomes induced by sexual conflict

Sex-determination genes are among the most fluid features of the genome in many groups of animals. In some taxa the master sex-determining gene moves frequently between chromosomes, whereas in other taxa different genes have been recruited to determine the sex of the zygotes. There is a well developed theory for the origin of stable and highly dimorphic sex chromosomes seen in groups such as the eutherian mammals. In contrast, the evolutionary lability of genetic sex determination in other groups remains largely unexplained. In this theoretical study, we show that an autosomal gene under sexually antagonistic selection can cause the spread of a new sex-determining gene linked to it. The mechanism can account for the origin of new sex-determining loci, the transposition of an ancestral sex-determining gene to an autosome, and the maintenance of multiple sex-determining factors in species that lack heteromorphic sex chromosomes.

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.

Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression.

Gonadal morphogenesis is very similar among mammals, birds, and reptiles. Despite this similarity, each group utilises quite different genetic triggers for sex determination. In mammals, testis development is initiated by action of the Y-chromosome gene SRY. Current evidence suggests that SRY may act together with a related gene, SOX9, to activate another gene(s) in the pathway of testicular differentiation. A downstream candidate for regulation by SRY and SOX9 is AMH. In mouse, Sox9 is expressed in the Sertoli cells of the embryonic testis and it precedes the onset of Amh expression. During mouse gonadogenesis, Amh is confined to the embryonic testis, although it later shows postnatal expression in the ovary. Reptiles such as the American alligator, which exhibit temperature-dependent sex determination (TSD) do not have dimorphic sex chromosomes and apparently no SRY orthologue. SOX9 is expressed during testis differentiation in the alligator; however, it appears to be expressed too late to cause testis determination. Here we describe the cloning and expression of the alligator AMH gene and show that AMH expression precedes SOX9 expression during testis differentiation. This is the opposite to that observed in the mouse where SOX9 precedes AMH expression. The data presented here, as well as findings from recent expression studies in the chick, suggest that AMH expression is not regulated by SOX9 in the non-mammalian vertebrates.

Evolution of a recent neo-Y sex chromosome in a laboratory population ofDrosophila

In many species of animals, one of the sexes has a chromosome that is structurally and functionally different from its socalled homologue. Conventionally, it is called Y chromosome or W chromosome depending on whether it is present in males or females respectively. The corresponding homologous chromosomes are called X and Z chromosomes. The dimorphic sex chromosomes are believed to have originated from undifferentiated autosomes. In extant species it is difficult to envisage the changes that have occurred in the evolution of dimorphic sex chromosomes. In our laboratory, interracial hybridization between twoDrosophila chromosomal races has resulted in the evolution of a novel race, which we have called Cytorace 1. Here we record that in the genome of Cytorace 1 one of the autosomes of its parents is inherited in a manner similar to that of a classical Y chromosome. Thus this unique Cytorace 1 has the youngest neo-Y sex chromosome (5000 days old; about 300 generations) and it can serve as a ‘window’ for following the transition of an autosome to a Y sex chromosome.

Monotreme Genetics and Cytology and a Model for Sex-Chromosome Evolution

The protherian mammals consist of three species: the platypus, the Australian echidna and the Niugini echidna. These mammals diverged from the therian line of descent about 150-200 million years ago; hence comparisons of gene arrangements and gene control mechanisms between prototherian and therian mammals may yield significant data about gene rearrangements during mammalian evolution and about the evolution of complex genetic control systems. The chromosome complements of the three monotreme species are highly conserved. In particular, the X (or X1) chromosomes are G-band identical and share considerable G-band homology with the Y chromosomes. Replication asynchrony between X chromosomes suggests that X chromosome inactivation operates in females, and is apparently tissue- specific (as it is in marsupials), and confined to the differential region of the X (X1) chromosome (as it is in eutherian mammals). These results suggest that sex chromosome differentiation in the monotremes represents an intermediate stage in the evolution of the dimorphic sex chromosomes of therian mammals and that X-chromosome inactivation may also represent a comparatively primitive stage. Studies of gene location in the platypus using platypus-rodent cell hybrids suggested that HPRT and PGK are syntenic in the platypus, but it was not possible to assign the syntenic group to a particular chromosome. In situ hybridisation was used to assign three genes, located on the X in eutherians and marsupials, to the monotreme X. However, human X short-arm markers were found by in situ hybridisation to be autosomal in monotremes (as they are in marsupials). A model for the evolution of mammalian sex chromosome differentiation and X-chromosome inactivation is presented in which a gradual reduction of the Y chromosome, and recruitment of newly unpaired loci on the X into a system of X-chromosome inactivation, has accompanied eutherian evolution.

