1. Evolutionary Biology
  2. Genetics and Genomics
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Evolution of gene dosage on the Z-chromosome of schistosome parasites

  1. Marion A L Picard
  2. Celine Cosseau
  3. Sabrina Ferré
  4. Thomas Quack
  5. Christoph G Grevelding
  6. Yohann Couté
  7. Beatriz Vicoso  Is a corresponding author
  1. Institute of Science and Technology Austria, Austria
  2. University of Perpignan Via Domitia, IHPE UMR 5244, CNRS, IFREMER, University Montpellier, France
  3. Université Grenoble Alpes, CEA, Inserm, BIG-BGE, France
  4. Justus-Liebig-University, Germany
Research Article
Cite this article as: eLife 2018;7:e35684 doi: 10.7554/eLife.35684
10 figures, 5 tables, 3 data sets and 2 additional files

Figures

Shared and lineage-specific evolutionary strata on the Z-chromosome.

The phylogeny of the three species is represented on the left. The female:male (F:M) ratio of coverage (y-axis) along the Z-chromosome of S. mansoni (x-axis) is shown for S. japonicum scaffolds (A) and S. mansoni 10 kb windows (B). Female coverage is shown for S. haematobium scaffolds (C). All species share an ancestral Z-linked stratum S0 (marked in orange). The stratum S1jap (in green) is specific to the Asian lineage represented by S. japonicum. The stratum S1mans (in blue) is specific to the African lineage, represented by S. mansoni and S. haematobium. Dot color is attributed depending on the window/scaffold location within each species: Z-specific regions in orange, pseudoautosomal regions in grey, and ambiguous regions in beige.

https://doi.org/10.7554/eLife.35684.003
Figure 1—source data 1

Comparative genomics: coverage analysis and strata identification.

https://doi.org/10.7554/eLife.35684.004
Figure 1—source data 2

S. mansoni reference species: coverage analysis and Z/Autosome assignment.

https://doi.org/10.7554/eLife.35684.005
Figure 1—source data 3

S. haematobium autosome vs Z-specific region assigment.

https://doi.org/10.7554/eLife.35684.006
Figure 1—source data 4

S. japonicum autosome vs Z-specific region assignment.

https://doi.org/10.7554/eLife.35684.007
Figure 2 with 17 supplements
Patterns of expression on the Z and autosomes of S.japonicum and S. mansoni.

Z-linked and autosomal gene expression patterns are shown for S. japonicum (A-D) and S. mansoni (E-H), in undifferentiated schistosomula and sexually mature adults. In panels A, C, E, and G, Fem-Z and Male-Z refer to the expression of Z-linked genes in females and males, respectively, and Fem-A and Male-A to the expression of the autosomal genes in females and males. In panels B, D, F, and H, Z refers to Z-linked genes and A to autosomal genes. In all conditions, a strong male bias is observed for the Z-linked genes (B, D, F, H). This male-biased expression of the Z-linked genes is accompanied by both an under-expression in females and an over-expression in males, compared to the level of autosomal expression (A, C, E, G). The level of significance of each comparison (Wilcoxon rank sum test with continuity correction) is indicated by asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001.

https://doi.org/10.7554/eLife.35684.009
Figure 2—source data 1

RPKM calculation for S. mansoni gene expression.

https://doi.org/10.7554/eLife.35684.027
Figure 2—source data 2

RPKM calculation for S. japonicum gene expression.

https://doi.org/10.7554/eLife.35684.028
Figure 2—figure supplement 1
Adult expression patterns (RPKM>1, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with RPKM >1 were used.

https://doi.org/10.7554/eLife.35684.010
Figure 2—figure supplement 2
Adult expression patterns (RPKM>0, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with RPKM >0 were used.

https://doi.org/10.7554/eLife.35684.011
Figure 2—figure supplement 3
Adult expression patterns (RPKM>1, stringent strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes previously mapped to the ZW linkage group were assigned to each Z-chromosome stratum based on their coverage patterns (stringent classification); only genes with RPKM >1 were used.

https://doi.org/10.7554/eLife.35684.012
Figure 2—figure supplement 4
Adult expression patterns (RPKM>0, stringent strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes previously mapped to the ZW linkage group were assigned to each Z-chromosome stratum based on their coverage patterns (stringent classification); only genes with RPKM >0 were used.

https://doi.org/10.7554/eLife.35684.013
Figure 2—figure supplement 5
Adult expression patterns (RPKM>1, exhaustive strata, Wormbase orthologs) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with RPKM >0 were used. This figure differs from Figure 2-figure supplement 1 as the Wormbase Parasite list 1:1 orthologs was used instead of our own reciprocal best hit results.

