Abstract
Sexual isolation, the reduced ability of organisms of different species to successfully mate, is one of the reproductive barriers that prevent gene flow between different taxa. Various species-specific signals during courtship are attributed to the sexual isolation between them. Drosophila pseudoobscura has been widely used to study the behavioral and genetic mechanisms underlying selection for sexual isolation, as a model system for speciation. D. pseudoobscura and its sibling species, D. persmilis, live together in many locations but are reproductively isolated from one another. North American geographic strains of D. pseudoobscura from the American West mate at random. Several decades ago, D. pseudoobscura was collected in the vicinity of Bogota, Colombia, and later named the subspecies D. pseudoobscura bogotana. Nearly 5,000 matings were observed in this study. We analyzed mating behavior and cuticular hydrocarbon profiles as well as courtship within and between North American and Bogota strains of D. pseudoobscura. Here we report for the first time that Bogota strains of D. pseudoobscura do show statistically significant sexual isolation from North American strains. In addition, there are quantitative variations in cuticular hydrocarbons as well as in courtship behavior between Bogota and North American strains, and females of both North American and Bogota strains show strong preference for North American strain males having high mating propensities, suggesting that the Bogota strains are at an early stage that could lead to a separate species.
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References
Anderson WW, Ehrman L (1969) Mating choice in crosses between geographic populations of Drosophila pseudoobscura. Am Midl Nat 81:47–53
Anderson WW, Kim Y-K (2005) Sexual isolation between sympatric and allopatric populations of Drosophila pseudoobscura and D. persimilis. Behav Genet 35:305–312
Anderson WW, Kim Y-K (2006) A further analysis of sexual isolation between sympatric and allopatric populations of Drosophila pseudoobscura and D. persimilis. Behav Genet 36:328–330
Anderson WW, Ayala FJ, Michod RE (1977) Chromosomal and allozymic diagnosis of three species of Drosophila: D. pseudoobscura, D. persimilis, and D. miranda. J Hered 68:71–74
Anholt RRH, Mackay TFC (2004) Quanatitative genetic analyses of complex behaviours in Drosophila. Nat Rev Genet 5:838–849
Ayala FJ, Dobzhansky Th (1974) A new subspecies of Drosophila pseudoobscura. Pan-Pacific Entomol 50:211–219
Blomquist GJ, Toolson EC, Nelson DR (1985) Epicuticular hydrocarbons of Drosophila pseudoobscura. Insect Biochem 15:25–34
Brown RGB (1965) Courtship behavior in the Drosophila obscura group. Part II. Comparative studies. Behaviour 25:281–323
Carson HL (1971) Speciation and the founder principle. Stadler Genet Symp 3:51–70
Carson HL (1975) The genetics of speciation at the diploid level. Am Nat 109:83–92
Carson HL (1987) Sexual selection: a driver of genetic change in Hawaiian Drosophila. J Hered 88:343–352
Carson HL (2003) Mate choice theory and the mode of selection in sexual populations. Proc Natl Acad Sci U S A 100:6584–6587
Carvajal-Rodriguez A, Rolán-Alvarez E (2006) JMATING: a software for the analysis of sexual selection and sexual isolation effects from mating frequency data. BMC Evol Biol 6:40
Casares P, Carracedo MC, Rio B, Pineiro R, Garcia-Florez L, Barros AR (1998) Disentangling the effects of mating propensity and mating choice in Drosophila. Evolution 52:126–133
Casares P, Piñeiro R, Carracedo MC (2005) Is premating isolation in Drosophila overestimated due to uncontrolled factors? J Genetics 84:259–264
Chang AS, Noor MA (2007) The genetics of hybrid male sterility between the allopatric species pair Drosophila persimilis and D. pseudoobscura bogotana: dominant sterility alleles in collinear autosomal regions. Genetics 176:343–349
Civetta A, Cantor EJF (2003) The genetics of mating recognition between Drosophila simulans and D. sechellia. Genet Res 82:117–126
Civetta A, Waldrip-Dail HM, Clark AG (2002) An introgression approach to mapping differences in mating success and sperm competitive ability in Drosophila simulans and D. sechellia. Genet Res 79:65–74
Coyne JA (1989) Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. Proc Natl Acd Sci U S A 86:5464–5468
Coyne JA (1993) The genetics of an isolating mechanism between two sibling species of Drosophila. Evolution 47:778–788
Coyne JA, Orr HA (1997) “Patterns of speciation in Drosophila” revisited. Evolution 51:295–303
Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland
Coyne JA, Kim YS, Chang AS, Lachaise D, Elwyn S (2002) Sexual isolation between two species with overlapping ranges: Drosophila santomea and Drosophila yakuba. Evolution 56:2424–2434
Dobzhansky Th (1934) Studies on hybrid sterility. I. Spermatogenesis in pure and hybrid Drosophila pseudoobscura. Z Zellforsch Mikrosk Anat 21:169–223
