Conflictual speciation: species formation via genomic conflict.

A remarkable suite of forms of genomic conflict has recently been implicated in speciation. We propose that these diverse roles of genomic conflict in speciation processes can be unified using the concept of 'conflictual speciation'. Conflictual speciation centers on the evolution of reproductive isolation as a byproduct of antagonistic selection among genomic elements with divergent fitness interests. Intragenomic conflicts are expected to readily generate Dobzhansky-Muller incompatibilities, due to population-specific interactions between opposing elements, and thus they could be especially important in speciation. Moreover, selection from genomic conflicts should be relatively unrelenting across ecological and evolutionary time scales. We explain how intragenomic conflicts can promote, or sometimes constrain, speciation, and describe evidence relating conflicts to the evolution of reproductive isolation.

[1]  M. Yano,et al.  Relationship between transmission ratio distortion and genetic divergence in intraspecific rice crosses , 2011, Molecular Genetics and Genomics.

[2]  D. Baulcombe,et al.  Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds , 2012, Proceedings of the National Academy of Sciences.

[3]  M. Egas,et al.  Wolbachia affects oviposition and mating behaviour of its spider mite host , 2004, Journal of evolutionary biology.

[4]  D. Segal,et al.  Bacteria-induced sexual isolation in Drosophila , 2011, Fly.

[5]  N. Barton Fitness Landscapes and the Origin of Species , 2004 .

[6]  B. Mcclintock Modified gene expressions induced by transposable elements , 1980 .

[7]  S. Frank,et al.  Programmed cell death and hybrid incompatibility. , 2003, The Journal of heredity.

[8]  M. Nachman,et al.  SPECIATION IN THE EUROPEAN RABBIT (ORYCTOLAGUS CUNICULUS): ISLANDS OF DIFFERENTIATION ON THE X CHROMOSOME AND AUTOSOMES , 2010, Evolution; international journal of organic evolution.

[9]  B. Payseur,et al.  Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice , 2011, Genetics.

[10]  M. Turelli,et al.  Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule , 2007, Genetics.

[11]  L. Hennig,et al.  Imprinting of the Polycomb Group Gene MEDEA Serves as a Ploidy Sensor in Arabidopsis , 2009, PLoS genetics.

[12]  C. Meiklejohn,et al.  Genetic conflict and sex chromosome evolution. , 2010, Trends in ecology & evolution.

[13]  F. Úbeda,et al.  The Red Queen theory of recombination hotspots , 2011, Journal of evolutionary biology.

[14]  T. Price,et al.  Selfish genetic elements and sexual selection: their impact on male fertility , 2008, Genetica.

[15]  P. Vrana GENOMIC IMPRINTING AS A MECHANISM OF REPRODUCTIVE ISOLATION IN MAMMALS , 2007 .

[16]  Zhiping Weng,et al.  Adaptation to P Element Transposon Invasion in Drosophila melanogaster , 2011, Cell.

[17]  S. Henikoff,et al.  The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA , 2001, Science.

[18]  R. O’Neill,et al.  Genomic Instability Within Centromeres of Interspecific Marsupial Hybrids , 2007, Genetics.

[19]  J. Piálek,et al.  Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone? , 2008, BMC Evolutionary Biology.

[20]  D. Presgraves,et al.  The molecular evolutionary basis of species formation , 2010, Nature Reviews Genetics.

[21]  Renate A Weizbauer,et al.  The Maternally Expressed WRKY Transcription Factor TTG2 Controls Lethality in Interploidy Crosses of Arabidopsis , 2008, PLoS biology.

[22]  Bao Liu,et al.  Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). , 2005, Molecular biology and evolution.

[23]  D. Schluter,et al.  Evidence for Ecological Speciation and Its Alternative , 2022 .

[24]  H. Walia,et al.  Dosage-Dependent Deregulation of an AGAMOUS-LIKE Gene Cluster Contributes to Interspecific Incompatibility , 2009, Current Biology.

[25]  M. White Chromosomal Rearrangements and Speciation in Animals , 1969 .

[26]  J. Willis,et al.  A CYTONUCLEAR INCOMPATIBILITY CAUSES ANTHER STERILITY IN MIMULUS HYBRIDS , 2006, Evolution; international journal of organic evolution.

[27]  Molly Przeworski,et al.  The Case of the Fickle Fingers: How the PRDM9 Zinc Finger Protein Specifies Meiotic Recombination Hotspots in Humans , 2011, PLoS biology.

[28]  C. M. Barr,et al.  Cytoplasmic male sterility in Mimulus hybrids has pleiotropic effects on corolla and pistil traits , 2011, Heredity.

[29]  D. Presgraves,et al.  Evolution of the Drosophila Nuclear Pore Complex Results in Multiple Hybrid Incompatibilities , 2009, Science.

[30]  B. Crespi,et al.  Pathology from evolutionary conflict, with a theory of X chromosome versus autosome conflict over sexually antagonistic traits , 2011, Proceedings of the National Academy of Sciences.