The karyotype of the hexaploid species Xenopus ruwenzoriensis Fischberg and Kobel (Anura: Pipidae).

The chromosome number of the hexaploid species Xenopus ruwenzoriensis is 108. The chromosomes fall into sets of six usually similar chromosomes (hextets) which can be classified into the morphological groups characteristic for the genus Xenopus. However, the three distinct secondary constrictions, typical for X. ruwenzoriensis, appear on two homologs only within a particular hextet, unmasking an underlying heterogeneity. The secondary constrictions on chromosome pair 11 show chromosomal association and are considered to represent the nucleolar organizer regions. There is no evidence of dimorphic sex chromosomes. Plates of spermatocyte metaphase I generally show bivalents, but single large multivalents have also been observed. In the majority of cases, 54 dyads are found in second spermatocyte metaphases. X. ruwenzoriensis is, therefore, either an ancient autohexaploid or, more likely, an allopolyploid of more recent origin.

Observations on spermatogenesis in Drosophila

1. Chromosome behavior during spermatogenesis is considered in several species ofDrosophila. The material is not favorable for detailed study. Perhaps the most favorable species isD. funebris; but since the genetic behavior of this species is not well known, others are used for the main account, supplemented by observations on funebris. 2. Homologous chromosomes undergo synapsis in the telophase of the last spermatogonial division, as in other Diptera, and apparently remain in intimate association during the growth stages. 3. The sex chromosomes remain relatively condensed and attached to or incorporated in the nucleolus, which shows wide divergence in size and appearance in different species. 4. The autosomes become diffuse at an early growth stage and are so indistinct that no account can be given of their detailed behavior. InD. funebris they form a granulated canopy or net-like cap at one side of the nucleus and arise in prophase by the condensation of this and coalescence of the granules. 5. No indications of definite threads such as seen during the leptotene and early diplotene stages of many insects and other animals are found here. 6. It is difficult to attach any positive significance to the chromosome behavior so far as the question of genetic crossing over is concerned. 7. The enormous growth of the spermatocytes brings into prominence many interesting cytoplasmic structures which have been noted here but not really studied, although they merit careful observation. 8. The nuclear wall remains intact at both divisions, permitting a distinction between cytoplasmic and nuclear components. 9. In some species numerous non-chromosomal bodies (fragments of nucleolus, cytoplasmic granules, etc.) stain deeply and sometimes bear a slight superficial resemblance to chromosomes, at the first division. 10. Both maturation divisions are normal as far as chromosome distribution is concerned — the first division being reductional so far as known (e. g. where dimorphic sex chromosomes are found). 11. At the first division the chromosomes tend to be drawn out and irregular in contour, especially when long and V-shaped. And they do not, as a rule, form a flat metaphase plate, save inD. obscura and its relatives. Figures are consequently best analysed in side view. 12. The second division is more nearly of the ordinary type and presents no special peculiarities. 13. The behavior of the sex-chromosomes in the first spermatocyte prophase is such as to permit their identification on this basis alone. 14. The evidence indicates that Y remains relatively dense and compact while X behaves more like the autosomes. This leads to the view that Y may remain relatively inert or passive while X is more active during the growth period. 15. X and Y appear to be connected only for a short region, or regions; from which it is inferred that they many be similar in constitution in these regions only.