Genetica

, 129:309 | Cite as

Natural selection and divergence in mate preference during speciation

  • Patrik Nosil
  • Bernard J. Crespi
  • Regine Gries
  • Gerhard Gries
Original Paper

Abstract

Sexual isolation can evolve due to natural selection against hybrids (reinforcement). However, many different forms of hybrid dysfunction, and selective processes that do not involve hybrids, can contribute to the evolution of sexual isolation. Here we review how different selective processes affect the evolution of sexual isolation, describe approaches for distinguishing among them, and assess how they contribute to variation in sexual isolation among populations of Timema cristinae stick-insects. Pairs of allopatric populations of T. cristinae living on different host-plant species exhibit greater sexual isolation than those on the same host, indicating that some sexual isolation has evolved due to host adaptation. Sexual isolation is strongest in regions where populations on different hosts are in geographic contact, a pattern of reproductive character displacement that is indicative of reinforcement. Ecological costs to hybridization do occur but traits under ecological selection (predation) do not co-vary strongly with the probability of between-population mating such that selection on ecological traits is not predicted to produce a strong correlated evolutionary response in mate preference. Moreover, F1 hybrid egg inviability is lacking and the factors contributing to reproductive character displacement require further study. Finally, we show that sexual isolation involves, at least in part, olfactory communication. Our results illustrate how understanding of the evolution of sexual isolation can be enhanced by isolating the roles of diverse ecological and evolutionary processes.

Keywords

Speciation Hybrid fitness Mate choice Reproductive isolation Pheromones 

References

  1. Albert A, Schluter D (2004) Reproductive character displacement of male stickleback mate preference: reinforcement or direct selection? Evolution 58:1099–1107PubMedGoogle Scholar
  2. Arn H, Städler E, Rauscher S (1975) The electroantennographic detector—a selective and sensitive tool in the gas chromatographic analysis of insect pheromones. Z Naturforsch 30c:722–725Google Scholar
  3. Arnold SJ (1992) Constraints on phenotypic evolution. Am Nat 140:S85–S107PubMedGoogle Scholar
  4. Barbash DA, Awadalla P, Tarone AM (2004) Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLOS Biol 2:839–848Google Scholar
  5. Barton NH, Turelli M (1991) Natural and sexual selection on many loci. Genetics 127:229–225PubMedGoogle Scholar
  6. Bateson W (1909) Heredity and variation in modern lights. In: Seward AC, (ed) Darwin and modern science. Cambridge University Press, Cambridge, pp 85–101Google Scholar
  7. Boake C, DeAngelis MP, Andreadis DK (1997) Is sexual selection and species recognition a continuum? Mating behavior of the stalk-eyed fly Drosophila heteroneura. Proc Natl Acad Sci USA 94:12442–12445PubMedGoogle Scholar
  8. Bordenstein SR, Drapeau MR, Werren JH (2000) Intraspecific variation in sexual isolation in the jewel wasp Nasonia. Evolution 54:567–573PubMedGoogle Scholar
  9. Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 10:1–7Google Scholar
  10. Boughman JW, Rundle HD, Schluter D (2005) Parallel evolution of sexual isolation in sticklebacks. Evolution 59:361–373PubMedGoogle Scholar
  11. Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178PubMedGoogle Scholar
  12. Butlin RK (1995) Reinforcement: an idea evolving. Trends Ecol Evol 10:432–433Google Scholar
  13. Cheverud JM (1988) A comparison of genetic and phenotypic correlations. Evolution 42:958–968Google Scholar
  14. Church SA, Taylor DR (2002) The evolution of reproductive isolation in spatially structured populations. Evolution 56:1859–1862PubMedGoogle Scholar
