scholarly journals A neutral model for the loss of recombination on sex chromosomes

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200096 ◽  
Author(s):  
Daniel L. Jeffries ◽  
Jörn F. Gerchen ◽  
Mathias Scharmann ◽  
John R. Pannell
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
Theme Issue ◽  
Recombination Rates ◽  
Natural Systems ◽  
Adaptive Processes ◽  
Sexually Antagonistic Selection ◽  
Suppressed Recombination

The loss of recombination between sex chromosomes has occurred repeatedly throughout nature, with important implications for their subsequent evolution. Explanations for this remarkable convergence have generally invoked only adaptive processes (e.g. sexually antagonistic selection); however, there is still little evidence for these hypotheses. Here we propose a model in which recombination on sex chromosomes is lost due to the neutral accumulation of sequence divergence adjacent to (and thus, in linkage disequilibrium with) the sex determiner. Importantly, we include in our model the fact that sequence divergence, in any form, reduces the probability of recombination between any two sequences. Using simulations, we show that, under certain conditions, a region of suppressed recombination arises and expands outwards from the sex-determining locus, under purely neutral processes. Further, we show that the rate and pattern of recombination loss are sensitive to the pre-existing recombination landscape of the genome and to sex differences in recombination rates, with patterns consistent with evolutionary strata emerging under some conditions. We discuss the applicability of these results to natural systems. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

scholarly journals Early sex-chromosome evolution in the diploid dioecious plant Mercurialis annua

2017 ◽  
Author(s):  
Paris Veltsos ◽  
Kate E. Ridout ◽  
Melissa A. Toups ◽  
Santiago C. González-Martínez ◽  
Aline Muyle ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Gene Loss ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
Sex Chromosome Evolution ◽  
Dioecious Plant ◽  
Suppressed Recombination ◽  
Mercurialis Annua

AbstractSuppressed recombination around a sex-determining locus allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. Both genetic mapping and exome resequencing of individuals across the species range independently identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about a third of the Y chromosome has ceased recombining, a region containing 568 transcripts and spanning 22.3 cM in the corresponding female map. Patterns of gene expression hint at the possible role of sexually antagonistic selection in having favored suppressed recombination. In total, the genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. There was limited evidence of Y-chromosome degeneration in terms of gene loss and pseudogenization, but sequence divergence between the X and Y copies of many sex-linked genes was higher than between M. annua and its dioecious sister species M. huetii with which it shares a sex-determining region. The Mendelian inheritance of sex in interspecific crosses, combined with the other observed pattern, suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining about one million years ago.Article summaryPlants that evolved separate sexes (dioecy) recently are ideal models for studying the early stages of sex-chromosome evolution. Here, we use karyological, whole genome and transcriptome data to characterize the homomorphic sex chromosomes of the annual dioecious plant Mercurialis annua. Our analysis reveals many typical hallmarks of dioecy and sex-chromosome evolution, including sex-biased gene expression and high X/Y sequence divergence, yet few premature stop codons in Y-linked genes and very little outright gene loss, despite 1/3 of the sex chromosome having ceased recombination in males. Our results confirm that the M. annua species complex is a fertile system for probing early stages in the evolution of sex chromosomes.

scholarly journals Interaction between sex-determining genes from two species: clues from Xenopus hybrids

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200104 ◽  
Author(s):  
Álvaro S. Roco ◽  
Adrián Ruiz-García ◽  
Mónica Bullejos
Keyword(s):  
Sex Chromosomes ◽  
Ovarian Development ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Parental Species ◽  
Z Chromosome ◽  
Gonadal Differentiation ◽  
Theme Issue ◽  
Testicular Differentiation

Hybrids provide an interesting model to study the evolution of sex-determining genes and sex chromosome systems as they offer the opportunity to see how independently evolving sex-determining pathways interact in vivo . In this context, the genus Xenopus represents a stimulating model, since species with non-homologous sex chromosomes and different sex-determining genes have been identified. In addition, the possibility of interspecies breeding is favoured in this group, which arose by alloploidization events, with species ploidy ranging from 2 n = 2 x = 20 in X. tropicalis (the only diploid representative of the genus) to 2 n = 12 x = 108 in X. ruwenzoriensis . To study how two sex-determining genes interact in vivo , X. laevis × X. tropicali s hybrids were produced. Gonadal differentiation in these hybrids revealed that the dm-w gene is dominant over X. tropicalis male-determining sex chromosomes (Y or Z), even though the Y chromosome is dominant in X. tropicalis (Y > W>Z). In the absence of the dm-w gene (the Z chromosome from X. laevis is present), the W chromosome from X. tropicalis is able to trigger ovarian development. Testicular differentiation will take place in the absence of W chromosomes from any of the parental species. The dominance/recessivity relationships between these sex-determining loci in the context of either parental genome remains unknown. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

scholarly journals Evolution of sex chromosomes is prior to speciation in the dioecious Phoenix species