Dobzhansky Th (1937) Genetics and the origin of species. Columbia University Press, New York
Dobzhansky Th (1940) Speciation as a stage in evolutionary divergence. Am Nat 74:312–321
Dobzhansky Th (1973) Is there gene exchange between Drosophila pseudoobscura and D. persimilis in their natural habitats? Am Nat 107:312–314
Dobzhansky Th, Epling C (1944) Contributions to the genetics, taxonomy, and ecology of Drosophila pseudoobscura and its relatives. Carnegie Inst Wash Pub 554:1–183
Dobzhansky Th, Powell J (1975) Drosophila pseudoobscura, and its American relatives, Drosophila persimilis and Drosophila miranda. In: King RC (ed) Handbook of genetics, 3rd edn. Academic Press, New York, pp 537–587
Doi M, Matsuda M, Tomaru M, Matsubayashi H, Oguma Y (2001) A locus for female discrimination behavior causing sexual isolation in Drosophila. Proc Natl Acad Sci U S A 98:6714–6719
Ehrman L (1961) The genetics of sexual isolation in Drosophila paulistorum. Genetics 46:1025–1038
Elens AA, Wattiaux JM (1964) Direct observation of sexual isolation. Dros Inf Serv 39:118–119
Etges WJ, De Oliveira CC, Gragg E, Oritz-Barrientos D, Norr MAF, Ritchie MG (2007) Genetics of incipient speciation in Drosophila mojavensis. I. Male courtship song, mating success, and genotype × environment interactions. Evolution 61:1106–1119
Etges WJ, De Oliveira CC, Ritchie MG, Noor MAF (2009) Genetics of incipient speciation in Drosophila mojavensis. II. Host plants and mating status influence cuticular hydrocarbon QTL expression and GxE interactions. Evolution 63:1712–1730
Ferveur J-F (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35:279–295
Ferveur J-F, Cobb M, Boukella H, Jallon J-M (1996) Worldwide variation in Drosophila melanogaster sex pheromone: behavioral effects, genetic bases and evolutionary consequences. Genetics 97:73–80
Gilbert DG, Starmer WT (1985) Statistics of sexual isolation. Evolution 39:1380–1383
Gleason JM (2005) Mutations and natural genetic variation in the courtship song of Drosophila. Behav Genet 35:265–277
Gleason JM, Nuzhdin SV, Ritchie MG (2002) Quantitative trait loci affecting a courtship signal in Drosophila melanogaster. Heredity 89:1–6
Gleason JM, Jallon J-M, Rouault J, Ritchie MG (2005) Quantitative trait loci for a difference in cuticular hydrocarbons between Drosophila simulans and D. sechellia associated with sexual isolation. Genetics 171:1789–1798
Gleason JM, James RA, Wicker-Thomas C, Ritchie MG (2009) Identification of quantitative trait loci function through analysis of multiple cuticular hydrocarbons differing between Drosophila simulans and D. sechellia females. Heredity 103:416–424
Greenspan RJ, Ferveur J-F (2000) Courtship in Drosophila. A Rev Genet 34:205–232
Hoikkala A (2005) Inheritance of male sound characteristics in Drosophila species. In: Drosopoulos S, Claridge MF (eds) Insect sounds, communication: physiology, behaviour, ecology, evolution. CRC Taylor & Francis, Boca Raton, pp 167–177
Hunter AS (1960) Drosophilidae of Bogota, Colombia. Dros Inf Serv 34:86
Huttunen S, Aspi J, Hoikkala A, Schlötterer C (2004) QTL analysis of variation in male courtship song characters in Drosophila virilis. Heredity 92:263–269
Kaneshiro KY (1983) Sexual selection and direction of evolution in the biosystematics of Hawaiian Drosophilidae. Ann Rev Entomol 28:161–178
Kaneshiro KY (1989) Dynamics of sexual selection and founder effects in species formation. In: Giddings LV, Kaneshiro KY, Anderson WW (eds) Genetics, speciation and the founder principle. Oxford University Press, New York, pp 279–296
Kim Y-K, Ehrman L (1998) Developmental isolation and subsequent adult behavior of Drosophila paulistorum. IV. Courtship. Behav Genet 28:57–65
Kim Y-K, Phillips D, Chao T, Ehrman L (2004) Developmental isolation and subsequent adult behavior of Drosophila paulistorum. VI. Quantitative variation in cuticular hydrocarbons. Behav Genet 34:385–394
Lewontin RC (1974) The genetic basis of evolutionary change. Columbia University Press, New York
Macdonald SJ, Goldstein DB (1999) A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics 153:1683–1699
Mackay TFC (2001) The genetic architecture of quantitative traits. Annu Rev Genet 35:303–339
Malogolowkin-Cohen Ch, Simmons AS, Levene H (1965) A study of sexual isolation between certain strains of Drosophila paulistorum. Evolution 19:95–103
Markow TA, Toolson EC (1990) Temperature effects on epicuticular hydrocarbons and sexual isolation in Drosophila mojavensis. In: Barker JSF, Starmer WT, MacIntyre RJ (eds) Ecological and evolutionary genetics of Drosophila. Plenum Press, New York, pp 315–331
Mayr E (1963) Animal species and evolution. The Belknap Press of Harvard University Press, Cambridge
Merrell DJ (1950) Measurement of sexual isolation and selective mating. Evolution 4:326–331
Moehring AJ, Li J, Schug MD, Smith SG, deAngelis M, Mackay TFC, Coyne JA (2004) Quantitative trait loci for sexual isolation between Drosophila similans and D.mauritiana. Genetics 167:1265–1274
