Identification of the homozygotic sex chromosome of non-model organisms

Whole genomes are commonly assembled into a collection of scaffolds and often lack annotations of autosomes, sex chromosomes and, and organelle genomes (i.e., mitochondrial and chloroplast). As these chromosome types can have highly disparate evolutionary histories, it is imperative to take this information into account when analyzing genomic variation. Here we assessed the accuracy of four methods for identifying the homogametic sex chromosome using two whole genome sequenced (WGS) and 133 RAD sequenced white-tailed eagles (Haliaeetus albicilla): i) difference in read depth per scaffold, ii) heterozygosity per scaffold in a male and female bird, iii) mapping to a reference genome of a related species (chicken) with identified sex chromosomes, and iv) an analysis of SNP-loadings from a principal components analysis (PCA), based on low-depth RADseq data from 133 individuals. In i and ii, the WGS were mapped to a reference genome consisting of 1142 assembled scaffolds from the golden eagle (Aquila chrysaetos) with no identified chromosomes. The read depth per scaffold identified 86.41% of the homogametic sex chromosome (Z) with few false positives. The SNP-loading scores found 78.6% of the Z-chromosome but had a false positive discovery rate of more than 10%. The heterozygosity per scaffold did not provide clear results due to a lack of diversity in both the Z and autosomal chromosomes, and potential interference from the heterogametic sex chromosome (W).

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Evaluation of Four Methods to Identify the Homozygotic Sex Chromosome in Small Populations

10.21203/rs.3.rs-892602/v1 ◽

2021 ◽

Author(s):

Charles Christian Riis Hansen ◽

Kristen M. Westfall ◽

Snaebjörn Pálsson

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Read Depth ◽

Mapping Method ◽

Small Population ◽

Genomic Variation ◽

Z Chromosome ◽

Effective Population ◽

Organelle Genomes ◽

Heterogametic Sex

Abstract BackgroundWhole genomes are commonly assembled into a collection of scaffolds and often lack annotations of autosomes, sex chromosomes, and organelle genomes (i.e., mitochondrial and chloroplast). As these chromosome types differ in effective population size and can have highly disparate evolutionary histories, it is imperative to take this information into account when analysing genomic variation. Here we assessed the accuracy of four methods for identifying the homogametic sex chromosome in a small population using two whole genome sequences (WGS) and 133 RAD sequences of white-tailed eagles (Haliaeetus albicilla): i) difference in read depth per scaffold in a male and a female, ii) heterozygosity per scaffold in a male and a female, iii) mapping to a reference genome of a related species (chicken) with identified sex chromosomes, and iv) analysis of SNP-loadings from a principal components analysis (PCA), based on the low-depth RADseq data. ResultsThe best performing approach was the reference mapping (method iii), which identified 98.12% of the expected homogametic sex chromosome (Z). The read depth per scaffold (method i) identified 86.41% of the homogametic sex chromosome with few false positives. The SNP-loading scores (method iv) found 78.6% of the Z-chromosome and had a false positive discovery rate of more than 10%. The heterozygosity per scaffold (method ii) did not provide clear results due to a lack of diversity in both the Z and autosomal chromosomes, and potential interference from the heterogametic sex chromosome (W). The evaluation of these methods also revealed 10 Mb of likely PAR and gametologous regions.ConclusionIdentification of the homogametic sex chromosome in a small population is best accomplished by reference mapping or examining read depth differences between sexes.

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Genomic evidence of neo-sex chromosomes in the eastern yellow robin

GigaScience ◽

10.1093/gigascience/giz111 ◽

2019 ◽

Vol 8 (9) ◽

Cited By ~ 7

Author(s):

Han Ming Gan ◽

Stephanie Falk ◽

Hernán E Morales ◽

Christopher M Austin ◽

Paul Sunnucks ◽

...

