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The Evolutionary Life Cycle of Sex Chromosomes

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A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (30 April 2018) | Viewed by 73794

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Prof. Dr. Leo W. Beukeboom

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Guest Editor

Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, The Netherlands
Interests: evolutionary genetics; entomology; ecological and evolutionary genomics; evolution of reproductive modes; genetics of sex determination; life history evolution; insect pest control

Mr. Martijn A. Schenkel

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Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, P.O. Box 11103, 9700 CC Groningen, The Netherlands
Interests: evolutionary ecology; evolutionary genetics and genomics; evolutionary theory; genomics of sex determination; reproductive parasitism; sex chromosome evolution; sexual selection; speciation

Special Issue Information

Dear Colleagues,

Sex chromosomes represent a specialized component of the genome. They play an important role in basal processes such as sex determination, but are also often involved in emergent evolutionary phenomena such as speciation. How sex chromosomes are born, mature and die is a major question in contemporary evolutionary biology. Sex chromosomes are believed to evolve from an ordinary pair of autosomes, originating when an autosome pair acquires a sex-determining function. How and why this transition takes place remains largely unknown. Sex chromosomes undergo many changes, such as recombination suppression, degeneration by accumulation of repetitive DNA and transposons, dosage compensation to balance the gene products of degenerated genes, and gene trafficking to and from other chromosomes. This often yields a pair of highly-differentiated chromosomes, one of which exhibits the extensive decay characteristic of late-stage sex chromosomes. Eventually, this decrepit chromosome may even be lost, resulting in males and females having different numbers of chromosomes. Much remains to be discovered about the processes that shape sex chromosomes, but the revolution in genomics, transcriptomics and other related technologies allows us to study the evolution of sex chromosomes in unprecedented detail. This issue will address questions about the lifecycle of sex chromosomes across different organismal groups.

Prof. Dr. Leo W. Beukeboom
Mr. Martijn A. Schenkel
Guest Editors

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Keywords

autosomes
degeneration
dosage compensation
gene silencing
gene trafficking
heterochromatization
Hill-Robertson interference
heterogamety
homogamety
intralocus sexual conflict
linkage
Muller’s ratchet
mutation accumulation
recombination
sex chromosomes
sex determination
sexual antagonism
sexual selection
repetitive DNA
retrotransposons

Published Papers (13 papers)

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Research

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16 pages, 802 KiB

Open AccessArticle

Insights into Avian Incomplete Dosage Compensation: Sex-Biased Gene Expression Coevolves with Sex Chromosome Degeneration in the Common Whitethroat

by Hanna Sigeman, Suvi Ponnikas, Elin Videvall, Hongkai Zhang, Pallavi Chauhan, Sara Naurin and Bengt Hansson

Genes 2018, 9(8), 373; https://doi.org/10.3390/genes9080373 - 26 Jul 2018

Cited by 9 | Viewed by 4511

Abstract

Non-recombining sex chromosomes (Y and W) accumulate deleterious mutations and degenerate. This poses a problem for the heterogametic sex (XY males; ZW females) because a single functional gene copy often implies less gene expression and a potential imbalance of crucial expression networks. Mammals counteract this by dosage compensation, resulting in equal sex chromosome expression in males and females, whereas birds show incomplete dosage compensation with significantly lower expression in females (ZW). Here, we study the evolution of Z and W sequence divergence and sex-specific gene expression in the common whitethroat (Sylvia communis), a species within the Sylvioidea clade where a neo-sex chromosome has been formed by a fusion between an autosome and the ancestral sex chromosome. In line with data from other birds, females had lower expression than males at the majority of sex-linked genes. Results from the neo-sex chromosome region showed that W gametologs have diverged functionally to a higher extent than their Z counterparts, and that the female-to-male expression ratio correlated negatively with the degree of functional divergence of these gametologs. We find it most likely that sex-linked genes are being suppressed in females as a response to W chromosome degradation, rather than that these genes experience relaxed selection, and thus diverge more, by having low female expression. Overall, our data of this unique avian neo-sex chromosome system suggest that incomplete dosage compensation evolves, at least partly, through gradual accumulation of deleterious mutations at the W chromosome and declining female gene expression. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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24 pages, 3892 KiB

Open AccessArticle

Tissue Specificity and Dynamics of Sex-Biased Gene Expression in a Common Frog Population with Differentiated, Yet Homomorphic, Sex Chromosomes

by Wen-Juan Ma, Paris Veltsos, Melissa A. Toups, Nicolas Rodrigues, Roberto Sermier, Daniel L. Jeffries and Nicolas Perrin