  15. Claridge MF, Morgan JC (1993) Geographical variation in acoustic signals of the planthopper, Nilaparvata bakeri (Muir), in Asia: species recognition and sexual selection. Biol J Linn Soc 48:267–281Google Scholar
  16. Cognato AI, Seybold SJ, F.Sperling FAH (1999) Incomplete barriers to mitochondrial gene flow between pheromone races of the North American pine engraver, Ips pini (Say) (Coleoptera : Scolytidae). Proc R Soc Lond B 266:1843–1850Google Scholar
  17. Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381Google Scholar
  18. Coyne JA, Orr HA (1997) Patterns of speciation in Drosophila revisited. Evolution 51:295–303Google Scholar
  19. Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland, MAGoogle Scholar
  20. Crespi BJ, Sandoval CP (2000) Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks. J Evol Biol 13:249–262Google Scholar
  21. Cruz R, Rolan-Alvarez E, Garcia C (2001) Sexual selection on phenotypic traits in a hybrid zone of Littorina saxatilis (Olivi). J Evol Biol 14:773–785Google Scholar
  22. Cruz R, Carballo M, Conde-Padin P, Rolan-Alvarez E, (2004) Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by-product ecological speciation? J Evol Biol 17:288–293PubMedGoogle Scholar
  23. Day T (2000) Sexual selection and the evolution of costly female preferences: spatial effects. Evolution 54:715–730PubMedGoogle Scholar
  24. Dobzhansky T (1936) Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 121:113–125Google Scholar
  25. Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  26. Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton, New JerseyGoogle Scholar
  27. Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:125–153Google Scholar
  28. Etges WJ (2002) Divergence in mate choice systems: does evolution play by the rules? Genetica 116:151–166PubMedGoogle Scholar
  29. Fisher RA (1930) The genetical theory of natural selection. Claredon press, OxfordGoogle Scholar
  30. Fordyce JA, Nice CC, Forister ML, Shapiro AM (2002) The significance of wing pattern diversity in the Lycaenidae: mate discrimination by two recently diverged species. J Evol Biol 15:871–879Google Scholar
  31. Fuller RC, Houle D, Travis J (2005) Sensory bias as an explanation for the evolution of mate preferences. Am Nat 166:437–446PubMedGoogle Scholar
  32. Funk DJ (1998) Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52:1744–1759Google Scholar
  33. Funk DJ, Filchak KE, Feder JL (2002) Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116:251–267PubMedGoogle Scholar
  34. Funk DJ, Nosil P, Etges W (2006) Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc Natl Acad Sci USA 103:3209–3213Google Scholar
  35. Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton Univ. Press, Princeton, NJGoogle Scholar
  36. Gries G, Gries R, Schaefer PW, Gotoh T, Higashiura Y (1999) Sex pheromone components of pink gypsy moth, Lymantria mathura. Naturwissenschaften 86:235–238Google Scholar
  37. Gries R, Khaskin G, Gries G, Bennett RG, King GG, Morewood P, Slessor KN, Moorewood WD (2002) (Z,Z)-4, 7-Tridecadien-(S)-2-yl acetate: sex pheromone of Douglas-fir cone gall midge, Contarinia oregonensis. J Chem Ecol 28:2283–2297PubMedGoogle Scholar
  38. Gries R, Khaskin G, Khaskin E, Foltz K, Schaefer PW, Gries G (2003) Enantiomers of (Z,Z)-6,9-heneicosadien-11-ol: sex pheromone components of Orgyia detrita. J Chem Ecol 29:2201–2212PubMedGoogle Scholar
  39. Hager BJ, Teale SA 1996. The genetic control of pheromone production and response in the pine engraver beetle Ips pini. Heredity 77:100–107Google Scholar
  40. Hatfield T, Schluter D (1999) Ecological speciation in sticklebacks: environment dependent hybrid fitness. Evolution 53:866–873Google Scholar
