Abstract
The review is devoted to the history of the formation of scientific interest in the genetic foundations of isolating barriers between species and the current state of the problem of prezygotic isolation mechanisms. The noncontradictory ideas about natural selection acting on traits and inheritance of traits are based on the synthesis of genetics and the Darwinian theory of evolution that took place in the mid-1920s. An experimental approach to studying genetic foundations of evolution using methods of distant and interspecies hybridization, proposed by Chetverikov, was widely introduced into the world practice by his student Theodosius Dobzhansky. As ideas about the role of geographical and ecological isolation in the isolation of populations and possible forms of selection involved in the formation of barriers, i.e., about allopatric and sympatric speciation, changed, ideas about the importance of pre- and postzygotic isolation mechanisms have also changed. From Dobzhansky–Muller incompatibility models (DMI models) and Wright’s “shifting balance theory,” without disputing their significance, interest has spread to polygenic models of genetic control of traits that determine the effectiveness of mating behavior and copulation. To date, the vast majority of experimental work on the genetic basis of isolating mechanisms between related species has been done using Drosophila. The review discusses classical genetic studies on traits causing incompatibility or “failure” in related Drosophila species, and works using modern methods of genetic engineering, genome editing, and genome and transcriptome analysis to identify target genes involved in the formation of isolation between diverging species.
Similar content being viewed by others
REFERENCES
Ala-Honkola, O., Kauranen, H., Tyukmaeva, V., Boetzl, F.A., Hoikkala, A., and Schmitt, T., Diapause affects cuticular hydrocarbon composition and mating behavior of both sexes in Drosophila montana, Insect Sci., 2020, vol. 27, no. 2, pp. 304–316. https://doi.org/10.1111/1744-7917.12639
Andersson, M.B., Sexual Selection, Princeton: Princeton University Press, 1994.
Andrianov, B.V., Gorelova, T.V., Sorokina, S.Yu., and Mitrofanov, V.G., Mitochondrial DNA polymorphism in natural populations of the Drosophila virilis species group, Russ. J. Genet., 2003, vol. 39, no. 6, pp. 630–635.
Astaurov, B.L., Artificial Parthenogenesis in the Silkworm, Moscow: Publishing House of the USSR Academy of Sciences, 1940.
Belkina, E.G., Seleznev, D.G., Sorokina, S.Yu., Kulikov, A.M., and Lazebny, O.E., The effect of chromosomes on courtship behavior in sibling species of the Drosophila virilis group, Insects, 2023, vol. 14, no. 7, p. 609. https://doi.org/10.3390/insects14070609
Boll, W. and Noll, M., The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers, Development, 2002, vol. 129, no. 24, pp. 5667–5681. https://doi.org/10.1242/dev.00157
Brennan, P.L.R. and Orbach, D.N., Copulatory behavior and its relationship to genital morphology, Advances in the Study of Behavior, Elsevier, 2020, Ch. 3, pp. 65–122. https://doi.org/10.1016/bs.asb.2020.01.001
Brennan, P.L.R. and Prum, R.O., Mechanisms and evidence of genital coevolution: the roles of natural selection, mate choice, and sexual conflict, Cold Spring Harbor Perspect. Biol., 2015, vol. 7, no. 7, p. a017749. https://doi.org/10.1101/cshperspect.a017749
Chatterjee, S.S., Uppendahl, L.D., Chowdhury, M.A., Ip, P.-L., and Siegal, M.L., The female-specific Doublesex isoform regulates pleiotropic transcription factors to pattern genital development in Drosophila, Development, 2011, vol. 138, no. 6, pp. 1099–1109. https://doi.org/10.1242/dev.055731
Chetverikov, S.S., On some aspects of the evolutionary process from the point of view of modern genetics, J. Exp. Biol., 1926, vol. 2, no. 1, pp. 3–45, no. 4, 237–240.
