Abstract
Drosophila ananassae and Drosophila pallidosa are closely related species that can produce viable and fertile hybrids of both sexes, although strong sexual isolation exists between the two species. Females are thought to discriminate conspecific from heterospecific males based on their courtship songs. The genetic basis of female discrimination behavior was analyzed using isogenic females from interspecific mosaic genome lines that carry homozygous recombinant chromosomes. Multiple regression analysis indicated a highly significant effect of the left arm of chromosome 2 (2L) on the willingness of females to mate with D. ananassae males. Not only 2L but also the left arm of chromosome X (XL) and the right arm of chromosome 3 (3R) had significant effects on the females’ willingness to mate with D. pallidosa males. All regions with strong effects on mate choice have chromosome arrangements characterized by species-specific inversions. Heterospecific combinations of 2L and 3R have previously been suggested to cause postzygotic reproductive isolation. Thus, genes involved in premating as well as postmating isolation are located in or near chromosomal inversions. This conclusion is consistent with the recently proposed hypothesis that "speciation genes" accumulate at a higher rate in non-recombining genome regions when species divergence occurs in the presence of gene flow.
Similar content being viewed by others
References
Barbash DA, Siino DF, Tarone AM, Roote J (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100:5302–5307
Bock IR, Wheeler MR (1972) The Drosophila melanogaster species group. Univ Texas Publ 7213:1–102
Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314:1292–1295
Brown KM, Burk LM, Henagan LM, Noor MAF (2004) A test of the chromosomal rearrangement model of speciation in Drosophila pseudoobscura. Evolution 58:1856–1860
Butlin RK (2005) Recombination and speciation. Mol Ecol 14:2621–2635
Civetta A, Cantor EJF (2003) The genetics of mating recognition between Drosophila simulans and D. sechellia. Genet Res 82:117–126
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, MA
Da Lage JL, Kergoat GJ, Maczkowiak F, Silvain JF, Cariou ML, Lachaise D (2007) A phylogeny of Drosophilidae using the Amyrel gene: questioning the Drosophila melanogaster species group boundaries. J Zool Syst Evol Res 45:47–63
Doi M, Nemoto T, Nakanishi H, Kuwahara Y, Oguma Y (1997) Behavioral response of males to major sex pheromone component, (Z,Z)-5, 25-hentriacontadiene, of Drosophila ananassae females. J Chem Ecol 23:2067–2078
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 USA 98:6741–6719
Fang S, Takahashi A, Wu CI (2002) A mutation in the promoter of desaturase 2 is correlated with sexual isolation between Drosophila behavioral races. Genetics 162:781–784
Feder JL, Roethele JB, Filchak K, Niedbalski J, Romero-Severson J (2003) Evidence of inversion polymorphism related to sympatric host race formation in apple maggot fly, Rhagoletis pomonella. Genetics 163:939–953
Futch DG (1966) A study of speciation in South Pacific populations of Drosophila ananassae. Univ Texas Publ 7215:79–120
Futch DG (1972) A preliminary note on parthenogenesis in D. ananassae. Drosophila Inf Serv 48:78
Futch DG (1973) On the ethological differentiation of Drosophila ananassae and Drosophila pallidosa in Samoa. Evolution 27:456–467
Gilbert DG (2007) DroSpeGe: rapid access database for new Drosophila species genomes. Nucl Acids Res 35:D480–D485
Gleason JM, Ritchie MG (2004) Do quantitative trait loci (QTL) for a courtship song difference between Drosophila simulans and D. sechellia coincide with candidate genes and intraspecific QTL? Genetics 166:1303–1311
Lemeunier F, David JR, Tsacas L, Ashburner M (1986) The melanogaster species group. In: Ashburner M, Carson HL, Thompson JN Jr. (eds) The genetics and biology of Drosophila, vol 3E. Academic Press, London, pp 147–256
Masly JP, Jones CD, Noor MAF, Locke J, Orr HA (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313:1448–1450
Matsuda M, Tobari YN (2004) Genetic analyses of several Drosophila ananassae-complex species show a low-frequency major gene for parthenogenesis that maps to chromosome 2. Genet Res 83:83–89
Mavárez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, Linares M (2006) Speciation by hybridization in Heliconius butterflies. Nature 441:868–871
Moehring AJ, Li J, Schug MD, Smith SG, de Angelis M, Mackay TFC, Coyne JA (2004) Quantitative trait loci for sexual isolation between Drosophila simulans and D. mauritiana. Genetics 167:1265–1274