  41. Higgie M, Chenoweth S, Blows MW (2000) Natural selection and the reinforcement of mate recognition. Science 290:519–521PubMedGoogle Scholar
  42. Hobel G, Gerhardt HC (2003) Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution 57:894–904PubMedGoogle Scholar
  43. Hoskin CJ, Higgie M, McDonald KR, Moritz C (2005) Reinforcement drives rapid allopatric speciation. Nature 437:1353–1356PubMedGoogle Scholar
  44. Howard DJ, Gregory PG (1993) Post-insemination signaling systems and reinforcement. Phil Trans R Soc Lond B 340:231–236Google Scholar
  45. Jiggins CD, Naisbit RE, Coe RL, Mallet J (2001) Reproductive isolation caused by colour pattern mimicry. Nature 411:302–305PubMedGoogle Scholar
  46. Jiggins CD, Estrada C, Rodrigues A (2004) Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. J Evol Biol 17:680–691PubMedGoogle Scholar
  47. Johannesson K, Larsson A, Cruz R, Garcia C, Rolan-Alvarez E, (2000) Hybrid fitness seems not to be an explanation for the partial reproductive isolation between ecotypes of Galician Littorina saxatilis. J Moll Stud 66:149–156Google Scholar
  48. Kelly JK, Noor MAF (1996) Speciation by reinforcement: a model derived from studies of Drosophila. Genetics 143:1485–1497PubMedGoogle Scholar
  49. Kirkpatrick M (1996) Good genes and direct selection in evolution of mating preferences. Evolution 50:2125–2140Google Scholar
  50. Kirkpatrick M (2001) Reinforcement during ecological speciation. Proc R Soc London B 268:1259–1263Google Scholar
  51. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38Google Scholar
  52. Kirkpatrick M, Barton NH (1997) The strength of indirect selection on female mating preferences. Proc Natl Acad Sci USA 94:1282–1286PubMedGoogle Scholar
  53. Kirkpatrick M, Servedio MR (1999) The reinforcement of mating preferences on an island. Genetics 151:865–884PubMedGoogle Scholar
  54. Kirkpatrick M, Ravigné V 2002. Speciation by natural and sexual selection: models and experiments. Am Nat 159:S22-S35PubMedGoogle Scholar
  55. Kirkpatrick M, Johnson T, Barton N (2002) General models of multilocus evolution. Genetics 161:1727–1750PubMedGoogle Scholar
  56. Leal M, Fleishman LJ (2004) Differences in visual signal design and detectability between allopatric populations of Anolis lizards. Am Nat 163:26–39PubMedGoogle Scholar
  57. Lemmon AR, Smadja C, Kirkpatrick M (2004) Reproductive character displacement is not the only possible outcome of reinforcement. J Evol Biol 17:177–183PubMedGoogle Scholar
  58. Lu G, Bernatchez L (1998) Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchell). Proc R Soc Lond B 265:1025–1030Google Scholar
  59. Mallet J, McMillan WO, Jiggins CD (1998) Mimicry and warning color at the boundary between races and species In: Howard DJ, Berlocher S (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 390–403Google Scholar
  60. Mayr E (1947) Ecological factors in speciation. Evolution 1:263–288Google Scholar
  61. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeGoogle Scholar
  62. McKinnon JS, Mori S, Blackman BK, Kingsley DL, Jamieson L, Chou J, Schluter D (2004) Evidence for ecology’s role in speciation. Nature 429:294–298PubMedGoogle Scholar
  63. Mendelson TC (2003) Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma). Evolution 57:317–327PubMedGoogle Scholar
  64. Millar JG, Giblin M, Barton D, Morrison A, Underhill EW (1990) Synthesis and field testing of enantiomers of 6Z,9Z-cis-epoxydienes as sex attractants for geometrid moths. Interaction of enantiomers and regioisomers J Chem Ecol 16:2317–2339Google Scholar
  65. Millar JG, Giblin M, Barton D, Underhill EW (1991) Chiral lepidopteran sex attractants: blends of optically active C20 and C21 diene epoxides as sex attractants for geometrid and noctuid moths (Lepidoptera). Environ Entomol 20:450–457Google Scholar