Coyne, J.A., Genetic basis of differences in genital morphology among three sibling species of Drosophila, Evolution, 1983, vol. 37, no. 6, pp. 1101–1118. https://doi.org/10.1111/j.1558-5646.1983.tb00225.x
Coyne, J.A. and Orr, H.A., The evolutionary genetics of speciation, Philos. Trans. R. Soc. London, B, 1998, vol. 353, no. 1366, pp. 287–305. https://doi.org/10.1098/rstb.1998.0210
Dobzhansky, T., Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids, Genetics, 1936, vol. 21, no. 2, pp. 113–135. https://doi.org/10.1093/genetics/21.2.113
Dobzhansky, T., Genetic nature of species differences, Am. Nat., 1937a, vol. 71, no. 735, pp. 404–420.
Dobzhansky, T., Genetics and the Origin of Species, New York: Columbia University Press, 1937b.
Dobzhansky, T., Rapid vs. flexible chromosomal polymorphism in Drosophila, Am. Nat., 1960, vol. 96, no. 891, pp. 321–328.
Dobzhansky, T.G., Genetics of the Evolutionary Process, New York: Columbia University Press, 1971.
Dufour, L., Anatomie générale des Dipteres, Annuare de Science Naturelle, 1848, no. 1, pp. 244–264.
Eberhard, W.G., Animal genitalia and female choice, Am. Sci., 1990, vol. 78, pp. 134–141.
Eberhard, W.G., Sexual Selection and Animal Genitalia, Cambridge, Massachusetts, USA: Harvard University Press, 1985.
Evgen’ev, M.B., Genetic regulation of mitosis in interspecific hybrids of Drosophila. I. Maternal effect on chromosome segregation and elimination, Genetika, 1973, vol. 9, pp. 92–99.
Evgeniev, M.B. and Gubenko, I.S., Genetic regulation of the replication pattern of polytene chromosomes in interspecific hybrids of Drosophila, Chromosoma, 1977, vol. 63, no. 1, pp. 89–100. https://doi.org/10.1007/bf00292944
Evgen’ev, M.B. and Sidorova, N.V., Genetic regulation of chromosome behaviour in interspecific hybrids of Drosophila, Theor. Appl. Genet., 1976, vol. 48, no. 2, pp. 55–61. https://doi.org/10.1007/bf00267312
Evgen’ev, M.B., Lakovaara, S., Poluektova, E.V., Saura, A., and Sokolov, N.N., What is Drosophila littoralis Meigen? (Diptera: Drosophilidae), Ent. Scand., 1981, no. 15, pp. 337–340.
Falileeva, L.I. and Mitrofanov, V.G., An electron microscopic study of the structure of the spermatozoa from sterile males from a crossing of Drosophila virilis × Drosophila lummei, Ontogenez, 1997a, vol. 28, pp. 223–231.
Falileeva, L.I. and Mitrofanov, V.G., Genomic incompatibility in Drosophila virilis Sturt. × Drosophila lummei Hackman hybrids, Genetika, 1997b, vol. 33, no. 4, pp. 458–463.
Fisher, R.A., The Genetical Theory of Natural Selection, UK: The Clarendon Press, 1930.
Frazee, S.R. and Masly, J.P., Multiple sexual selection pressures drive the rapid evolution of complex morphology in a male secondary genital structure, Ecol. Evol., 2015, vol. 5, no. 19, pp. 4437–4450. https://doi.org/10.1002/ece3.1721
Frazee, S.R., Harper, A.R., Afkhami, M., Wood, M.L., McCrory, J.C., and Masly, J.P., Interspecific introgression reveals a role of male genital morphology during the evolution of reproductive isolation in Drosophila, Evolution, 2021, vol. 75, no. 5, pp. 989–1002. https://doi.org/10.1111/evo.14169
Ford, E.B., Mendelism and Evolution, Methuen, 1949.
Glassford, W.J., Johnson, W.C., Dall, N.R., Smith, S.J., Liu, Ya., Boll, W., Noll, M., and Rebeiz, M., Co-option of an ancestral hox-regulated network underlies a recently evolved morphological novelty, Dev. Cell, 2015, vol. 34, no. 5, pp. 520–531. https://doi.org/10.1016/j.devcel.2015.08.005
Gornostaev, N.G., Kulikov, A.M., and Mitrofanov, V.G., Morphological diagnosis of males of the species group Drosophila virilis s.l. (Diptera, Drosophilidae), Entomological Review (Rus.), 1998, vol. 77, no. 3, pp. 700–703.
