Current Science

Open Access Open Access  Restricted Access Subscription Access

Hundred Years of Research on Inversion Polymorphism in Drosophila


Affiliations
1 Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi 221 005, India
 

Paracentric inversions are widespread in the genus Drosophila. Naturally occurring chromosome inversions were detected very early indirectly as far as genetics history is concerned. Sturtevant in 1917 found that in certain strains of D. melanogaster reduced recombination was due to inversions in order of genes in chromosomes, a proposal which was subsequently verified by him in 1926 and 1931 based on the data of genetic mapping. The physical reality of chromosomal inversions was confirmed with the discovery of giant salivary gland chromosomes in Drosophila by Painter in 1933. From which the gene order could be known from the banding pattern. Since the initial work of Sturtevant in 1917 on inversions in Drosophila, hundred years have lapsed and chromosomal polymorphism due to inversions in a large number of species of the genus Drosophila has been extensively studied by using polytene chromosome maps. About one hundred species of Drosophila have been found to be chromosomally polymorphic. Hundred years of research on inversion polymorphism in Drosophila have revealed that inversions in Drosophila are important from view point of population and evolutionary studies. This review briefly summarizes the important findings pertaining to the research of hundred years on inversion polymorphism in different species of Drosophila.

Keywords

Drosophila, Genetic Coadaptation, Inversion Polymorphism, Population Dynamics.
User
Notifications
Font Size

  • White, M. J. D., Animal Cytology and Evolution, Cambridge University Press, Cambridge, UK, 1973.

  • Ayala, F. J. and Coluzzi, M., Chromosome speciation: humans, Drosophila and mosquitoes. Proc. Natl. Acad. Sci. USA, 2005, 102, 6535–6542.

  • White, M. J. D., Modes of Speciation, Freeman Press, San Francisco, 1978.

  • de Vries, H., Die Mutationstheorie, Veit, Leipzig, Germany, 1901.

  • Da Cunha, A. B., Chromosomal variation and adaptation in insects. Annu. Rev. Entomol., 1960, 5, 85–110.

  • Sperlich, D. and Pfriem, P., Chromosomal polymorphism in natural and experimental populations. In The Genetics and Biology of Drosophila (eds Ashburner, M., Carson, H. L. and Thompson Jr, J. M.), Academic Press, New York, USA, 1986, vol. 3e, pp. 257– 309.

  • Singh, B. N., Chromosomal variability in Drosophila. In Perspectives in Entomological Research (ed. Agarwal, O. P.), Scientific Publishers, Jodhpur, 1994, pp. 177–188.

  • Powell, J. R., Progress and Prospects in Evolutionary Biology: The Drosophila Model, Oxford University Press, New York, USA, 1997.

  • Sturtevant, A. H., Genetic factors affecting the strength of linkage in Drosophila. Proc. Natl. Acad. Sci. USA, 1917, 3, 555– 558.

  • Sturtevant, A. H., A crossover reducer in Drosophila melanogaster due to inversion of a section of the third chromosome. Biol. Zentralbl., 1926, 46, 697–702.

  • Sturtevant, A. H., Known and probable inverted sections of the autosomes of Drosophila melanogaster. Carnegie Inst. Washington Publ., 1931, 42, 1–27.

  • Beadle, G. W. and Sturtevant, A. H., X Chromosome inversions and meiosis in Drosophila melanogaste. Proc. Natl. Acad. Sci. USA, 1935, 21, 384–390.

  • Painter, T. S., A new method for the study of chromosome rearrangements and the plotting of chromosome maps. Science, 1933, 78, 585–586.

  • Heitz, E. and Bauer, H., Beweise fur chromosomennatur der kernschleifen in den knauelkernen von Bibio hortulanus. Zeit. Zellf. Mikr. Anat., 1933, 17, 67–83.

  • Patau, K., Chromosomenmorphologie bei Drosophila melanogaster and Drosophila simulans und ihre genetische Bedeutung. Naturwiss, 1935, 23, 537–543.

  • Tan, C. C., Salivary gland chromosomes in two races of Drosophila pseudoobscura. Genetics, 1935, 20, 392–402.

  • Koller, P. C., Structural hybridity in Drosophila pseudoobscura. J. Genet., 1936, 32, 79–102.

  • Carson, H. L., Chromosomal morphism in geographically widespread species of Drosophila. In The Genetics of Colonizing Species (eds Baker, H. G. and Stebins, G. L.), Academic Press, New York, USA, 1965, pp. 503–531.

  • Dobzhansky, Th., Adaptive changes induced by natural selection in wild populations of Drosophila. Evolution, 1947, 1, 1–16.

  • Dobzhansky, Th., Genetics of natural populations. XIX. Origin of heterosis through natural selection in populations of Drosophila pseudoobscura. Genetics, 1950, 35, 288–302.

  • Dobzhansky, Th., Burla, H. and Da Cunha, A. B., Adaptive chromosomal polymorphism in Drosophila willistoni. Evolution, 1950, 4, 212–235.

  • Da Cunha, A. B. and Dobzhansky, Th., A further study of chromosomal polymorphism in Drosophila willistoni in its relation to environment. Evolution, 1954, 8, 119–134.

  • Carson, H. L., The population genetics of Drosophila robusta. Adv. Genet., 1958, 9, 1–40.

  • Levitan, M., Non-random associations of inversions. Cold Spring Harbor Symp. Quant. Biol., 1958, 23, 251–268.

  • Singh, B. N., Chromosome inversions and linkage disequilibrium in Drosophila. Curr. Sci., 2008, 94, 459–464.

