Sex chromosomes evolved from independent ancestral linkage groups in winged insects.

The evolution of a pair of chromosomes that differ in appearance between males and females (heteromorphic sex chromosomes) has occurred repeatedly across plants and animals. Recent work has shown that the male heterogametic (XY) and female heterogametic (ZW) sex chromosomes evolved independently from different pairs of homomorphic autosomes in the common ancestor of birds and mammals but also that X and Z chromosomes share many convergent molecular features. However, little is known about how often heteromorphic sex chromosomes have either evolved convergently from different autosomes or in parallel from the same pair of autosomes and how universal patterns of molecular evolution on sex chromosomes really are. Among winged insects with sequenced genomes, there are male heterogametic species in both the Diptera (e.g., Drosophila melanogaster) and the Coleoptera (Tribolium castaneum), female heterogametic species in the Lepidoptera (Bombyx mori), and haplodiploid species in the Hymenoptera (e.g., Nasonia vitripennis). By determining orthologous relationships among genes on the X and Z chromosomes of insects with sequenced genomes, we are able to show that these chromosomes are not homologous to one another but are homologous to autosomes in each of the other species. These results strongly imply that heteromorphic sex chromosomes have evolved independently from different pairs of ancestral chromosomes in each of the insect orders studied. We also find that the convergently evolved X chromosomes of Diptera and Coleoptera share genomic features with each other and with vertebrate X chromosomes, including excess gene movement from the X to the autosomes. However, other patterns of molecular evolution--such as increased codon bias, decreased gene density, and the paucity of male-biased genes on the X--differ among the insect X and Z chromosomes. Our results provide evidence for both differences and nearly universal similarities in patterns of evolution among independently derived sex chromosomes.

[1]  W. Black,et al.  Mosquito genomes: structure, organization, and evolution. , 1999, Advances in genetics.

[2]  Thomas J. Hardcastle,et al.  Getting a Full Dose? Reconsidering Sex Chromosome Dosage Compensation in the Silkworm, Bombyx mori , 2011, Genome biology and evolution.

[3]  M. Long,et al.  General gene movement off the X chromosome in the Drosophila genus. , 2009, Genome research.

[4]  H. Abe,et al.  Identification of the female-determining region of the W chromosome in Bombyxmori , 2008, Genetica.

[5]  Gregory R. Madey,et al.  VectorBase: a data resource for invertebrate vector genomics , 2008, Nucleic Acids Res..

[6]  P. D. de Jong,et al.  Genomic degradation of a young Y chromosome in Drosophila miranda , 2008, Genome Biology.

[7]  M. Hahn,et al.  Retrogenes Reveal the Direction of Sex-Chromosome Evolution in Mosquitoes , 2010, Genetics.

[8]  Kevin R. Thornton,et al.  Retroposed new genes out of the X in Drosophila. , 2002, Genome research.

[9]  W. Rice.  THE ACCUMULATION OF SEXUALLY ANTAGONISTIC GENES AS A SELECTIVE AGENT PROMOTING THE EVOLUTION OF REDUCED RECOMBINATION BETWEEN PRIMITIVE SEX CHROMOSOMES , 1987, Evolution; international journal of organic evolution.

[10]  A. Moya,et al.  The pea aphid phylome: a complete catalogue of evolutionary histories and arthropod orthology and paralogy relationships for Acyrthosiphon pisum genes , 2010, Insect molecular biology.

[11]  H. Cooke.  Faculty Opinions recommendation of The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression. , 2008 .

[12]  M. Long,et al.  Retrogene movement within- and between-chromosomes in the evolution of Drosophila genomes. , 2006, Gene.

[13]  D. Petrov,et al.  X-Linked Genes Evolve Higher Codon Bias in Drosophila and Caenorhabditis , 2005, Genetics.

[14]  J. Mank,et al.  The Birds and the Bees and the Flowers and the Trees: Lessons from Genetic Mapping of Sex Determination in Plants and Animals , 2010, Genetics.