https://doi.org/10.7554/eLife.35684.014
Figure 2—figure supplement 6
Adult expression patterns (TPM>1, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with TPM >1 were used.

https://doi.org/10.7554/eLife.35684.015
Figure 2—figure supplement 7
Adult expression patterns (TPM>0, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with TPM >0 were used.

https://doi.org/10.7554/eLife.35684.016
Figure 2—figure supplement 8
Schistosomula expression patterns (RPKM>1, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with RPKM >1 were used.

https://doi.org/10.7554/eLife.35684.017
Figure 2—figure supplement 9
Schistosomula expression patterns (RPKM>0, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with RPKM >0 were used.

https://doi.org/10.7554/eLife.35684.018
Figure 2—figure supplement 10
Schistosomula expression patterns (RPKM>1, stringent strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes previously mapped to the ZW linkage group were assigned to each Z-chromosome stratum based on their coverage patterns (stringent classification); only genes with RPKM >1 were used.

https://doi.org/10.7554/eLife.35684.019
Figure 2—figure supplement 11
Schistosomula expression patterns (RPKM>0, stringent strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes previously mapped to the ZW linkage group were assigned to each Z-chromosome stratum based on their coverage patterns (stringent classification); only genes with RPKM >0 were used.

https://doi.org/10.7554/eLife.35684.020
Figure 2—figure supplement 12
Schistosomula expression patterns (RPKM>1, exhaustive strata, Wormbase orthologs) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with RPKM >0 were used. This figure differs from Figure 2—figure supplement 8 as the Wormbase Parasite list 1:1 orthologs was used instead of our own reciprocal best hit results.

https://doi.org/10.7554/eLife.35684.021
Figure 2—figure supplement 13
Schistosomula expression patterns (TPM>1, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with TPM >1 were used.

https://doi.org/10.7554/eLife.35684.022
Figure 2—figure supplement 14
Schistosomula expression patterns (TPM>0, exhaustive strata) of genes located in the different strata of the Z (S0, S1man and S1jap), as well as pseudoautosomal and autosomal genes.

The distribution of expression values is shown for (A) S. mansoni females, (B) S. mansoni males, (C) S. mansoni female:male, (D) S. japonicum females, (E) S. japonicum males, (F) S. japonicum female:male, (G) Female expression in S. japonicum divided by female expression in S. mansoni, (H) Male expression in S. japonicum divided by male expression in S. mansoni, (I) female:male ratio of expression in S. japonicum divided by female:male ratio of expression in S. mansoni. Asterisks represent levels of significance of comparisons to the control autosomal genes (*p-value<0.05, **p-value<0.001, ***p-value<0.0001). Genes were assigned to each Z-chromosome stratum based only on their coverage patterns; only genes with TPM >0 were used.

https://doi.org/10.7554/eLife.35684.023
Figure 2—figure supplement 15
Z-linked and autosomal female:male ratio of gene expression using different filters.

The Z-linked and autosomal gene expression patterns are shown in S. japonicum and S. mansoni. Different filters were applied: a minimum threshold of expression of 1 RPKM in all libraries (A–D), a minimum threshold of expression of 3 RPKM in all libraries (E–H), or a minimum threshold of expression of 1 RPKM per stage (as in the main manuscript), together with a filter on fold change to account for strong sex-biases (FC <2 for female:male ratio and male:female ratio) (I-L). Z refers to the female:male ratio of expression in the Z-specific region and A refers to the female:male ratio of expression on autosomes. The level of significance of each comparison is denoted with asterisks: ***p-value<0.0001.

https://doi.org/10.7554/eLife.35684.024
Figure 2—figure supplement 16
Z-linked and autosomal gene expression in females and males using different filters.

The Z-linked and autosomal gene expression patterns are shown for S. japonicum and S. mansoni. Different filters were applied: a minimum threshold of expression of 1 RPKM in all libraries (A–D), a minimum threshold of expression of 3 RPKM in all libraries (E–H), or a minimum threshold of expression of 1 RPKM per stage (as in the main manuscript), together with a filter on fold change to account for strong sex biases (FC <2 for female:male ratio and male:female ratio) (I-L). Fem-Z and Male-Z refers to the female:male ratio of expression in the Z-specific region and Fem-A and Male-A refers to the female:male ratio of expression on autosomes, in female and male, respectively. The level of significance of each comparison is denoted with asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001.

https://doi.org/10.7554/eLife.35684.025
Figure 2—figure supplement 17
Z-linked and autosomal female:male ratio of gene expression according to presence/absence of known protein-protein interactions.

