Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins

Examining the consequences of selfing The Caenorhabditis genus of nematodes includes a mix of closely related outcrossing and self-fertilizing (selfing) species. Genome size differs widely among these different species. Yin et al. generated a genome assembly for the outcrossing nematode C. nigoni and compared it with that of its close relative, the selfing C. briggsae. C. briggsae has experienced a substantial decrease in genome size since the two species' recent divergence. The underlying causes of this size difference appear to involve a decrease in protein-coding genes and changes in other types of sequences that have homology with RNAs expressed primarily in C. nigoni males. One of the implicated gene families, the mss family, compromises sperm competitiveness. Thus, in nematodes, selfing appears to result in a decrease in genome size owing to selection to reduce male reproductive function. Science, this issue p. 55 Caenorhabditis genomes exhibit size differences related to whether they self-fertilize or outcross. To reveal impacts of sexual mode on genome content, we compared chromosome-scale assemblies of the outcrossing nematode Caenorhabditis nigoni to its self-fertile sibling species, C. briggsae. C. nigoni’s genome resembles that of outcrossing relatives but encodes 31% more protein-coding genes than C. briggsae. C. nigoni genes lacking C. briggsae orthologs were disproportionately small and male-biased in expression. These include the male secreted short (mss) gene family, which encodes sperm surface glycoproteins conserved only in outcrossing species. Sperm from mss-null males of outcrossing C. remanei failed to compete with wild-type sperm, despite normal fertility in noncompetitive mating. Restoring mss to C. briggsae males was sufficient to enhance sperm competitiveness. Thus, sex has a pervasive influence on genome content that can be used to identify sperm competition factors.

[1]  G. Stanfield,et al.  COMP-1 promotes competitive advantage of nematode sperm , 2015, eLife.

[2]  Silvio C. E. Tosatto,et al.  InterPro in 2017—beyond protein family and domain annotations , 2016, Nucleic Acids Res..

[3]  S. Kelly,et al.  OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy , 2015, Genome Biology.

[4]  Tessa G. Montague,et al.  Efficient Mutagenesis by Cas9 Protein-Mediated Oligonucleotide Insertion and Large-Scale Assessment of Single-Guide RNAs , 2014, PloS one.

[5]  M. Félix,et al.  Molecular population genetics and phenotypic sensitivity to ethanol for a globally diverse sample of the nematode Caenorhabditis briggsae , 2010, Molecular ecology.

[6]  A. Moorman,et al.  Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data , 2009, Nucleic acids research.

[7]  C. Lively,et al.  The Cost of Biparental Sex Under Individual Selection , 1990, The American Naturalist.

[8]  A. Cutter,et al.  Intense Sperm-Mediated Sexual Conflict Promotes Reproductive Isolation in Caenorhabditis Nematodes , 2014, PLoS biology.

[9]  R. Percudani.  A Microbial Metagenome (Leucobacter sp.) in Caenorhabditis Whole Genome Sequences , 2013, Bioinformatics and biology insights.

[10]  Cristel G. Thomas,et al.  Detecting heterozygosity in shotgun genome assemblies: Lessons from obligately outcrossing nematodes. , 2008, Genome research.

[11]  W. Wood.  The Nematode Caenorhabditis elegans , 1988 .

[12]  A. Lupas.  Prediction and analysis of coiled-coil structures. , 1996, Methods in enzymology.

[13]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[14]  B. LeBoeuf,et al.  Diversity in Mating Behavior of Hermaphroditic and Male–Female Caenorhabditis Nematodes , 2007, Genetics.

[15]  Alejandro A. Schäffer,et al.  WindowMasker: window-based masker for sequenced genomes , 2006, Bioinform..

[16]  M. Lenhard,et al.  The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. , 2011, Annals of botany.

[17]  Sean R. Eddy,et al.  nhmmer: DNA homology search with profile HMMs , 2013, Bioinform..

[18]  D. Pilgrim,et al.  Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes. , 2006, Developmental cell.

[19]  M. Rockman,et al.  Natural Variation in plep-1 Causes Male-Male Copulatory Behavior in C. elegans , 2015, Current Biology.

[20]  Rob Patro,et al.  Salmon provides fast and bias-aware quantification of transcript expression , 2017, Nature Methods.