[15]  C. Wills.  The Evolutionary Biology of Flies , 2006 .

[16]  N. Vinckenbosch,et al.  Chromosomal Gene Movements Reflect the Recent Origin and Biology of Therian Sex Chromosomes , 2008, PLoS biology.

[17]  K. Gharbi,et al.  Comparative genome analysis of the primary sex-determining locus in salmonid fishes. , 2003, Genome research.

[18]  M. Miles,et al.  An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. , 2002, Molecular biology and evolution.

[19]  B. S. Baker,et al.  The evolutionary dynamics of sex determination. , 1998, Science.

[20]  Colin N. Dewey,et al.  Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution , 2004, Nature.

[21]  J. Mank,et al.  Evolution of alternative sex-determining mechanisms in teleost fishes , 2006 .

[22]  H. Ellegren.  Sex-chromosome evolution: recent progress and the influence of male and female heterogamety , 2011, Nature Reviews Genetics.

[23]  M. Shapiro,et al.  Turnover of Sex Chromosomes in the Stickleback Fishes (Gasterosteidae) , 2009, PLoS genetics.

[24]  Evgeny M. Zdobnov,et al.  Genome Sequence of Aedes aegypti, a Major Arbovirus Vector , 2007, Science.

[25]  C. Peichel,et al.  Are homologies in vertebrate sex determination due to shared ancestry or to limited options? , 2010, Genome Biology.

[26]  Peer Bork,et al.  Comparative Genome and Proteome Analysis of Anopheles gambiae and Drosophila melanogaster , 2002, Science.

[27]  Yoshiaki Nagamura,et al.  KAIKObase: An integrated silkworm genome database and data mining tool , 2009, BMC Genomics.

[28]  W. Rice.  Evolution of the Y Sex Chromosome in Animals Y chromosomes evolve through the degeneration of autosomes , 1996 .

[29]  P. Divina,et al.  Nonrandom Representation of Sex-Biased Genes on Chicken Z Chromosome , 2006, Journal of Molecular Evolution.

[30]  Steve Rozen,et al.  Convergent Evolution of Chicken Z and Human X Chromosomes by Expansion and Gene Acquisition , 2010, Nature.

[31]  David Osumi-Sutherland,et al.  FlyBase: enhancing Drosophila Gene Ontology annotations , 2008, Nucleic Acids Res..

[32]  I. Mackay,et al.  Evolution of dominance , 1979, Nature.

[33]  Melissa A. Wilson,et al.  Genomic analyses of sex chromosome evolution. , 2009, Annual review of genomics and human genetics.

[34]  D. Page,et al.  Functional coherence of the human Y chromosome. , 1997, Science.

[35]  M. Karin,et al.  Human metallothionein genes—primary structure of the metallothionein-II gene and a related processed gene , 1982, Nature.

[36]  Mira V. Han,et al.  A Complex Suite of Forces Drives Gene Traffic from Drosophila X Chromosomes , 2009, Genome biology and evolution.

[37]  B. Charlesworth,et al.  Evolution on the X chromosome: unusual patterns and processes , 2006, Nature Reviews Genetics.

[38]  J. Bull.  Evolution of sex determining mechanisms , 1983 .

[39]  Jeffery P. Demuth,et al.  Hyperexpression of the X Chromosome in Both Sexes Results in Extensive Female Bias of X-Linked Genes in the Flour Beetle , 2010, Genome biology and evolution.

[40]  F. Wright.  The 'effective number of codons' used in a gene. , 1990, Gene.

[41]  David L. Steffen,et al.  The DNA sequence of the human X chromosome , 2005, Nature.

[42]  Doina Caragea,et al.  BeetleBase in 2010: revisions to provide comprehensive genomic information for Tribolium castaneum , 2009, Nucleic Acids Res..

