The role of reinforcement in speciation: Theory and data

▪ Abstract To assess the frequency and importance of reinforcement in nature we must begin by looking for its signature in the most likely places. Theoretical studies can pinpoint conditions that favor and inhibit reinforcement, and empirical studies can identify both how often these conditions occur and whether reinforcement results. We examine how well these tools have addressed these questions by searching for gaps and mismatches in theoretical and empirical studies of reinforcement. We concentrate on five areas: (a) a broad assessment of selection against interspecific mating, (b) the mode and genetic basis of nonrandom mating, (c) the geography of speciation, (d) divergent selection on mating cues, (e) and the genetics of reproductive isolation. We conclude that reinforcement has probably not been looked for where it is most likely to occur. We pinpoint however, many further areas of study that may ultimately provide a strong assessment of the importance of reinforcement in speciation. “The grossest ...

[1]  W. Rice Speciation via habitat specialization: the evolution of reproductive isolation as a correlated character , 1987, Evolutionary Ecology.

[2]  M. Noor,et al.  Recombination and the Divergence of Hybridizing Species , 2002, Genetica.

[3]  James Mallet,et al.  Causes and Consequences of a Lack of Coevolution in Müllerian mimicry , 1999, Evolutionary Ecology.

[4]  H. Naveira,et al.  A three-locus system of interspecific incompatibility underlies male inviability in hybrids between Drosophila buzzatii and D. koepferae , 1996, Genetica.

[5]  M. Hołyńska Is the spinule pattern on the leg 4 coxopodite a tactile signal in the specific mate recognition system of Mesocyclops (Copepoda, Cyclopidae)? , 2004, Hydrobiologia.

[6]  B. Crespi,et al.  Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  M. Servedio,et al.  Speciation as a positive feedback loop between postzygotic and prezygotic barriers to gene flow , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  G. Höbel,et al.  REPRODUCTIVE CHARACTER DISPLACEMENT IN THE ACOUSTIC COMMUNICATION SYSTEM OF GREEN TREE FROGS (HYLA CINEREA) , 2003, Evolution; international journal of organic evolution.

[9]  N. Barton,et al.  ACCUMULATING POSTZYGOTIC ISOLATION GENES IN PARAPATRY: A NEW TWIST ON CHROMOSOMAL SPECIATION , 2003, Evolution; international journal of organic evolution.

[10]  A. Syvänen,et al.  Sex chromosome evolution and speciation in Ficedula flycatchers , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[11]  S. Gabriel,et al.  Paternal inheritance of a female moth's mating preference , 2002, Nature.

[12]  T. Price,et al.  THE EVOLUTION OF F1 POSTZYGOTIC INCOMPATIBILITIES IN BIRDS , 2002, Evolution; international journal of organic evolution.

[13]  R. Burton,et al.  Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  K. Pfennig,et al.  DIFFERENTIAL SELECTION TO AVOID HYBRIDIZATION IN TWO TOAD SPECIES , 2002, Evolution; international journal of organic evolution.

[15]  D. Levitan THE RELATIONSHIP BETWEEN CONSPECIFIC FERTILIZATION SUCCESS AND REPRODUCTIVE ISOLATION AMONG THREE CONGENERIC SEA URCHINS , 2002, Evolution; international journal of organic evolution.

[16]  D. Presgraves,et al.  PATTERNS OF POSTZYGOTIC ISOLATION IN LEPIDOPTERA , 2002, Evolution; international journal of organic evolution.

[17]  H. Slabbekoorn,et al.  Bird song, ecology and speciation. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  Mark Kirkpatrick,et al.  Speciation by Natural and Sexual Selection: Models and Experiments , 2002, The American Naturalist.

[19]  Manfred Gahr,et al.  The honesty of bird song: multiple constraints for multiple traits , 2002 .

[20]  S. Via,et al.  The Genetic Architecture of Ecological Specialization: Correlated Gene Effects on Host Use and Habitat Choice in Pea Aphids , 2002, The American Naturalist.

[21]  W. Swanson,et al.  The rapid evolution of reproductive proteins , 2002, Nature Reviews Genetics.

[22]  H. Rundle A TEST OF ECOLOGICALLY DEPENDENT POSTMATING ISOLATION BETWEEN SYMPATRIC STICKLEBACKS , 2002, Evolution; international journal of organic evolution.