[31]  W. Chȩtnicki,et al.  Preferential segregation of metacentric chromosomes in simple Robertsonian heterozygotes of Sorex araneus , 2007, Heredity.

[32]  D. Barbash,et al.  Species-Specific Heterochromatin Prevents Mitotic Chromosome Segregation to Cause Hybrid Lethality in Drosophila , 2009, PLoS biology.

[33]  I. Pašakinskienė,et al.  Genome conflict in the gramineae. , 2004, The New phytologist.

[34]  D. Hartl,et al.  A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. , 2007, PLoS biology.

[35]  N. Besansky,et al.  No evidence for biased co-transmission of speciation islands in Anopheles gambiae , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  D. Haig,et al.  Gestational drive and the green-bearded placenta. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  J Tooby,et al.  Cytoplasmic inheritance and intragenomic conflict. , 1981, Journal of theoretical biology.

[38]  Caroline Josefsson,et al.  Parent-Dependent Loss of Gene Silencing during Interspecies Hybridization , 2006, Current Biology.

[39]  R. Ishikawa,et al.  Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. , 2011, The Plant journal : for cell and molecular biology.

[40]  M. Nachman,et al.  Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  Joe Hereford,et al.  A Quantitative Survey of Local Adaptation and Fitness Trade‐Offs , 2009, The American Naturalist.

[42]  R. O’Neill,et al.  Retroelement Demethylation Associated with Abnormal Placentation in Mus musculus × Mus caroli Hybrids1 , 2012, Biology of reproduction.

[43]  N. Johnson Hybrid incompatibility genes: remnants of a genomic battlefield? , 2010, Trends in genetics : TIG.

[44]  J. Werren,et al.  INFLUENCE OF ANTIBIOTIC TREATMENT AND WOLBACHIA CURING ON SEXUAL ISOLATION AMONG DROSOPHILA MELANOGASTER CAGE POPULATIONS , 2006, Evolution; international journal of organic evolution.

[45]  Robert M. Brucker,et al.  Speciation by symbiosis. , 2012, Trends in ecology & evolution.

[46]  L. Rieseberg,et al.  Speciation genes in plants. , 2010, Annals of botany.

[47]  Harmit S. Malik,et al.  Altered Heterochromatin Binding by a Hybrid Sterility Protein in Drosophila Sibling Species , 2009, Science.

[48]  P. Hammerstein,et al.  Wolbachia-Induced Unidirectional Cytoplasmic Incompatibility and Speciation: Mainland-Island Model , 2007, PloS one.

[49]  J. Werren Selfish genetic elements, genetic conflict, and evolutionary innovation , 2011, Proceedings of the National Academy of Sciences.

[50]  Kohta Yoshida,et al.  THE CONTRIBUTION OF FEMALE MEIOTIC DRIVE TO THE EVOLUTION OF NEO-SEX CHROMOSOMES , 2012, Evolution; international journal of organic evolution.

[51]  P. Nosil,et al.  Ecological Divergence and the Origins of Intrinsic Postmating Isolation with Gene Flow , 2011 .

[52]  A. Sweigart The Genetics of Postmating, Prezygotic Reproductive Isolation Between Drosophila virilis and D. americana , 2010, Genetics.

[53]  R. Martienssen Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. , 2010, The New phytologist.

[54]  S. Henikoff,et al.  Major Evolutionary Transitions in Centromere Complexity , 2009, Cell.

[55]  K. Dyer LOCAL SELECTION UNDERLIES THE GEOGRAPHIC DISTRIBUTION OF SEX‐RATIO DRIVE IN DROSOPHILA NEOTESTACEA , 2012, Evolution; international journal of organic evolution.

[56]  C. Köhler,et al.  Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants. , 2011, Biochimica et biophysica acta.

[57]  H. Rundle,et al.  Ecological speciation: Ecological speciation , 2005 .

[58]  M. Ungerer,et al.  Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation , 2006, Current Biology.

[59]  M. Noor,et al.  The role of meiotic drive in hybrid male sterility , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[60]  B. Crespi Turner syndrome and the evolution of human sexual dimorphism , 2008, Evolutionary applications.

[61]  S. Nasuda,et al.  Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids , 2011, Proceedings of the National Academy of Sciences.

[62]  Frederick R Adler,et al.  Interaction between the X chromosome and an autosome regulates size sexual dimorphism in Portuguese Water Dogs. , 2005, Genome research.

[63]  Matthew D Dean,et al.  Widespread Over-Expression of the X Chromosome in Sterile F1 Hybrid Mice , 2010, PLoS genetics.

[64]  C. Sapienza,et al.  Female meiosis drives karyotypic evolution in mammals. , 2001, Genetics.

[65]  P. Nosil,et al.  Conditions for mutation-order speciation , 2011, Proceedings of the Royal Society B: Biological Sciences.

[66]  J. M. Nicholson,et al.  Is carcinogenesis a form of speciation? , 2011, Cell cycle.