The Z-linked and autosomal gene expression patterns are shown for schistosomula and adults, in S. japonicum (A–B) and S. mansoni (C–D). We considered only genes with minimum level of expression RPKM >1 in all stages, did not take into account the ancestral state of expression, and used the ‘exhaustive strata’ set of genes. -PPIs and +PPIs refer to the female:male ratio of expression in the lineage-specific Z-linked strata S1jap and S1mans, respectively. The level of significance of each comparison is denoted with asterisks: ***p-value<0.0001.

https://doi.org/10.7554/eLife.35684.026
Figure 3 with 2 supplements
Convergent changes in the expression of Z-linked genes in S. japonicum and S. mansoni after sex chromosome differentiation.

The Z-linked and autosomal gene expression patterns (normalized by ancestral pseudoautosomal or autosomal expression, to show changes since the appearance of the two S1 strata) are shown for S1jap in S. japonicum (A-D) and S1mans in S. mansoni (E-F). Fem-S1j and Male-S1j refer to the normalized expression levels of genes in the stratum S1jap in females and males, Fem-S1m and Male-S1m refer to the normalized expression levels in S1mans, and Fem-A and Male-A refer to the normalized expression levels of autosomal genes in females and in males, respectively. The level of significance of each comparison (Wilcoxon rank sum test with continuity correction) is denoted with asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001.

https://doi.org/10.7554/eLife.35684.029
Figure 3—source data 1

One-to-one orthology S. mansoni vs S. japonicum.

https://doi.org/10.7554/eLife.35684.032
Figure 3—source data 2

Transcriptomic data, for blat 1-to-1 orthologs.

https://doi.org/10.7554/eLife.35684.033
Figure 3—source data 3

Transcriptomic data, for WormBase Biomart orthologs.

https://doi.org/10.7554/eLife.35684.034
Figure 3—figure supplement 1
Z-linked and autosomal female:male ratio of gene expression, normalized by ancestral autosomal expression, and using different filters.

The Z-linked and autosomal gene expression patterns (normalized by ancestral pseudoautosomal or autosomal expression, to show changes since the appearance of the two S1 strata) are shown for S1jap in S. japonicum and S1mans in S. mansoni. Different filters were applied: a minimum threshold of expression of 1 RPKM in all libraries (A–D), a minimum threshold of expression of 3 RPKM in all libraries (E–H), or a minimum threshold of expression of 1 RPKM per stage (as in the main manuscript), together with a filter on fold change to account for strong sex biases (FC<2 for female:male ratio and male:female ratio) (I-L). S1jap and S1mans refer to the female:male ratio of expression in the lineage specific Z-linked strata S1jap and S1mans, respectively. The level of significance of each comparison is denoted with asterisks: ***p-value<0.0001.

https://doi.org/10.7554/eLife.35684.030
Figure 3—figure supplement 2
Z-linked and autosomal gene expression in females and males, normalized by ancestral autosomal expression, and using different filters.

The Z-linked and autosomal gene expression patterns (normalized by ancestral pseudoautosomal or autosomal expression, to show changes since the appearance of the two S1 strata) are shown for S1jap in S. japonicum and S1mans in S. mansoni. Different filters were applied: a minimum threshold of expression of 1 RPKM in all libraries (A–D), a minimum threshold of expression of 3 RPKM in all libraries (E–H), or a minimum threshold of expression of 1 RPKM per stage (as in the main manuscript), together with a filter on fold change to account for strong sex biases (FC <2 for female:male ratio and male:female ratio) (I¬-L). Fem-S1j and Male-S1j refer to the normalized expression levels of genes in the stratum S1jap in females and males, Fem-S1m and Male-S1m refer to the normalized expression levels in S1mans, and Fem-A and Male-A refer to the normalized expression levels of autosomal genes in females and in males, respectively. The level of significance of each comparison is denoted with asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001.

https://doi.org/10.7554/eLife.35684.031
Figure 4 with 3 supplements
Transcript and protein dosage of Z-linked and autosomal genes in S.mansoni heads and gonads.