Genes 2018, 9(6), 294; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9060294 - 12 Jun 2018

Cited by 17 | Viewed by 5278

Abstract

Sex-biased genes are central to the study of sexual selection, sexual antagonism, and sex chromosome evolution. We describe a comprehensive de novo assembled transcriptome in the common frog Rana temporaria based on five developmental stages and three adult tissues from both sexes, obtained from a population with karyotypically homomorphic but genetically differentiated sex chromosomes. This allows the study of sex-biased gene expression throughout development, and its effect on the rate of gene evolution while accounting for pleiotropic expression, which is known to negatively correlate with the evolutionary rate. Overall, sex-biased genes had little overlap among developmental stages and adult tissues. Late developmental stages and gonad tissues had the highest numbers of stage- or tissue-specific genes. We find that pleiotropic gene expression is a better predictor than sex bias for the evolutionary rate of genes, though it often interacts with sex bias. Although genetically differentiated, the sex chromosomes were not enriched in sex-biased genes, possibly due to a very recent arrest of XY recombination. These results extend our understanding of the developmental dynamics, tissue specificity, and genomic localization of sex-biased genes. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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18 pages, 1181 KiB

Open AccessArticle

Investigating the Molecular Genetic Basis of Cytoplasmic Sex Determination Caused by Wolbachia Endosymbionts in Terrestrial Isopods

by Myriam Badawi, Bouziane Moumen, Isabelle Giraud, Pierre Grève and Richard Cordaux

Genes 2018, 9(6), 290; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9060290 - 08 Jun 2018

Cited by 12 | Viewed by 5110

Abstract

In animals, sexual differences between males and females are usually determined by sex chromosomes. Alternatively, sex may also be determined by vertically transmitted intracellular microbial endosymbionts. The best known cytoplasmic sex manipulative endosymbiont is Wolbachia which can, for instance, feminize genetic males into phenotypic females in the terrestrial isopod Armadillidium vulgare. However, the molecular genetic basis of cytoplasmic sex determination is unknown. To identify candidate genes of feminization induced by Wolbachia strain wVulC from A. vulgare, we sequenced the genome of Wolbachia strain wCon from Cylisticus convexus, the most closely related known Wolbachia strain to wVulC that does not induce feminization, and compared it to the wVulC genome. Then, we performed gene expression profiling of the 216 resulting wVulC candidate genes throughout host developmental stages in A. vulgare and the heterologous host C. convexus. We identified a set of 35 feminization candidate genes showing differential expression during host sexual development. Interestingly, 27 of the 35 genes are present in the f element, which is a piece of a feminizing Wolbachia genome horizontally transferred into the nuclear genome of A. vulgare and involved in female sex determination. Assuming that the molecular genetic basis of feminization by Wolbachia and the f element is the same, the 27 genes are candidates for acting as master sex determination genes in A. vulgare females carrying the f element. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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18 pages, 1118 KiB

Open AccessArticle

Genetic Diversity in the UV Sex Chromosomes of the Brown Alga Ectocarpus

by Komlan Avia, Agnieszka P. Lipinska, Laure Mignerot, Alejandro E. Montecinos, Mahwash Jamy, Sophia Ahmed, Myriam Valero, Akira F. Peters, J. Mark Cock, Denis Roze and Susana M. Coelho

Genes 2018, 9(6), 286; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9060286 - 06 Jun 2018

Cited by 13 | Viewed by 6170

Abstract

Three types of sex chromosome system exist in nature: diploid XY and ZW systems and haploid UV systems. For many years, research has focused exclusively on XY and ZW systems, leaving UV chromosomes and haploid sex determination largely neglected. Here, we perform a detailed analysis of DNA sequence neutral diversity levels across the U and V sex chromosomes of the model brown alga Ectocarpus using a large population dataset. We show that the U and V non-recombining regions of the sex chromosomes (SDR) exhibit about half as much neutral diversity as the autosomes. This difference is consistent with the reduced effective population size of these regions compared with the rest of the genome, suggesting that the influence of additional factors such as background selection or selective sweeps is minimal. The pseudoautosomal region (PAR) of this UV system, in contrast, exhibited surprisingly high neutral diversity and there were several indications that genes in this region may be under balancing selection. The PAR of Ectocarpus is known to exhibit unusual genomic features and our results lay the foundation for further work aimed at understanding whether, and to what extent, these structural features underlie the high level of genetic diversity. Overall, this study fills a gap between available information on genetic diversity in XY/ZW systems and UV systems and significantly contributes to advancing our knowledge of the evolution of UV sex chromosomes. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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16 pages, 6809 KiB