  • Tobari, Y. N. (ed.), Drosophila ananassae: Genetical and Biological Aspects, Japan Scientific Societies Press, Karger, Tokyo, Japan, 1993.

  • Singh, B. N., Population and behaviour genetics of Drosophila ananassae, Genetica, 1996, 97, 321–332.

  • Singh, B. N., Genetic polymorphisms in Drosophila. Curr. Sci., 2013, 105, 461–469.

  • Singh, B. N., The Dobzhansky’s concept of genetic coadaptation: Drosophila ananassae is an exception to this concept. J. Genet., 2018, 97, 1039–1046.

  • Sturtevant, A. H. and Dobzhansky, Th., Inversions in the third chromosome of wild races of Drosophila pseudoobscura and their use in the study of the history of the species. Proc. Natl. Acad. Sci. USA, 1936, 22, 448–450.

  • Dubinin, N. P. and Tiniakov, G. G., Structural chromosomal variability in urban and rural populations of Drosophila funebris. Am. Natl., 1946, 80, 393–396.

  • Levitan, M., Chromosome variation in Drosophila robusta. In Drosophila Inversion Polymorphism (eds Krimbas, C. B. and Powell, J. R.), CRC Press, Boca Raton, Florida, USA, 1992, pp. 212–238.

  • Levitan, M. and Etges, W. J., Climate change and recent genetic flux in populations of Drosophila robusta. BMC Evol. Biol., 2005, 5, 4; doi:101186/1471-2148-5-4.

  • Krimbas, C. B. and Loukas, M., The inversion polymorphism in Drosophila subobscura. Evol. Biol., 1980, 12, 163–234.

  • Prevosti, A., Serra, L., Ribo, G., Aguade, M., Sagarra, E., Monclus, M. and Gracia, M. P., The colonization of Drosophila subobscura in Chile. II. Clines in the chromosomal arrangements. Evolution, 1985, 39, 838–844.

  • Krimbas, C. B., The inversion polymorphism of Drosophila subobscura. In Drosophila Inversion Polymorphism (eds Krimbas, C. B. and Powell, J. R.), CRC Press, Boca Raton, Florida, USA, 1992, pp. 127–220.

  • Santos, M., Recombination load in a chromosome inversion polymorphism of Drosophila subobscura. Genetics, 2009, 181, 803–809.

  • Beckenbach, A. T. and Prevosti, A., Colonization of North America by the European species Drosophila subobscura and D. ambigua. Am. Midl. Nat., 1986, 115, 10–18.

  • Ayala, F. J., Serra, L. and Prevosti, A., A grand experiment in evolution: the Drosophila subobscura colonization of the America. Genome, 1989, 31, 246–255.

  • Prevosti, A., Ribo, G., Serra, L., Aguade, M., Balana, J., Monclus, M. and Mestres F, Colonization of America by Drosophila subobscura: experiment in natural populations that supports the adaptive role of chromosomal inversion polymorphism. Proc. Natl. Acad. Sci. USA, 1988, 85, 5597–5600.

  • Mukai, T., Watanabe, T. K. and Yamaguchi, O., The genetic structures of natural populations of Drosophila melanogaster XII. Linkage disequilibrium in a large local population. Genetics, 1974, 77, 771–793.

  • Stalker, H. D., Chromosome studies in wild populations of Drosophila melanogaster. Genetics, 1976, 82, 323–347.

  • Mettler, L. E., Voelker, R. A. and Mukai, T., Inversion clines in populations of Drosophila melanogaster. Genetics, 1977, 87, 169–176.

  • Voelker, R. A., Mukai, T. and Johnson, F. M., Genetic variations in populations of Drosophila melanogaster from the western United States. Genetica, 1977, 47, 143–148.

  • Choi, Y., Chromosomal polymorphism in a Korean natural populations of Drosophila melanogaster. Genetica, 1977, 47, 155–160.

  • Inoue, Y. and Watanabe, T. K., Inversion polymorphism in Japanese natural populations of Drosophila melanogaster. Jpn. J. Genet., 1979, 54, 69–82.

  • Knibb, W. R., Oakeshott, J. G. and Gibson, J. B., Chromosome inversion polymorphism in Drosophila melanogaster. I Latitudinal clines and associations between inversions in Australasian populations. Genetics, 1981, 98, 833–847.

  • Knibb, W. R., Chromosome inversion polymorphism in Drosophila melanogaster. II. Geographic clines and climatic associations in Australasia, North America and Asia. Genetica, 1982, 58, 213–221.

  • Das, A. and Singh, B. N., Chromosomal polymorphism in Indian natural populations of Drosophila melanogaster. Korean J. Genet., 1991, 13, 97–112.

  • Das, A. and Singh, B. N., Genetic differentiation and inversion clines in Indian natural populations of Drosophila melanogaster. Genome, 1991, 34, 618–625.

  • Singh, B. N. and Das, A., Inversion polymorphism in Indian natural populations of Drosophila melanogaster. Genome, 1990, 33, 311–316.

  • Singh, B. N. and Das, A., Further evidence for latitudinal inversion clines in natural populations of Drosophila melanogaster from India. J. Hered., 1992, 83, 227–230.

  • Lemeunier, F. and Aulard, S., Inversion polymorphism in Drosophila melanogaster. In Drosophila Inversion Polymorphism (eds Krimbas, C. B. and Powell, J. R.), CRC Press, Boca Raton, Florida, USA, 1992, pp. 339–406.

  • Aulard, S., David, J. R. and Lemeunier, F., Chromosomal inversion polymorphism in Afrotropical populations of Drosophila melanogaster. Genet. Res., 2002, 79, 49–63.