(A), (B) The female:male (F:M) ratio of protein dosage in S. mansoni heads (A) and gonads (B), for Z-specific (Z), pseudoautosomal (PSA) or autosomal (A) genes. The dotted line shows the autosomal median of F:M expression. The level of significance of each comparison (Wilcoxon rank sum test with continuity correction) is denoted with asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001. (C), (D) Pearson correlation between the female:male ratio of expression obtained by proteomics (y-axes) and by microarrays (x-axes) in S.mansoni heads (C) and gonads (D). A positive correlation (coefficients ρ) is observed for Z-linked (Z, in orange), pseudoautosomal (PSA, in grey) and autosomal genes (A, in darkgrey). The level of significance of each correlation is denoted by asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001, N.S. p-value>0.05. No significant difference was found between the correlation obtained for Z-linked and autosomal genes in either tissue (using a Fisher r-to-z transformation).

https://doi.org/10.7554/eLife.35684.035
Figure 4—source data 1

Proteomic data with imputed values – GONADS.

https://doi.org/10.7554/eLife.35684.039
Figure 4—source data 2

Proteomic data with imputed values – HEADS.

https://doi.org/10.7554/eLife.35684.040
Figure 4—source data 3

Proteomic data without imputed values – GONADS.

https://doi.org/10.7554/eLife.35684.041
Figure 4—source data 4

Proteomic data without imputed values – HEADS.

https://doi.org/10.7554/eLife.35684.042
Figure 4—source data 5

Correspondance between Gene_Id and Protein_ID.

https://doi.org/10.7554/eLife.35684.043
Figure 4—source data 6

Microarray data.

https://doi.org/10.7554/eLife.35684.044
Figure 4—figure supplement 1
Pearson correlations between gene dosage at the transcript and protein levels in male heads and gonads.

A positive correlation (coefficients R) is observed for Z-linked (Z, in light blue), pseudo-autosomal (PSA, in grey) and autosomal genes (A, in dark blue). The level of significance of each correlation is denoted by asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001. No significant difference was found between the correlations obtained for Z-linked and autosomal genes in either tissue (using a Fisher r-to-z transformation).

https://doi.org/10.7554/eLife.35684.036
Figure 4—figure supplement 2
Pearson correlations between gene dosage at the transcript and protein levels in female heads and gonads.

A positive correlation (coefficients R) is observed for Z-linked (Z, in light pink), pseudo-autosomal (PSA, in grey) and autosomal genes (A, in dark pink. The level of significance of each correlation is denoted by asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001. No significant difference was found between the correlations obtained for Z-linked and autosomal genes in either tissue (using a Fisher r-to-z transformation).

https://doi.org/10.7554/eLife.35684.037
Figure 4—figure supplement 3
Pearson correlations between the female:male ratio of expression obtained by proteomics (y-axes) and by microarrays (x-axes) in S. mansoni heads and gonads, using only genes with male-biased expression in the microarray data.

A positive correlation (coefficients R) is observed for Z-linked (Z, in orange), pseudo-autosomal (PSA, in grey) and autosomal genes (A, in darkgrey). The level of significance of each correlation is denoted by asterisks: *p-value<0.05, **p-value<0.001, ***p-value<0.0001, N.S. p-value>0.05. No significant difference was found between the correlations obtained for Z-linked and autosomal genes in either tissue (using a Fisher r-to-z transformation).

https://doi.org/10.7554/eLife.35684.038
Appendix 1—figure 1
Determination of Z-specific maximum coverage threshold for S. mansoni reference species.
https://doi.org/10.7554/eLife.35684.048
Appendix 1—figure 2
Determination of Z-specific maximum coverage threshold for S. japonicum species.
https://doi.org/10.7554/eLife.35684.049
Appendix 1—figure 3
Determination of Z-specific maximum coverage threshold for S. haematobium species.
https://doi.org/10.7554/eLife.35684.050
Appendix 1—figure 4
Correlation analysis between RNAseq libraries: heatmaps.
https://doi.org/10.7554/eLife.35684.051
Author response image 1
Enrichment of the Z-chromosome for genes highly expressed in three male tissues (testis, head, hind), for three different expression cut-offs.

*p<0.05 **p<0.01, Pearsonʹs Chi-squared test with Yatesʹ continuity correction.

https://doi.org/10.7554/eLife.35684.054
Author response image 2
Depletion of the Z-chromosome for genes highly expressed in three female tissues (ovary, head, hind), for three different expression cut-offs.