[21]  Dee R. Denver,et al.  High mutation rate and predominance of insertions in the Caenorhabditis elegans nuclear genome , 2004, Nature.

[22]  Fabio Piano,et al.  Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  S. E. Baird.  Natural and experimental associations of Caenorhabditis remanei with Trachelipus rathkii and other terrestrial isopods , 1999 .

[24]  Shengfeng Huang,et al.  HaploMerger2: rebuilding both haploid sub-assemblies from high-heterozygosity diploid genome assembly , 2017, Bioinform..

[25]  J. Landolin,et al.  Assembling large genomes with single-molecule sequencing and locality-sensitive hashing , 2014, Nature Biotechnology.

[26]  A. Cutter,et al.  Gametic selection, developmental trajectories, and extrinsic heterogeneity in Haldane's rule , 2015, Evolution; international journal of organic evolution.

[27]  M. Félix,et al.  A Streamlined System for Species Diagnosis in Caenorhabditis (Nematoda: Rhabditidae) with Name Designations for 15 Distinct Biological Species , 2014, PloS one.

[28]  J. Rumbley,et al.  Fertilization in C. elegans requires an intact C-terminal RING finger in sperm protein SPE-42 , 2011, BMC Developmental Biology.

[29]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[30]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[31]  Ewan Birney,et al.  Automated generation of heuristics for biological sequence comparison , 2005, BMC Bioinformatics.

[32]  Richard Durbin,et al.  A large genome center's improvements to the Illumina sequencing system , 2008, Nature Methods.

[33]  S. Ward,et al.  The initiation of spermiogenesis in the nematode Caenorhabditis elegans. , 1983, Developmental biology.

[34]  Paramvir S. Dehal,et al.  FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments , 2010, PloS one.

[35]  E. Charnov.  The theory of sex allocation. , 1984, Monographs in population biology.

[36]  Vaqaar-un-Nisa Dar,et al.  Effective population size and tests of neutrality at cytoplasmic genes in Arabidopsis. , 2008, Genetics research.

[37]  W. Hamilton.  Extraordinary Sex Ratios , 1967 .

[38]  K. Kiontke,et al.  Phylogeny of Rhabditis subgenus Caenorhabditis (Rhabditidae, Nematoda)* , 2009 .

[39]  Jiongtang Li,et al.  L_RNA_scaffolder: scaffolding genomes with transcripts , 2013, BMC Genomics.

[40]  W. J. Kent,et al.  BLAT--the BLAST-like alignment tool. , 2002, Genome research.

[41]  Raymond K. Auerbach,et al.  Integrative Analysis of the Caenorhabditis elegans Genome by the modENCODE Project , 2010, Science.

[42]  Lincoln Stein,et al.  nGASP – the nematode genome annotation assessment project , 2008, BMC Bioinformatics.

[43]  Robert D. Finn,et al.  The Pfam protein families database: towards a more sustainable future , 2015, Nucleic Acids Res..

[44]  S. Salzberg,et al.  Versatile and open software for comparing large genomes , 2004, Genome Biology.

[45]  M. Blaxter,et al.  Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots , 2013, Front. Genet..

[46]  John C. Wootton,et al.  Non-globular Domains in Protein Sequences: Automated Segmentation Using Complexity Measures , 1994, Comput. Chem..

[47]  John Wang,et al.  Non-Mendelian assortment of homologous autosomes of different sizes in males is the ancestral state in the Caenorhabditis lineage , 2017, Scientific Reports.

[48]  M V Olson,et al.  When less is more: gene loss as an engine of evolutionary change. , 1999, American journal of human genetics.

[49]  L. Keller,et al.  Chromosome Size Differences May Affect Meiosis and Genome Size , 2010, Science.

[50]  D. Koboldt,et al.  Caenorhabditis briggsae Recombinant Inbred Line Genotypes Reveal Inter-Strain Incompatibility and the Evolution of Recombination , 2011, PLoS genetics.

[51]  Aaron A. Klammer,et al.  Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data , 2013, Nature Methods.

[52]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[53]  L. Duret,et al.  Comparative population genomics in animals uncovers the determinants of genetic diversity , 2014, Nature.