Moehring AJ, Llopart A, Elwyn S, Coyne JA, Mackay TFC (2006) The genetic basis of prezygotic reproductive isolation between Drosophila santomea and D. yakuba due to mating preference. Genetics 173:215–223
Moriwaki D, Tobari YN (1993) Catalog of mutants. In: Tobari YN (ed) Drosophila ananassae: genetical and biological aspects. Japanese Scientific Societies Press/Kargar, Tokyo Basel, pp 209–259
Navarro A, Barton NH (2003) Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447–459
Nemoto T, Doi M, Oshio K, Matsubayashi H, Oguma Y, Suzuki T, Kuwahara Y (1994) (Z,Z)-5, 27-tritriacontadien: major sex pheromone of Drosophila pallidosa (Diptera: Drosophilidae). J Chem Ecol 20:3029–3037
Noor MAF (1997) Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and Drosophila persimilis. Evolution 51:809–815
Noor MAF, Grams KL, Bertucci LA, Reiland J (2001) Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci USA 98:12084–12088
Noor MAF, Feder JL (2006) Speciation genetics: evolving approaches. Nature Rev Genet 7:851–861
Oguma Y (1993) Sexual isolation. In: Tobari YN (ed) Drosophila ananassae: genetical and biological aspects. Japanese Scientific Societies Press/Kargar, Tokyo Basel, pp 199–207
Panithanarak T, Hauffe HC, Dallas JF, Glover A, Ward RG, Searles JB (2004) Linkage-dependent gene flow in a house mouse chromosomal hybrid zone. Evolution 58:184–192
Presgraves DC, Balagopalan L, Abmayr SM, Orr AH (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423:715–719
Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16:351–358
Sawamura K, Tomaru M (2002) Biology of reproductive isolation in Drosophila: toward a better understanding of speciation. Pop Ecol 44:209–219
Sawamura K, Tomimura Y, Sato H, Yamada H, Matsuda M, Oguma Y (2006) Establishing interspecific mosaic genome lines between Drosophila ananassae and Drosophila pallidosa by means of parthenogenesis. Genet Res 88:1–11
Spieth HT (1966) Mating behavior of D. ananassae and ananassae-like flies from the Pacific. Univ Texas Publ 6615:133–145
Stone WS, Wheeler MR, Wilson FD, Gerstenberg VL, Yang H (1966) Genetic studies of natural populations of Drosophila. II. Pacific island populations. Univ Texas Publ 6615:1–36
Stump AD, Fitzpatrick MC, Lobo NF, Traoré S, Sagnon NF, Costantini C, Collins FH, Besansky NJ (2005) Centromere-proximal differentiation and speciation in Anopheles gambiae. Proc Natl Acad Sci USA 102:15930–15935
Ting CT, Tsaur SC, Wu ML, Wu CI (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282:1501–1504
Ting CT, Takahashi A, Wu CI (2001) Incipient speciation by sexual isolation in Drosophila: concurrent evolution at multiple loci. Proc Natl Acad Sci USA 98:6709–6713
Tobari YN (1993) Geographic distribution. In: Tobari YN (ed) Drosophila ananassae: genetical and biological aspects. Japanese Scientific Societies Press/Kargar, Tokyo Basel, pp 19–22
Tomimura Y, Matsuda M, Tobari YN (1993) Polytene chromosome variations of Drosophila ananassae and its relatives. In: Tobari YN (ed) Drosophila ananassae: genetical and biological aspects. Japanese Scientific Societies Press/Kargar, Tokyo Basel, pp 139–151
Wheeler DA, Kyriacou CP, Greenacre ML, Yu Q, Rutila JE, Rosbash M, Hall JC (1991) Molecular transfer of a species-specific behavior from Drosophila simulans to Drosophila melanogaster. Science 251:1082–1085
Williams MA, Blouin AG, Noor MAF (2001) Courtship songs of Drosophila pseudoobscura and D. persimilis. Heredity 86:68–77
Wu CI, Ting CT (2004) Genes and speciation. Nature Rev Genet 5:114–122
Yamada H, Matsuda M, Oguma Y (2002a) Genetics of sexual isolation based on courtship song between two sympatric species: Drosophila ananassae and D. pallidosa. Genetica 116:225–237
Yamada H, Sakai T, Tomaru M, Doi M, Matsuda M, Oguma Y (2002b) Search for species-specific mating signal in courtship songs of sympatric sibling species, Drosophila ananassae and D. pallidosa. Genes Genet Syst 77:97–106
Acknowledgements
We are grateful to Drs Y. N. Tobari, L. Pierce, and A. Kopp for providing us with useful advice and comments. The present research was supported by Grants-in-Aid for Scientific Research on Priority Areas from the Ministry of Education, Culture, Sports, Science and Technology (MEXT). M. M. also thanks National Bio-Resource Project (NBRP) of MEXT for supporting him for Drosophila resources.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sawamura, K., Zhi, H., Setoguchi, K. et al. Genetic analysis of female mating recognition between Drosophila ananassae and Drosophila pallidosa: application of interspecific mosaic genome lines. Genetica 133, 179–185 (2008). https://doi.org/10.1007/s10709-007-9198-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-007-9198-6