  66. Miller DR, Borden JH, Slessor KN (1996) Enantiospecific pheromone production and response profiles for populations of pine engraver, Ips pini (Say) (Coleoptera: Scolytidae), in British Columbia. J Chem Ecol 22:2157–2172Google Scholar
  67. Morton ES (1975) Ecological sources of selection on avian sounds. Am Nat 109:17–34Google Scholar
  68. Muller HJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6:71–125Google Scholar
  69. Nagel L, Schluter D (1998) Body size, natural selection, and speciation in sticklebacks. Evolution 52:209–218Google Scholar
  70. Naisbit RE, Jiggins CD, Mallet J (2001) Disruptive sexual selection against hybrids contributes to speciation between Helioconius cydno and Helioconius melpomene. Proc R Soc Lond B 268:1849–1854Google Scholar
  71. Nei N, Li W-H, (1973) Linkage disequilibrium in subdivided populations. Genetics 75:213–219PubMedGoogle Scholar
  72. Noor MAF, (1995) Speciation driven by natural selection in Drosophila. Nature 375:674–675PubMedGoogle Scholar
  73. Noor MAF, (1997) Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and Drosphila persimilis. Evolution 51:809–815Google Scholar
  74. Norusis MN (1993) SPSS for Windows. Advanced Statistics. SPSS Inc., MichiganGoogle Scholar
  75. Nosil P (2004) Reproductive isolation caused by visual predation on migrants between divergent environments. Proc R Soc Lond B 271:1521–1528Google Scholar
  76. Nosil P, Crespi BJ (2004) Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks. Evolution 58:102–112PubMedGoogle Scholar
  77. Nosil P, Crespi BJ, Sandoval CP (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417:441–443Google Scholar
  78. Nosil P, Crespi BJ, Sandoval CP (2003) Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proc R Soc Lond B 270:1911–1918Google Scholar
  79. Nosil P, Vines TH, Funk DJ (2005) Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59:705–719PubMedGoogle Scholar
  80. Nosil P, Crespi BJ, Sandoval CP, 2006a. The evolution of host preference in allopatric versus parapatric populations of T. cristinae walking-sticks. J Evol Biol 19:929–942Google Scholar
  81. Nosil P, Crespi BJ, Sandoval CP, Kirkpatrick M, 2006b. Migration and the genetic covariance between habitat preference and performance. Am Nat 167:E66–E78Google Scholar
  82. Nosil P, Crespi BJ (2006) Cryptic reproductive isolation driven by ecological divergence. Proc R Soc Lond B 273:991–997Google Scholar
  83. Orr HA, Turelli M (2001) The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55:1085–1094PubMedGoogle Scholar
  84. Orr HA, Orr LH (1996) Waiting for speciation: the effect of population subdivision on the time to speciation. Evolution 50:1742–1749Google Scholar
  85. Ortiz-Barrientos D., Counterman BA, Noor MAF (2004) The genetics of speciation by reinforcement. PLOS Biol 2:2256–2263Google Scholar
  86. Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371PubMedGoogle Scholar
  87. Patten MA, Rotenberry JT, Zuk M (2004) Habitat selection, acoustic adaptation, and the evolution of reproductive isolation. Evolution 58:2144–2155PubMedGoogle Scholar
  88. Palumbi SR (1998) Species formation and the evolution of gamete recognition loci. In: Howard DJ, Berlocher SH (eds) Endless forms: Species and Speciation. Oxford University Press, New York, pp 271–278Google Scholar
  89. Phelan PL, Baker TC (1987) Evolution of male pheromones in moths: reproductive isolation through sexual selection? Science 235:205–207PubMedGoogle Scholar
  90. Podos J (2001) Correlated evolution of morphology and vocal signal structure in Darwin’s finches. Nature 409:185–188PubMedGoogle Scholar
  91. Presgraves DC, Balagopalan L, Abmayr SM, Orr HA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423:715–719PubMedGoogle Scholar