[54]  P. Sarkies,et al.  Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression , 2016, Genome research.

[55]  Cristel G. Thomas,et al.  Context-dependent function of a conserved translational regulatory module , 2012, Development.

[56]  Pavel A. Pevzner,et al.  De novo identification of repeat families in large genomes , 2005, ISMB.

[57]  S. W. Emmons,et al.  Caenorhabditis Vulgaris Sp.N. (Nematoda: Rhabditidae): a Necromenic Associate of Pill Bugs and Snails , 1994 .

[58]  D. Riddle,et al.  Comparison of a new wild-type caenorhabditis briggsae with laboratory strains of C. Briggsae and C. Elegans , 1983 .

[59]  Cristel G. Thomas,et al.  Correction: Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes , 2015, PLoS genetics.

[60]  Sean R. Eddy,et al.  Accelerated Profile HMM Searches , 2011, PLoS Comput. Biol..

[61]  Diana S Chu,et al.  Spermatogenesis-Specific Features of the Meiotic Program in Caenorhabditis elegans , 2009, PLoS genetics.

[62]  J. Chasnov,et al.  Why are there males in the hermaphroditic species Caenorhabditis elegans? , 2002, Genetics.

[63]  G. Barton,et al.  How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? , 2015, RNA.

[64]  Keith Bradnam,et al.  Assessing the gene space in draft genomes , 2008, Nucleic acids research.

[65]  S. Glémin,et al.  ADAPTATION AND MALADAPTATION IN SELFING AND OUTCROSSING SPECIES: NEW MUTATIONS VERSUS STANDING VARIATION , 2013, Evolution; international journal of organic evolution.

[66]  Christina A. Cuomo,et al.  Pilon: An Integrated Tool for Comprehensive Microbial Variant Detection and Genome Assembly Improvement , 2014, PloS one.

[67]  Ronald E. Ellis,et al.  Supplemental Data Independent Recruitment of F Box Genes to Regulate Hermaphrodite Development during Nematode Evolution , 2009 .

[68]  A. Cutter,et al.  GENETIC VARIATION FOR POSTZYGOTIC REPRODUCTIVE ISOLATION BETWEEN CAENORHABDITIS BRIGGSAE AND CAENORHABDITIS SP. 9 , 2012, Evolution; international journal of organic evolution.

[69]  Cristel G. Thomas,et al.  Simplification and Desexualization of Gene Expression in Self-Fertile Nematodes , 2012, Current Biology.

[70]  M. Robles,et al.  University of Birmingham High throughput functional annotation and data mining with the Blast2GO suite , 2022 .

[71]  Thomas Lengauer,et al.  Improved scoring of functional groups from gene expression data by decorrelating GO graph structure , 2006, Bioinform..

[72]  Sean R Eddy,et al.  A new generation of homology search tools based on probabilistic inference. , 2009, Genome informatics. International Conference on Genome Informatics.

[73]  P. Phillips,et al.  Selection and maintenance of androdioecy in Caenorhabditis elegans. , 2002, Genetics.

[74]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[75]  R. Gibbs,et al.  Mind the Gap: Upgrading Genomes with Pacific Biosciences RS Long-Read Sequencing Technology , 2012, PloS one.

[76]  B. Cassone,et al.  Comparative Transcriptomics of Malaria Mosquito Testes: Function, Evolution, and Linkage , 2017, G3: Genes, Genomes, Genetics.

[77]  Kimberly Van Auken,et al.  WormBase 2016: expanding to enable helminth genomic research , 2015, Nucleic Acids Res..

[78]  J. Wootton,et al.  Analysis of compositionally biased regions in sequence databases. , 1996, Methods in enzymology.

[79]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[80]  S. Brunak,et al.  Precision mapping of the human O‐GalNAc glycoproteome through SimpleCell technology , 2013, The EMBO journal.

[81]  M. Félix,et al.  Insights Into Species Divergence and the Evolution of Hermaphroditism From Fertile Interspecies Hybrids of Caenorhabditis Nematodes , 2010, Genetics.

[82]  David Haussler,et al.  Using native and syntenically mapped cDNA alignments to improve de novo gene finding , 2008, Bioinform..