[23]  J. Jokela,et al.  Reproductive character displacement between the closely related freshwater snails Lymnaea peregra and L. ovata , 2002 .

[24]  J. Feder,et al.  Sympatric speciation in phytophagous insects: moving beyond controversy? , 2002, Annual review of entomology.

[25]  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.

[26]  M. Servedio,et al.  BEYOND REINFORCEMENT: THE EVOLUTION OF PREMATING ISOLATION BY DIRECT SELECTION ON PREFERENCES AND POSTMATING, PREZYGOTIC INCOMPATIBILITIES , 2001, Evolution; international journal of organic evolution.

[27]  J. Willis,et al.  EVIDENCE FOR DOBZHANSKY‐MULLER INCOMPATIBILITES CONTRIBUTING TO THE STERILITY OF HYBRIDS BETWEEN MIMULUS GUTTATUS AND M. NASUTUS , 2001, Evolution; international journal of organic evolution.

[28]  J. Mallet,et al.  Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  R. Burton,et al.  VIABILITY OF CYTOCHROME C GENOTYPES DEPENDS ON CYTOPLASMIC BACKGROUNDS IN TIGRIOPUS CALIFORNICUS , 2001, Evolution; international journal of organic evolution.

[30]  H. A. Orr,et al.  Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. , 2001, Genetics.

[31]  D. Schluter Ecology and the origin of species. , 2001, Trends in ecology & evolution.

[32]  N. Barton,et al.  Theory and speciation. , 2001, Trends in ecology & evolution.

[33]  M. Kirkpatrick Reinforcement during ecological speciation , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  Chung-I Wu,et al.  Incipient speciation by sexual isolation in Drosophila: Concurrent evolution at multiple loci , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Matsuda,et al.  A locus for female discrimination behavior causing sexual isolation in Drosophila , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  James Mallet,et al.  Reproductive isolation caused by colour pattern mimicry , 2001, Nature.

[37]  A. Helbig,et al.  Male‐biased gene flow across an avian hybrid zone: evidence from mitochondrial and microsatellite DNA , 2001 .

[38]  M. Noor,et al.  THE GENETICS OF REPRODUCTIVE ISOLATION AND THE POTENTIAL FOR GENE EXCHANGE BETWEEN DROSOPHILA PSEUDOOBSCURA AND D. PERSIMILIS VIA BACKCROSS HYBRID MALES , 2001, Evolution; international journal of organic evolution.

[39]  M. Noor,et al.  Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences , 2001, Heredity.

[40]  J. Podos Correlated evolution of morphology and vocal signal structure in Darwin's finches , 2001, Nature.

[41]  H. Rundle,et al.  A GENETIC INTERPRETATION OF ECOLOGICALLY DEPENDENT ISOLATION , 2001, Evolution; international journal of organic evolution.

[42]  M. Kirkpatrick Reinforcement and divergence under assortative mating , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[43]  B. Drossel,et al.  Competitive speciation in quantitative genetic models. , 2000, Journal of theoretical biology.

[44]  H. A. Orr,et al.  Dominance, epistasis and the genetics of postzygotic isolation. , 2000, Genetics.

[45]  J. Werren,et al.  INTRASPECIFIC VARIATION IN SEXUAL ISOLATION IN THE JEWEL WASP NASONIA , 2000, Evolution; international journal of organic evolution.

[46]  M. Servedio REINFORCEMENT AND THE GENETICS OF NONRANDOM MATING , 2000, Evolution; international journal of organic evolution.

[47]  Jin Yoshimura,et al.  Speciation by sexual selection in hybridizing populations without viability selection , 2000 .

[48]  M. Higashi,et al.  Sympatric speciation by sexual selection , 1999, Nature.

[49]  R. Wyatt,et al.  POLLINATOR‐MEDIATED COMPETITION, REPRODUCTIVE CHARACTER DISPLACEMENT, AND THE EVOLUTION OF SELFING IN ARENARIA UNIFLORA (CARYOPHYLLACEAE) , 1999, Evolution; international journal of organic evolution.

[50]  D. J. Howard Conspecific Sperm and Pollen Precedence and Speciation , 1999 .

[51]  M. Noor Reinforcement and other consequences of sympatry2 , 1999, Heredity.

[52]  M. Cain,et al.  REINFORCING SELECTION IS EFFECTIVE UNDER A RELATIVELY BROAD SET OF CONDITIONS IN A MOSAIC HYBRID ZONE , 1999, Evolution; international journal of organic evolution.