Open AccessArticle

Sex Chromosomes of the Iconic Moth Abraxas grossulariata (Lepidoptera, Geometridae) and Its Congener A. sylvata

by Magda Zrzavá, Irena Hladová, Martina Dalíková, Jindra Šíchová, Erki Õunap, Svatava Kubíčková and František Marec

Genes 2018, 9(6), 279; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9060279 - 31 May 2018

Cited by 18 | Viewed by 5626

Abstract

The magpie moth, Abraxas grossulariata, is an iconic species in which female heterogamety was discovered at the beginning of the 20th century. However, the sex chromosomes of this species have not yet been cytologically identified. We describe the sex chromosomes of A. grossulariata and its congener, A. sylvata. Although these species split only around 9.5 million years ago, and both species have the expected WZ/ZZ chromosomal system of sex determination and their sex chromosomes share the major ribosomal DNA (rDNA) representing the nucleolar organizer region (NOR), we found major differences between their karyotypes, including between their sex chromosomes. The species differ in chromosome number, which is 2n = 56 in A. grossularita and 2n = 58 in A. sylvata. In addition, A. grossularita autosomes exhibit massive autosomal blocks of heterochromatin, which is a very rare phenomenon in Lepidoptera, whereas the autosomes of A. sylvata are completely devoid of distinct heterochromatin. Their W chromosomes differ greatly. Although they are largely composed of female-specific DNA sequences, as shown by comparative genomic hybridization, cross-species W-chromosome painting revealed considerable sequence differences between them. The results suggest a relatively rapid molecular divergence of Abraxas W chromosomes by the independent spreading of female-specific repetitive sequences. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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15 pages, 2104 KiB

Open AccessArticle

Size and Content of the Sex-Determining Region of the Y Chromosome in Dioecious Mercurialis annua, a Plant with Homomorphic Sex Chromosomes

by Paris Veltsos, Guillaume Cossard, Emmanuel Beaudoing, Genséric Beydon, Dessislava Savova Bianchi, Camille Roux, Santiago C. González-Martínez and John R. Pannell

Genes 2018, 9(6), 277; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9060277 - 29 May 2018

Cited by 16 | Viewed by 6098

Abstract

Dioecious plants vary in whether their sex chromosomes are heteromorphic or homomorphic, but even homomorphic sex chromosomes may show divergence between homologues in the non-recombining, sex-determining region (SDR). Very little is known about the SDR of these species, which might represent particularly early stages of sex-chromosome evolution. Here, we assess the size and content of the SDR of the diploid dioecious herb Mercurialis annua, a species with homomorphic sex chromosomes and mild Y-chromosome degeneration. We used RNA sequencing (RNAseq) to identify new Y-linked markers for M. annua. Twelve of 24 transcripts showing male-specific expression in a previous experiment could be amplified by polymerase chain reaction (PCR) only from males, and are thus likely to be Y-linked. Analysis of genome-capture data from multiple populations of M. annua pointed to an additional six male-limited (and thus Y-linked) sequences. We used these markers to identify and sequence 17 sex-linked bacterial artificial chromosomes (BACs), which form 11 groups of non-overlapping sequences, covering a total sequence length of about 1.5 Mb. Content analysis of this region suggests that it is enriched for repeats, has low gene density, and contains few candidate sex-determining genes. The BACs map to a subset of the sex-linked region of the genetic map, which we estimate to be at least 14.5 Mb. This is substantially larger than estimates for other dioecious plants with homomorphic sex chromosomes, both in absolute terms and relative to their genome sizes. Our data provide a rare, high-resolution view of the homomorphic Y chromosome of a dioecious plant. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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16 pages, 3116 KiB

Open AccessArticle

Reorganization of the Y Chromosomes Enhances Divergence in Israeli Mole Rats Nannospalax ehrenbergi (Spalacidae, Rodentia): Comparative Analysis of Meiotic and Mitotic Chromosomes

by Sergey Matveevsky, Elena Ivanitskaya, Victor Spangenberg, Irina Bakloushinskaya and Oxana Kolomiets

Genes 2018, 9(6), 272; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9060272 - 24 May 2018

