Abstract
Drosophila prolongata exhibits extreme sexual dimorphism in terms of different morphological, behavioral, and life-history traits. To clarify the biological function of genes underpinning such unique traits, the strains for phiC31 integrase-mediated transgenesis of D. prolongata have been established. This study aimed to make further use of the strains by identifying the chromosomal location of attP landing sites with reference to the D. melanogaster genome in silico. The results showed that some inverted orders of genes may have occurred between D. prolongata and D. melanogaster. Such chromosomal rearrangements might be important evolutionary driving forces for the emergence of unique traits in D. prolongata.
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References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Amino K, Matsuo T (2020) Intra- versus inter-sexual selection on sexually dimorphic traits in Drosophila prolongata. Zool Sci 37:1–7. https://doi.org/10.2108/zs200010
Ayala FJ, Coluzzi M (2005) Chromosome speciation: Humans, Drosophila, and mosquitoes. Proc Natl Acad Sci USA 102:6535–6542. https://doi.org/10.1073/pnas.0501847102
Bellen HJ, Levis RW, Liao G, He Y, Carlson JW et al (2004) The BDGP gene disruption project. Genetics 167:761–781. https://doi.org/10.1534/genetics.104.026427
Bellen HJ, Levis RW, He Y, Carlson JW, Evans-Holm M et al (2011) The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188:731–743. https://doi.org/10.1534/genetics.111.126995
Bischof J, Maeda RK, Hediger M, Karch F, Basler K (2007) An optimized transgenesis system for Drosophila using germ-line-specific ɸC31 integrases. Proc Natl Acad Sci USA 104:3312–3317. https://doi.org/10.1073/pnas.0611511104
del Valle RA, Didiano D, Desplan C (2012) Power tools for gene expression and clonal analysis in Drosophila. Nat Methods 9:47–55. https://doi.org/10.1038/nmeth.1800
Goñi B, Matsuda M, Yamamoto M, Vilela CR, Tobari YN (2012) Crossing over does occur in males of Drosophila ananassae from natural populations. Genome 55:505–511. https://doi.org/10.1139/g2012-037
Groth AC, Fish M, Nusse R, Calos MP (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage ϕC31. Genetics 166:1775–1782. https://doi.org/10.1534/genetics.166.4.1775
Hitoshi Y, Ishikawa Y, Matsuo T (2016a) Intraspecific variation in heat tolerance of Drosophila prolongata (Diptera: Drosophilidae). App Entomol Zool 51:515–520. https://doi.org/10.1007/s13355-016-0425-4
Hitoshi Y, Ishikawa Y, Matsuo T (2016b) Inheritance pattern of female receptivity in Drosophila prolongata. Zool Sci 33:455–460. https://doi.org/10.2108/zs160047
Hoskins R, Evans-Holm M (2004) Inverse PCR and sequencing of P-element, piggyBac, and Minos insertion sites in the Drosophila gene disruption project. http://www.fruitfly.org/about/methods/inverse.pcr.html
Jones WD (2009) The expanding reach of the GAL4/UAS system into the behavioral neurobiology of Drosophila. BMB Rep 42:705–712. https://doi.org/10.5483/bmbrep.2009.42.11.705
Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugenics 12:172–175. https://doi.org/10.1111/j.1469-1809.1943.tb02321.x
Kudo A, Takamori H, Watabe H, Ishikawa Y, Matsuo T (2015) Variation in morphological and behavioral traits among isofemale strains of Drosophila prolongata (Diptera: Drosophilidae). Entomol Sci 18:221–229. https://doi.org/10.1111/ens.12116
Kudo A, Awasaki T, Ishikawa Y, Matsuo T (2017a) piggyBac-and phiC31 integrase-mediated transgenesis in Drosophila prolongata. Genes Genet Syst 92:277–285. https://doi.org/10.1266/ggs.17-00024
Kudo A, Shigenobu S, Kadota K, Nozawa M, Shibata TM, Ishikawa Y, Matsuo T (2017b) Comparative analysis of the brain transcriptome in a hyper-aggressive fruit fly, Drosophila prolongata. Insect Biochem Mol Biol 82:11–20. https://doi.org/10.1016/j.ibmb.2017.01.006
Luecke DM, Kopp A (2019) Sex-specific evolution of relative leg size in Drosophila prolongata results from changes in the intersegmental coordination of tissue growth. Evolution 73:2281–2294. https://doi.org/10.1111/evo.13847
Luo Y, Zhang Y, Farine JP, Ferveur JF, Ramírez S, Kopp A (2019) Evolution of sexually dimorphic pheromone profiles coincides with increased number of male-specific chemosensory organs in Drosophila prolongata. Ecol Evol 9:13608–13618. https://doi.org/10.1002/ece3.5819
Matsuo T (2018) Effect of social condition on behavioral development during early adult phase in Drosophila prolongata. J Ethol 36:15–22. https://doi.org/10.1007/s10164-017-0524-x
McKee BD (2009) Homolog pairing and segregation in Drosophila meiosis. Genome Dyn 5:56–68. https://doi.org/10.1159/000166619
Minekawa K, Miyatake T, Ishikawa Y, Matsuo T (2018) The adaptive role of a species-specific courtship behaviour in coping with remating suppression of mated females. Anim Behav 140:29–37. https://doi.org/10.1016/j.anbehav.2018.04.002
Muller HJ (1940) Bearings of the ‘Drosophila’ work on systematics. pp. 185–268. In: The New Systematics, edited by Huxley J. Clarendon Press, Oxford.
Ranz JM, Casals F, Ruiz A (2001) How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the Genus Drosophila. Genome Res 11:230–239. https://doi.org/10.1101/gr.162901
Schaeffer SW (2018) Muller “elements” in Drosophila: How the search for the genetic basis for speciation led to the birth of comparative genomics. Genetics 210:3–13. https://doi.org/10.1534/genetics.118.301084
Setoguchi S, Takamori H, Aotsuka T, Sese J, Ishikawa Y, Matsuo T (2014) Sexual dimorphism and courtship behavior in Drosophila prolongata. J Ethol 32:91–102. https://doi.org/10.1007/s10164-014-0399-z
Setoguchi S, Kudo A, Takanashi T, Ishikawa Y, Matuso T (2015) Social context-dependent modification of courtship behaviour in Drosophila prolongata. Proc R Soc Lond B 282:1818. https://doi.org/10.1098/rspb.2015.1377
Singh BK, Gupta JP (1977) Two new and two unrecorded species of the genus Drosophila Fallen (Diptera: Drosophilidae) from Shillong, Meghalaya, India. Proc Zool Soc Lond 30:31–38
Singh BK, Gupta JP (1979) Karyological study in some Indian species of Drosophilidae. Caryologia 32:265–278. https://doi.org/10.1080/00087114.1979.10796792
Thibault ST, Singer MA, Miyazaki WY, Milash B, Dompe NA et al (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36:283–287. https://doi.org/10.1038/ng1314
Thorpe HM, Smith MCM (1998) In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc Natl Acad Sci USA 95:5505–5510. https://doi.org/10.1073/pnas.95.10.5505
Toda MJ (1991) Drosophilidae (Diptera) in Myanmar (Burma) VII. The Drosophila melanogaster species-group, excepting the D. montium species-subgroup. Oriental Insects 25:69–94. https://doi.org/10.1080/00305316.1991.10432216
Tsoumani KT, Augustinos AA, Kakani EG, Drosopoulou E, Mavragani-Tsipidou P, Mathiopoulos KD (2011) Isolation, annotation and applications of expressed sequence tags from the olive fly, Bactrocera oleae. Mol Genet Genomics 285:33–45. https://doi.org/10.1007/s00438-010-0583-y
Venken KJT, He Y, Hoskins RA, Bellen HJ (2006) P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314:1747–1751. https://doi.org/10.1126/science.1134426
Acknowledgements
I would like to thank Dr. Takashi Matsuo (University of Tokyo, Japan) for his technical advice; Dr. Tsunaki Asano (Tokyo Metropolitan University, Japan) for observation of flies; technicians Mr. Toshikazu Ide, Mrs. Kana Kashiwagi, Mrs. Yukiko Uchida and Mrs. Tamami Sonobe for fly maintenance; Dr. Wataru Kojima (Yamaguchi University, Japan) and Dr. Yukio Ishikawa (Setsunan University, Japan) for his comments on this manuscript. I also thank two anonymous reviewers for helpful comments on this manuscript.
Funding
This work was supported by a Grant-in-Aid for JSPS fellows (19J00023) to A. K. The author declares no competing interests.
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Kudo, A. Chromosome mapping of attP landing sites in the strains for phiC31 integrase-mediated transgenesis of Drosophila prolongata (Diptera: Drosophilidae). Appl Entomol Zool 56, 91–98 (2021). https://doi.org/10.1007/s13355-020-00715-5
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DOI: https://doi.org/10.1007/s13355-020-00715-5