[43]  Christine G. Elsik,et al.  Hymenoptera Genome Database: integrated community resources for insect species of the order Hymenoptera , 2010, Nucleic Acids Res..

[44]  P. Leder,et al.  Processed genes: a dispersed human immunoglobulin gene bearing evidence of RNA-type processing , 1982, Nature.

[45]  J. Ironside.  No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[46]  N. Vinckenbosch,et al.  Evolutionary fate of retroposed gene copies in the human genome. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[47]  J. Pease,et al.  No Excess Gene Movement Is Detected off the Avian or Lepidopteran Z Chromosome , 2011, Genome biology and evolution.

[48]  J. Haldane,et al.  SEX LINKAGE AND SEX DETERMINATION IN A MOSQUITO, CULEX MOLESTUS , 2010 .

[49]  M. Long,et al.  Extensive Gene Traffic on the Mammalian X Chromosome , 2004, Science.

[50]  J. Rinn,et al.  Sexual dimorphism in mammalian gene expression. , 2005, Trends in genetics : TIG.

[51]  G. Wilkinson,et al.  Comparative Genomic Hybridization (CGH) Reveals a Neo-X Chromosome and Biased Gene Movement in Stalk-Eyed Flies (Genus Teleopsis) , 2010, PLoS genetics.

[52]  T. Graves,et al.  The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes , 2003, Nature.

[53]  S. Dongen.  A cluster algorithm for graphs , 2000 .

[54]  B. Charlesworth,et al.  Steps in the evolution of heteromorphic sex chromosomes , 2005, Heredity.

[55]  David K Yeates,et al.  Single-copy nuclear genes resolve the phylogeny of the holometabolous insects , 2009, BMC Biology.

[56]  J. Parsch,et al.  Patterns of Synonymous Codon Usage in Drosophila melanogaster Genes With Sex-Biased Expression , 2005, Genetics.

[57]  Erik L. L. Sonnhammer,et al.  InParanoid 7: new algorithms and tools for eukaryotic orthology analysis , 2009, Nucleic Acids Res..

[58]  D. Page,et al.  The mouse X chromosome is enriched for multi-copy testis genes exhibiting post-meiotic expression , 2008, Nature Genetics.

[59]  Andrea Crisanti,et al.  A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector, Anopheles gambiae , 2011, BMC Genomics.

[60]  J. A. Marshall Graves.  Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. , 2008, Annual review of genetics.

[61]  T. Honjo,et al.  Long terminal repeat‐like elements flank a human immunoglobulin epsilon pseudogene that lacks introns. , 1982, The EMBO journal.

[62]  V. B. Kaiser,et al.  Evolution of sex chromosomes in insects. , 2010, Annual review of genetics.

[63]  Justen Andrews,et al.  Paucity of Genes on the Drosophila X Chromosome Showing Male-Biased Expression , 2003, Science.

[64]  R. Fisher.  THE EVOLUTION OF DOMINANCE , 1931 .

[65]  Matthew W. Hahn,et al.  Female-biased gene expression in the malaria mosquito Anopheles gambiae , 2005, Current Biology.

[66]  D. Bachtrog.  A dynamic view of sex chromosome evolution. , 2006, Current opinion in genetics & development.

[67]  Arjun Bhutkar,et al.  Chromosomal Rearrangement Inferred From Comparisons of 12 Drosophila Genomes , 2008, Genetics.

[68]  B. Oliver,et al.  Demasculinization of X chromosomes in the Drosophila genus , 2007, Nature.

[69]  J. Nagaraju,et al.  The Silkworm Z Chromosome Is Enriched in Testis-Specific Genes , 2009, Genetics.

[70]  Hans Ellegren,et al.  The evolution of sex-biased genes and sex-biased gene expression , 2007, Nature Reviews Genetics.

[71]  Q. Xia,et al.  Dosage analysis of Z chromosome genes using microarray in silkworm, Bombyx mori. , 2009, Insect biochemistry and molecular biology.