  92. Ramsey J, Bradshaw HD, Schemske DW (2003) Components of␣reproductive isolation between the monkeyflowers Mimulus lewissii and M. cardinalis (Phrymaceae). Evolution 57: 1520–1534PubMedGoogle Scholar
  93. Richmond JQ, Reeder TW (2002) Evidence for parallel ecological speciation in scincid lizards of the Eumeces skiltonianus species group (Squamata: Scincidae). Evolution 56:1498–1513PubMedGoogle Scholar
  94. Rolan-Alvarez E, Johannesson K, Erlandsson J (1997) The maintenance of a cline in the marine snail Littorina saxatilis: the role of home site advantage and hybrid fitness. Evolution 51:1838–1847Google Scholar
  95. Rolan-Alvarez E, Caballero A (2000) Estimating sexual selection and sexual isolation effects from mating frequencies. Evolution 54:30–36PubMedGoogle Scholar
  96. Rundle HD (2002) A test of ecologically dependent postmating isolation between sympatric sticklebacks. Evolution 56:322–329PubMedGoogle Scholar
  97. Rundle HD, Schluter D (1998) Reinforcement of stickleback mating preferences: sympatry breeds contempt. Evolution 52:200–208Google Scholar
  98. Rundle HD, Nagel L, Boughman JW, Schluter D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306–308PubMedGoogle Scholar
  99. Rundle HD, Whitlock M (2001) A genetic interpretation of ecologically dependent isolation. Evolution 55:198–201PubMedGoogle Scholar
  100. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Letts 8:336–352Google Scholar
  101. Ryan MJ, Cocroft RB, Wilczynski W (1990) The role of environmental selection in intraspecific divergence of mate recognition signals in the cricket frog, Acris crepitans. Evolution 44:1869–1872Google Scholar
  102. Ryan MJ, Wilczynski W (1991) Evolution of intraspecific variation in the advertisement call of a cricket frog (Acris crepitans, Hylidae). Biol J Linn Soc 44:249–271Google Scholar
  103. Ryan MJ, Rand AS (1993) Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647–657Google Scholar
  104. Saetre GP, Moum T, Bures S, Kral M, Adamjan M, Moreno J. 1997. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387:589–592Google Scholar
  105. Saldamando CI, Tatsuta H, Butlin RK (2005) Hybrids between Chorthippus brunneus and C-jacobsi (Orthoptera: Acrididae) do not show endogenous postzygotic isolation. Biol J Linn Soc 84:195–203Google Scholar
  106. Sandoval CP (1993) Geographic, ecological and behavioral factors affecting spatial variation in color or morph frequency in the walking-stick Timema cristinae. PhD Thesis. University of California, Santa BarbaraGoogle Scholar
  107. Sandoval CP, 1994a. The effects of relative geographic scales of gene flow and selection on morph frequencies in the walking stick Timema cristinae. Evolution 48:1866–1879Google Scholar
  108. Sandoval CP, 1994b. Differential visual predation on morphs of Timema cristinae (Phasmatodeae: Timemidae) and its consequences for host range. Biol J Linn Soc 52:341–356Google Scholar
  109. Sandoval CP, Nosil P (2005) Counteracting selective regimes and host preference evolution in ecotypes of two species of walking-sticks. Evolution 59:2405–2413PubMedGoogle Scholar
  110. Schemske DW, Bradshaw HD (1999) Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA 96:11910–11915PubMedGoogle Scholar
  111. Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774Google Scholar
  112. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, OxfordGoogle Scholar
  113. Seddon N (2005) Ecological adaptation and species recognition drives vocal evolution in neotropical suboscine birds. Evolution 59:200–215PubMedGoogle Scholar
  114. Servedio MR (2000) Reinforcement and the genetics of nonrandom mating. Evolution 54:21–29PubMedGoogle Scholar
  115. Servedio M (2001) Beyond reinforcement: the evolution of premating isolation by direct selection on preferences and␣postmating, prezygotic incompatibilities. Evolution 55: 1909–1920PubMedGoogle Scholar