  • Ashburner, M. and Lemeunier, F., Relationships within the melanogaster species group of the genus Drosophila (Sophophora). I. Inversion polymorphism in Drosophila melanogaster and Drosophila simulans. Proc. R. Soc. London Ser. B, 1976, 193, 137–157.

  • Stalker, H. D., Chromosome studies in wild populations of Drosophila melanogaster. II Relationships of inversion frequencies to latitude, season, wing loading and flight activity. Genetics, 1980, 95, 211–223.

  • Inoue, Y., Watanabe, T. and Watanabe, T. K., Evolutionary change of the chromosomal polymorphism in Drosophila melanogaster populations. Evolution, 1984, 38, 753–765.

  • Singh, B. N., Patterns of inversion polymorphism in three species of the Drosophila melanogaster species group. Indian J. Exp. Biol., 2001, 39, 611–622.

  • Singh, B. N., Drosophila ananassae – a species characterized by several unusual genetic features. Curr. Sci., 2000, 78, 391– 398.

  • Singh, B. N., Drosophila ananassae: a good model species for genetical, behavioural and evolutionary studies. Indian J. Exp. Biol., 2010, 48, 333–345.

  • Singh, B. N., Drosophila ananassae – why it is considered as a unique species in the genus Drosophila. Curr. Sci., 2018, 114, 11–12.

  • Singh, B. N., Drosophila ananassae – a genetically unique species. Nucleus, 1985, 28, 169–176.

  • Ray-Chaudhuri, S. P. and Jha, A. P., Genetics of Indian populations of Drosophila ananassae. Nucleus, 1967, 10, 81–89.

  • Singh, B. N., Distribution of most common inversions of Drosophila ananassae in different parts of India including Andaman and Nicobar Islands. Indian Biol., 1970, 2, 78–81.

  • Singh, B. N., Quantitative variation of chromosomal polymorphism in natural populations of Drosophila ananassae. Cytologia, 1974, 39, 309–314.

  • Singh, B. N., High frequency of cosmopolitan inversions in natural populations of Drosophila ananassae from Kerala, South India. J. Hered., 1984, 75, 504–505.

  • Singh, B. N., Inversion polymorphism in Indian populations of Drosophila ananassae. Hereditas, 1989, 110, 133–138.

  • Singh, B. N., Population genetics of inversion polymorphism in Drosophila ananassae. Indian J. Exp. Biol., 1998, 36, 739–748.

  • Singh, B. N., Chromosomal polymorphism in Drosophila ananassae: similarity between widely distant populations from India. Korean J. Genet., 1991, 13, 27–33.

  • Singh, B. N., Species and genetic diversity in the genus Drosophila inhabiting the Indian subcontinent. J. Genet., 2015, 94, 351–361.

  • Singh, P. and Singh, B. N., Population genetics of Drosophila ananassae: genetic differentiation among Indian natural populations at the level of inversion polymorphism. Genet. Res., 2007, 89, 191–199.

  • Singh, P. and Singh, B. N., Population genetics of Drosophila ananassae. Genet. Res., 2008, 90, 409–419.

  • Singh, B. N. and Yadav, J. P., Status of research on Drosophila ananassae at global level. J. Genet., 2015, 94, 785–792.

  • Singh, B. N., Genetic distance in inversion polymorphism among natural populations of Drosophila ananassae. Genetica, 1984, 64, 211–224.

  • Singh, B. N., Genetic similarity between natural populations of Drosophila ananassae from Kerala and Andaman and Nicobar Islands. Genetica, 1986, 69, 143–147.

  • Singh, B. N. and Anand, S., Genetic divergence at the level of inversion polymorphism in Indian populations of Drosophila ananassae. Evol. Biol., 1995, 8 and 9, 177–190.

  • Singh, P. and Singh, B. N., Population genetics of Drosophila ananassae. Evidence for population sub-structuring at the level of inversion polymorphism in Indian natural populations. Int. J. Biol. (Canada), 2010, 2, 19–28.

  • Reddy, G. S. and Krishnamurthy, N. B., Altitudinal gradients in the frequencies of three common inversions in Drosophila ananassae. Drosoph. Inf. Serv., 1974, 51, 136–137.

  • Singh, B. N., An inversion within the subterminal inversion in Drosophila ananassae. Experientia, 1983, 39, 231–235.

  • Yadav, J. P. and Singh, B. N., Evolutionary genetics of Drosophila ananassae I. Effect of selection on body size and inversion frequencies. J. Zool. Syst. Evol. Res., 2006, 44, 323–329.

  • Bock, I. R., Intra and interspecific chromosomal inversions in the Drosophila bipectinata species complex. Chromosoma, 1971, 34, 206–229.

  • Jha, A. P. and Rahman, S. M. Z., Cytogenetics of natural populations of Drosophila. I. Role of chromosomal inversions in the evolution of the Drosophila bipectinata species complex. Chromosoma, 1972, 37, 445–454.

  • Gupta, J. P. and Panigrahy, K. K., Chromosomal polymorphism in Indian populations of Drosophila bipetinata Duda. Genetica, 1990, 82, 45–49.

  • Singh, B. N. and Das, A., Linkage disequilibrium between inversions in Drosophila bipectinata. Biol. Zentbl., 1991, 110, 157– 162.

  • Das, A. and Singh, B. N., Heterosis associated with chromosome inversions in Drosophila bipectinata. Korean J. Genet., 1992, 14, 173–178.

  • Banerjee, R. and Singh, B. N., Inversion polymorphism in natural populations of Drosophila bipectinata. Cytobios, 1996, 87, 31– 43.

  • Singh, B. N. and Banerjee, R., Increase in the degree of inversion polymorphism in Drosophila bipectinata populations transferred to laboratory conditions. J. Zool. Syst. Evol. Res., 1997, 35, 153– 157.

  • Banerjee, R. and Singh, B. N., Evidence for coadaptation in geographic populations of Drosophila bipectinata. J. Zool. Syst. Evol. Res., 1998, 36, 1–6.

  • Tomimura, Y., Matsuda, M. and Tobari, Y. N., Chromosomal phylogeny and geographical divergence in the Drosophila bipectinata complex. Genome, 2005, 48, 487–502.

  • Singh, B. N. and Sisodia, S., Phylogenetic relationship among four members of the Drosophila bipectinata species complex. J. Sci. Res., BHU, 2008, 52, 81–97.

  • Singh, B. N. and Banerjee, P., Population genetical, behavioural and evolutionary studies in the Drosophila bipectinata species complex. Proc. Indian Natl. Sci. Acad., 2016, 82, 99–115.

  • Banerjee, P. and Singh, B. N., The Drosophila bipectinata species complex: phylogenetic relationship among different members based on chromosomal variations. J. Genet., 2017, 96, 97–107.

  • Singh, G. and Singh, A. K., Excessive occurrence of paracentric inversions in a natural population of Drosophila bipectinata. J. Exp. Zool., India, 2018, 21, 29–33.

  • Ranganath, H. A. and Krishnamurthy, N. B., Chromosomal polymorphism in Drosophila nasuta II. Coexistence of heteroselection and flexibility of polymorphic system of South Indian populations. Genetica, 1975, 48, 215–221.

  • Rajasekarasetty, M. R., Ramesh, S. R. and Krishnamurthy, N. B., Inversions in natural populations of Drosophila nasuta. Nucleus, 1979, 22, 92–95.

  • Kumar, A. and Gupta, J. P., Linkage disequilibrium, natural selection and epistatic gene interaction in Drosophila nasuta. Genome, 1988, 30, 495–498.

  • Carson, H. L., Chromosomal morphism in geographically widespread species of Drosophila. In The Genetics of Colonizing Species (eds Baker, H. G. and Stebbins, G. L.), Academic Press, London, UK, 1965, pp. 503–531.

  • Brncic, D., Studies on the evolutionary biology of Chilean species of Drosophila. In Essays in Evolution and Genetics in Honour of Theodosius Dobzhansky (eds Hecht and Steere, W. C), Appleton–Century–Crofts, New York, 1970, pp. 401–436.

  • Brncic, D., Further studies on chromosomal polymorphism in Drosophila pavani. J. Hered., 1973, 64, 175–180.

  • Mather, W. B., Temporal variation in Drosophila rubida inversion polymorphism. Heredity, 1964, 19, 231–234.

  • Brncic, D., Seasonal fluctuations of inversion polymorphism in Drosophila flavopilosa and relationships with certain ecological factors. Univ. Texas Publ., 1972, 7213, 103–116.

  • Borisov, A. I., Adaptive value of chromosomal polymorphism. IV. The prolonged observation on a population of Drosophila funebris in Moscow town. Genetika (Moscow), 1970, 6, 115–122.

  • Levene, H. and Dobzhansky, Th., New evidence of heterosis in naturally occurring inversion heterozygotes in Drosophila pseudoobscura. Heredity, 1958, 12, 37–49.

  • Brncic, D., Integration of the genotypes in geographic populations of Drosophila pavani. Evolution, 1961, 15, 92–97.

  • Dobzhansky, Th., Genetics and the Origin of Species, Third Edition, Columbia University Press, New York, USA, 1951.

  • Spiess, E. B., Experimental populations of Drosophila persimilis from an altitudinal transect of the Sierra Nevada. Evolution, 1950, 4, 14–33.

  • Levitan, M., Experiments on chromosomal variability in Drosophila robusta. Genetics, 1951, 36, 285–305.

  • Dobzhansky, Th. and Pavlovasky, O., An experimental study of interaction between genetic drift and natural selection. Evolution, 1957, 11, 311–319.

  • Tobari, Y. N., Heterosis relating to a terminal inversion in artificial population of Drosophila ananassae. Jpn. J. Genet., 1962, 37, 302–309.

  • Singh, B. N. and Ray-Chaudhuri, S. P., Balanced chromosomal polymorphism in experimental populations of Drosophila ananassae. Indian J. Exp. Biol., 1972, 10, 301–303.

  • Singh, B. N., Persistence of chromosomal polymorphism in various strains of Drosophila ananassae. Genetica, 1982, 59, 151– 156.

  • Singh, B. N., Evidence for random genetic drift in laboratory populations of Drosophila ananassae. Indian J. Exp. Biol., 1988, 26, 85–87.

  • Singh, B. N., On the degree of genetic divergence in Drosophila ananassae populations transferred to laboratory conditions. Zeit. Zool. Syst. Evol., 1987, 25, 180–187.

  • Das, A. and Singh, B. N., Chromosome inversions in Indian Drosophila melanogaster. Genetica, 1990, 81, 85–88.

  • Singh, B. N. and Das, A., Changes of inversion polymorphism in laboratory populations of Drosophila melanogastaer. Zeit. Zool. Syst. Evol., 1992, 30, 268–280.

  • Singh, B. N. and Banerjee, R., Increase in the degree of inversion polymorphism in Drosophila bipectinata populations transferred to laboratory conditions. J. Zool. Syst. Evol. Res., 1997, 35, 153– 157.

  • Dobzhansky, Th., Observations and experiments on natural selection in Drosophila (Suppl. Vol.). Hereditas, 1949, pp. 210–224.

  • Dobzhansky, Th., Genetics of natural populations XIX. Origin of heterosis through selection in populations of Drosophila pseudoobscura. Genetics, 1950, 35, 288–302.

  • Dobzhansky, Th., Mendelian populations as genetic systems. Cold Spring Harbor Symp. Quant. Biol., 1957, 22, 385–393.

  • Darlington, C. D. and Mather, K., The Elements of Genetics, Allen and Unwin, London, UK, 1949.

  • Wright, S., Biology and philosophy of science. Monist, 1964, 48, 265–290.

  • Singh, B. N., The Dobzhansky’s concept of genetic coadaptation: Drosophila ananassae is an exception to this concept. J. Genet., 2018, 97, 1039–1046.

  • Singh, B. N., Darwin of the 20th century-Mayr or Dobzhansky? Curr. Sci., 2012, 103, 125.

  • Dobzhansky, Th. and Pavlovasky, O., Interracial hybridization and breakdown of coadapted gene complexes in Drosophila paulistorum and D. willistoni. Proc. Natl. Acad. Sci. USA, 1958, 44, 622–629.

  • Singh, B. N. and Banerjee, R., Chromosomal variability and interracial hybridization in Drosophila bipectinata. Cytobios, 1995, 82, 219–227.

  • Kumar, A. and Gupta, J. P., Heterosis and the lack of coadaptation in Drosophila nasuta. Heredity, 1991, 67, 275–279.

  • Singh, B. N., The lack of evidence for coadaptation in geographic populations of Drosophila ananassae. Genetica, 1972, 43, 582– 588.

  • Singh, B. N., Persistence of heterosis in crosses between geographic races of Drosophila ananassae. Indian J. Exp. Biol., 1974, 12, 376–377.

  • Singh, B. N., Interracial hybridization in Drosophila ananassae. Genetica, 1981, 57, 139–142.

  • Singh, B. N., Heterosis without selectional coadaptation in Drosophila ananassae. Theor. Appl. Genet., 1985, 69, 437–441.

  • Carson, H. L., Heterosis and fitness in experimental populations of Drosophila melanogaster. Evolution, 1961, 15, 496–509.

  • Schaeffer, S. W. et al., Evolutionary genomics of inversions in Drosophila pseudoobscura: evidence for epistasis. Proc. Natl. Acad. Sci. USA, 2003, 100, 8319–8324.

  • Hoffmann, A. A., Sagro, C. M. and Weeks, A. R., Chromosomal inversion polymorphism and adaptation. Tends Ecol. Evol., 2004, 19, 422–488.

  • Barker, J. S. F., Inter-locus interaction: a review of experimental evidence. Theor. Popul. Biol., 1979, 16, 323–346.

  • Singh, B. N., Genetic coadaptation in Drosophila. Indian Rev. Life Sci., 1991, 11, 205–231.

  • Zivanovic, G., Andjelkovic, M. and Marinkovic, D., Genetic load and coadaptation of chromosomal inversions. II. O chromosomes in Drosophila subobscura populations. Hereditas, 2000, 133, 105–113.

  • Kennington, W. J., Partridge, L. and Hoffmann, A. A., Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion in (3R) Payne in Drosophila melanogaster are indicative of coadaptation. Genetics, 2006, 172, 1655–1663.

  • Fuller, Z. L., Haynes, G. D., Richards, S. and Schaffer, S. W., Genomics of natural populations: how differentially expressed genes shape the evolution of chromosomal inversions in Drosophila pseudoobscura. Genetics, 2016, 204, 287–301.

  • Chang, C. and Chang, H., Genetic analysis of parthenogenetic capability and fecundity in Drosophila albomicans. Zool. Stud., 2014, 53, 1–8.

  • Bridges, C. B. and Brehme, K. F., The mutants of Drosophila melanogaster. Carnegie Inst. Washington Publ., 1944, 552.

  • Lindsley, D. L. and Grell, E. H., Genetic Variations of Drosophila melanogaster. Carnegie Inst. Washington Publ., 1968, p. 627.

  • Dobzhansky, Th. and Epling, C., The suppression of crossingover in inversion heterozygotes of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 1948, 34, 137–141.

  • Sturtevant, A. H. and Beadle, G. W., The relations of inversions in the X-chromosome of Drosophila melanogaster to crossingover and disjunction. Genetics, 1936, 21, 554–604.

  • Dobzhansky, Th. and Sturtevant, A. H., Translocations between the second and third chromosomes of Drosophila and their beraing on Oenothera problems. Carnegie Inst. Washington Publ., 1931, 421, 29–59.

  • Dobzhansky, Th., Studies on chromosome conjugation II. The relation between crossing over and disjunction of chromosomes. Z. Indukt. Abstramm. Vererbungsl., 1933, 64, 269–309.

  • Grell, R. F., A new model for secondary non-disjunction: the role of distributive pairing. Genetics, 1962, 47, 1737–1754.

  • Komai, T. and Takau, T., Two independent inversions in the X-chromosome of Drosophila virilis and their effects on crossing over and disjunction. Cytologia, 1940, 11, 245–260.

  • Komai, T. and Takau, T., On the effect of the X-chromosome inversions on crossing over in Drosophila virilis. Cytologia, 1942, 12, 357–365.

  • Schultz, J. and Redfield, H., Interchromosomal effect on crossingover in Drosophila. Cold Spring Harbor Symp. Quant. Biol., 1951, 16, 175–197.

  • Ramel, C., Interchromosomal effects of inversions in Drosophila melanogaster. I. Crossing over. Hereditas, 1962, 48, 1–58.

  • Luccchesi, J. C., Interchromosomal effects. In The Genetics and Biology of Drosophila (eds Ashburner, M. and Novitski, E.), Academic Press, New York, USA, 197, vol. 1a, pp. 315–329.

  • Da Cunha, A. B., Chromosomal polymorphism in the Diptera. Adv. Genet., 1955, 7, 93–138.

  • Singh, B. N. and Singh, A. K., The effects of heterozygous inversions on crossing over in Drosophila ananassae. Genome, 1987, 29, 802–805.

  • Singh, B. N. and Mohanty, S., Intra- and interchromosomal effects of heterozygous inversions on crossing-over in the third chromosome of Drosophila ananassae. Indian J. Exp. Biol., 1991, 29, 23–27.

  • Singh, A. K. and Singh, B. N., Heterozygous inversions and spontaneous male crossing-over in Drosophila ananassae. Genome, 1988, 30, 445–450.

  • Franca, Z. M., Da Cunha, A. B. and Garrido, M. C., Recombination in Drosophila willistoni. Heredity, 1968, 23, 199–204.

  • Sperlich, D. and Freuerbach-Mravlag, H., Epistatic gene interaction, crossing over and linked and unlinked inversions in Drosophila subobscura. Evolution, 1974, 28, 67–75.

  • Singh, B. N., Recombination between heterozygous inversions in Drosophila ananassae. Genetica, 1973, 44, 602–607.

  • Singh, B. N. and Singh, A. K., Crossing-over between linked inversions in Drosophila ananassae. Hereditas, 1988, 109, 15–19.

  • Singh, B. N. and Mohanty, S., Lack of correlation between crossingover and chromosome distance between inversions in Drosophila ananassae. Genome, 1990, 33, 592–595.

  • Levitan, M., Position effects in natural populations. Am. Nat., 1954, 88, 419–423.

  • Hedrick, P. W., Genes in Populations, Jones and Bartlett, Sudbury, MA, USA, 2005, 3rd edn.

  • Singh, B. N. and Singh, A. K., Linkage disequilibrium in laboratory strains of Drosophila ananassae is due to drift. Hereditas, 1990, 112, 203–208.

  • Spiess, E. B. and Langer, B., Chromosomal adaptive polymorphism in Drosophila persimilis. III. Mating propensity of homokaryotypes. Evolution, 1961, 15, 535–544.

  • Spiess, E. B. and Langer, B., Mating speed control by gene arrangements in Drosophila pseudoobscura homokaryotypes. Proc. Natl. Acad. Sci. USA, 1964, 51, 1015–1019.

  • Brncic, D. and Koref-Santibanez, S., Mating activity of homoand hetetrokaryotypes in Drosophila pavani. Genetics, 1964, 49, 585–591.

  • Kaul, D. and Parsons, P. A., The genotypic control of mating speed and duration of copulation in Drosophila pseudoobscura. Heredity, 1965, 20, 381–392.

  • Sperlich, D., Unterschiediche Paarungsaktivitat innerhalb und zwischen verschiedensen geographischen stamen von Drosophila subobscura. Z. Verebungsl., 1966, 98, 10–15.

  • Ehrman, L., Mating success and genotype frequency in Drosophila. Anim. Behav., 1966, 14, 332–339.

  • Ehrman, L., The mating advantage of rare males in Drosophila. Proc. Natl. Acad. Sci. USA, 1970, 65, 345–348.

  • Prakash, S., Chromosome interactions affecting mating speed in Drosophila robusta. Genetics, 1968, 60, 589–600.

  • Som, A. and Singh, B. N., Rare male mating advantage for inversion karyotype in Drosophila ananassae. Behav. Genet., 2004, 34, 335–342.

  • Singh, B. N. and Chatterjee, S., Mating ability of homo- and heterokaryotypes of Drosophila ananassae from natural populations. Heredity, 1986, 57, 75–78.

  • Singh, B. N. and Chatterjee, S., Parallelism between male mating propensity and Chromosome arrangement frequency in natural populations of Drosophila ananassae. Heredity, 1988, 60, 269– 272.

  • Dobzhansky, Th. and Sokolov, D., Structure and variation of the chromosome in Drosophila azteca. J. Hered., 1939, 30, 3–19.

  • Kastritsis, C. D. and Crumpacker, D. W., Gene arrangements in the third chromosome of Drosophila pseudoobscura. J. Hered., 1967, 58, 113–129.

  • Kaneshiro, K. Y., RCL Perkins’ legacy to evolutionary research on Hawaiian Drosophilidae (Diptera). Pac. Sci., 1997, 51, 450– 461.

  • Cason, H. L., Chromosomal races of Drosophila crucigera from the islands of Oahu and Kauai, State of Hawaii. Univ. Texas Publ., 1966, 6615, 405–412.

  • Carson, H. L., Ancient chromosomal polymoprphism in Hawaiian Drosophila. Nature, 1973, 241, 200–202.

  • Carson, H. L., Patterns of speciation in Hawaiian Drosophila inferred from ancient chromosomal polymorphism. In Genetic Mechanisms of Speciation in Insects (ed. White, M. J. D.), Australia and New Zealand Book, Sydney, Australia, 1987, pp. 81–93.

  • Carson, H. L., Chromosomal tracing of evolution in a phylad of species related to Drosophila hawaiiensis. In Evolution and Speciation (eds Atchley, W. R. and Woodruff, D.), Cambridge University Press, New York, USA, 1981.

  • Carson, H. L., Tracing ancestry with chromosomal sequences. Trends Ecol. Evol., 1987, 2, 203–207.