*p<0.05 **p<0.01, Pearson'ʹs Chi-squared test with Yates' continuity correction.

https://doi.org/10.7554/eLife.35684.055

Tables

Table 1
Number of orthologs assigned as Z-linked and autosomal in S. mansoni, S. haematobium and S. japonicum, based on the female:male (or female for S. haematobium) coverage patterns.
https://doi.org/10.7554/eLife.35684.008

Categories
Schistosoma japonicumSchistosoma haematobium
Z-specificAutosomalAmbiguousNot coveredZ-specificAutosomalAmbiguousNot covered
Schistosoma mansoniZ-specific476
(S0)
306
(S1mans)
203847362310
 Autosomal137
(S1jap)
706291132167462262105
 Excluded5738343105411207
 Orthologs total85559504
Author response table 1
Expression values excluding sex-bias FC>2 (ancestry not considered).
https://doi.org/10.7554/eLife.35684.052
S. japonicum
schistosomula
S. japonicum
adults
S. mansoni
schistosomula
S. mansoni
adults
Female Z:A0.86 N.S.0.81 N.S.0.93 N.S.0.69 *
Male Z:A1.55 ***1.18 N.S.1.21*1.14 N.S.
Z(F:M) / A(F:M)0.58 ***0.68 ***0.67 ***0.63 ***
Z(fem): Z(male)0.61 **0.76 *0.70 *0.73 *
A(fem): A(male)1.04 N.S.1.11 *1.05 N.S.1.15 *
N (Z)237189298224
N (A)2,3641,4472,3641,447
Author response table 2
Expression values excluding sex-bias FC>2 (considering ancestry).
https://doi.org/10.7554/eLife.35684.053
S. japonicum schistosomulaS. japonicum adultsS. mansoni schistosomulaS. mansoni adults
Female Z:A0.83*0.71*0.92 N.S.0.72 N.S.
Male Z:A1.23 N.S.1.38 N.S.1.20*1.34 N.S.
Z(F:M) / A(F:M)0.67 ***0.52***O.77***0.54***
Z(fem): Z(male)0.65*0.50*0.78 N.S.0.56*
A(fem): A(male)0.98 N.S.0.97 N.S.1.02 N.S.1.03 N.S.
N (Z)503111166
N (A)2,3641,4472,3641,447
Author response table 3
Ratio of expression values, with minimum threshold of RPKM>1 and maximum expression threshold of RPKM<5.

We did not account for ancestry. Level of significance (Wilcoxon test): *P-value<0.05, **P-value<0.001, ***P-value<0.0001, N.S. P-value>0.05.

https://doi.org/10.7554/eLife.35684.056
S. japonicum
schistosomula
S. japonicum
adults
S. mansoni
schistosomula
S. mansoni
adults
Female Z:A0.76**0.67**0.76***0.76*
Male Z:A1.39***1.22*1.18*1.33*
Z(F:M) / A(F:M)0.57***0.63***0.69***0.64***
Z(fem): Z(male)0.59***0.68**0.73***0.72**
A(fem): A(male)1.041.071.06*1.12*
N (Z)43385546
N (A)486321486321
Author response table 4
Ratio of expression values, with minimum expression threshold of RPKM>1 and maximum expression threshold of RPKM<5.

We normalized by the ancestral state of expression. Level of significance (Wilcoxon test *P-value<0.05, **P-value<0.001, ***P-value<0.0001, N.S. P-value>0.05.

https://doi.org/10.7554/eLife.35684.057
S. japonicum
schistosomula
S. japonicum
adults
S. mansoni
schistosomula
S. mansoni
adults
Female Z:A0.82*0.79 N.S.0.90 N.S.1.05 N.S.
Male Z:A1.22 N.S.1.17 N.S.1.22 N.S.1.50*
Z(F:M) / A(F:M)0.67***0.67*0.74*0.70*
Z(fem): Z(male)0.62*0.66 N.S.0.79 N.S.0.72 N.S.
A(fem): A(male)0.93 N.S.0.98 N.S.1.07 N.S.1.02 N.S.
N (Z)1182316
N (A)486321486321

Data availability

Sequencing data have been deposited to the NCBI short reads archive (PRJNA432803). Proteomic dosage values as well as final versions of the processed datasets (genomic coverage, expression values, chromosomal assignments) have been deposited into the IST Austria Data Repository (http://dx.doi.org/10.15479/AT:ISTA:109).

The following data sets were generated
    1. Vicoso B
    (2018) DNA reads of male and female S. japonicum
    Publicly available at NCBI BioProject (accession no: PRJNA432803).
The following previously published data sets were used
    1. Nawaratna SSK
    2. McManus DP
    3. Moertel L
    4. Gobert GN
    5. Jones MK
    (2010) Gene atlasing of digestive and reproductive tissues in Schistosoma mansoni
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE23942).

Additional files

Supplementary file 1

Comparison of the ratio of expression between the Z-linked and autosomal genes (Z:A), and comparison of expression between males and females (F:M) in the different species, stages and methods (Supplementary Table 1).

Comparison of female:male ratios of expression (F:M) using microarray and proteomics (Supplementary Table 2)

https://doi.org/10.7554/eLife.35684.045
Transparent reporting form
https://doi.org/10.7554/eLife.35684.046

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