Recurrent gene amplification on Drosophila Y chromosomes suggests cryptic sex chromosome drive is common on young sex chromosomes

Theory predicts that selfish genetic elements that increase their transmission are prone to originate on sex chromosomes but create strong selective pressure to evolve suppressors due to reduced fertility and distorted population sex ratios. Here we show that recurrent genetic conflict over sex chromosome transmission appears to be an important evolutionary force that has shaped gene content evolution of sex chromosomes in Drosophila. We demonstrate that convergent acquisition and amplification of spermatid expressed gene families are common on Drosophila sex chromosomes, and especially on recently formed ones, and harbor characteristics typical of meiotic drivers. We carefully characterize one putative novel cryptic sex chromosome distortion system that arose independently several times in members of the Drosophila obscura group. Co-amplification of the S-Lap1/GAPsec gene pair on both the X and the Y chromosome occurred independently several times in members of the D. obscura group, where this normally autosomal gene pair is sex-linked due to a sex chromosome - autosome fusion. Investigation of gene expression and short RNA profiles at the S-Lap1/GAPsec system suggest that meiotic drive and suppression likely involves RNAi mechanisms. Our finding suggests that recurrent conflict over sex chromosome transmission has shaped widespread genomic and evolutionary patterns, including the epigenetic regulation of sex chromosomes, the distribution of sex-biased genes, and the evolution of hybrid sterility.

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Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

10.1101/024711 ◽

2015 ◽

Cited By ~ 1

Author(s):

Colin D. Meiklejohn ◽

Emily L. Landeen ◽

Kathleen E. Gordon ◽

Thomas Rzatkiewicz ◽

Sarah B. Kingan ◽

...

Keyword(s):

Gene Flow ◽

Sex Chromosomes ◽

Population Genomics ◽

Sex Chromosome ◽

Hybrid Sterility ◽

Meiotic Drive ◽

Hybrid Male ◽

Selfish Genetic Elements ◽

Cryptic Sex

ABSTRACTDuring speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that, rather than contributing to interspecific divergence, a known drive element has recently migrated between species, caused a strong reduction in local divergence, and undermined the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

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Differential regulation of mouse hippocampal gene expression sex differences by chromosomal content and gonadal sex

10.1101/2021.09.01.458115 ◽

2021 ◽

Author(s):

Sarah R Ocanas ◽

Victor A Ansere ◽

Kyla B Tooley ◽

Niran Hadad ◽

Ana J Chucair-Elliott ◽

...

Keyword(s):

Gene Expression ◽

Dna Methylation ◽

Sex Differences ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Chromosome Complement ◽

Experimental Models ◽

Ctcf Binding ◽

Autosomal Gene ◽

Sex Effects

Sex differences in the brain as they relate to health and disease are often overlooked in experimental models. Many neurological disorders, like Alzheimer's disease (AD), multiple sclerosis (MS), and autism, differ in prevalence between males and females. Sex differences originate either from differential gene expression on sex chromosomes or from hormonal differences, either directly or indirectly. To disentangle the relative contributions of genetic sex (XX v. XY) and gonadal sex (ovaries v. testes) to the regulation of hippocampal sex effects, we use the "sex-reversal" Four Core Genotype (FCG) mouse model which uncouples sex chromosome complement from gonadal sex. Transcriptomic and epigenomic analyses of hippocampal RNA and DNA from ~12 month old FCG mice, reveals differential regulatory effects of sex chromosome content and gonadal sex on X- versus autosome-encoded gene expression and DNA modification patterns. Gene expression and DNA methylation patterns on the X chromosome were driven primarily by sex chromosome content, not gonadal sex. The majority of DNA methylation changes involved hypermethylation in the XX genotypes (as compared to XY) in the CpG context, with the largest differences in CpG islands, promoters, and CTCF binding sites. Autosomal gene expression and DNA modifications demonstrated regulation by sex chromosome complement and gonadal sex. These data demonstrate the importance of sex chromosomes themselves, independent of hormonal status, in regulating hippocampal sex effects. Future studies will need to further interrogate specific CNS cell types, identify the mechanisms by which sex chromosome regulate autosomes, and differentiate organizational from activational hormonal effects.