  116. Servedio M (2004) The evolution of premating isolation: local adaptation and natural and sexual selection against hybrids. Evolution 58:913–924PubMedGoogle Scholar
  117. Servedio M, Noor M (2003) The role of reinforcement in speciation: theory and data. Annu R Ecol Syst 34:339–364Google Scholar
  118. Seybold SJ, Quilici DR, Tillman JA, Vanderwel D, Wood DL, Blomquist GJ (1995) De novo biosynthesis of the aggregation pheromone components ipsenol and ipsdienol by the pine bark beetles Ips paraconfusus Lanier and Ips pini (Say) (Coleoptera: Scolytidae). Proc Natl Acad Sci USA 92:8393–8397PubMedGoogle Scholar
  119. Shaw KL, Parsons YM (2002) Divergence of mate recognition behavior and its consequences for genetic architectures of speciation. Am Nat 159:S61–S75PubMedGoogle Scholar
  120. Shuker DM, Underwood K, King TM, Butlin RK (2005) Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proc R Soc Lond B 272:2491–2497Google Scholar
  121. Slabbekoorn H, Smith TB (2002) Habitat-dependent song divergence in the little greenbul: an analysis of selection pressures on acoustic signals. Evolution 56:1849–1858PubMedGoogle Scholar
  122. Staddon BW, Everton IJ (1980) Haemolymph of milkweed bug Oncopeltus fasciatus (Heteroptera: Lygaeidae): inorganic constituents and amino acids. Comp Biochem Physiol 65:371–374Google Scholar
  123. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3:137–144PubMedGoogle Scholar
  124. Takacs S, Gries G (2001) Communication ecology of webbing cloth moth: evidence for male produced aggregation signal(s). Can Entomol 133:725–727CrossRefGoogle Scholar
  125. Teale SA, Hager BJ, Webster FX (1994) Pheromone-based assortative mating in a bark beetle. Anim Behav 48:569–578Google Scholar
  126. Ting CT, Tsaur SC, Wu ML, Wu CI (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282:1501–1504PubMedGoogle Scholar
  127. Vacquier VD, Swanson WJ, Lee YH (1997) Positive Darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence? J Mol Evol 44:S15–S22PubMedGoogle Scholar
  128. Vamosi SM, Schluter D (1999) Sexual selection against hybrids between sympatric stickleback species: evidence from a field experiment. Evolution 53:874–879Google Scholar
  129. Van den Dool H, Kratz PD (1963) A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J Chromatogr 2:463–471Google Scholar
  130. Vet LEM, (1983) Host-habitat location through olfactory cues by Leptopilina clavipes (Hartig) (Hym.: Eucoilidae), a parasitoid of fungivorous Drosophila: the influence of conditioning. Netherlands J Zool 33:225–248CrossRefGoogle Scholar
  131. Vines TH, Schluter D (2006) Strong assortative mating between allopatric sticklebacks as a by-product of adaptation to different environments. Proc R Soc Lond B 273:911–916Google Scholar
  132. Wasserman M, Koepfer HR (1977) Character displacement for␣sexual isolation between Drosophila mojavensis and Drosophila arizonensis. Evolution 31:812–823Google Scholar
  133. Williams MA, Blouin AG, Noor MAF (2001) Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences. Heredity 86:68–77PubMedGoogle Scholar
  134. Willis JH, Coyne JA, Kirkpatrick M (1991) Can one predict the␣evolution of quantitative characters without genetics? Evolution 45:441–444Google Scholar
  135. Wu CI, Ting CT (2004) Genes and speciation. Nat Rev Genet 5:114–122PubMedGoogle Scholar
  136. Zouros E, d’Entremont CJ, (1980) Sexual isolation among populations of Drosophila mojavensis: response to pressure from a related species. Evolution 34:421–430Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Patrik Nosil
    • 1
  • Bernard J. Crespi
    • 1
  • Regine Gries
    • 1
  • Gerhard Gries
    • 1
  1. 1.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada

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