[53]  Fyodor A. Kondrashov,et al.  Interactions among quantitative traits in the course of sympatric speciation , 1999, Nature.

[54]  U. Dieckmann,et al.  On the origin of species by sympatric speciation , 1999, Nature.

[55]  Dolph Schluter,et al.  SEXUAL SELECTION AGAINST HYBRIDS BETWEEN SYMPATRIC STICKLEBACK SPECIES: EVIDENCE FROM A FIELD EXPERIMENT , 1999, Evolution; international journal of organic evolution.

[56]  D. Schluter,et al.  ECOLOGICAL SPECIATION IN STICKLEBACKS: ENVIRONMENT‐DEPENDENT HYBRID FITNESS , 1999, Evolution; international journal of organic evolution.

[57]  D. Irwin,et al.  Sexual imprinting, learning and speciation , 1999, Heredity.

[58]  M Kirkpatrick,et al.  The reinforcement of mating preferences on an island. , 1999, Genetics.

[59]  K. Kral,et al.  Dynamics of a clinal hybrid zone and a comparison with island hybrid zones of flycatchers (Ficedula hypoleuca and F. albicollis) , 1999 .

[60]  M. Noor Reinforcement and other consequences of sympatry. , 1999, Heredity.

[61]  A. Kondrashov,et al.  On the origin of species by means of assortative mating , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  Daniel J. Howard,et al.  Endless Forms: Species and Speciation , 1998 .

[63]  M. Sasa,et al.  PATTERNS OF POSTZYGOTIC ISOLATION IN FROGS , 1998, Evolution; international journal of organic evolution.

[64]  P. Hogeweg,et al.  Sympatric speciation and extinction driven by environment dependent sexual selection , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[65]  T. Sota,et al.  GENITAL LOCK‐AND‐KEY AS A SELECTIVE AGENT AGAINST HYBRIDIZATION , 1998, Evolution; international journal of organic evolution.

[66]  H. A. Orr,et al.  The evolutionary genetics of speciation. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[67]  Dolph Schluter,et al.  BODY SIZE, NATURAL SELECTION, AND SPECIATION IN STICKLEBACKS , 1998, Evolution; international journal of organic evolution.

[68]  H. Rundle,et al.  REINFORCEMENT OF STICKLEBACK MATE PREFERENCES: SYMPATRY BREEDS CONTEMPT , 1998, Evolution; international journal of organic evolution.

[69]  T. Kawecki SYMPATRIC SPECIATION VIA HABITAT SPECIALIZATION DRIVEN BY DELETERIOUS MUTATIONS , 1997, Evolution; international journal of organic evolution.

[70]  P. Michalak,et al.  TESTS FOR SEXUAL INCOMPATIBILITY BETWEEN TWO NEWT SPECIES, TRITURUS VULGARIS AND TRITURUS MONTANDONI: NO‐CHOICE MATING DESIGN , 1997, Evolution; international journal of organic evolution.

[71]  M. Kirkpatrick,et al.  THE EFFECTS OF GENE FLOW ON REINFORCEMENT , 1997, Evolution; international journal of organic evolution.

[72]  B. Grant,et al.  Genetics and the origin of bird species. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[73]  T. Markow,et al.  Assortative fertilization in Drosophila. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[74]  J. Mallet,et al.  Speciation in two neotropical butterflies: extending Haldane's rule , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[75]  Glenn-Peter Stre,et al.  A sexually selected character displacement in flycatchers reinforces premating isolation , 1997, Nature.

[76]  M. Noor How Often Does Sympatry Affect Sexual Isolation in Drosophila? , 1997, The American Naturalist.

[77]  M. Noor GENETICS OF SEXUAL ISOLATION AND COURTSHIP DYSFUNCTION IN MALE HYBRIDS OF DROSOPHILA PSEUDOOBSCURA AND DROSOPHILA PERSIMILIS , 1997, Evolution; international journal of organic evolution.

[78]  M. Kirkpatrick,et al.  The strength of indirect selection on female mating preferences. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[79]  D. Krakauer,et al.  SEXUAL SELECTION, SPACE, AND SPECIATION , 1997, Evolution; international journal of organic evolution.

[80]  H. A. Orr,et al.  “PATTERNS OF SPECIATION IN DROSOPHILA” REVISITED , 1997, Evolution; international journal of organic evolution.