  • Carson, H. L., Inversions in Hawaiian Drosophila. In Drosophila Inversion Polymorphism (eds Krimbas, C. B. and Powell, J. R.), CRC Press, Boca Raton, Florida, USA, 1992, pp. 407–439.

  • Carson, H. L., Clayton, F. E. and Stalker, H. D., Karyotypic stability and speciation in Hawaiian Drosophila. Proc. Natl. Acad. Sci. USA, 1967, 57, 1280–1285.

  • Carson, H. L. and Stalker, H. D., Polytene chromosome relationships in Hawaiian species of Drosophila. Univ. Texas Publ., 1968, 6818, 335–354.

  • Kaneshiro, K. Y., Carson, H. L., Clayton, F. E. and Heed, W. B., Niche in a pair of homosequential Drosophila species from the island of Hawaii. Am. Nat., 1973, 107, 766–774.

  • Cradock, E. M. and Johnson, W. E., Chromosomal and allozymic diversity in Drosophila silvestris and its homosequential species. Evolution, 1979, 33, 137.

  • DeSalle, R., Giddings, L. V. and Kaneshiro, K. Y., Mitochondrial DNA variability in Natural populations of Hawaiian Drosophila. II. Genetic and phylogenetic relationships of natural populations of D. silvestris and D. heteroneura. Heredity, 1986, 56, 87–96.

  • Ahearn, J. N. and Baimai, V., Cytogenetic study of three closely related species of Hawaiian Drosophila. Genome, 1987, 29, 47.

  • Cradock, E. M. and Carson, H. L., Chromosomal inversion patterning and population differentiation in a young insular species, Drosophila silvestris. Proc. Natl. Acad. Sci. USA, 1989, 86, 4798.

  • O’Grady, P. and DeSalle, R., Hawaiian Drosophila as an evolutionary model clade: days of future past. BioEssays, 2018; doi:10.1002/bies. 201700246, 1–11.

  • O’Grady, P. and DeSalle, R., Phylogeny of the genus Drosophila. Genetics, 2018, 209, 1–25.

  • Kaneshiro, K. Y., Ethological isolation and phylogeny in the planitibia subgroup of Hawaiian Drosophila. Evolution, 1976, 30, 740–745.

  • O’Grady, P. M. et al., Phylogenetic and ecological relationships of the Hawaiian Drosophila inferred by mitochondrial DNA analysis. Mol. Phylogenet. Evol., 2011, 58, 244–256.

  • Lewontin, R. C. and Hubby, J. L., A molecular approach to the study of genic heterozygosity in natural populations II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics, 1966, 54, 595–609.

  • Cross, S. R. H. and Birley, A. J., Restriction endonuclease map variation in the Adh region in populations of Drosophila melanogaster. Biochem. Genet., 1986, 24, 415–433.

  • Kumar, S. and Singh, A. K., Allozyme polymorphism in Drosophila. Proc. Zool. Soc. Kolkata, 2016, 69, 22–31.

  • Kreitman, M., Nucleotide polymorphism at the alcohol dehydogenase locus of Drosophila melanogaster. Nature, 1983, 304, 412–417.

  • Stephan, W. and Langley, C. F., Molecular genetic variation in the centromeric region of the X-chromosome in three Drosophila ananassae populations. I. Contrasts between the vermilion and forked loci. Genetics, 1989, 121, 88–99.

  • Hale, L. R. and Singh, R. S., Contrasting patterns of genetic structure and evolutionary history as revealed by mitochondrial DNA and nuclear gene–enzyme variation between Drosophila melanogaster and D. simulans. J. Genet., 1991, 70, 79–90.

  • Hartl, D. L. and Clark, A. G., Principles of Population Genetics, Sinaaur Associates, Massachusetts, USA, 2007.

  • Lakovara, S. and Saura, A., Genic variation in marginal popuilations of Drosophila subobscura. Hereditas, 1971, 69, 77–82.

  • Prakash, S. and Lewontin, R. C., A moleculkar approact to the study of genic heterozygosity in natural populations. V. Further direct evidence of coadaptation in inversions of Drosophila. Genetics, 1971, 69, 405–408.

  • Loukas, M. and Krimbas, C. B., The genetics of Drosophila subobscura populations. V. A study of linkage disequilibrium in natural populations between genes and inversions of the E chromosome. Genetics, 1975, 80, 331–347.

  • Norman, R. A. and Prakash, S., Developmental variation in amylase allozyme activity associated with chromosome inversions. Genetics, 1980, 95, 1001–1011.

  • Pinsker, W. and Sperlich, D., Geographic pattern of allozyme and inversion polymorphism on chromosome O of Drosophila subobscur and its evolutionary origin. Genetics, 1981, 57, 51–64.

  • Fontdevila, A., Zapata, C., Alvarez, G., Sanchez, L., Mendez, J. and Enriquez, I., Genetic coadaptation in the chromosomal polymorphism of Drosophila subobscura. I. Seasonal changes of genetic disequilibrium in natural populations. Genetics, 1983, 105, 935–955.

  • Cabrera, V. M., Gonzalez, A. M., Laruga, J. M. and Vega, C., Linkage disequilibrium in chromosome A of Drosophila subobscura. Genetica, 1983, 61, 3–8.

  • Barker, J. S. F., East, P. D. and Weir, B. S., Temporal and microgeographic variation in allozyme frequencies in natural populations of Drosophila buzzatii. Genetics, 1986, 112, 577–611.

  • Zapata, C., Alvarez, G., Dosdil, M. and Fontdevila, A., Genetic coadaptation in the chromosomal polymorphism of Drosophila subobscura. II. Changes of gametic disequilibrium in experimental populations. Genetica, 1986, 71, 149–160.

