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Massive gene amplification on a recently formed Drosophila Y chromosome

Nature Ecology & Evolution volume 3, pages 1587–1597 (2019)Cite this article

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Abstract

Widespread loss of genes on the Y is considered a hallmark of sex chromosome differentiation. Here we show that the initial stages of Y evolution are driven by massive amplification of distinct classes of genes. The neo-Y chromosome of Drosophila miranda initially contained about 3,000 protein-coding genes, but has gained over 3,200 genes since its formation about 1.5 million years ago primarily by tandem amplification of protein-coding genes ancestrally present on this chromosome. We show that distinct evolutionary processes may account for this drastic increase in gene number on the Y. Testis-specific and dosage-sensitive genes appear to have amplified on the Y to increase male fitness. A distinct class of meiosis-related multi-copy Y genes independently co-amplified on the X, and their expansion is probably driven by conflicts over segregation. Co-amplified X/Y genes are highly expressed in testis, enriched for meiosis and RNA interference functions and are frequently targeted by small RNAs in testis. This suggests that their amplification is driven by X versus Y antagonism for increased transmission, where sex chromosome drive suppression is probably mediated by sequence homology between the suppressor and distorter through the RNA interference mechanism. Thus, our analysis suggests that newly emerged sex chromosomes are a battleground for sexual and meiotic conflict.

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Fig. 1: Gene content evolution of newly formed sex chromosomes.
Fig. 2: Distinct evolutionary processes may drive the accumulation of multi-copy Y genes, or co-amplified X and Y genes.
Fig. 3: Characterization of ampliconic Y genes.
Fig. 4: Co-amplified X/Y genes are enriched for meiosis-related and RNAi functions.
Fig. 5: Co-amplified X/Y gene families produce anti-sense transcripts and small RNAs in testis.
Fig. 6: Examples of co-amplified X and Y genes.

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Data availability

All data that were used and generated for this project are given in Supplementary Table 10 and have been deposited on NCBI under BioProject ID PRJNA545539.

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Acknowledgements

D.B. was funded by NIH grants (nos. R01GM076007, GM101255 and R01GM093182). We thank L. Gibilisco for generating small RNA libraries and K. Chatla and A. Tran for generating genomic libraries.

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  1. These authors contributed equally: Doris Bachtrog, Shivani Mahajan.

Authors and Affiliations

  1. Department of Integrative Biology, University of California Berkeley, Berkeley, CA, USA

    Doris Bachtrog, Shivani Mahajan & Ryan Bracewell

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  1. Doris Bachtrog
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Contributions

D.B. conceived and oversaw the project, generated and analysed data and wrote the manuscript. S.M. analysed data. R.B. generated and analysed data.

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Correspondence to Doris Bachtrog.

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Extended data

Extended Data Fig. 1 Phylogenetic relationships of co-amplified X/Y genes in D. miranda.

Maximum-likelihood trees of D. miranda X and Y gene copies with nodes showing >70 bootstrap support highlighted with black circles. X-linked copies are shown in red, Y-linked copies shown in blue, with distinct X and Y groupings collapsed. Fasta alignments are in Data Supplement 14.

Extended Data Fig. 2 Copy number estimates for co-amplified Y genes, multi-copy Y genes, and multi-copy autosome and X genes.

For co-amplified Y genes we show all genes that were identified as co-amplified. For the multi-copy Y genes we only show genes with >3 copies on the Y. For multi-copy autosome and X genes we show only genes with >4 total copies. Multi-copy autosome and X estimates are predicted to be highly similar given that the autosome and X background in each Y-chromosome replacement line is nearly identical. Slight deviations are probably due to stochasticity in sequencing and read mapping, residual heterozygosity in the MSH22 line, or unique Y-chromosome gene amplifications.

Extended Data Fig. 3 Dosage compensation status of neo-X homologs of single-copy (left) and multi-copy (right) Y genes.

Shown are the relative numbers of neo-X genes that are bound by the MSL-complex (and are thus dosage compensated), and those not bound (and thus not dosage compensated). MSL-binding data were generated for male D. miranda larvae. Genes with multiple copies on the Y are less likely to be dosage compensated on the X. The data are presented in Data Supplement 15.

Supplementary information

Supplementary Information

Supplementary Figs. 1–8 and Tables 4 and 6–10.