[81]  B. Grant,et al.  Hybridization, Sexual Imprinting, and Mate Choice , 1997, The American Naturalist.

[82]  J. Coyne Genetics of sexual isolation in male hybrids of Drosophila simulans and D. mauritiana. , 1996, Genetical research.

[83]  T. Kawecki Sympatric speciation driven by beneficial mutations , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[84]  W. Searcy,et al.  The reproductive success of secondary females relative to that of monogamous and primary females in Red-winged Blackbirds , 1996 .

[85]  G. S. Albuquerque,et al.  POSTMATING REPRODUCTIVE ISOLATION BETWEEN CHRYSOPA QUADRIPUNCTATA AND CHRYSOPA SLOSSONAE: MECHANISMS AND GEOGRAPHIC VARIATION , 1996, Evolution; international journal of organic evolution.

[86]  M. Noor,et al.  Speciation by reinforcement: a model derived from studies of Drosophila. , 1996, Genetics.

[87]  K. Lamnissou,et al.  Incompatibilities between Y chromosome and autosomes are responsible for male hybrid sterility in crosses between Drosophila virilis and Drosophila texana , 1996, Heredity.

[88]  Dave R. Vos The role of sexual imprinting for sex recognition in zebra finches: a difference between males and females , 1995, Animal Behaviour.

[89]  J Mallet,et al.  A species definition for the modern synthesis. , 1995, Trends in ecology & evolution.

[90]  M. Noor Speciation driven by natural selection in Drosophila , 1995, Nature.

[91]  H. A. Orr,et al.  The dominance theory of Haldane's rule. , 1995, Genetics.

[92]  H. A. Orr,et al.  The population genetics of speciation: the evolution of hybrid incompatibilities. , 1995, Genetics.

[93]  M. Schilthuizen,et al.  Regular articleLife on the edge: a hybrid zone inAlbinaria hippolyti(Gastropoda: Clausiliidae) from Crete , 1995 .

[94]  M. Schilthuizen,et al.  Life on the edge: a hybrid zone in Albinaria hippolyti (Gastropoda: Clausiliidae) from Crete , 1995 .

[95]  M. Arnold,et al.  Are natural hybrids fit or unfit relative to their parents? , 1995, Trends in ecology & evolution.

[96]  T. Price,et al.  SPECIATION BY REINFORCEMENT OF PREMATING ISOLATION , 1994, Evolution; international journal of organic evolution.

[97]  R. Butlin,et al.  Recombination suppressors and the evolution of new species , 1994, Heredity.

[98]  J. Feder,et al.  Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[99]  F. Sperling SEX-LINKED GENES AND SPECIES DIFFERENCES IN LEPIDOPTERA , 1994, The Canadian Entomologist.

[100]  H. Gerhardt Reproductive character displacement of female mate choice in the grey treefrog, Hyla chrysoscelis , 1994, Animal Behaviour.

[101]  A. Baker,et al.  A POPULATION MEMETICS APPROACH TO CULTURAL EVOLUTION IN CHAFFINCH SONG: DIFFERENTIATION AMONG POPULATIONS , 1994, Evolution; international journal of organic evolution.

[102]  C. Clark,et al.  Population dynamics of sexual and resource competition. , 1994, Theoretical population biology.

[103]  Chung-I Wu,et al.  Genetics of hybrid male sterility between drosophila sibling species: a complex web of epistasis is revealed in interspecific studies. , 1994, Genetics.

[104]  M. King Species Evolution: The Role of Chromosome Change , 1993 .

[105]  Andrew W. Davis Evolution of Postmating Reproductive Isolation: The Composite Nature of Haldane's Rule and Its Genetic Bases , 1993, The American Naturalist.

[106]  P. Sniegowski,et al.  The fertility effects of pericentric inversions in Drosophila melanogaster. , 1993, Genetics.

[107]  E. Zouros,et al.  An autosomal factor from Drosophila arizonae restores normal spermatogenesis in Drosophila mojavensis males carrying the D. arizonae Y chromosome. , 1993, Genetics.

[108]  M. J. Littlejohn,et al.  REINFORCEMENT AND REPRODUCTIVE CHARACTER DISPLACEMENT IN GASTROPHRYNE CAROLINENSIS AND G. OLIVACEA (ANURA: MICROHYLIDAE): A REEXAMINATION , 1992, Evolution; international journal of organic evolution.