Keyword(s):

Zebra Finch ◽

Sex Chromosomes ◽

Reference Genome ◽

Sex Chromosome ◽

Read Depth ◽

Large Chromosome ◽

Z Chromosome ◽

Total Length ◽

Chromosome Fragments ◽

In The Wild

Abstract Background Understanding sex-biased natural selection can be enhanced by access to well-annotated chromosomes including ones inherited in sex-specific fashion. The eastern yellow robin (EYR) is an endemic Australian songbird inferred to have experienced climate-driven sex-biased selection and is a prominent model for studying mitochondrial-nuclear interactions in the wild. However, the lack of an EYR reference genome containing both sex chromosomes (in birds, a female bearing Z and W chromosomes) limits efforts to understand the mechanisms of these processes. Here, we assemble the genome for a female EYR and use low-depth (10×) genome resequencing data from 19 individuals of known sex to identify chromosome fragments with sex-specific inheritance. Findings MaSuRCA hybrid assembly using Nanopore and Illumina reads generated a 1.22-Gb EYR genome in 20,702 scaffolds (94.2% BUSCO completeness). Scaffolds were tested for W-linked (female-only) inheritance using a k-mer approach, and for Z-linked inheritance using median read-depth test in male and female reads (read-depths must indicate haploid female and diploid male representation). This resulted in 2,372 W-linked scaffolds (total length: 97,872,282 bp, N50: 81,931 bp) and 586 Z-linked scaffolds (total length: 121,817,358 bp, N50: 551,641 bp). Anchoring of the sex-linked EYR scaffolds to the reference genome of a female zebra finch revealed 2 categories of sex-linked genomic regions. First, 653 W-linked scaffolds (25.7 Mb) were anchored to the W sex chromosome and 215 Z-linked scaffolds (74.4 Mb) to the Z. Second, 1,138 W-linked scaffolds (70.9 Mb) and 179 Z-linked scaffolds (51.0 Mb) were anchored to a large section (coordinates ∼5 to ∼60 Mb) of zebra finch chromosome 1A. The first ∼5 Mb and last ∼14 Mb of the reference chromosome 1A had only autosomally behaving EYR scaffolds mapping to them. Conclusions We report a female (W chromosome–containing) EYR genome and provide genomic evidence for a neo-sex (neo-W and neo-Z) chromosome system in the EYR, involving most of a large chromosome (1A) previously only reported to be autosomal in passerines.

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Bisection of the X chromosome disrupts the initiation of chromosome silencing during meiosis in Caenorhabditis elegans

Nature Communications ◽

10.1038/s41467-021-24815-0 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Yisrael Rappaport ◽

Hanna Achache ◽

Roni Falk ◽

Omer Murik ◽

Oren Ram ◽

...

Keyword(s):

Caenorhabditis Elegans ◽

Rna Polymerase Ii ◽

X Chromosome ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Transcription Analysis ◽

X Chromosomes ◽

Unique Character ◽

Active Transcription ◽

Heterogametic Sex

AbstractDuring meiosis, gene expression is silenced in aberrantly unsynapsed chromatin and in heterogametic sex chromosomes. Initiation of sex chromosome silencing is disrupted in meiocytes with sex chromosome-autosome translocations. To determine whether this is due to aberrant synapsis or loss of continuity of sex chromosomes, we engineered Caenorhabditis elegans nematodes with non-translocated, bisected X chromosomes. In early meiocytes of mutant males and hermaphrodites, X segments are enriched with euchromatin assembly markers and active RNA polymerase II staining, indicating active transcription. Analysis of RNA-seq data showed that genes from the X chromosome are upregulated in gonads of mutant worms. Contrary to previous models, which predicted that any unsynapsed chromatin is silenced during meiosis, our data indicate that unsynapsed X segments are transcribed. Therefore, our results suggest that sex chromosome chromatin has a unique character that facilitates its meiotic expression when its continuity is lost, regardless of whether or not it is synapsed.