2015 ◽  
Author(s):  
Emira Cherif ◽  
Salwa Zehdi ◽  
Amandine Crabos ◽  
Karina Castillo ◽  
Nathalie Chabrillange ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Applied Research ◽  
Date Palm ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Driving Forces ◽  
Molecular Processes ◽  
Dioecious Species ◽  
The Family ◽  
Suppressed Recombination

Understanding the driving forces and molecular processes underlying dioecy and sex chromosome evolution, leading from hermaphroditism to the occurrence of male and female individuals, is of considerable interest in fundamental and applied research. The genus Phoenix, belonging to the family Arecaceae, consists of only dioecious species. Phylogenetic data suggests that the genus Phoenix diverged from a hermaphroditic ancestor shared with its closest relatives. Here we investigated the evolution of suppressed recombination within the genus Phoenix as a whole by extending the analysis of P. dactylifera sex-related loci to eight other species within the genus. We also performed a phylogenetic analysis of a date palm sex-linked PdMYB1 gene in these species. We found that X and Y sex-linked alleles clustered in a species-independent fashion. Our data show that sex chromosomes evolved before the diversification of the extant dioecious species. Furthermore, the distribution of Y haplotypes revealed two male ancestral paternal lineages which may have emerged prior to speciation.

scholarly journals Evolution of master sex determiners: TGF-β signalling pathways at regulatory crossroads

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200091 ◽  
Author(s):  
Qiaowei Pan ◽  
Tomas Kay ◽  
Alexandra Depincé ◽  
Mateus Adolfi ◽  
Manfred Schartl ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Sex Chromosomes ◽  
Regulatory Network ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Signalling Pathway ◽  
Signalling Pathways ◽  
Sex Chromosome Evolution ◽  
Theme Issue ◽  
Gene Regulatory

To date, more than 20 different vertebrate master sex-determining genes have been identified on different sex chromosomes of mammals, birds, frogs and fish. Interestingly, six of these genes are transcription factors ( Dmrt1 - or Sox3 - related) and 13 others belong to the TGF-β signalling pathway ( Amh , Amhr2 , Bmpr1b , Gsdf and Gdf6 ). This pattern suggests that only a limited group of factors/signalling pathways are prone to become top regulators again and again. Although being clearly a subordinate member of the sex-regulatory network in mammals, the TGF-β signalling pathway made it to the top recurrently and independently. Facing this rolling wave of TGF-β signalling pathways, this review will decipher how the TGF-β signalling pathways cope with the canonical sex gene regulatory network and challenge the current evolutionary concepts accounting for the diversity of sex-determining mechanisms. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

scholarly journals Sex chromosome degeneration, turnover, and sex-biased expression of sex-linked transcripts in African clawed frogs ( Xenopus )

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200095 ◽  
Author(s):  
Xue-Ying Song ◽  
Benjamin L. S. Furman ◽  
Tharindu Premachandra ◽  
Martin Knytl ◽  
Caroline M. S. Cauret ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Z Chromosome ◽  
Sex Chromosome Evolution ◽  
Theme Issue ◽  
Recombination Suppression ◽  
Closely Related Species ◽  
African Clawed Frog ◽  
Clawed Frog