Reporting Summary

Supplementary Table 1

Gene loss on the different Muller elements of D. miranda. Shown are genes in D. pseudoobscura for different chromosomes that are absent on their homologous chromosome arm in D. miranda. The table gives D. pseudoobscura gene ID (FBgn), D. melanogaster orthologue, the chromosomal location of the gene in D. pseudoobscura, the tissue of highest expression in D. pseudoobscura, the category of the gene, and whether the gene is present somewhere else in the D. miranda genome. a, Genes missing from the neo-X chromosome. b, Genes missing from the neo-Y chromosome. c, Genes missing from Muller A-AD (X chromosome). d, Genes missing from Muller B (chr4). e, Genes missing from Muller E (chr2). f, Genes that moved between chromosomes.

Supplementary Table 2

Overview of multi-copy Y genes. a, Shown are total copy numbers for multi-copy Y genes, as well as the number of full-length (>90%) and partial Y copies (50–90%; 25–50%; and less than 25% compared to the length of the orthologous gene in D. pseudoobscura). b, Expression of orthologues of multi-copy Y genes in D. pseudoobscura. c, GO analysis for orthologous genes in D. melanogaster. No significant GO enrichment terms were detected.

Supplementary Table 3

Overview of co-amplified X/Y genes. a, Shown are total copy number for co-amplified X and Y genes, as well as the numbers of full-length (>90%) and partial X and Y copies (50–90%; 25–50%; and less than 25% compared to the length of the orthologous gene in D. pseudoobscura). b, Expression of orthologues of co-amplified X/Y genes in D. pseudoobscura. c, Expression of orthologues of co-amplified X/Y genes in D. melanogaster. d, GO analysis for orthologous genes in D. melanogaster. Shown are GO terms that were significantly enriched among co-amplified X/Y genes (using either Gorilla or PantherDB).

Supplementary Table 5

Clustering of multi-copy Y and co-amplified X/Y genes. a, Genome intervals of clustered (within 100 kb of each other) multi-copy genes and their D. pseudoobscura gene ID (FBgn). b, Genome intervals of clustered (within 100 kb of each other) co-amplified genes and their D. pseudoobscura gene ID (FBgn).

Supplementary Dataset 1

Repeat library used for masking the D. miranda genome.

Supplementary Dataset 2

Repeat annotation of the D. miranda genome.

Supplementary Dataset 3

Gene annotation (all genes) of the D. miranda genome.

Supplementary Dataset 4

Gene annotation of multi-copy Y genes and their orthologues in the D. miranda genome.

Supplementary Dataset 5

Gene annotation of co-amplified X and Y genes in the D. miranda genome.

Supplementary Dataset 6

Gene expression values (TPM) for multi-copy Y genes, and co-amplified Y genes, in different D. miranda male tissues, and tissue-specificity index tau.

Supplementary Dataset 7

Gene copy numbers for co-amplified X/Y genes.

Supplementary Dataset 8

Gene expression values (TPM) for co-amplified X and Y gene families, in different D. miranda male tissues.

Supplementary Datast 9

Gene expression values (FPKM) for orthologues of co-amplified X/Y genes in different D. pseudoobscura male and female tissues.

Supplementary Dataset 10

Sense and anti-sense testis total RNA summed counts for co-amplified genes.

Supplementary Dataset 11

Sense and anti-sense testis small RNA summed counts for co-amplified genes.

Supplementary Dataset 12

Testis total RNA counts for all copies of a gene family for different categories of genes on the X/neo-X and Y/neo-Y chromosome.

Supplementary Dataset 13

Testis small RNA raw counts for different categories of genes on the X/neo-X and Y/neo-Y chromosome.

Supplementary Dataset 14

Fasta alignment of co-amplified X/Y genes and their D. pseudoobscura orthologue.

Supplementary Dataset 15

MSL ChIP and Input counts (normalized to library size) for neo-X genes whose homologue is classified as single-copy or multi-copy Y/neo-Y.

Supplementary Dataset 16

Gene expression values (TPM) for single-copy Y genes, multi-copy Y genes, and co-amplified Y genes, and their neo-X/X homologues in different D. miranda tissues. Expression values for all copies of a gene family are shown individually.

Supplementary Dataset 17

Gene expression values (TPM) for multi-copy Y genes, and co-amplified X and Y genes in different D. miranda tissues. Expression values for all copies of a gene family are summed.

Supplementary Dataset 18

Gene expression values (FPKM) for orthologues of co-amplified X/Y genes in different D. melanogaster tissues.

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Bachtrog, D., Mahajan, S. & Bracewell, R. Massive gene amplification on a recently formed Drosophila Y chromosome. Nat Ecol Evol 3, 1587–1597 (2019). https://doi.org/10.1038/s41559-019-1009-9

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