Cited by 3 | Viewed by 4359

Abstract

The Y chromosome in mammals is variable, even in closely related species. Middle East blind mole rats Nannospalax ehrenbergi demonstrate autosomal variability, which probably leads to speciation. Here, we compare the mitotic and meiotic chromosomes of mole rats. For the first time, we studied the behavior of their sex chromosomes in the meiotic prophase I using electron microscopy and immunocytochemical analysis. Unexpectedly, the sex chromosomes of the 52- and 60-chromosome forms of mole rats showed different synaptic and recombination patterns due to distinct locations of the centromeres on the Y chromosomes. The absence of recombination in the 60-chromosome form, the asymmetric synapsis, and the short-term disturbance in the synaptic co-orientation of the telomeric regions of the X and Y chromosomes were revealed as specific features of mole rat sex bivalents. We suggest several scenarios of Y chromosome alteration in connection with species differentiation in mole rats. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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13 pages, 400 KiB

Open AccessFeature PaperArticle

Regulation of the X Chromosome in the Germline and Soma of Drosophila melanogaster Males

by Eliza Argyridou and John Parsch

Genes 2018, 9(5), 242; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9050242 - 04 May 2018

Cited by 10 | Viewed by 4784

Abstract

During the evolution of heteromorphic sex chromosomes, the sex-specific Y chromosome degenerates, while the X chromosome evolves new mechanisms of regulation. Using bioinformatic and experimental approaches, we investigate the expression of the X chromosome in Drosophila melanogaster. We observe nearly complete X chromosome dosage compensation in male somatic tissues, but not in testis. The X chromosome contains disproportionately fewer genes with high expression in testis than the autosomes, even after accounting for the lack of dosage compensation, which suggests that another mechanism suppresses their expression in the male germline. This is consistent with studies of reporter genes and transposed genes, which find that the same gene has higher expression when autosomal than when X-linked. Using a new reporter gene that is expressed in both testis and somatic tissues, we find that the suppression of X-linked gene expression is limited to genes with high expression in testis and that the extent of the suppression is positively correlated with expression level. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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12 pages, 821 KiB

Open AccessArticle

Shared and Species-Specific Patterns of Nascent Y Chromosome Evolution in Two Guppy Species

by Jake Morris, Iulia Darolti, Natasha I. Bloch, Alison E. Wright and Judith E. Mank

Genes 2018, 9(5), 238; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9050238 - 03 May 2018

Cited by 20 | Viewed by 5481

Abstract

Sex chromosomes form once recombination is halted around the sex-determining locus between a homologous pair of chromosomes, resulting in a male-limited Y chromosome. We recently characterized the nascent sex chromosome system in the Trinidadian guppy (Poecilia reticulata). The guppy Y is one of the youngest animal sex chromosomes yet identified, and therefore offers a unique window into the early evolutionary forces shaping sex chromosome formation, particularly the rate of accumulation of repetitive elements and Y-specific sequence. We used comparisons between male and female genomes in P. reticulata and its sister species, Endler’s guppy (P. wingei), which share an ancestral sex chromosome, to identify male-specific sequences and to characterize the degree of differentiation between the X and Y chromosomes. We identified male-specific sequence shared between P. reticulata and P. wingei consistent with a small ancestral non-recombining region. Our assembly of this Y-specific sequence shows substantial homology to the X chromosome, and appears to be significantly enriched for genes implicated in pigmentation. We also found two plausible candidates that may be involved in sex determination. Furthermore, we found that the P. wingei Y chromosome exhibits a greater signature of repetitive element accumulation than the P. reticulata Y chromosome. This suggests that Y chromosome divergence does not necessarily correlate with the time since recombination suppression. Overall, our results reveal the early stages of Y chromosome divergence in the guppy. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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18 pages, 1592 KiB

Open AccessArticle

A Comparison of Selective Pressures in Plant X-Linked and Autosomal Genes

by Marc Krasovec, Bruno Nevado and Dmitry A. Filatov

Genes 2018, 9(5), 234; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9050234 - 03 May 2018