The tempo of sex chromosome evolution—how quickly, in what order, why and how their particular characteristics emerge during evolution—remains poorly understood. To understand this further, we studied three closely related species of African clawed frog (genus Xenopus ), that each has independently evolved sex chromosomes. We identified population polymorphism in the extent of sex chromosome differentiation in wild-caught Xenopus borealis that corresponds to a large, previously identified region of recombination suppression. This large sex-linked region of X. borealis has an extreme concentration of genes that encode transcripts with sex-biased expression, and we recovered similar findings in the smaller sex-linked regions of Xenopus laevis and Xenopus tropicalis . In two of these species, strong skews in expression (mostly female-biased in X. borealis , mostly male-biased in X. tropicalis ) are consistent with expectations associated with recombination suppression, and in X. borealis , we hypothesize that a degenerate ancestral Y-chromosome transitioned into its contemporary Z-chromosome. These findings indicate that Xenopus species are tolerant of differences between the sexes in dosage of the products of multiple genes, and offer insights into how evolutionary transformations of ancestral sex chromosomes carry forward to affect the function of new sex chromosomes. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

scholarly journals Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200097
Author(s):  
Lukáš Kratochvíl ◽  
Matthias Stöck ◽  
Michail Rovatsos ◽  
Mónica Bullejos ◽  
Amaury Herpin ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Gonadal Differentiation ◽  
Sex Chromosome Evolution ◽  
Theme Issue ◽  
Recombination Suppression ◽  
Evolutionary Forces ◽  
Individual Fitness ◽  
Genomic Material

Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexually antagonistic/advantageous alleles, resulting in Y or W degeneration and potentially culminating in their disappearance. Based mostly on empirical vertebrate research, we challenge and expand each conceptual step of this canonical model and present observations by numerous experts in two parts of a theme issue of Phil. Trans. R. Soc. B. We suggest that greater theoretical and empirical insights into the events at the origins of sex-determining genes (rewiring of the gonadal differentiation networks), and a better understanding of the evolutionary forces responsible for recombination suppression are required. Among others, crucial questions are: Why do sex chromosome differentiation rates and the evolution of gene dose regulatory mechanisms between male versus female heterogametic systems not follow earlier theory? Why do several lineages not have sex chromosomes? And: What are the consequences of the presence of (differentiated) sex chromosomes for individual fitness, evolvability, hybridization and diversification? We conclude that the classical scenario appears too reductionistic. Instead of being unidirectional, we show that sex chromosome evolution is more complex than previously anticipated and principally forms networks, interconnected to potentially endless outcomes with restarts, deletions and additions of new genomic material. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

scholarly journals Phylogeny, transposable element and sex chromosome evolution of the basal lineage of birds

2019 ◽  
Author(s):  
Zongji Wang ◽  
Jilin Zhang ◽  
Xiaoman Xu ◽  
Christopher Witt ◽  
Yuan Deng ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sequence Divergence ◽  
South American ◽  
Sex Chromosome Evolution ◽  
Rapid Speciation ◽  
Genome Wide ◽  
Divergence Pattern ◽  
Female Specific

AbstractSex chromosomes of mammals and most birds are heteromorphic, while those of many paleognaths (ratites and tinamous) are inexplicably homomorphic. To dissect the mechanisms underlying the different tempo of sex chromosome evolution, we produced high-quality genomes of 12 paleognathous species, and reconstructed their phylogeny based on alignments of the non-coding sequences extending to nearly 40% of the genome. Our phylogenomic tree grouped the South American rheas and tinamous together, and supported the independent evolution of gigantism and loss of flight among ratites. The small-bodied tinamous have much higher rates of genome-wide substitutions and transposon turnovers. Yet majorities of both have retained exceptionally long recombining regions occupying over half of the entire sex chromosome, with the rest sex-linked regions diverging from each other at a much lower rate relative to neognathous birds. Each species exhibits a punctuated sequence divergence pattern between sex chromosomes termed ‘evolutionary strata’, because of stepwise suppression of recombination. We concluded that all paleognaths share one evolutionary stratum with all other birds, and convergently formed between one to three strata after their rapid speciation. Contrary to the classic notion, we provided clear evidence that the youngest stratum of some tinamous formed without chromosomal inversion. Intriguingly, some of the encompassing W-linked genes have upregulated their expression levels in ovary, probably due to the female-specific selection. We proposed here that the unique male-only parental care system of paleognaths has reduced the intensity of sexual selection, and contributed to these species’ low rates of sex chromosome evolution. We also provided novel insights into the evolution of W-linked genes at their early stages.

scholarly journals Early Sex-Chromosome Evolution in the Diploid Dioecious Plant Mercurialis annua

Genetics ◽  
2019 ◽  
Vol 212 (3) ◽  
pp. 815-835 ◽  
Author(s):  
Paris Veltsos ◽  
Kate E. Ridout ◽  
Melissa A. Toups ◽  
Santiago C. González-Martínez ◽  
Aline Muyle ◽  
...  
Keyword(s):  
Genetic Mapping ◽  
Y Chromosome ◽  
Sex Chromosomes ◽  
Genome Assembly ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
De Novo ◽  
Sex Chromosome Evolution ◽  
Suppressed Recombination ◽  
Mercurialis Annua

