Transition from environmental to partial genetic sex determination in Daphnia through the evolution of a female-determining incipient W-chromosome

AbstractSex chromosomes can evolve during the evolution of genetic sex determination (GSD) from environmental sex determination (ESD). Despite theoretical attention, early mechanisms involved in the transition from ESD to GSD have yet to be studied in nature. No mixed ESD-GSD animal species have been reported, except for some species of Daphnia, small freshwater crustaceans in which sex is usually determined solely by the environment, but in which a dominant female sex-determining locus is present in some populations. This locus follows Mendelian single-locus inheritance, but has otherwise not been characterized genetically. We now show that the sex-determining genomic region maps to the same low-recombining peri-centromeric region of linkage group 3 (LG3) in three highly divergent populations of D. magna, and spans 3.6 Mb. Despite low levels of recombination, the associated region contains signs of historical recombination, suggesting a role for selection acting on several genes thereby maintaining linkage disequilibrium among the 36 associated SNPs. The region carries numerous genes involved in sex differentiation in other taxa, including transformer2 and sox9. Taken together, the region determining the NMP phenotype shows characteristics of a sex-related supergene, suggesting that LG3 is potentially an incipient W chromosome despite the lack of significant additional restriction of recombination between Z and W. The occurrence of the female-determining locus in a pre-existing low recombining region illustrates one possible form of recombination suppression in sex chromosomes. D. magna is a promising model for studying the evolutionary transitions from ESD to GSD and early sex chromosome evolution.

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Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1608979113 ◽

2016 ◽

Vol 113 (52) ◽

pp. 15036-15041 ◽

Cited By ~ 52

Author(s):

Sébastien Leclercq ◽

Julien Thézé ◽

Mohamed Amine Chebbi ◽

Isabelle Giraud ◽

Bouziane Moumen ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Nuclear Genome ◽

Closely Related Species ◽

Evolutionary Transitions ◽

Female Sex ◽

Bacterial Endosymbionts ◽

The Common ◽

And Behavior

Sex determination is a fundamental developmental pathway governing male and female differentiation, with profound implications for morphology, reproductive strategies, and behavior. In animals, sex differences between males and females are generally determined by genetic factors carried by sex chromosomes. Sex chromosomes are remarkably variable in origin and can differ even between closely related species, indicating that transitions occur frequently and independently in different groups of organisms. The evolutionary causes underlying sex chromosome turnover are poorly understood, however. Here we provide evidence indicating that Wolbachia bacterial endosymbionts triggered the evolution of new sex chromosomes in the common pillbug Armadillidium vulgare. We identified a 3-Mb insert of a feminizing Wolbachia genome that was recently transferred into the pillbug nuclear genome. The Wolbachia insert shows perfect linkage to the female sex, occurs in a male genetic background (i.e., lacking the ancestral W female sex chromosome), and is hemizygous. Our results support the conclusion that the Wolbachia insert is now acting as a female sex-determining region in pillbugs, and that the chromosome carrying the insert is a new W sex chromosome. Thus, bacteria-to-animal horizontal genome transfer represents a remarkable mechanism underpinning the birth of sex chromosomes. We conclude that sex ratio distorters, such as Wolbachia endosymbionts, can be powerful agents of evolutionary transitions in sex determination systems in animals.

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A frog with three sex chromosomes that co-mingle together in nature: Xenopus tropicalis has a degenerate W and a Y that evolved from a Z chromosome

PLoS Genetics ◽

10.1371/journal.pgen.1009121 ◽

2020 ◽

Vol 16 (11) ◽

pp. e1009121

Author(s):

Benjamin L. S. Furman ◽

Caroline M. S. Cauret ◽

Martin Knytl ◽

Xue-Ying Song ◽

Tharindu Premachandra ◽

...