Hackett, J.L., Wang, X., Smith, B.R., and MacDonald, S.J., Mapping QTL contributing to variation in posterior lobe morphology between strains of Drosophila melanogaster, PLoS One, 2016, vol. 11, no. 9, p. e0162573. https://doi.org/10.1371/journal.pone.0162573
Hagen, J.F.D., Mendes, C.C., Blogg, A., Payne, A., Tanaka, K.M., Gaspar, P., Figueras Jimenez, J., and Kittelmann, M., McGregor, A.P., and and Nunes, M.D.S., tartan underlies the evolution of Drosophila male genital morphology, Proc. Natl. Acad. Sci., 2019, vol. 116, pp. 19025–19030.
Hagen, J.F.D., Mendes, C.C., Booth, Sh.R., Figueras Jimenez, J., Tanaka, K.M., Franke, F.A., Baudouin-Gonzalez, L., Ridgway, A.M., Arif, S., Nunes, M.D.S., and McGregor, A.P., Unraveling the genetic basis for the rapid diversification of male genitalia between Drosophila species, Mol. Biol. Evol., 2021, vol. 38, no. 2, pp. 437–448. https://doi.org/10.1093/molbev/msaa232
Haldane, J.B.S., A mathematical theory of natural and artificial selection, part V: selection and mutation, Proc. Camb. Philos. Soc., 1927, no. 28, pp. 838–844.
Haldane, J.B.S., The Causes of Evolution, London: Longmans, Green, 1932.
Henderson, C.R., Estimation of changes in herd environment, J. Dairy Sci., 1949, no. 32, pp. 706–711.
Hosken, D.J. and Stockley, P., Sexual selection and genital evolution, Trends Ecol. Evol., 2004, vol. 19, no. 2, pp. 87–93. https://doi.org/10.1016/j.tree.2003.11.012
House, C.M., Lewis, Z., Hodgson, D.J., Wedell, N., Sharma, M.D., Hunt, J., and Hosken, D.J., Sexual and natural selection both influence male genital evolution, PLoS One, 2013, vol. 8, no. 5, p. e63807. https://doi.org/10.1371/journal.pone.0063807
House, C.M., Lewis, Z., Sharma, M.D., Hodgson, D.J., Hunt, J., Wedell, N., and Hosken, D.J., Sexual selection on the genital lobes of male Drosophila simulans, Evolution, 2021, vol. 75, no. 2, pp. 501–514. https://doi.org/10.1111/evo.14158
Hunt, J., Wolf, J.B., and Moore, A.J., The biology of multivariate evolution, J. Evol. Biol., 2007, vol. 20, no. 1, pp. 24–27. https://doi.org/10.1111/j.1420-9101.2006.01222.x
Hunt, J., Breuker, C.J., Sadowski, J.A., and Moore, A.J., Male-male competition, female mate choice and their interaction: determining total sexual selection, J. Evol. Biol., 2008, vol. 20, pp. 24–27.
Huxley, J.S., Darwin’s theory of natural selection and the data subsumed by it, in the light of recent research, Am. Nat., 1938, vol. 72, pp. 416–433.
Huxley, J.S., Evolution. The Modern Synthesis, London: George Allen, Unwin Ltd., 1942.
Krstic, D., Boll, W., and Noll, M., Sensory integration regulating male courtship behavior in Drosophila, PLoS One, 2009, vol. 4, no. 2, p. e4457. https://doi.org/10.1371/journal.pone.0004457
Kulikov, A.M., Melnikov, A.I., Gornostaev, N.G., and Mitrofanov, V.G., Divergence of Drosophila virilis group species of the according to the phallus shape, Dokl. Acad. Nauk, 2001, vol. 376, no. 6, pp. 841–884.
