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Satellite DNA-mediated diversification of a sex-ratio meiotic drive gene family in Drosophila

Abstract

Sex chromosomes are susceptible to the evolution of selfish meiotic drive elements that bias transmission and distort progeny sex ratios. Conflict between such sex-ratio drivers and the rest of the genome can trigger evolutionary arms races resulting in genetically suppressed ‘cryptic’ drive systems. The Winters cryptic sex-ratio drive system of Drosophila simulans comprises a driver, Distorter on the X (Dox) and an autosomal suppressor, Not much yang, a retroduplicate of Dox that suppresses via production of endogenous small interfering RNAs (esiRNAs). Here we report that over 22 Dox-like (Dxl) sequences originated, amplified and diversified over the ~250,000-year history of the three closely related species, D. simulans, D. mauritiana and D. sechellia. The Dxl sequences encode a rapidly evolving family of protamines. Dxl copy numbers amplified by ectopic exchange among euchromatic islands of satellite DNAs on the X chromosome and separately spawned four esiRNA-producing suppressors on the autosomes. Our results reveal the genomic consequences of evolutionary arms races and highlight complex interactions among different classes of selfish DNAs.

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Fig. 1: Physical distribution of known Dxl genes in D. simulans, D. mauritiana and D. sechellia.
Fig. 2: Inferred stepwise historical origins of Dox.
Fig. 3: Dxl genes encode a rapidly evolving protamine.
Fig. 4: Structural and sequence evolution among Dxl gene copies.
Fig. 5: Autosomal hpRNA suppressor loci in the D. simulans clade species.
Fig. 6: Species-specific small RNAs (≤22 nt) map to Dxl-matching hairpin regions of each species’ autosomal suppressors.

Data availability

All data used in our analyses are publicly available via the Sequence Read Archive. Data accessions are listed in Supplementary Tables 2 and 4.

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Acknowledgements

This work was supported by funds from NIH grant no. R01 GM123194 and the University of Rochester to D.C.P. We thank J. J. Emerson, A. Larracuente, C. Meiklejohn, K. Montooth and J. Vedanayagam for early access to the PacBio-based genome assemblies. And we thank B. Navarro Dominguez and C. Meiklejohn for valuable feedback on the manuscript.

Author information

Authors and Affiliations

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Contributions

C.A.M. and D.C.P. conceived and designed the study. C.A.M. performed all analyses. C.A.M. and D.C.P. wrote the paper.

Corresponding author

Correspondence to Daven C. Presgraves.

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The authors declare no competing interests.

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Peer review information Nature Ecology & Evolution thanks Aaron Vogan and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Schematic alignment of inserted sat359 islands in X:9.4-10.4 Mb, colour-coded by putative sequence homology.

Segments of the same colour aligned vertically are high-confidence nucleotide alignments, whereas segments of different colour do not share sequence homology regardless of vertical alignment in the figure. One insertion into a sat359 island, the transposase-like sequence inserted into the D. sechellia Dxl-2 location, does not share sequence homology with any of the other loci, and has been omitted from this figure.

Extended Data Fig. 2 Alignment of the putative source material for Dxl genes found at approximate coordinates X:17.1 and X:17.2 Mb.

Segments of the same colour aligned vertically are high-confidence nucleotide alignments. At X:17.2, the three D. simulans clade species all have remnants of an insertion (total span = ~3 kb) that interrupts the CG8664 gene. This sequence, along with some of CG8664 and additional material, is alignable with insertion at the second position, X:17.1 Mb. Putative homology of the inserted sequence at both locations, along with CG8664, are colour-coded and the span of present-day Dxl homology is indicated.

Extended Data Fig. 3 Chromosomal distribution of sat359 islands in X:9.4-10.4 Mb region with all identified inserted sequence, including Dxl genes, in D. simulans, D. mauritiana, and D. sechellia.

Tick marks indicate locations of conserved sat359 islands, blue dots indicate protein-coding genes of interest in the region, and the different coloured squares represent the homologies of sequences inserted into sat359 islands (green=Dxl; purple=Ptpmeg2 fragment; brown=mkg-p retrotransposition; red=transposase-like sequence; yellow=cubn fragment; pink=CARPB intron fragments).

Extended Data Fig. 4 Evidence for transfer of Dxl material via a circular DNA intermediate molecule.

Dxl-12mau (green) is flanked by sat359 repeats (blue arrows) and by CARPB intronic sequence (boxes labelled A and B). These flanking sequence match sequences present in Dxl-10mau and Dxl-14mau, but the order of the two CARPB segments A and B differs from Dxl-12mau. The re-ordering of homologous sequences, as well as their intervening sequence, is consistent with a transfer of material via circular DNA intermediate.

Supplementary information

Supplementary Information

Supplementary text and Figs. 1–4.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–4.

Supplementary Data 1

Alignment of inserted sat359 clusters.

Supplementary Data 2

Dxl protamines—positions 1–66, aligned with known protamines.

Supplementary Data 3

D. simulans r2.02, curated transcript set (‘base’ sequence set).

Supplementary Data 4

Consensus hairpin sequences of autosomal suppressors.

Supplementary Data 5

Species-specific consensus sequences, all Dxl-related sequence.

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Muirhead, C.A., Presgraves, D.C. Satellite DNA-mediated diversification of a sex-ratio meiotic drive gene family in Drosophila. Nat Ecol Evol 5, 1604–1612 (2021). https://doi.org/10.1038/s41559-021-01543-8

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