[109]  J. Coyne Genetics of sexual isolation in females of the Drosophila simulans species complex. , 1992, Genetical research.

[110]  J. Mcphail Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texada Island, British Columbia , 1992 .

[111]  C. Carlton,et al.  Evidence of Genetic Dominance of the 13-year Life Cycle in Periodical Cicadas (Homoptera: Cicadidae: Magicicada spp.) , 1991 .

[112]  A. Grafen Biological signals as handicaps. , 1990, Journal of theoretical biology.

[113]  C. Löfstedt,et al.  No linkage between genes controlling female pheromone production and male pheromone response in the European corn borer, Ostrinia nubilalis Hübner (Lepidoptera; Pyralidae). , 1989, Genetics.

[114]  N. Sanderson CAN GENE FLOW PREVENT REINFORCEMENT? , 1989, Evolution; international journal of organic evolution.

[115]  H. A. Orr,et al.  PATTERNS OF SPECIATION IN DROSOPHILA , 1989, Evolution; international journal of organic evolution.

[116]  E. Zouros,et al.  MALE HYBRID STERILITY IN DROSOPHILA: INTERACTIONS BETWEEN AUTOSOMES AND SEX CHROMOSOMES IN CROSSES OF D. MOJAVENSIS AND D. ARIZONENSIS , 1988, Evolution; international journal of organic evolution.

[117]  André A. Dhondt,et al.  The anti-exhaustion hypothesis: a new hypothesis to explain song performance and song switching in the great tit , 1988, Animal Behaviour.

[118]  J. A. Martin,et al.  Reproductive Incompatibility Between Host Strains of the Fall Armyworm (Lepidoptera: Noctuidae) , 1987 .

[119]  H. A. Orr,et al.  Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. , 1987, Genetics.

[120]  R. Butlin Speciation by reinforcement. , 1987, Trends in ecology & evolution.

[121]  J. Mcphail Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia , 1984 .

[122]  Joseph H. Connell,et al.  On the Prevalence and Relative Importance of Interspecific Competition: Evidence from Field Experiments , 1983, The American Naturalist.

[123]  C. Simon,et al.  A SIMPLE MENDELIAN MODEL FOR 13‐ AND 17‐ YEAR LIFE CYCLES OF PERIODICAL CICADAS, WITH HISTORICAL EVIDENCE OF HYBRIDIZATION BETWEEN THEM , 1983, Evolution; international journal of organic evolution.

[124]  A. Kondrashov Multilocus model of sympatric speciation. I: One character , 1983 .

[125]  Thomas W. Schoener,et al.  Field Experiments on Interspecific Competition , 1983, The American Naturalist.

[126]  M. Kirkpatrick SEXUAL SELECTION AND THE EVOLUTION OF FEMALE CHOICE , 1982, Evolution; international journal of organic evolution.

[127]  R. Lande Models of speciation by sexual selection on polygenic traits. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[128]  E. Zouros The chromosomal basis of sexual isolation in two sibling species of Drosophila: D. arizonensis and D. mojavensis. , 1981, Genetics.

[129]  J. Felsenstein SKEPTICISM TOWARDS SANTA ROSALIA, OR WHY ARE THERE SO FEW KINDS OF ANIMALS? , 1981, Evolution; international journal of organic evolution.

[130]  M. Wasserman,et al.  CHARACTER DISPLACEMENT FOR SEXUAL ISOLATION BETWEEN DROSOPHILA MOJAVENSIS AND DROSOPHILA ARIZONENSIS , 1977, Evolution; international journal of organic evolution.

[131]  T. J. Walker,et al.  Character Displacement and Acoustic Insects , 1974 .

[132]  M. Feldman,et al.  Selection for migration modification. , 1973, Genetics.

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

[134]  R. Bigelow HYBRID ZONES AND REPRODUCTIVE ISOLATION , 1965 .

[135]  K. Lorenz,et al.  King Solomon's Ring , 1949 .

[136]  T. Dobzhansky Genetics and the Origin of Species , 1937 .

[137]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[138]  V. Volterra Variations and Fluctuations of the Number of Individuals in Animal Species living together , 1928 .

[139]  V. Volterra Fluctuations in the Abundance of a Species considered Mathematically , 1926 .

[140]  B. Dreyfus,et al.  Divergent sexual selection enhances reproductive isolation in sticklebacks , 2022 .