eISSN: 2221-6197 DOI: 10.31301/2221-6197

Гаплодиплоидность и пол-определяющий каскад генов у перепончатокрылых насекомых

Год: 2019

Страницы: 108–119

Номер: Том 11, № 2

Аннотация:

В данном обзоре рассмотрены существующие и предполагаемые генетические системы, характерные для перепончатокрылых насекомых, а также показано, как устроен и функционирует пол-определяющий каскад у отдельных видов. Большинство перепончатокрылых насекомых  являются гаплодиплоидными – самки имеют диплоидный набор хромосом, а самцы гаплоидный. Однако пол–определяющие механизмы внутри этого отряда значительно варьируют не только в отдельных семействах, но даже в пределах одного рода. Общей чертой для них является наличие иерархичного пол-определяющего каскада, где продукты одних генов регулируют пол-специфичный сплайсинг других. Регуляция экспрессии осуществляется как при помощи альтернативного сплайсинга, так и положительных авторегуляторных петель.

Ключевые слова:

определение пола; гаплодиплоидность; Hymenoptera; csd; fem; tra; dsx

Библиографический список:

1. Adachi– Hagimori T., Miura K., Stouthamer R. A new cytogenetic mechanism for bacterial endosymbiont–induced parthenogenesis in Hymenoptera. Proceedings Biological Sciences. 2008. V. 275 (1652). P. 2667–2673. doi: 10.1098/rspb.2008.0792

2. Aguiar A.P., Deans A.R., Engel M.S., Forshage M., Huber J.T., Jennings J.T., Johnson N.F., Lelej A.S., Longino J.T., Lohrmann V., Mikо I., Ohl M., Rasmussen C., Taeger A., Sick Ki Yu D. Order hymenoptera. Zootaxa. 2013. V. 3703 (1). doi: 10.11646/zootaxa.3703.1.12

3. Aldrich, J.C. et al. Genome silencing and elimination: insights from a “Selfish” B chromosome / J.C. Aldrich, P.M. Ferree. Frontiers in Genetics. 2017. V. 8 (50). doi: 10.3389/fgene.2017.00050

4. Baudry E., Kryger P., Allsopp M., Koeniger N., Vautrin D., Mougel F., Cornuet J.–M., Solignac M. Whole–genome scan in thelytokous–laying workers of the cape honeybee (Apis mellifera capensis): central fusion, reduced recombination rates and centromere mapping using half–tetrad analysis. Genetics. 2004. V. 167 (1). Р.243–252. doi: 10.1534/genetics.167.1.243

5. Beukeboom L.W., Kamping A., van de Zande L. Sex determination in the haplodiploid wasp Nasonia vitripennis (Hymenoptera: Chalcidoidea): a critical consideration of models and evidence. Semin Cell Dev Biol. 2007. V. 18 (3). P. 3718.

6. Beye M., Moritz R.F.A., Epplen C. Sex linkage in the honeybee Apis mellifera detected by multilocus DNA fingerprinting. Naturwissenschaften. 1994. V. 81. Р.460–462. doi: 10.1007/BF01136650

7. Beye M., Moritz R.F.A. Mapping the sex locus of the honeybee (Apis mellifera). Naturwissenschaften. 1996. № 83. Р. 424 – 426.

8. Beye M., Hunt G.J., Page R.E., Fondrk M.K., Grohmann L., Moritz R.F. Unusually high recombination rate detected in the sex locus region of the honey bee (Apis mellifera). Genetics. 1999. V. 153. P.1701–1708.

9. Beye M., Hasselmann M., Fondrk M., Page R.E., Omholt S.W. The gene csd is the primary signal for sexual development in the Honeybee and encodes an SR–type protein. Cell. 2003. V. 114. P. 419–429. doi: 10.1016/S0092–8674(03)00606–8

10. Beye M., Hasselmann M., Vekemans X., Fondrk M.K., Page R.E.Jr. Gradual molecular evolution of a sex determination switch through incomplete penetrance of femaleness. Current Biology. 2013. V. 23. P.2559–2564. doi: 10.1016/j.cub.2013.10.070

11. Biewer M., Lechner S., Hasselmann M. Similar but not the same: insights into the evolutionary history of paralogous sex-determining genes of the dwarf honey bee Apis florea. Heredity (Edinb). 2016. V. 116 (1). P. 12-22. doi: 10.1038/hdy.2015.60

12. Biewer M., Schlesinger F., Hasselmann M. The evolutionary dynamics of major regulators for sexual development among Hymenoptera species. Frontiers in Genetics. 2015. V.6. Р. 11. doi: 10.3389/fgene.2015.00124

13. Blackmon H., Ross L., Bachtrog D. Sex determination, sex chromosomes, and karyotype evolution in Insects. Journal of Heredity. 2016. P.1–16. doi:10.1093/jhered/esw047

14. Bratus A., Slota E. DMRT1/Dmrt1, the sex determining or sex differentiating gene in Vertebrata. Folia Biol. 2006. V. 54. P. 81 – 86.

15. Burghardt G., Hediger M., Siegenthaler C., Moser M., Dübendorfer A., Bopp D. The transformer2 gene in Musca domestica is required for selecting and maintaining the female pathway of development. Development Genes and Evolution. 2005. V. 215(4). P.165 – 176. doi: 10.1007/s00427–004–0464–7

16. Butcher R.D.J., Whitfield W.G.F., Hubbard S.F. Complementary sex determination in the genus Diadegma (Hymenoptera: Ichneumonidae). J. Evol. Biol. 2000. P. 13593 – 13606.

17. Chapman N.C., Beekman M., Allsopp M.H., Rinderer T.E., Lim J., Oxley P.R., Oldroyd B.P. Inheritance of thelytoky in the honey bee Apis mellifera capensis. Heredity (Edinb). 2015. V. 114 (6). P. 584 – 592. doi: 10.1038/hdy.2014.127

18. Cho S., Huang Z.Y., Green D.R., Smith D.R., Zhang J. Evolution of the complementary sex– determination gene of honey bees: Balancing selection and trans–species polymorphisms. Genome Research. 2006. № 2. P. 1366 – 1375. doi: 10.1101gr.4695306

19. Cho S., Huang Z.Y., Zhang J. Sex–specific splicing of the honeybee doublesex gene reveals 300 million years of evolution at the bottom of the insect sex– determination pathway. Genetics. 2007. V.177. P. 1733–1741. doi: 10.1534/genetics.107.078980

20. Cole–Clark M.P., Barton D.A., Allsopp M.H., Beekman M., Gloag R.S., Wossler T.C., Ronai I., Smith N., Reid R.J., Oldroyd B.P. Cytogenetic basis of thelytoky in Apis mellifera capensis. Apidologie. 2017. V. 48 (5). P.623–634. doi: 10.1007s13592–017–0505–7

21. Cristino A.S., Nascimento A.M., Costa L.F., Simoes Z.L.P. A comparative analysis of highly conserved sex–determining genes between Apis mellifera and Drosophila melanogaster. Genetics and Molecular Research. 2006. V. 5 (1). P.154 – 168.

22. de Boer J.G., Ode P.J., Rendahl A.K., Rendahl A.K., Vet L.E.M., Whitfield J.B., Heimpel G.E. Experimental support for multiple–locus complementary sex determination in the parasitoid Cotesia vestalis. Genetics. 2008. V. 180 (3). P. 1525–1535. doi: 10.1534genetics.107.083907

23. de Boer J.G., Kuijper B., Heimpel G.E., Beukeboom L.W. Sex determination meltdown upon biological control introduction of the parasitoid Cotesia rubecula? Evol Appl. 2012. V. 5. P. 444–454. doi: 10.1111j.1752– 4571.2012.00270.x

24. Dobata S., Sasaki T., Mori H., Hasegawa E., Shimada M., Tsuji K. Cheater genotypes in the parthenogenetic ant Pristomyrmex punctatus. Proceedings of the Royal Society London Series B. 2009. V. 276. P. 567–574.

25. Doums C., Cronin A.L., Ruel C., Federici P., Haussy C., Tirard C., Monnin T. Facultative use of thelytokous parthenogenesis for queen production in the polyandrous ant Cataglyphis cursor. J Evol Biol. 2013. V. 26 (7). P. 143 – 144. doi:10.1111jeb.12142

26. Dyer A.G., Boyd–Gerny S., McLoughlin S., Rosa M.G., Simonov V., Wong B.B. Parallel evolution of angiosperm colour signals: common evolutionary pressures linked to hymenopteran vision. Proc. R. Soc. B. 2012. V. 279. P. 3606–3615. doi:10.1098rspb.2012.0827

27. Eirin–Lopez J.M., Sanchez L. The comparative study of five sex–determining proteins across insects unveils high rates of evolution at basal components of the sex determination cascade. Development Genes and Evolution. 2015. V. 225 (1). P. 23 – 30. doi:10.1007s0042701504916

28. Elias J., Mazzi D., Dorn S. No need to discriminate? Reproductive diploid males in a parasitoid with complementary sex determination. PLoS One. 2009. V. 4 (6). e6024. doi:10.1371journal.pone.0006024

29. Escriba M.C., Giardini M.C., Goday C. Histone H3 phosphorylation and non–disjunction of the maternal X chromosome during male meiosis in sciarid flies. Journal of Cell Science. 2011. V. 124 (10). P. 1715– 1725. doi: 10.1242jcs.083022

30. Espinosa M.S., Virla E.G., Cuozzo S. Wolbachia infections responsible for thelytoky in Dryinid wasps. The case of Gonatopus bonaerensis Virla (Hymenoptera: Dryinidae). Neotrop Entomol. 2017. V. 46 (4). P. 409– 413. doi:10.1007s137440160475x

31. Gadau J. A linkage analysis of the sex determination in Bombus terrestris (L.) (Hymenoptera: Apidae). Heredity. 2001. V.87. P. 234–242.

32. Gempe T., Hasselmann M., Schiott M., Hause G., Otte M., Beye M. Sex determination in honeybees: two separate mechanisms induce and maintain the female pathway. PLoS Biology. 2009. V. 7 (10). doi:10.1371journal.pbio.1000222

33. Geuverink E., Verhulst E.C., van Leussen M., van de Zande L., Beukeboom L.W. Maternal provision of non sex–specific transformer messenger RNA in sex determination of the wasp Asobara tabida. Insect Mol Biol. 2018. V. 27 (1). P. 99-109. doi: 10.1111/imb.12352

34. Geuverink E., Beukeboom L.W. Phylogenetic distribution and evolutionary dynamics of the sex determination genes doublesex and transformer in insects. Sex Dev. 2014. V. 8. