Rapid and Predictable Evolution of Admixed Populations Between Two Drosophila Species Pairs

In this article, Matute et al. report an experiment in which they generated eight interspecific admixed populations using two species pairs of Drosophila. They found that in both species pairs, and across all experimental replicates... The consequences of hybridization are varied, ranging from the origin of new lineages, introgression of some genes between species, to the extinction of one of the hybridizing species. We generated replicate admixed populations between two pairs of sister species of Drosophila: D. simulans and D. mauritiana; and D. yakuba and D. santomea. Each pair consisted of a continental species and an island endemic. The admixed populations were maintained by random mating in discrete generations for over 20 generations. We assessed morphological, behavioral, and fitness-related traits from each replicate population periodically, and sequenced genomic DNA from the populations at generation 20. For both pairs of species, species-specific traits and their genomes regressed to those of the continental species. A few alleles from the island species persisted, but they tended to be proportionally rare among all sites in the genome and were rarely fixed within the populations. This paucity of alleles from the island species was particularly pronounced on the X-chromosome. These results indicate that nearly all foreign genes were quickly eliminated after hybridization and that selection against the minor species genome might be similar across experimental replicates.

[1]  T. Giraud,et al.  Higher Gene Flow in Sex-Related Chromosomes than in Autosomes during Fungal Divergence , 2019, Molecular biology and evolution.

[2]  A. McGregor,et al.  tartan underlies the evolution of Drosophila male genital morphology , 2019, Proceedings of the National Academy of Sciences.

[3]  Scott A. Taylor,et al.  Insights from genomes into the evolutionary importance and prevalence of hybridization in nature , 2019, Nature Ecology & Evolution.

[4]  Aaron A. Comeault,et al.  Genetic divergence and the number of hybridizing species affect the path to homoploid hybrid speciation , 2018, Proceedings of the National Academy of Sciences.

[5]  Aaron A. Comeault,et al.  A Maladaptive Combination of Traits Contributes to the Maintenance of a Drosophila Hybrid Zone , 2018, Current Biology.

[6]  Lucas W. Hemmer The Evolution of Recombination Landscapes and Mechanisms in Drosophila in Light of Intragenomic Conflict , 2018 .

[7]  D. Presgraves,et al.  Evaluating genomic signatures of “the large X‐effect” during complex speciation , 2018, Molecular ecology.

[8]  J. Montoya-Burgos,et al.  Effect of hybridization with genome exclusion on extinction risk , 2018, Conservation biology : the journal of the Society for Conservation Biology.

[9]  Daniel L. Powell,et al.  Natural selection interacts with recombination to shape the evolution of hybrid genomes , 2018, Science.

[10]  David L. Stern,et al.  Correlated Evolution of Two Copulatory Organs via a Single cis-Regulatory Nucleotide Change , 2018, Current Biology.

[11]  S. Kingan,et al.  Molecular Evolution at a Meiosis Gene Mediates Species Differences in the Rate and Patterning of Recombination , 2018, Current Biology.

[12]  Camilo Salazar,et al.  Recombination rate variation shapes barriers to introgression across butterfly genomes , 2018, bioRxiv.

[13]  A. Comeault The genomic and ecological context of hybridization affects the probability that symmetrical incompatibilities drive hybrid speciation , 2017, bioRxiv.

[14]  Simon H. Martin,et al.  Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography , 2017, bioRxiv.

[15]  E. Mandeville,et al.  Analysis of Population Genomic Data from Hybrid Zones , 2017 .

[16]  Daniel R. Schrider,et al.  Supervised machine learning reveals introgressed loci in the genomes of Drosophila simulans and D. sechellia , 2017, bioRxiv.

[17]  D. R. Matute,et al.  Fine scale mapping of genomic introgressions within the Drosophila yakuba clade , 2017, bioRxiv.

[18]  David L. Aylor,et al.  Male Infertility Is Responsible for Nearly Half of the Extinction Observed in the Mouse Collaborative Cross , 2017, Genetics.

[19]  G. Wallis,et al.  Interspecific hybridization causes long‐term phylogenetic discordance between nuclear and mitochondrial genomes in freshwater fishes , 2017, Molecular ecology.

[20]  J. David,et al.  The Rate of Evolution of Postmating-Prezygotic Reproductive Isolation in Drosophila , 2017, bioRxiv.

[21]  Aaron A. Comeault,et al.  Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement in Drosophila yakuba , 2016, Proceedings of the Royal Society B: Biological Sciences.

[22]  Russell B. Corbett-Detig,et al.  A Hidden Markov Model Approach for Simultaneously Estimating Local Ancestry and Admixture Time Using Next Generation Sequence Data in Samples of Arbitrary Ploidy , 2016, bioRxiv.

[23]  Daniel L. Powell,et al.  Ancient hybridization and genomic stabilization in a swordtail fish , 2016, Molecular ecology.

[24]  Dan G. Bock,et al.  Hybridization and extinction , 2016, Evolutionary applications.

[25]  C. Muirhead,et al.  Hybrid Incompatibilities, Local Adaptation, and the Genomic Distribution of Natural Introgression between Species , 2016, The American Naturalist.

[26]  James Mallet,et al.  How reticulated are species? , 2015, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  R. Nielsen,et al.  The Genetic Cost of Neanderthal Introgression , 2015, Genetics.

[28]  G. Coop,et al.  The Strength of Selection against Neanderthal Introgression , 2015, bioRxiv.

[29]  A. Llopart,et al.  Gene flow between Drosophila yakuba and Drosophila santomea in subunit V of cytochrome c oxidase: A potential case of cytonuclear cointrogression , 2015, Evolution; international journal of organic evolution.

[30]  Scott A. Taylor,et al.  Hybrid zones: windows on climate change. , 2015, Trends in ecology & evolution.

[31]  C. Schlötterer,et al.  The recent invasion of natural Drosophila simulans populations by the P-element , 2015, Proceedings of the National Academy of Sciences.

[32]  J. David,et al.  The evolution of reproductive isolation in the Drosophila yakuba complex of species , 2015, Journal of evolutionary biology.

[33]  Mathias Currat,et al.  Modelling interspecific hybridization with genome exclusion to identify conservation actions: the case of native and invasive Pelophylax waterfrogs , 2015, Evolutionary applications.

[34]  Xiaofang Jiang,et al.  Extensive introgression in a malaria vector species complex revealed by phylogenomics , 2015, Science.

[35]  D. Greig,et al.  The effect of hybrid transgression on environmental tolerance in experimental yeast crosses , 2014, Journal of evolutionary biology.

[36]  H. Burbano,et al.  The Genomic Architecture of Population Divergence between Subspecies of the European Rabbit , 2014, PLoS genetics.

[37]  D. R. Matute,et al.  The magnitude of behavioral isolation is affected by characteristics of the mating community , 2014, Ecology and evolution.

[38]  Daniel L. Powell,et al.  High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species , 2014, eLife.

[39]  P. Andolfatto,et al.  HOW COMMON IS HOMOPLOID HYBRID SPECIATION? , 2014, Evolution; international journal of organic evolution.

[40]  Russell B. Corbett-Detig,et al.  Genetic Incompatibilities are Widespread Within Species , 2013, Nature.

[41]  S. Kingan,et al.  A selective sweep across species boundaries in Drosophila. , 2013, Molecular biology and evolution.

[42]  A. McGregor,et al.  Genetic and developmental analysis of differences in eye and face morphology between Drosophila simulans and Drosophila mauritiana , 2013, Evolution & development.

[43]  Heng Li Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[44]  C. Schlötterer,et al.  Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana , 2013, Genome research.

[45]  Kevin R. Thornton,et al.  A second-generation assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence , 2013, Genome research.

[46]  P. Andolfatto,et al.  Revisiting an Old Riddle: What Determines Genetic Diversity Levels within Species? , 2012, PLoS biology.

[47]  Kevin R. Thornton,et al.  Genome sequencing reveals complex speciation in the Drosophila simulans clade , 2012, Genome research.

[48]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[49]  A. McGregor,et al.  Evolution of Eye Morphology and Rhodopsin Expression in the Drosophila melanogaster Species Subgroup , 2012, PloS one.

[50]  Luke J. Harmon,et al.  Goldilocks Meets Santa Rosalia: An Ephemeral Speciation Model Explains Patterns of Diversification Across Time Scales , 2012, Evolutionary Biology.

[51]  Robert Kofler,et al.  PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq) , 2011, Bioinform..

[52]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[53]  William N. Venables,et al.  Modern Applied Statistics with S , 2010 .

[54]  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.

[55]  Sanford Weisberg,et al.  An R Companion to Applied Regression , 2010 .

[56]  C. Schlötterer,et al.  Multiple hybridization events between Drosophila simulans and Drosophila mauritiana are supported by mtDNA introgression , 2010, Molecular ecology.

[57]  Anna-Sophie Fiston-Lavier,et al.  Drosophila melanogaster recombination rate calculator. , 2010, Gene.

[58]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[59]  D. R. Matute,et al.  Reinforcement of Gametic Isolation in Drosophila , 2010, PLoS biology.

[60]  S. Carroll,et al.  Evolution of the tan Locus Contributed to Pigment Loss in Drosophila santomea: A Response to Matute et al. , 2009, Cell.

[61]  J. Coyne,et al.  INTRINSIC REPRODUCTIVE ISOLATION BETWEEN TWO SISTER SPECIES OF DROSOPHILA , 2009, Evolution; international journal of organic evolution.

[62]  J. Coyne,et al.  Temperature-Based Extrinsic Reproductive Isolation in Two Species of Drosophila , 2009, Evolution; international journal of organic evolution.

[63]  H. Ellegren Genomic evidence for a large-Z effect , 2009, Proceedings of the Royal Society B: Biological Sciences.

[64]  J. Mavárez,et al.  Homoploid hybrid speciation in animals , 2008, Molecular ecology.

[65]  D. Presgraves,et al.  Sex chromosomes and speciation in Drosophila. , 2008, Trends in genetics : TIG.

[66]  Colin N. Dewey,et al.  Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans , 2007, PLoS biology.

[67]  D. Presgraves,et al.  High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila , 2007, PLoS biology.

[68]  M. Chapman,et al.  GENETIC DIVERGENCE AND HYBRID SPECIATION , 2007, Evolution; international journal of organic evolution.

[69]  L. Rieseberg,et al.  Rampant Gene Exchange Across a Strong Reproductive Barrier Between the Annual Sunflowers, Helianthus annuus and H. petiolaris , 2007, Genetics.

[70]  J. Piálek,et al.  GENETIC ANALYSIS OF AUTOSOMAL AND X-LINKED MARKERS ACROSS A MOUSE HYBRID ZONE , 2007, Evolution; international journal of organic evolution.

[71]  K. Hornik,et al.  A Lego System for Conditional Inference , 2006 .

[72]  C. Niederberger,et al.  Male infertility. , 2006, Reviews in urology.

[73]  T. Mackay,et al.  The Genetic Basis of Postzygotic Reproductive Isolation Between Drosophila santomea and D. yakuba Due to Hybrid Male Sterility , 2006, Genetics.

[74]  A. Kopp,et al.  Historical biogeography of Drosophila simulans based on Y-chromosomal sequences. , 2006, Molecular phylogenetics and evolution.

[75]  Kevin R. Thornton,et al.  EXTENSIVE INTROGRESSION OF MITOCHONDRIAL DNA RELATIVE TO NUCLEAR GENES IN THE DROSOPHILA YAKUBA SPECIES GROUP , 2006, Evolution; international journal of organic evolution.

[76]  J. Coyne,et al.  AN ANOMALOUS HYBRID ZONE IN DROSOPHILA , 2005, Evolution; international journal of organic evolution.

[77]  T. Mackay,et al.  Quantitative Trait Loci Affecting the Difference in Pigmentation Between Drosophila yakuba and D. santomea , 2005, Genetics.

[78]  J. Coyne,et al.  Multilocus Analysis of Introgression Between Two Sympatric Sister Species of Drosophila: Drosophila yakuba and D. santomea , 2005, Genetics.

[79]  J. Mallet Hybridization as an invasion of the genome. , 2005, Trends in ecology & evolution.

[80]  Dmitri A Petrov,et al.  Genomic Heterogeneity of Background Substitutional Patterns in Drosophila melanogaster , 2005, Genetics.

[81]  M. Nachman,et al.  DIFFERENTIAL PATTERNS OF INTROGRESSION ACROSS THE X CHROMOSOME IN A HYBRID ZONE BETWEEN TWO SPECIES OF HOUSE MICE , 2004, Evolution; international journal of organic evolution.

[82]  Matthew D Dean,et al.  Linking phylogenetics with population genetics to reconstruct the geographic origin of a species. , 2004, Molecular phylogenetics and evolution.

[83]  Susannah Elwyn,et al.  Genetic studies of two sister species in the Drosophila melanogaster subgroup, D. yakuba and D. santomea. , 2004, Genetical research.

[84]  T. Mackay,et al.  Quantitative Trait Loci for Sexual Isolation Between Drosophila simulans and D. mauritiana , 2004, Genetics.

[85]  Audrey S. Chang CONSPECIFIC SPERM PRECEDENCE IN SISTER SPECIES OF DROSOPHILA WITH OVERLAPPING RANGES , 2004, Evolution; international journal of organic evolution.

[86]  D. Lachaise,et al.  How Two Afrotropical Endemics Made Two Cosmopolitan Human Commensals: the Drosophila Melanogaster–D. Simulans Palaeogeographic Riddle , 2004, Genetica.

[87]  L. Rieseberg,et al.  Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization , 2003, Science.