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Does degeneration or genetic conflict shape gene content on UV sex chromosomes?

10.32942/osf.io/hs6w3 ◽

2020 ◽

Author(s):

Sarah Carey ◽

Leslie Kollar ◽

Stuart McDaniel

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Gene Content ◽

Transmission Ratio Distortion ◽

Gene Gain ◽

Genetic Conflict ◽

Evolutionary Genomic ◽

Ratio Distortion ◽

Suppressed Recombination ◽

Drive Gene

Studies of sex chromosomes have played a central role in understanding the consequences of suppressed recombination and sex-specific inheritance among several genomic phenomena. However, we argue that these efforts will benefit from a more rigorous examination of haploid UV sex chromosome systems, in which both the female-limited (U) and male-limited (V) experience suppressed recombination and sex-limited inheritance, and both are transcriptionally active in the haploid and diploid states. We review the life cycle differences that generate UV sex chromosomes and genomic data showing that ancient UV systems have evolved independently in many eukaryotic groups, but gene movement on and off the sex chromosomes, and potentially degeneration continue to shape the current gene content of the U and V chromosomes. Although both theory and empirical data show that the evolution of UV sex chromosomes is shaped by many of the same processes that govern diploid sex chromosome systems, we highlight how the symmetrical inheritance between the UV chromosomes provide an important test of sex-limited inheritance in shaping genome architecture. We conclude by examining how genetic conflict (over sexual dimorphism, transmission-ratio distortion, or parent-offspring conflict) may drive gene gain on UV sex chromosomes, and highlight the role of breeding system in governing the action of these processes. Collectively these observations demonstrate the potential for evolutionary genomic analyses of varied UV sex chromosome systems, combined with natural history studies, to understand how genetic conflict shapes sex chromosome gene content.

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Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

eLife ◽

10.7554/elife.35468 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 18

Author(s):

Colin D Meiklejohn ◽

Emily L Landeen ◽

Kathleen E Gordon ◽

Thomas Rzatkiewicz ◽

Sarah B Kingan ◽

...

Keyword(s):

Gene Flow ◽

Sex Chromosomes ◽

Population Genomics ◽

Sex Chromosome ◽

Hybrid Sterility ◽

Sequence Divergence ◽

Meiotic Drive ◽

Hybrid Male ◽

Local Sequence

During speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that a known drive element recently migrated between species and, rather than contributing to interspecific divergence, caused a strong reduction in local sequence divergence, undermining the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

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THE ROLE OF GENETICS AND OTHER PRENATAL FACTORS IN DISORDERS OF CHILDHOOD

PEDIATRICS ◽

10.1542/peds.18.2.314 ◽

1956 ◽

Vol 18 (2) ◽

pp. 314-317

Author(s):

Josef Warkany ◽

F. C. Fraser

Keyword(s):

Sex Chromosomes ◽

Gene Pair ◽

Sex Chromosome ◽

Rare Event ◽

Round Table ◽

X Chromosomes ◽

Prenatal Factors ◽

Biochemical Factor ◽

Hereditary Factors

THE PHYSICIAN interested in the etiology of a disease should always try to ascertain as many etiologic factors as possible, because the causal pathogenic web can often be disturbed from different angles. Although hereditary factors will be the main topic of this round table, we shall stress that they never act in a vacuum. The genes direct the development of the embryo and fetus, but the development depends also upon an environment limited by the mother's body and surroundings. Certain terms are fundamental to an understanding of heredity: Chromosomes. The nuclear carriers of the hereditary factors, the genes. Each nucleated somatic cell of a person's body has 24 pairs of chromosomes, each pair carrying hundreds of genes. One member of each pair is derived from the person's mother and one from the father. In the female there are 23 pairs of autosomes (non-sex chromosomes) and 1 pair of like sex chromosomes (X-chromosomes). In the male there are 23 pairs of autosomes and 1 pair of unlike sex chromosomes (one X and one Y-chromosome). Gene. The particulate biochemical factor responsible for a particular hereditary characteristic. As the genes are carried on the chromosomes, they also occur in pairs. Each pair occupies a particular locus on the chromosomes. Genes located at the same locus are termed alleles. A child gets 1 member of each gene pair from each parent. Sometimes by the rare event of mutation, a gene becomes changed into one that may function abnormally—a "pathologic" gene. Homozygote. An individual in whom the gene pair in question consists of 2 like genes. Heterozygote. An individual in whom the gene pair in question consists of unlike genes. Depending upon the type (dominant or recessive) and location (autosome or sex chromosome) of the gene, several types of inheritance patterns are possible.

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Male mice with large inversions or deletions of X-palindrome arms are fertile and express their associated genes post-meiosis

10.1101/245860 ◽

2018 ◽

Author(s):

Alyssa N. Kruger ◽

Quinn Ellison ◽

Michele A. Brogley ◽

Emma R. Gerlinger ◽

Jacob L. Mueller

Keyword(s):

Gene Expression ◽

Sex Chromosomes ◽

Transcriptional Repression ◽

Sex Chromosome ◽

Gene Families ◽

Single Copy ◽

Male Mice ◽

Expression Levels ◽

Gene Copies ◽

Palindromic Structure

AbstractLarge (>10 kb) palindromic sequences are enriched on mammalian sex chromosomes. In mice, these palindromes harbor gene families (≥2 gene copies) expressed exclusively in post-meiotic testicular germ cells, at a time when most single-copy sex-linked genes are transcriptionally repressed. This distinct expression pattern led to the hypothesis that containment within palindrome structures or having ≥2 gene enables post-meiotic gene expression. We tested these two hypotheses by using CRISPR to precisely engineer large (10’s of kb) inversions and deletions of X chromosome palindrome arms for two regions carrying the mouse 4930567H17Rik and Mageb5 gene families. We found that 4930567H17Rik and Mageb5 gene expression is unaffected in mice carrying palindrome arm inversions, suggesting that palindromic structure is not important for mediating palindrome-associated gene expression. We also found that 4930567H17Rik and Mageb5 gene expression is reduced by half in mice carrying palindrome arm deletions, allowing us to test whether palindrome-associated genes are sensitive to reduced expression levels resulting in spermatogenic defects. Male mice carrying palindrome arm deletions of 4930567H17Rik or Mageb5, however, are fertile, have normal testis histology, and show no aberrations in spermatogenic cell population frequencies via FACS quantification. Together, these findings suggest that large palindromic structures on the sex chromosomes are not necessary for their associated genes to evade post-meiotic transcriptional repression and that these genes are not sensitive to reduced expression levels. Large sex chromosome palindromes may thus be important for other reasons, such as the long-term evolutionary stability of their associated gene families.

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Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing

10.1101/2021.10.13.462063 ◽

2021 ◽

Author(s):

Zexian Zhu ◽

Kazumi Matsubara ◽

Foyez Shams ◽

Jason Dobry ◽

Erik Wapstra ◽

...

Keyword(s):

Sex Determination ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Cost Effective ◽

Chromosome Variation ◽

Specific Expression ◽

Monitor Lizard ◽

Compensation Mechanisms ◽

Cryptic Sex

Reptile sex determination is attracting much attention because the great diversity of sex-determination and dosage compensation mechanisms permits us to approach fundamental questions about sex chromosome turnover and evolution. However, reptile sex chromosome variation remains largely uncharacterized and no reptile master sex determination genes have yet been identified. Here we describe a powerful and cost-effective chromosomics approach, combining probes generated from the microdissected sex chromosomes with transcriptome sequencing to explore this diversity in non-model Australian reptiles with heteromorphic or cryptic sex chromosomes. We tested the pipeline on a turtle, a gecko, and a worm-lizard, and we also identified sequences located on sex chromosomes in a monitor lizard using linked-read sequencing. Genes identified on sex chromosomes were compared to the chicken genome to identify homologous regions among the four species. We identified candidate sex determining genes within these regions, including conserved vertebrate sex-determining genes pdgfa, pdgfra amh and wt1, and demonstrated their testis or ovary-specific expression. All four species showed gene-by-gene rather than chromosome-wide dosage compensation. Our results imply that reptile sex chromosomes originated by the independent acquisition of sex-determining genes on different autosomes, as well as translocations between different ancestral macro- and micro-chromosomes. We discuss the evolutionary drivers of the slow differentiation, but rapid turnover, of reptile sex chromosomes.