  • Rodriguez, C., Piccinali, R., Levy, E. and Hasson, E., Gametic association between inversion and allozyme polymorphism in Drosophila buzzatii. J. Hered., 2001, 92, 382–391.

  • Rodriguez-Trelles, F., Seasonal cycles of allozyme-by-chromosomalinversion gametic disequilibrium in Drosophila subobscura. Evolution, 2003, 57, 839–848.

  • McGaugh, S. E. and Noor, M. A. F., Genomic impacts of chromosomal inversions in parapatric Drosophila species. Philos. Trans. R. Soc. London, Ser. B, 2012, 367, 422–429.

  • Levington, E. and Kern, A. D., The effect of common inversion polymorphisms In (2L)t and In(3R) Mo on patterns of transcriptional variation in Drosophila melanogaster. G3 Genes/Genomes/ Genetics, 2017, 7, 3659–3668.

  • Hoffmann, A. A. and Rieseberg, L. H., Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation. Annu. Rev. Ecol. Evol. Syst., 2008, 39, 21–42.

  • Kennington, W. J. and Hoffmann, A. A., Patterns of genetic variation across inversions geographic variation in the In(2L)t inversion in populations of Drosophila melanogaster from eastern Australia. BMC Evol. Biol., 2013, 13, 100; doi:10.1186/14712148-13-100.

  • Kapun, M., Schalkwyk, H. V., Mcallister, B., Flatt, T. and Schlotterer, C., Inference of chromosomal inversion dynamics from Pool-seq data in natural and laboratory populations of Drosophila melanogaster. Mol. Ecol., 2014, 23, 1813–1827.

  • Kapun, M., Fabian, D. K., Goudet, J. and Flatt, T., Genomic evidence for adaptive inversion clines in Drosophila melanogaster. Mol. Biol. Evol., 2016, 31, 1317–1336.

  • Corbett-Detig, R. B. and Hartl, D. L., Population genomics of inversion polymorphis in Drosophila melanogaster. PLOS Genetics, 2012, 8, 12-e1003056.

  • Navarro, A., Barbadilla, A. and Ruiz, A., Effect of inversion polymorphism on the neutral nucleotide variability of linked chromosomal regions in Drosophila. Genetics, 2000, 155, 685– 698.

  • Wallace, A. G., Detweiler, D. and Schaeffer, S. W., Evolutionary history of the third chromosome gene arrangements of Drosophila pseudoobscura inferred from inversion breakpoints. Mol. Biol. Evol., 2011, 28, 2219–2229.

  • Gomez, G. A. and Hasson, E., Transpecific polymorphisms in an inversion linked esterase locus in Drosophila buzzatii. Mol. Biol. Evol., 2003, 20, 410–423.

  • Laayouni, H., Hasson, E., Santos, M. and Fontdevila, A., The evolutionary history of Drosophila buzzatii. XXXV. Inversion polymorphism and nucleotide variability in different regions of the second chromosome. Mol. Biol. Evol., 2003, 20, 931–944.

  • Evgen’ev, M. B. et al., Mobile elements and chromosomal evolution in the virilis group of Drosophila. Proc. Natl. Acad. Sci. USA, 2000, 97, 11337–11342.

  • Schlotterer, C., Kofler, R., Versace, E., Tobler, R. and Franssen, S. U., Combining experimental evolution with next generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity, 2015, 114, 431–440.

  • Barghi, N., Tobler, R., Nolte, V. and Schlotterer, C., Drosophila simulans: a species with improved resolution in evolve and resequence studies. G3 Genes/Genomes/Genetics, 2017, 7, 2337–2343.

  • Charlesworth, B., Inversion polymorphism in a two-locus genetic system. Genet. Res., 1974, 23, 259–280.

  • Charlesworth, B. and Charlesworth, D., Selection of new inversion in multilocus genetic systems. Genet. Res., 1973, 21, 167–183.

  • Puerma, E., Orengo, D. J. and Aguade, M., The origin of chromosomal inversions as a source of segmental duplications in the Sophophora subgenus of Drosophila. Sci. Rep., 2016, 6, 30715-1-8.


Abstract Views: 492

PDF Views: 142




  • Hundred Years of Research on Inversion Polymorphism in Drosophila

Abstract Views: 492  |  PDF Views: 142

Authors

B. N. Singh
Department of Zoology, Institute of Science, Banaras Hindu University, Varanasi 221 005, India

Abstract


Paracentric inversions are widespread in the genus Drosophila. Naturally occurring chromosome inversions were detected very early indirectly as far as genetics history is concerned. Sturtevant in 1917 found that in certain strains of D. melanogaster reduced recombination was due to inversions in order of genes in chromosomes, a proposal which was subsequently verified by him in 1926 and 1931 based on the data of genetic mapping. The physical reality of chromosomal inversions was confirmed with the discovery of giant salivary gland chromosomes in Drosophila by Painter in 1933. From which the gene order could be known from the banding pattern. Since the initial work of Sturtevant in 1917 on inversions in Drosophila, hundred years have lapsed and chromosomal polymorphism due to inversions in a large number of species of the genus Drosophila has been extensively studied by using polytene chromosome maps. About one hundred species of Drosophila have been found to be chromosomally polymorphic. Hundred years of research on inversion polymorphism in Drosophila have revealed that inversions in Drosophila are important from view point of population and evolutionary studies. This review briefly summarizes the important findings pertaining to the research of hundred years on inversion polymorphism in different species of Drosophila.

Keywords


Drosophila, Genetic Coadaptation, Inversion Polymorphism, Population Dynamics.

References





DOI: https://doi.org/10.18520/cs%2Fv117%2Fi5%2F761-775