[67]  R. Sachidanandam,et al.  An Epigenetic Role for Maternally Inherited piRNAs in Transposon Silencing , 2008, Science.

[68]  J. Jurka,et al.  Families of transposable elements, population structure and the origin of species , 2011, Biology Direct.

[69]  R. O’Neill,et al.  Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. , 2010, Annual review of genomics and human genetics.

[70]  Y. Brandvain,et al.  Divergent Mating Systems and Parental Conflict as a Barrier to Hybridization in Flowering Plants , 2005, The American Naturalist.

[71]  P. Mishra,et al.  Genetic interactions underlying hybrid male sterility in the Drosophila bipectinata species complex. , 2006, Genes & genetic systems.

[72]  Jun Wang,et al.  Two Dobzhansky-Muller Genes Interact to Cause Hybrid Lethality in Drosophila , 2006, Science.

[73]  W. Shi,et al.  Widespread disruption of genomic imprinting in adult interspecies mouse (Mus) hybrids , 2005, Genesis.

[74]  W. Rice,et al.  Sexually Antagonistic “Zygotic Drive” of the Sex Chromosomes , 2008, PLoS genetics.

[75]  M. Kirkpatrick,et al.  Turnover of sex chromosomes induced by sexual conflict , 2007, Nature.

[76]  M. Noor,et al.  Chromosomal inversions and the reproductive isolation of species , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[77]  T. Price Speciation in birds , 2008 .

[78]  S. Pilder,et al.  The Mouse t Complex Gene Tsga2, Encoding Polypeptides Located in the Sperm Tail and Anterior Acrosome, Maps to a Locus Associated with Sperm Motility and Sperm-Egg Interaction Abnormalities1 , 2006, Biology of reproduction.

[79]  H. A. Orr,et al.  A Single Gene Causes Both Male Sterility and Segregation Distortion in Drosophila Hybrids , 2009, Science.

[80]  L. Rieseberg,et al.  Ecological selection maintains cytonuclear incompatibilities in hybridizing sunflowers. , 2008, Ecology letters.

[81]  Timothy B Sackton,et al.  Interspecific Y chromosome introgressions disrupt testis-specific gene expression and male reproductive phenotypes in Drosophila , 2011, Proceedings of the National Academy of Sciences.

[82]  Yoichi Ishida,et al.  Transposable elements and an epigenetic basis for punctuated equilibria , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[83]  L. Ehrman,et al.  Infectious Speciation Revisited: Impact of Symbiont-Depletion on Female Fitness and Mating Behavior of Drosophila paulistorum , 2010, PLoS pathogens.

[84]  C. Vieira,et al.  Jumping genes and epigenetics: Towards new species. , 2010, Gene.

[85]  R. Leimu,et al.  A Meta-Analysis of Local Adaptation in Plants , 2008, PloS one.

[86]  Arpiar Saunders,et al.  Centromere-Associated Female Meiotic Drive Entails Male Fitness Costs in Monkeyflowers , 2008, Science.

[87]  L. Rieseberg,et al.  Plant Speciation , 2007, Science.

[88]  R. Herrmann,et al.  The role of plastids in plant speciation , 2011, Molecular ecology.

[89]  R. Ishikawa,et al.  Epigenetic programming: the challenge to species hybridization. , 2009, Molecular plant.

[90]  J. Leu,et al.  Speciation through cytonuclear incompatibility: Insights from yeast and implications for higher eukaryotes , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[91]  Jean-Nicolas Volff,et al.  Transposable elements as drivers of genomic and biological diversity in vertebrates , 2008, Chromosome Research.

[92]  R. Trivers,et al.  Genes in Conflict , 2006 .

[93]  A. Widmer,et al.  Polymorphism of postmating reproductive isolation within plant species , 2010 .

[94]  V. Schmidt,et al.  Decoupling of Host–Symbiont–Phage Coadaptations Following Transfer Between Insect Species , 2011, Genetics.

[95]  A. Sweigart Simple Y-Autosomal Incompatibilities Cause Hybrid Male Sterility in Reciprocal Crosses Between Drosophila virilis and D. americana , 2010, Genetics.

[96]  C. Gilbert,et al.  Chromosome evolution in the subtribe Bovina (Mammalia, Bovidae): The karyotype of the Cambodian banteng (Bos javanicus birmanicus) suggests that Robertsonian translocations are related to interspecific hybridization , 2008, Chromosome Research.

[97]  INTRAPARENTAL GAMETE COMPETITION PROVIDES A SELECTIVE ADVANTAGE FOR THE DEVELOPMENT OF HYBRID STERILITY VIA MEIOTIC DRIVE , 2005, Evolution; international journal of organic evolution.

[98]  W. Potts,et al.  FITNESS EFFECTS OF A SELFISH GENE (THE MUS T COMPLEX) ARE REVEALED IN AN ECOLOGICAL CONTEXT , 2004, Evolution; international journal of organic evolution.