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Mammalian Sex Chromosome Structure, Gene Content, and Function in Male Fertility

Annual Review of Animal Biosciences ◽

10.1146/annurev-animal-020518-115332 ◽

2019 ◽

Vol 7 (1) ◽

pp. 103-124 ◽

Cited By ~ 8

Author(s):

Wan-Sheng Liu

Keyword(s):

Sex Chromosomes ◽

Sexual Development ◽

Brain Function ◽

Male Fertility ◽

Sex Chromosome ◽

Size Structure ◽

Gene Families ◽

Gene Content ◽

Meiotic Sex Chromosome Inactivation ◽

And Function

Mammalian sex chromosomes evolved from an ordinary pair of autosomes. The X chromosome is highly conserved, whereas the Y chromosome varies among species in size, structure, and gene content. Unlike autosomes that contain randomly mixed collections of genes, the sex chromosomes are enriched in testis-biased genes related to sexual development and reproduction, particularly in spermatogenesis and male fertility. This review focuses on how sex chromosome dosage compensation takes place and why meiotic sex chromosome inactivation occurs during spermatogenesis. Furthermore, the review also emphasizes how testis-biased genes are enriched on the sex chromosomes and their functions in male fertility. It is concluded that sex chromosomes are critical to sexual development and male fertility; however, our understanding of how sex chromosome genes direct sexual development and fertility has been hampered by the structural complexities of the sex chromosomes and by the multicopy nature of the testis gene families that also play a role in immunity, cancer development, and brain function.

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Patterns of Sex Chromosome Differentiation in Spiders: Insights from Comparative Genomic Hybridisation

Genes ◽

10.3390/genes11080849 ◽

2020 ◽

Vol 11 (8) ◽

pp. 849

Author(s):

Alexandr Sember ◽

Michaela Pappová ◽

Martin Forman ◽

Petr Nguyen ◽

František Marec ◽

...

Keyword(s):

X Chromosome ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Intraspecific Variability ◽

Comparative Genomic Hybridisation ◽

Comparative Genomic ◽

Chromosome Differentiation ◽

Molecular Differentiation ◽

Y Chromosomes ◽

Cryptic Sex

Spiders are an intriguing model to analyse sex chromosome evolution because of their peculiar multiple X chromosome systems. Y chromosomes were considered rare in this group, arising after neo-sex chromosome formation by X chromosome-autosome rearrangements. However, recent findings suggest that Y chromosomes are more common in spiders than previously thought. Besides neo-sex chromosomes, they are also involved in the ancient X1X2Y system of haplogyne spiders, whose origin is unknown. Furthermore, spiders seem to exhibit obligatorily one or two pairs of cryptic homomorphic XY chromosomes (further cryptic sex chromosome pairs, CSCPs), which could represent the ancestral spider sex chromosomes. Here, we analyse the molecular differentiation of particular types of spider Y chromosomes in a representative set of ten species by comparative genomic hybridisation (CGH). We found a high Y chromosome differentiation in haplogyne species with X1X2Y system except for Loxosceles spp. CSCP chromosomes exhibited generally low differentiation. Possible mechanisms and factors behind the observed patterns are discussed. The presence of autosomal regions marked predominantly or exclusively with the male or female probe was also recorded. We attribute this pattern to intraspecific variability in the copy number and distribution of certain repetitive DNAs in spider genomes, pointing thus to the limits of CGH in this arachnid group. In addition, we confirmed nonrandom association of chromosomes belonging to particular CSCPs at spermatogonial mitosis and spermatocyte meiosis and their association with multiple Xs throughout meiosis. Taken together, our data suggest diverse evolutionary pathways of molecular differentiation in different types of spider Y chromosomes.

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