Kulikov, A.M., Melnikov, A.I., Gornostaev, N.G., Lazebny, O.E., and Mitrofanov, V.G., Morphological analysis of male mating organ in the Drosophila virilis species group: a multivariate approach, J. Zool. Syst. Evol. Res., 2004, vol. 42, no. 2, pp. 135–144. https://doi.org/10.1111/j.1439-0469.2004.00246.x
Kulikov, A.M., Gornostaev, N.G., and Lazebnyĭ, O.E., Interspecies variability of number of bristles on dorsal surface of aedeagus in D. virilis species group and its genetic mapping with interspecies hybrids of D. virilis and D. lummei, Russ. J. Genet., 2013a, vol. 49, no. 2, pp. 158–163. https://doi.org/10.1134/S1022795413020075
Kulikov, A.M., Mel’nikov, A.I., Gornostaev, N.G., and Lazebny, O.E., Dominance status of shape of male genitalia in interspecific crosses of some Drosophila virilis group species, Russ. J. Genet., 2013b, vol. 49, no. 6, pp. 588–601. https://doi.org/10.1134/S1022795413060069
Kulikov, A.M., Sorokina, S.Yu., Melnikov, A.I., Gornostaev, N.G., Seleznev, D.G., and Lazebny, O.E., The effects of the sex chromosomes on the inheritance of species-specific traits of the copulatory organ shape in Drosophila virilis and Drosophila lummei, PLoS One, 2020, vol. 15, no. 12, p. e0244339. https://doi.org/10.1371/journal.pone.0244339
Lande, R. and Arnold, S.J., The measurement of selection on correlated characters, Evolution, 1983, vol. 37, no. 6, pp. 1210–1226. https://doi.org/10.2307/2408842
Laurie, C.C., True, J.R., Liu, J., and Mercer, J.M., An introgression analysis of quantitative trait loci that contribute to a morphological difference between Drosophila simulans and D. mauritiana, Genetics, 1997, vol. 145, no. 2, pp. 339–348. https://doi.org/10.1093/genetics/145.2.339
LeVasseur-Viens, H., Polak, M., and Moehring, A.J., No evidence for external genital morphology affecting cryptic female choice and reproductive isolation in Drosophila, Evolution, 2015, vol. 69, no. 7, pp. 1797–1807. https://doi.org/10.1111/evo.12685
Liu, J., Mercer, J.M., Stam, L.F., Gibson, G.C., Zeng, Z.-B., and Laurie, C.C., Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana, Genetics, 1996, vol. 142, no. 4, pp. 1129–1145. https://doi.org/10.1093/genetics/142.4.1129
Liu, J., Stam, L.F., Mercer, J.M., Gibson, G.C., and Laurie, C.C., Morphological differences in the male genitalia of D. simulans and D. mauritiana, Abs. Dros. Res. Conf., 1995, p. 305a.
Lush, J.L., Animal Breeding Plans, Ames: Collegiate Press, 1943.
Masly, J.P., Dalton, J.E., Srivastava, S., Chen, L., and Arbeitman, M.N., The genetic basis of rapidly evolving male genital morphology in Drosophila, Genetics, 2011, vol. 189, no. 1, pp. 357–374. https://doi.org/10.1534/genetics.111.130815
Mayr, E., Ecological factors in speciation, Evolution, 1947, vol. 1, no. 4, pp. 263–288. https://doi.org/10.2307/2405327
Mayr, B.F., Animal Species and Evolution, Cambridge, Mass: Harvard University Press, 1966.
Minocha, Sh., Boll, W., and Noll, M., Crucial roles of Pox neuro in the developing ellipsoid body and antennal lobes of the Drosophila brain, PLoS One, 2017, vol. 12, no. 4, p. e0176002. https://doi.org/10.1371/journal.pone.0176002
Mitrofanov, V.G. and Sidorova, N.V., Role of the female genotype in the formation of structural anomalies in the organs of Drosophila virilis female times D. litoralis male hybrids, Sov. J. Dev. Biol., 1975, no. 5, pp. 82–83.