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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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Genetic sex determination and sex-specific lifespan in tetrapods – evidence of a toxic Y effect

10.1101/2020.03.09.983700 ◽

2020 ◽

Author(s):

Zahida Sultanova ◽

Philip A. Downing ◽

Pau Carazo

Keyword(s):

Sex Chromosomes ◽

Alternative Hypothesis ◽

Z Chromosome ◽

W Chromosome ◽

Deleterious Mutations ◽

Recessive Mutations ◽

Y Chromosomes ◽

Heterogametic Sex ◽

Taxonomic Patterns

ABSTRACTSex-specific lifespans are ubiquitous across the tree of life and exhibit broad taxonomic patterns that remain a puzzle, such as males living longer than females in birds and vice versa in mammals. The prevailing “unguarded-X” hypothesis (UXh) explains this by differential expression of recessive mutations in the X/Z chromosome of the heterogametic sex (e.g., females in birds and males in mammals), but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y/W chromosome might lower the survival of the heterogametic sex (“toxic Y” hypothesis). Here, we report lower survival of the heterogametic relative to the homogametic sex across 138 species of birds, mammals, reptiles and amphibians, as expected if sex chromosomes shape sex-specific lifespans. We then analysed bird and mammal karyotypes and found that the relative sizes of the X and Z chromosomes are not associated with sex-specific lifespans, contrary to UXh predictions. In contrast, we found that Y size correlates negatively with male survival in mammals, where toxic Y effects are expected to be particularly strong. This suggests that small Y chromosomes benefit male lifespans. Our results confirm the role of sex chromosomes in explaining sex differences in lifespan, but indicate that, at least in mammals, this is better explained by “toxic Y” rather than UXh effects.

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Rapture-ready darters: choice of reference genome and genotyping method (whole-genome or sequence capture) influence population genomic inference in Etheostoma

10.1101/2020.05.21.108274 ◽

2020 ◽

Author(s):

Brendan N. Reid ◽

Rachel L. Moran ◽

Christopher J. Kopack ◽

Sarah W. Fitzpatrick

Keyword(s):

Reference Genome ◽

Sequence Data ◽

Low Cost ◽

Read Depth ◽

Model Organisms ◽

Whole Genome ◽

Reduced Representation ◽

Sequence Capture ◽

Population Genomic ◽

The Impact

AbstractResearchers studying non-model organisms have an increasing number of methods available for generating genomic data. However, the applicability of different methods across species, as well as the effect of reference genome choice on population genomic inference, are still difficult to predict in many cases. We evaluated the impact of data type (whole-genome vs. reduced representation) and reference genome choice on data quality and on population genomic and phylogenomic inference across several species of darters (subfamily Etheostomatinae), a highly diverse radiation of freshwater fish. We generated a high-quality reference genome and developed a hybrid RADseq/sequence capture (Rapture) protocol for the Arkansas darter (Etheostoma cragini). Rapture data from 1900 individuals spanning four darter species showed recovery of most loci across darter species at high depth and consistent estimates of heterozygosity regardless of reference genome choice. Loci with baits spanning both sides of the restriction enzyme cut site performed especially well across species. For low-coverage whole-genome data, choice of reference genome affected read depth and inferred heterozygosity. For similar amounts of sequence data, Rapture performed better at identifying fine-scale genetic structure compared to whole-genome sequencing. Rapture loci also recovered an accurate phylogeny for the study species and demonstrated high phylogenetic informativeness across the evolutionary history of the genus Etheostoma. Low cost and high cross-species effectiveness regardless of reference genome suggest that Rapture and similar sequence capture methods may be worthwhile choices for studies of diverse species radiations.

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The probability of fusions joining sex chromosomes and autosomes

Biology Letters ◽

10.1098/rsbl.2020.0648 ◽

2020 ◽

Vol 16 (11) ◽

pp. 20200648

Author(s):