Keyword(s):

Sex Differences ◽

Y Chromosome ◽

Sex Chromosomes ◽

Sexual Differentiation ◽

Sex Chromosome ◽

Xenopus Tropicalis ◽

Z Chromosome ◽

W Chromosome ◽

Recombination Suppression ◽

Determining Factor

In many species, sexual differentiation is a vital prelude to reproduction, and disruption of this process can have severe fitness effects, including sterility. It is thus interesting that genetic systems governing sexual differentiation vary among—and even within—species. To understand these systems more, we investigated a rare example of a frog with three sex chromosomes: the Western clawed frog, Xenopus tropicalis. We demonstrate that natural populations from the western and eastern edges of Ghana have a young Y chromosome, and that a male-determining factor on this Y chromosome is in a very similar genomic location as a previously known female-determining factor on the W chromosome. Nucleotide polymorphism of expressed transcripts suggests genetic degeneration on the W chromosome, emergence of a new Y chromosome from an ancestral Z chromosome, and natural co-mingling of the W, Z, and Y chromosomes in the same population. Compared to the rest of the genome, a small sex-associated portion of the sex chromosomes has a 50-fold enrichment of transcripts with male-biased expression during early gonadal differentiation. Additionally, X. tropicalis has sex-differences in the rates and genomic locations of recombination events during gametogenesis that are similar to at least two other Xenopus species, which suggests that sex differences in recombination are genus-wide. These findings are consistent with theoretical expectations associated with recombination suppression on sex chromosomes, demonstrate that several characteristics of old and established sex chromosomes (e.g., nucleotide divergence, sex biased expression) can arise well before sex chromosomes become cytogenetically distinguished, and show how these characteristics can have lingering consequences that are carried forward through sex chromosome turnovers.

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Genome-wide association mapping uncovers sex-associated copy number variation markers and female hemizygous regions on the W chromosome in Salix viminalis

BMC Genomics ◽

10.1186/s12864-021-08021-2 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Henrik R. Hallingbäck ◽

Pascal Pucholt ◽

Pär K. Ingvarsson ◽

Ann Christin Rönnberg-Wästljung ◽

Sofia Berlin

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Chromosome 9 ◽

Genome Wide Association ◽

Salix Viminalis ◽

Chromosome 15 ◽

W Chromosome ◽

Genome Wide ◽

Heterogametic Sex

Abstract Background Sex chromosomes are in some species largely undifferentiated (homomorphic) with restricted sex determination regions. Homomorphic but different sex chromosomes are found in the closely related genera Populus and Salix indicating flexible sex determination systems, ideal for studies of processes involved in sex chromosome evolution. We have performed genome-wide association studies of sex and analysed sex chromosomes in a population of 265 wild collected Salix viminalis accessions and studied the sex determining locus. Results A total of 19,592 markers were used in association analyses using both Fisher’s exact tests and a single-marker mixed linear model, which resulted in 48 and 41 sex-associated (SA) markers respectively. Across all 48 SA markers, females were much more often heterozygous than males, which is expected if females were the heterogametic sex. The majority of the SA markers were, based on positions in the S. purpurea genome, located on chromosome 15, previously demonstrated to be the sex chromosome. Interestingly, when mapping the genotyping-by-sequencing sequence tag harbouring the two SA markers with the highest significance to the S. viminalis genomic scaffolds, five regions of very high similarity were found: three on a scaffold that represents a part of chromosome 15, one on a scaffold that represents a part of chromosome 9 and one on a scaffold not anchored to the genome. Based on segregation differences of the alleles at the two marker positions and on differences in PCR amplification between females and males we conclude that females had multiple copies of this DNA fragment (chromosome 9 and 15), whereas males only had one (chromosome 9). We therefore postulate that the female specific sequences have been copied from chromosome 9 and inserted on chromosome 15, subsequently developing into a hemizygous W chromosome linked region. Conclusions Our results support that sex determination in S. viminalis is controlled by one locus on chromosome 15. The segregation patterns observed at the SA markers furthermore confirm that S. viminalis females are the heterogametic sex. We also identified a translocation from chromosome 9 to the W chromosome.

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Developmental Systems Drift and the Drivers of Sex Chromosome Evolution

Molecular Biology and Evolution ◽

10.1093/molbev/msz268 ◽

2019 ◽

Vol 37 (3) ◽

pp. 799-810 ◽

Cited By ~ 1

Author(s):

Caroline M S Cauret ◽

Marie-Theres Gansauge ◽

Andrew S Tupper ◽

Benjamin L S Furman ◽

Martin Knytl ◽

...