Mitrofanov, V.G. and Sidorova, N.V., Genetics of the sex ratio anomaly in Drosophila hybrids of the Virilis group, Theor. Appl. Genet., 1981, vol. 59, no. 1, pp. 17–22. https://doi.org/10.1007/bf00275769
Mitrofanov, V.G., Sidorova, N.V., Grigor’eva, G.A., and Falileeva, L.I., Genetic control of isolating mechanisms in the genus Drosophila, Genetika, 1998, vol. 34, no. 9, pp. 189–199.
Mitrofanov, V.G., Sorokina, S.Iu., and Andrianov, B.V., Variation of the mitochondrial genome in the evolution of Drosophila, Russ. J. Genet., 2002, vol. 38, no. 8, pp. 895–907.
Muller, H.J., Bearing of the Drosophila work on systematics, The New Systematics, Huxley, J.S., Ed., Oxford: Clarendon Press, 1940, pp. 185–268.
Muller, H.J., Isolating mechanisms, evolution, and temperature, Biol. Symp., 1942, no. 6, pp. 71–125.
Parker, D.J., Wiberg, R.A.W., Trivedi, U., Tyukmaeva, V.I., Gharbi, K., Butlin, R.K., Hoikkala, A., Kankare, M., and Ritchie, M.G., Inter and intraspecific genomic divergence in Drosophila montana shows evidence for cold adaptation, Genome Biol. Evol., 2018, vol. 10, no. 8, pp. 2086–2101. https://doi.org/10.1093/gbe/evy147
Patterson, J.T. and Stone, W.S., Evolution in the Genus Drosophila, Macmillan, 1952.
Phillips, P.C. and Arnold, S.J., Visualizing multivariate selection, Evolution, 1989, vol. 43, no. 6, pp. 1209–1222. https://doi.org/10.2307/2409357
Ridgway, A.M., Hood, E.J., Jimenez, J.F., Nunes, M.D.S., and McGregor, A.P., Sox21b underlies the rapid diversification of a novel male genital structure between Drosophila species, Curr. Biol., 2024, vol. 34, no. 5, pp. 1114–1121. https://doi.org/10.1016/j.cub.2024.01.022
Robertson, H.M. and Paterson, H.E.H., Mate recognition and mechanical isolation in Enallagma damselflies (Odonata: Coenagrionidae), Evolution, 1982, vol. 36, no. 2, pp. 243–250. https://doi.org/10.2307/2408042
Schmalhausen, I.I., Factors of Evolution (Theory of Stabilizing Selection), Moscow: Publishing House of the USSR Academy of Sciences, 16th printing house trust Polygraphbook in Moscow, 1946.
Schmalhausen, I.I., Factors of Evolution: The Theory of Stabilizing Selection, Philadelphia: Blakiston, 1949.
Simmons, L.W., Sexual selection and genital evolution, Austral. Entomol., 2014, vol. 53, no. 1, pp. 1–17. https://doi.org/10.1111/aen.12053
Simpson, G.G., Tempo and Mode in Evolution, New York: Columbia Univ. Press, 1944.
Smith, J.M., Disruptive selection, polymorphism and sympatric speciation, Nature, 1962, vol. 195, pp. 60–62. https://doi.org/10.1038/195060a0
Smith, J.M., Sympatric speciation, Am. Nat., 1966, vol. 100, no. 916, pp. 637–650. https://doi.org/10.1086/282457
Sokolov, N.N., Elimination of chromosomes in interspecific hybrids of Drosophila and the problems of distant hybrids, Dokl. Acad. Nauk, 1948, vol. 59, pp. 163–166.
Sokolov, N.N., Interaction of the Nucleus and Cytoplasm during Distal Hybridization of Animals, Publishing House of the Academy of Sciences of the USSR, 1959.
Tanaka, K.M., Hopfen, C., Herbert, M.R., Schlötterer, Ch., Stern, D.L., Masly, J.P., Mcgregor, A.P., and Nunes, M.D.S., Genetic architecture and functional characterization of genes underlying the rapid diversification of male external genitalia between Drosophila simulans and Drosophila mauritiana, Genetics, 2015, vol. 200, no. 1, pp. 357–369. https://doi.org/10.1534/genetics.114.174045
Tanaka, K.M., Kamimura, Yo., and Takahashi, A., Mechanical incompatibility caused by modifications of multiple male genital structures using genomic introgression in Drosophila, Evolution, 2018, vol. 72, no. 11, pp. 2406–2418. https://doi.org/10.1111/evo.13592
True, J.R., Liu, J., Stam, L.F., Zeng, Z.-B., and Laurie, C.C., Quantitative genetic analysis of divergence in male secondary sexual traits between Drosophila simulans and Drosophila mauritiana, Evolution, 1997, vol. 51, no. 3, pp. 816–832. https://doi.org/10.1111/j.1558-5646.1997.tb03664.x
Tyukmaeva, V.I., Salminen, T.S., Kankare, M., Knott, K.E., and Hoikkala, A., Adaptation to a seasonally varying environment: a strong latitudinal cline in reproductive diapause combined with high gene flow in Drosophila montana, Ecol. Evol., 2011, vol. 1, no. 2, pp. 160–168. https://doi.org/10.1002/ece3.14
Tyukmaeva, V.I., Veltsos, P., Slate, J., Gregson, E., Kauranen, H., Kankare, M., Ritchie, M.G., Butlin, R.K., and Hoikkala, A., Localization of quantitative trait loci for diapause and other photoperiodically regulated life history traits important in adaptation to seasonally varying environments, Mol. Ecol., 2015, vol. 24, no. 11, pp. 2809–2819. https://doi.org/10.1111/mec.13202
Vorontsov, N.N., The rate of hamster evolution, and some factors determining its rate, Dokl. Akad. Nauk, 1960, vol. 133, no. 4, pp. 980–983.
Wright, S., On the nature of size factors, Genetics, 1918, vol. 3, no. 4, pp. 367–374. https://doi.org/10.1093/genetics/3.4.367
Wright, S., Evolution in Mendelian populations, Genetics, 1931, vol. 16, no. 2, pp. 97–159. https://doi.org/10.1093/genetics/16.2.97
Wright, S., The roles of mutation, inbreeding, crossbreeding and selection in evolution, Proc. 6th Int. Congr. Genet, 1932, no. 1, pp. 356–366.
Zeng, Z.-B., Liu, J., Stam, L.F., Kao, C.-H., Mercer, J.M., and Laurie, C.C., Genetic architecture of a morphological shape difference between two Drosophila species, Genetics, 2000, vol. 154, no. 1, pp. 299–310. https://doi.org/10.1093/genetics/154.1.299
Zhdanov, M.Iu, Poluéktova, E.V., and Mitrofanov, V.G., The role of inversions in adaptation and speciation, Ontogenez, 1994, vol. 25, no. 2, pp. 20–23.
Zhdanov, M.Iu., Mitrofanov, V.G., and Poluèktova, E.V., Character of ecological adaptation in connection with inversion polymorphism in Drosophila lummei, Hackman, Dokl. Akad. Nauk, 1997, vol. 355, no. 3, pp. 422–423.
Funding
The work was performed within the framework of the State Assignment of the Koltzov Institute of Developmental Biology, Russian Academy of Sciences, 2024, no. 0088-2024-0011.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
This work does not contain any studies involving human and animal subjects.
CONFLICT OF INTEREST
The author of this work declares that he has no conflicts of interest.
Additional information
The article is dedicated to the 120th anniversary of the birth of the outstanding Russian geneticist, Academician Boris Lvovich Astaurov
Translated by A. S. Ermakov
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
AI tools may have been used in the translation or editing of this article.
Rights and permissions
About this article
Cite this article
Kulikov, A.M. “Genes of Speciation”: History and Present: A Brief Review. Russ J Dev Biol 55, 239–249 (2024). https://doi.org/10.1134/S1062360424700231
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1134/S1062360424700231