Cited by 4 | Viewed by 4084

Abstract

Selection is expected to work differently in autosomal and X-linked genes because of their ploidy difference and the exposure of recessive X-linked mutations to haploid selection in males. However, it is not clear whether these expectations apply to recently evolved sex chromosomes, where many genes retain functional X- and Y-linked gametologs. We took advantage of the recently evolved sex chromosomes in the plant Silene latifolia and its closely related species to compare the selective pressures between hemizygous and non-hemizygous X-linked genes as well as between X-linked genes and autosomal genes. Our analysis, based on over 1000 genes, demonstrated that, similar to animals, X-linked genes in Silene evolve significantly faster than autosomal genes—the so-called faster-X effect. Contrary to expectations, faster-X divergence was detectable only for non-hemizygous X-linked genes. Our phylogeny-based analyses of selection revealed no evidence for faster adaptation in X-linked genes compared to autosomal genes. On the other hand, partial relaxation of purifying selection was apparent on the X-chromosome compared to the autosomes, consistent with a smaller genetic diversity in S. latifolia X-linked genes (π_x = 0.016; π_aut = 0.023). Thus, the faster-X divergence in S. latifolia appears to be a consequence of the smaller effective population size rather than of a faster adaptive evolution on the X-chromosome. We argue that this may be a general feature of “young” sex chromosomes, where the majority of X-linked genes are not hemizygous, preventing haploid selection in heterogametic sex. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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Review

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18 pages, 1612 KiB

Open AccessFeature PaperReview

The Guppy Sex Chromosome System and the Sexually Antagonistic Polymorphism Hypothesis for Y Chromosome Recombination Suppression

by Deborah Charlesworth

Genes 2018, 9(5), 264; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9050264 - 19 May 2018

Cited by 29 | Viewed by 7626

Abstract

Sex chromosomes regularly evolve suppressed recombination, distinguishing them from other chromosomes, and the reason for this has been debated for many years. It is now clear that non-recombining sex-linked regions have arisen in different ways in different organisms. A major hypothesis is that a sex-determining gene arises on a chromosome and that sexually antagonistic (SA) selection (sometimes called intra-locus sexual conflict) acting at a linked gene has led to the evolution of recombination suppression in the region, to reduce the frequency of low fitness recombinant genotypes produced. The sex chromosome system of the guppy (Poecilia reticulata) is often cited as supporting this hypothesis because SA selection has been demonstrated to act on male coloration in natural populations of this fish, and probably contributes to maintaining polymorphisms for the genetic factors involved. I review classical genetic and new molecular genetic results from the guppy, and other fish, including approaches for identifying the genome regions carrying sex-determining loci, and suggest that the guppy may exemplify a recently proposed route to sex chromosome evolution. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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16 pages, 6321 KiB

Open AccessReview

The Colorful Sex Chromosomes of Teleost Fish

by Verena A. Kottler and Manfred Schartl

Genes 2018, 9(5), 233; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9050233 - 03 May 2018

Cited by 30 | Viewed by 7598

Abstract

Teleost fish provide some of the most intriguing examples of sexually dimorphic coloration, which is often advantageous for only one of the sexes. Mapping studies demonstrated that the genetic loci underlying such color patterns are frequently in tight linkage to the sex-determining locus of a species, ensuring sex-specific expression of the corresponding trait. Several genes affecting color synthesis and pigment cell development have been previously described, but the color loci on the sex chromosomes have mostly remained elusive as yet. Here, we summarize the current knowledge about the genetics of such color loci in teleosts, mainly from studies on poeciliids and cichlids. Further studies on these color loci will certainly provide important insights into the evolution of sex chromosomes. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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13 pages, 1369 KiB

Open AccessReview

The Methylome of Vertebrate Sex Chromosomes

by Shafagh A. Waters, Alexander Capraro, Kim L. McIntyre, Jennifer A. Marshall Graves and Paul D. Waters

Genes 2018, 9(5), 230; https://0-doi-org.brum.beds.ac.uk/10.3390/genes9050230 - 01 May 2018

Cited by 9 | Viewed by 5870

Abstract

DNA methylation is a key epigenetic modification in vertebrate genomes known to be involved in the regulation of gene expression, X chromosome inactivation, genomic imprinting, chromatin structure, and control of transposable elements. DNA methylation is common to all eukaryote genomes, but we still lack a complete understanding of the variation in DNA methylation patterns on sex chromosomes and between the sexes in diverse species. To better understand sex chromosome DNA methylation patterns between different amniote vertebrates, we review literature that has analyzed the genome-wide distribution of DNA methylation in mammals and birds. In each system, we focus on DNA methylation patterns on the autosomes versus the sex chromosomes. Full article

(This article belongs to the Special Issue The Evolutionary Life Cycle of Sex Chromosomes)

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