Suppressed recombination allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. The genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. Genetic mapping and exome resequencing of individuals across the species range both identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about one-third of the Y chromosome, containing 568 transcripts and spanning 22.3 cM in the corresponding female map, has ceased recombining. Nevertheless, we found limited evidence for Y-chromosome degeneration in terms of gene loss and pseudogenization, and most X- and Y-linked genes appear to have diverged in the period subsequent to speciation between M. annua and its sister species M. huetii, which shares the same sex-determining region. Taken together, our results suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining ∼1 MYA. Patterns of gene expression within the nonrecombining region are consistent with the idea that sexually antagonistic selection may have played a role in favoring suppressed recombination.

scholarly journals Why Do Some Sex Chromosomes Degenerate More Slowly Than Others? The Odd Case of Ratite Sex Chromosomes

Genes ◽  
2020 ◽  
Vol 11 (10) ◽  
pp. 1153 ◽  
Author(s):  
Homa Papoli Yazdi ◽  
Willian T. A. F. Silva ◽  
Alexander Suh
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Current Data ◽  
W Chromosome ◽  
Sex Chromosome Evolution ◽  
History Of ◽  
Sexually Antagonistic Selection ◽  
Ratite Birds ◽  
Genome Assemblies

The hallmark of sex chromosome evolution is the progressive suppression of recombination which leads to subsequent degeneration of the non-recombining chromosome. In birds, species belonging to the two major clades, Palaeognathae (including tinamous and flightless ratites) and Neognathae (all remaining birds), show distinctive patterns of sex chromosome degeneration. Birds are female heterogametic, in which females have a Z and a W chromosome. In Neognathae, the highly-degenerated W chromosome seems to have followed the expected trajectory of sex chromosome evolution. In contrast, among Palaeognathae, sex chromosomes of ratite birds are largely recombining. The underlying reason for maintenance of recombination between sex chromosomes in ratites is not clear. Degeneration of the W chromosome might have halted or slowed down due to a multitude of reasons ranging from selective processes, such as a less pronounced effect of sexually antagonistic selection, to neutral processes, such as a slower rate of molecular evolution in ratites. The production of genome assemblies and gene expression data for species of Palaeognathae has made it possible, during recent years, to have a closer look at their sex chromosome evolution. Here, we critically evaluate the understanding of the maintenance of recombination in ratites in light of the current data. We conclude by highlighting certain aspects of sex chromosome evolution in ratites that require further research and can potentially increase power for the inference of the unique history of sex chromosome evolution in this lineage of birds.

scholarly journals Evolution of recombination rates between sex chromosomes

2017 ◽  
Vol 372 (1736) ◽  
pp. 20160456 ◽  
Author(s):  
Deborah Charlesworth
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Molecular Genetic ◽  
Rate Variation ◽  
Recombination Rates ◽  
Recombination Suppression ◽  
Proximate Mechanisms ◽  
Chromosomal Heteromorphism ◽  
Suppressed Recombination ◽  
Recombination Rate Variation

In species with genetic sex-determination, the chromosomes carrying the sex-determining genes have often evolved non-recombining regions and subsequently evolved the full set of characteristics denoted by the term ‘sex chromosomes’. These include size differences, creating chromosomal heteromorphism, and loss of gene functions from one member of the chromosome pair. Such characteristics and changes have been widely reviewed, and underlie molecular genetic approaches that can detect sex chromosome regions. This review deals mainly with the evolution of new non-recombining regions, focusing on how certain evolutionary situations select for suppressed recombination (rather than the proximate mechanisms causing suppressed recombination between sex chromosomes). Particularly important is the likely involvement of sexually antagonistic polymorphisms in genome regions closely linked to sex-determining loci. These may be responsible for the evolutionary strata of sex chromosomes that have repeatedly formed by recombination suppression evolving across large genome regions. More studies of recently evolved non-recombining sex-determining regions should help to test this hypothesis empirically, and may provide evidence about whether other situations can sometimes lead to sex-linked regions evolving. Similarities with other non-recombining genome regions are discussed briefly, to illustrate common features of the different cases, though no general properties apply to all of them. This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

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