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Purifying Selection ◽

W Chromosome ◽

Developmental Systems ◽

Recombination Suppression ◽

Evolutionary Origins ◽

Evolutionary Context ◽

Genomic Locations ◽

Developmental Systems Drift

Abstract Phenotypic invariance—the outcome of purifying selection—is a hallmark of biological importance. However, invariant phenotypes might be controlled by diverged genetic systems in different species. Here, we explore how an important and invariant phenotype—the development of sexually differentiated individuals—is controlled in over two dozen species in the frog family Pipidae. We uncovered evidence in different species for 1) an ancestral W chromosome that is not found in many females and is found in some males, 2) independent losses and 3) autosomal segregation of this W chromosome, 4) changes in male versus female heterogamy, and 5) substantial variation among species in recombination suppression on sex chromosomes. We further provide evidence of, and evolutionary context for, the origins of at least seven distinct systems for regulating sex determination among three closely related genera. These systems are distinct in their genomic locations, evolutionary origins, and/or male versus female heterogamy. Our findings demonstrate that the developmental control of sexual differentiation changed via loss, sidelining, and empowerment of a mechanistically influential gene, and offer insights into novel factors that impinge on the diverse evolutionary fates of sex chromosomes.

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Differences in Homomorphic Sex Chromosomes Are Associated with Population Divergence in Sex Determination in Carinascincus ocellatus (Scincidae: Lygosominae)

Cells ◽

10.3390/cells10020291 ◽

2021 ◽

Vol 10 (2) ◽

pp. 291

Author(s):

Peta Hill ◽

Foyez Shams ◽

Christopher P. Burridge ◽

Erik Wapstra ◽

Tariq Ezaz

Keyword(s):

Sex Determination ◽

Y Chromosome ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Population Divergence ◽

Sex Chromosome Evolution ◽

Evolutionary Transitions ◽

Evolutionary Origins ◽

Probe Set

Sex determination directs development as male or female in sexually reproducing organisms. Evolutionary transitions in sex determination have occurred frequently, suggesting simple mechanisms behind the transitions, yet their detail remains elusive. Here we explore the links between mechanisms of transitions in sex determination and sex chromosome evolution at both recent and deeper temporal scales (<1 Myr; ~79 Myr). We studied a rare example of a species with intraspecific variation in sex determination, Carinascincus ocellatus, and a relative, Liopholis whitii, using c-banding and mapping of repeat motifs and a custom Y chromosome probe set to identify the sex chromosomes. We identified both unique and conserved regions of the Y chromosome among C. ocellatus populations differing in sex determination. There was no evidence for homology of sex chromosomes between C. ocellatus and L. whitii, suggesting independent evolutionary origins. We discuss sex chromosome homology between members of the subfamily Lygosominae and propose links between sex chromosome evolution, sex determination transitions, and karyotype evolution.

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Differential Gene Expression between Fungal Mating Types Is Associated with Sequence Degeneration

Genome Biology and Evolution ◽

10.1093/gbe/evaa028 ◽

2020 ◽

Vol 12 (4) ◽

pp. 243-258 ◽

Cited By ~ 3

Author(s):

Wen-Juan Ma ◽

Fantin Carpentier ◽

Tatiana Giraud ◽

Michael E Hood

Keyword(s):

Differential Expression ◽

Differentially Expressed Genes ◽

Mating Type ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Gc Content ◽

Differentially Expressed ◽

Mating Types ◽

Sexual Antagonism ◽

Recombination Suppression

Abstract Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.

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The Diversity and Evolution of Sex Chromosomes in Frogs

Genes ◽

10.3390/genes12040483 ◽

2021 ◽

Vol 12 (4) ◽

pp. 483

Author(s):

Wen-Juan Ma ◽

Paris Veltsos

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Comparative Genomic ◽

Ancestral State ◽

Heteromorphic Sex Chromosomes ◽

Genomic Studies ◽

Evolutionary Trajectories ◽

Heterogametic Sex

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.