[83]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[84]  A. Cutter.  Caenorhabditis evolution in the wild , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[85]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[86]  L. Kruglyak,et al.  Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans , 2008, Nature.

[87]  William Stafford Noble,et al.  How does multiple testing correction work? , 2009, Nature Biotechnology.

[88]  Aaron R. Quinlan,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2022 .

[89]  R. Durbin,et al.  The Genome Sequence of Caenorhabditis briggsae: A Platform for Comparative Genomics , 2003, PLoS biology.

[90]  A. Cutter,et al.  When natural selection gives gene function the cold shoulder , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[91]  K. Kiontke,et al.  Comparison of the cryptic nematode species Caenorhabditis brenneri sp. n. and C. remanei (Nematoda: Rhabditidae) with the stem species pattern of the Caenorhabditis Elegans group , 2007 .

[92]  Katharina J. Hoff,et al.  WebAUGUSTUS—a web service for training AUGUSTUS and predicting genes in eukaryotes , 2013, Nucleic Acids Res..

[93]  Juancarlos Chan,et al.  Gene Ontology Consortium: going forward , 2014, Nucleic Acids Res..

[94]  Zhongying Zhao,et al.  A Genome-Wide Hybrid Incompatibility Landscape between Caenorhabditis briggsae and C. nigoni , 2015, PLoS genetics.

[95]  Richard M. Clark,et al.  The Arabidopsis lyrata genome sequence and the basis of rapid genome size change , 2011, Nature Genetics.

[96]  S. Ward,et al.  Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans , 1981, The Journal of cell biology.

[97]  Cristel G. Thomas,et al.  Full-genome evolutionary histories of selfing, splitting, and selection in Caenorhabditis , 2014, bioRxiv.

[98]  T. Schedl,et al.  GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. , 1996, Developmental biology.

[99]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[100]  Zhongying Zhao,et al.  A Method for Rapid and Simultaneous Mapping of Genetic Loci and Introgression Sizes in Nematode Species , 2012, PloS one.

[101]  Christian Braendle,et al.  A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits , 2011, BMC Evolutionary Biology.

[102]  Pier Luigi Martelli,et al.  PredGPI: a GPI-anchor predictor , 2008, BMC Bioinformatics.

[103]  A. Moorman,et al.  Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data , 2003, Neuroscience Letters.

[104]  E. Harlow,et al.  Using Antibodies: A Laboratory Manual , 1999 .

[105]  J. Logsdon,et al.  Signs of Sex: What We Know and How We Know It , 2022 .

[106]  Geoffrey J. Barton,et al.  Jalview Version 2—a multiple sequence alignment editor and analysis workbench , 2009, Bioinform..

[107]  G. Benson,et al.  Tandem repeats finder: a program to analyze DNA sequences. , 1999, Nucleic acids research.

[108]  A. Krogh,et al.  A combined transmembrane topology and signal peptide prediction method. , 2004, Journal of molecular biology.

[109]  Linda Partridge.  The Masterpiece of Nature: The Evolution and Genetics of Sexuality, Graham Bell. Croom Helm, London and Canberra (1982), 635, Price £25.00 , 1983 .

[110]  Brian Charlesworth,et al.  INBREEDING AND OUTBREEDING DEPRESSION IN CAENORHABDITIS NEMATODES , 2007, Evolution; international journal of organic evolution.

[111]  Jun Xiao,et al.  PEP_scaffolder: using (homologous) proteins to scaffold genomes , 2016, Bioinform..

[112]  Cheng Shi,et al.  Mating and male pheromone kill Caenorhabditis males through distinct mechanisms , 2017, eLife.

[113]  J. Chasnov.  The evolution from females to hermaphrodites results in a sexual conflict over mating in androdioecious nematode worms and clam shrimp , 2010, Journal of evolutionary biology.

[114]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[115]  P. Gagneux,et al.  Sugar‐coated sperm: Unraveling the functions of the mammalian sperm glycocalyx , 2015, Molecular reproduction and development.

[116]  Metagenome-Assembled Draft Genome Sequence of a Novel Microbial Stenotrophomonas maltophilia Strain Isolated from Caenorhabditis remanei Tissue , 2017, Genome Announcements.