Noor MAF (1997) Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and D. persimilis. Evolution 51:809–815
Noor MAF, Coyne JA (1996) Genetics of a difference in cuticular hydrocarbons between Drosophila pseudoobscura and D. persimilis. Genet Res Camb 68:117–123
Noor MAF, Willimas MA, Alvarez D, Ruiz-García M (2000) Lack of evolutionary divergence in courthip songs of Drosophila pseudoobscura subspecies. J Insect Behav 13:255–262
Noor MAF, Grams KL, Bertucci LA, Almendarez Y, Reiland J et al (2001) The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. persimilis via backcross hybrid males. Evolution 55:512–521
Orr HA (1987) Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics 116:555–563
Orr HA (1989) Genetics of sterility in hybrids between two subspecies of Drosophila. Evolution 43:180–189
Orr HA, Irwing S (2001) Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics 158:1089–1100
Orr HA, Irwing S (2005) Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169:671–682
Paterson HEH (1978) More evidence against speciation by reinforcement. S African J Sci 74:369–371
Paterson HEH (1985) The recognition concept of species. In: ES Vrba (ed) Species and Speciation. Transvaal Museum Monograph No. 4, Pretoria
Pérez-Figueroa A, Caballero A, Rolán-Alvarez E (2005) Comparing the estimation properties of different statistics for measuring sexual isolation from mating frequencies. Biol J Linn Soc 85:307–318
Phadnis N, Orr HA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323:376–379
Powell JR (1978) The founder-flush speciation theory: an experimental approach. Evolution 32:465–474
Powell JR (1983) Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. Proc Natl Acad Sci USA 80:492–495
Powell JR (1997) Progress and prospects in evolutionary biology: the Drosophila model. Oxford, Oxford University Press
Prakash S (1972) Origin of reproductive isolation in the absence of apparent genetic differentiation in a geographic isolate of Drosophila pseudoobscura. Genetics 72:143–155
Regan JL, Meffert LM, Bryant EH (2003) A direct experimental test of founder-flush effects on the evolutionary potential for assortative mating. J Evol Biol 16:302–312
Ringo J, Wood D, Rockwell R, Dowse H (1985) An experiment testing two hypotheses of speciation. Am Nat 126:642–661
Ritchie MG, Halsey EJ, Gleason JM (1999) Drosophila song as a species-specific mating signal and the behavioural importance of Kyriacou & Hall cycles in D. melanogaster song. Anim Behav 58:649–657
Rolán-Alvarez E, Caballero A (2000) Estimating sexual selection and sexual isolation effects from mating frequencies. Evolution 54:30–36
Schaeffer SW, Miller EL (1991) Nucleotide sequence analysis of Adh genes estimates the time of geographic isolation of the Bogota population of Drosophila pseudoobscura. Proc Natl Acad Sci U S A 88:6097–6101
Shaw KL, Parsons YM (2002) Divergence of mate recognition behavior and its consequences for genetic architectures of speciation. Am Nat 159:S61–S75
Tan CC (1946) Genetics of sexual isolation between Drosophila pseudoobscura and Drosophila persimilis. Genetics 31:558–573
Ting C-T, Takahashi A, Wu C-I (2001) Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci. Proc Natl Acad Sci U S A 98:6709–6713
Toolson EC, Kuper-Simbrón R (1989) Laboratory evolution of epicuticular hydrocarbon composition and cuticular permeability in Drosophila pseudoobscura: effects on sexual dimorphism and thermal-acclimation ability. Evolution 43:468–473
Wang RL, Wakely J, Hey J (1997) Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics 147:1091–1106
Williams MA, Blouin AG, Noor MAF (2001) Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences. Heredity 86:68–77
Wu C-I, Hollocher H, Begun DJ, Aquadro CF, Xu Y (1995) Sexual isolation in Drosophila: a possible case of incipient speciation. Proc Natl Acad Sci U S A 92:2519–2523
Zouros E (1981) The chromosomal basis of sexual isolation in two sibling species of Drosophila. Genetics 97:703–778
Acknowledgments
We are grateful to Ms. Kyungsun Kim for her technical assistance with the experiments, to Lee Ehrman, Jean-Marc Jallon and Yun Tao for discussions, to Therese Markow for providing old Bogota strains, and to three anonymous reviewers whose comments improved the earlier version of the manuscript. This project was supported by NIH Grant 5R01 GM048528-06 (to WWA) and UGA Faculty Grant 10-21-RR-064-069 (to Y.-K.K).
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We dedicate this paper to Professor Francisco J. Ayala who was a mentor and longterm colleague.
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Kim, YK., Ruiz-García, M., Alvarez, D. et al. Sexual isolation between North American and Bogota strains of Drosophila pseudoobscura . Behav Genet 42, 472–482 (2012). https://doi.org/10.1007/s10519-011-9517-7
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DOI: https://doi.org/10.1007/s10519-011-9517-7