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Evolutionary transitions between mechanisms of sex determination in vertebrates

Biology Letters ◽

10.1098/rsbl.2010.1126 ◽

2011 ◽

Vol 7 (3) ◽

pp. 443-448 ◽

Cited By ~ 62

Author(s):

Alexander E. Quinn ◽

Stephen D. Sarre ◽

Tariq Ezaz ◽

Jennifer A. Marshall Graves ◽

Arthur Georges

Keyword(s):

Sex Determination ◽

Chromosome Pair ◽

Sex Chromosome ◽

Molecular Pathways ◽

Genetic Contribution ◽

Temperature Dependent ◽

Trait Evolution ◽

Evolutionary Transitions ◽

Dichotomous Outcome ◽

Threshold Trait

Sex in many organisms is a dichotomous phenotype—individuals are either male or female. The molecular pathways underlying sex determination are governed by the genetic contribution of parents to the zygote, the environment in which the zygote develops or interaction of the two, depending on the species. Systems in which multiple interacting influences or a continuously varying influence (such as temperature) determines a dichotomous outcome have at least one threshold. We show that when sex is viewed as a threshold trait, evolution in that threshold can permit novel transitions between genotypic and temperature-dependent sex determination (TSD) and remarkably, between male (XX/XY) and female (ZZ/ZW) heterogamety. Transitions are possible without substantive genotypic innovation of novel sex-determining mutations or transpositions, so that the master sex gene and sex chromosome pair can be retained in ZW–XY transitions. We also show that evolution in the threshold can explain all observed patterns in vertebrate TSD, when coupled with evolution in embryonic survivorship limits.

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Weak male-determining genes and female heterogamety in Chironomus tentans

Canadian Journal of Genetics and Cytology ◽

10.1139/g84-118 ◽

1984 ◽

Vol 26 (6) ◽

pp. 748-751

Author(s):

Ray Feraday

Keyword(s):

Sex Determination ◽

Sex Chromosome ◽

Chironomus Tentans ◽

Female Development ◽

Female Heterogamety ◽

Dominant Female

Female heterogamety in the midge Chironomus tentans has been previously reported and attributed to a dominant female determiner. Published results are not consistent with the interpretation, and the female heterogamety, if any, can be better explained by a model involving a weakened male determiner. Suggestions are made for crosses between populations with different sex-determining mechanisms that would discriminate between models for the evolution of female heterogamety, and serve to determine whether indeed female development is the norm in the absence of any parental sex chromosomes.Key words: Chironomus, heterogamety, sex determination, sex chromosome.

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Telomere-to-telomere assembly of a fish Y chromosome reveals the origin of a young sex chromosome pair

Genome Biology ◽

10.1186/s13059-021-02430-y ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Lingzhan Xue ◽

Yu Gao ◽

Meiying Wu ◽

Tian Tian ◽

Haiping Fan ◽

...

Keyword(s):

Y Chromosome ◽

Sex Chromosomes ◽

Chromosome Pair ◽

Sex Chromosome ◽

Structural Variations ◽

Recombination Suppression ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Recent Origin ◽

Mastacembelus Armatus

Abstract Background The origin of sex chromosomes requires the establishment of recombination suppression between the proto-sex chromosomes. In many fish species, the sex chromosome pair is homomorphic with a recent origin, providing species for studying how and why recombination suppression evolved in the initial stages of sex chromosome differentiation, but this requires accurate sequence assembly of the X and Y (or Z and W) chromosomes, which may be difficult if they are recently diverged. Results Here we produce a haplotype-resolved genome assembly of zig-zag eel (Mastacembelus armatus), an aquaculture fish, at the chromosomal scale. The diploid assembly is nearly gap-free, and in most chromosomes, we resolve the centromeric and subtelomeric heterochromatic sequences. In particular, the Y chromosome, including its highly repetitive short arm, has zero gaps. Using resequencing data, we identify a ~7 Mb fully sex-linked region (SLR), spanning the sex chromosome centromere and almost entirely embedded in the pericentromeric heterochromatin. The SLRs on the X and Y chromosomes are almost identical in sequence and gene content, but both are repetitive and heterochromatic, consistent with zero or low recombination. We further identify an HMG-domain containing gene HMGN6 in the SLR as a candidate sex-determining gene that is expressed at the onset of testis development. Conclusions Our study supports the idea that preexisting regions of low recombination, such as pericentromeric regions, can give rise to SLR in the absence of structural variations between the proto-sex chromosomes.

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