DOI: 10.5061/dryad.00000008q
title: Phylogenomics and evolution of the synaptonemal complex in Drosophila

description: The synaptonemal complex (SC) is a protein-rich structure necessary to
 tether homologous chromosomes for meiotic recombination and faithful
 segregation. Despite being found in most major eukaryotic taxa implying a
 deep evolutionary origin, components of the complex can exhibit unusually
 high rates of sequence evolution, particularly in Drosophila where
 orthologs of several components could not be identified outside of the
 genus. To understand the cause of this paradoxical lack of conservation,
 we examine the evolutionary history of the SC in Drosophila, taking a
 comparative phylogenomic approach with high species density to circumvent
 obscured homology due to rapid sequence evolution. We find that in
 addition to elevated rates of coding evolution due to recurrent and
 widespread positive selection, components of the SC, in particular the
 central element cona and transverse filament c(3)G have diversified
 through tandem and retro-duplications, repeatedly generating paralogs with
 novel germline functions. Strikingly, independent c(3)G duplicates under
 positive selection in separate lineages both evolved to have high testes
 expression and similar structural changes to the proteins, suggesting
 molecular convergence of novel function. In other instances of germline
 novelty, two cona-derived paralogs were independently
 incorporated into testes-expressed lncRNA.  Surprisingly, the
 expression of SC genes in the germline is exceedingly prone to change
 suggesting recurrent regulatory evolution which, in many species, resulted
 in high testes expression even though Drosophila males are achiasmic.
 Overall, our comprehensive study recapitulates the adaptive sequence
 evolution of several components of the SC and further uncovers that the
 lack of conservation not only extends to other modalities including copy
 number, genomic locale, and germline regulation, it may also underlie
 repeated germline novelties, especially in the testes. Given the
 unexpected and frequently elevated testes expression in a large number of
 species and the ancestor, we speculate that the function of SC genes in
 the male germline, while still poorly understood, maybe a prime target of
 constant evolutionary pressures driving repeated adaptations and
 innovations.
description: # Phylogenomics and evolution of the synaptonemal complex in Drosophila
 [https://doi.org/10.5061/dryad.00000008q](https://doi.org/10.5061/dryad.00000008q) ## Description of the data and file structure This is the data associated with the publication "Diversification and recurrent adaptation of the synaptonemal complex in Drosophila" ([https://doi.org/10.1371/journal.pgen.1011549](https://doi.org/10.1371/journal.pgen.1011549)). In this study, the molecular evolution of five genes in the Synaptonemal complex (c(3)G, corolla, ord, cona, and c(2)M) are examined across the Drosophila genus. The datasets in this release include two assembled genomes (in fasta format), updated and curated gene annotations (in gff format), multiple sequence alignments of the CDS of synaptonemal complex orthologs and paralogs (in fasta format), the results of rate of evolution analyses by the HYPHY ABSREL program (in json format), and the RNA-seq read count data as reported by featureCounts (data structure can be found at [https://subread.sourceforge.net/featureCounts.html](https://subread.sourceforge.net/featureCounts.html)). All datasets are released in standard file formats or formats that are well documented. Multiple sequence alignments (with Mafft) of synaptonemal complex genes: (Protein sequences were aligned with Mafft and then converted to CDS alignments). c3G.species.CDS.mafft.nt_ali.fasta corolla.species.CDS.mafft.nt_ali.fasta ord.species.CDS.mafft.nt_ali.fasta cona.species.CDS.mafft.nt_ali.fasta c2M.species.CDS.mafft.nt_ali.fasta **HYPHY ABSREL analyses for rate of protein evolution (json file):** cona.species.CDS.mafft.nt_ali.fasta.ABSREL.json c2M.species.CDS.mafft.nt_ali.fasta.ABSREL.json ord.species.CDS.mafft.nt_ali.fasta.ABSREL.json corolla.species.CDS.mafft.nt_ali.fasta.ABSREL.json c3G.species.CDS.mafft.nt_ali.fasta.ABSREL.json **Release of the genomes assembled (D. hypocausta and D. niveifrons) - nanopore sequencing, Canu assembly:** dniv_1.0.fa dhyp_1.0.fa **de novo, updated, and hand curated annotations (gff files):** dkep.rnd3.kw.sort.gff dsul.rnd3.kw2.sort.gff dinn.v2.rob.kw.sort.gff dfun.rnd3.kw.sort.gff dpaul.stringtie.kw.sort.gff dtri.stringtie.kw.sort.gff dobs.GCF_018151105.kw.sort.gff daff.v4.0.kw.sort.gff Pi_PN175.rnd3.kw.sort.gff ddun.rnd3.all.kw2.sort.gff dleb.SlebRS2.kw.sort.gff dimm.rnd3.kw.sort.gff dser.Dser1.kw.sort.gff dniv.rnd3.kw.sort.gff dwil.UCI.kw.sort.gff dath.EB_2.0.kw.sort.gff dhyp.rnd3.kw.sort.gff dgriGCF_018153295.kw.sort.gff dfic.GCF_018152265.kw.sort.gff dbip_GCF_018153845.kw.sort.gff dbus.GCF_011750605.kw.sort.gff dnov.DnovRS2.kw.sort.gff Am_03.rnd3.kw2.sort.gff dara.rnd3.all.kw2.sort **Germline RNAseq read counts (from Hisat2 alignments and featurecount).** dhyp.OMp.fc dmoj.OMp.fc dnas.OMp.fc dmir.OMp.fc dmau.OMp.fc dkep.OMp.fc dkik.OMp.fc dhyd.OMp.fc dinn.OMp.fc dmel.OMu.fc dimm.OMp.fc dgri.OMu.fc dfun.OMp.fc dath.OMp.fc ddun.OMp.fc dana.OMp.fc dara.OMp.fc dalb.OMp.fc dsul.OMp.fc dwil.OMp.fc sleb.OMu.fc dyak.OMp.fc dsuz.OMu.fc dtei.OMp.fc dvir.OMp.fc dsub.OMp.fc dsim.OMp.fc daff.OMu.fc dser.OMp.fc dsec.OMp.fc dpse.OMp.fc dper.OMu.fc dobs.OMp.fc dpal.OMp.fc dnov.OMp.fc dniv.OMp.fc