[88]  U. Ligges Review of An R and S-PLUS companion to applied regression by J. Fox, Sage Publications, Thousand Oaks, California 2002 , 2003 .

[89]  P. David,et al.  Deleterious mutations in a hybrid zone: can mutational load decrease the barrier to gene flow? , 2002, Genetical research.

[90]  J. Coyne,et al.  SEXUAL ISOLATION BETWEEN TWO SIBLING SPECIES WITH OVERLAPPING RANGES: DROSOPHILA SANTOMEA AND DROSOPHILA YAKUBA , 2002, Evolution; international journal of organic evolution.

[91]  L. Rieseberg,et al.  Predicting the Risk of Extinction through Hybridization , 2001 .

[92]  P. Keim,et al.  HYBRID POPULATIONS SELECTIVELY FILTER GENE INTROGRESSION BETWEEN SPECIES , 2001, Evolution; international journal of organic evolution.

[93]  A. Sugden The Strength of Selection , 2001, Science.

[94]  D. Lachaise,et al.  Divergence between Drosophila santomea and allopatric or sympatric populations of D. yakuba using paralogous amylase genes and migration scenarios along the Cameroon volcanic line , 2001, Molecular ecology.

[95]  C. Gronlund,et al.  CRYPTIC REPRODUCTIVE ISOLATION IN THE DROSOPHILA SIMULANS SPECIES COMPLEX , 2001, Evolution; international journal of organic evolution.

[96]  F. Lemeunier,et al.  Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[97]  Loren H Rieseberg,et al.  The likelihood of homoploid hybrid speciation , 2000, Heredity.

[98]  J. True,et al.  QUANTITATIVE GENETIC ANALYSIS OF DIVERGENCE IN MALE SECONDARY SEXUAL TRAITS BETWEEN DROSOPHILA SIMULANS AND DROSOPHILA MAURITIANA , 1997, Evolution; international journal of organic evolution.

[99]  J. True,et al.  An introgression analysis of quantitative trait loci that contribute to a morphological difference between Drosophila simulans and D. mauritiana. , 1997, Genetics.

[100]  D. Simberloff,et al.  Extinction by hybridization and introgression , 1996 .

[101]  Z B Zeng,et al.  Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. , 1996, Genetics.

[102]  R. Jansen,et al.  Hybridization and the Extinction of Rare Plant Species , 1996 .

[103]  J. True,et al.  Differences in crossover frequency and distribution among three sibling species of Drosophila. , 1996, Genetics.

[104]  L. Zeng,et al.  The genetic basis of Haldane's rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. , 1993, Genetics.

[105]  J. Coyne Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[106]  B. Burnet,et al.  Sexual isolation and courtship behavior inDrosophila simulans, D. mauritiana, and their interspecific hybrids , 1988, Behavior genetics.

[107]  T. W. Lyttle,et al.  Induced and natural break sites in the chromosomes of Hawaiian Drosophila. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[108]  M. Ashburner,et al.  THE REPRODUCTIVE RELATIONSHIPS OF DROSOPHILA SECHELLIA WITH D. MAURITIANA, D. SIMULANS, AND D. MELANOGASTER FROM THE AFROTROPICAL REGION , 1986, Evolution; international journal of organic evolution.

[109]  J. Coyne,et al.  Genetic studies of three sibling species of Drosophila with relationship to theories of speciation. , 1985, Genetical research.

[110]  J. Coyne Genetic basis of male sterility in hybrids between two closely related species of Drosophila. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[111]  M. Ashburner,et al.  Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora) , 1984, Chromosoma.

[112]  W. Moore An Evaluation of Narrow Hybrid Zones in Vertebrates , 1977, The Quarterly Review of Biology.

[113]  M. Ashburner,et al.  Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora) - II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[114]  G. Ledyard Stebbins,et al.  Variation and Evolution in Plants , 1951 .

[115]  Achim Zeileis,et al.  Diagnostic Checking in Regression Relationships , 2015 .

[116]  A. Qvarnström,et al.  Speciation through evolution of sex-linked genes , 2009, Heredity.

[117]  Claude-Alain H. Roten,et al.  Fast and accurate short read alignment with Burrows–Wheeler transform , 2009, Bioinform..

[118]  J. Mallet Hybrid speciation , 2007, Nature.

[119]  V. Hartenstein,et al.  Drosophila melanogaster , 2005 .

[120]  Z B Zeng,et al.  Genetic architecture of a morphological shape difference between two Drosophila species. , 2000, Genetics.

[121]  J. David,et al.  Drosophila mauritiana n. sp. du groupe melanogaster de l'Ile Maurice [Dipt. Drosophilidae] , 1974, Bulletin de la Société entomologique de France.