Nathan W. Anderson ◽

Carl E. Hjelmen ◽

Heath Blackmon

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Null Model ◽

Closed Form Expression ◽

Sexual Antagonism ◽

Form Expression ◽

Chromosome Fusion ◽

Sex Chromosome System ◽

Males And Females ◽

Heterogametic Sex

Chromosome fusion and fission are primary mechanisms of karyotype evolution. In particular, the fusion of a sex chromosome and an autosome has been proposed as a mechanism to resolve intralocus sexual antagonism. If sexual antagonism is common throughout the genome, we should expect to see an excess of fusions that join sex chromosomes and autosomes. Here, we present a null model that provides the probability of a sex chromosome autosome fusion, assuming all chromosomes have an equal probability of being involved in a fusion. This closed-form expression is applicable to both male and female heterogametic sex chromosome systems and can accommodate unequal proportions of fusions originating in males and females. We find that over 25% of all chromosomal fusions are expected to join a sex chromosome and an autosome whenever the diploid autosome count is fewer than 16, regardless of the sex chromosome system. We also demonstrate the utility of our model by analysing two contrasting empirical datasets: one from Drosophila and one from the jumping spider genus Habronattus . We find that in the case of Habronattus , there is a significant excess of sex chromosome autosome fusions but that in Drosophila there are far fewer sex chromosome autosome fusions than would be expected under our null model.

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Evolutionary Dynamics of Sex Chromosomes of Paleognathous Birds

Genome Biology and Evolution ◽

10.1093/gbe/evz154 ◽

2019 ◽

Vol 11 (8) ◽

pp. 2376-2390 ◽

Cited By ~ 13

Author(s):

Luohao Xu ◽

Simon Yung Wa Sin ◽

Phil Grayson ◽

Scott V Edwards ◽

Timothy B Sackton

Keyword(s):

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Z Chromosome ◽

Recombination Suppression ◽

Evolutionary Forces ◽

Genomic Level ◽

Standard Models ◽

Pseudoautosomal Regions

Abstract Standard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large nondegenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over >100 Myr, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analyzed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in differentiated regions for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species, PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.

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Evolutionary dynamics of sex chromosomes of paleognathous birds

10.1101/295089 ◽

2018 ◽

Cited By ~ 3

Author(s):

Luohao Xu ◽

Simon Yung Wa Sin ◽

Phil Grayson ◽

Scott V. Edwards ◽

Timothy B. Sackton

Keyword(s):

Sex Chromosomes ◽

Evolutionary Dynamics ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Z Chromosome ◽

Recombination Suppression ◽

Evolutionary Forces ◽

Genomic Level ◽

Standard Models ◽

Pseudoautosomal Regions

AbstractStandard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large non-degenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over more than 100 MY, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analysed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions or DRs), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in DRs for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.

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A comparison of methodological approaches to the study of young sex chromosomes: A case study in Poecilia

10.1101/2021.11.29.470452 ◽

2021 ◽

Author(s):

Iulia Darolti ◽

Pedro Almeida ◽

Alison E Wright ◽

Judith E Mank

Keyword(s):

Sex Chromosomes ◽

Reference Genome ◽

Sex Chromosome ◽

De Novo ◽

Sequence Similarity ◽

Sequence Evolution ◽

Structural Variations ◽

Recombination Suppression ◽

Custom Made ◽

Methodological Approaches

Studies of sex chromosome systems at early stages of divergence are key to understanding the initial process and underlying causes of recombination suppression. However, identifying signatures of divergence in homomorphic sex chromosomes can be challenging due to high levels of sequence similarity between the X and the Y. Variations in methodological precision and underlying data can make all the difference between detecting subtle divergence patterns or missing them entirely. Recent efforts to test for X-Y sequence differentiation in the guppy have led to contradictory results. Here we apply different analytical methodologies to the same dataset to test for the accuracy of different approaches in identifying patterns of sex chromosome divergence in the guppy. Our comparative analysis reveals that the most substantial source of variation in the results of the different analyses lies in the reference genome used. Analyses using custom-made de novo genome assemblies for the focal species successfully recover a signal of divergence across different methodological approaches. By contrast, using the distantly related Xiphophorus reference genome results in variable patterns, due to both sequence evolution and structural variations on the sex chromosomes between the guppy and Xiphophorus. Changes in mapping and filtering parameters can additionally introduce noise and obscure the signal. Our results illustrate how analytical differences can alter perceived results and we highlight best practices for the study of nascent sex chromosomes.

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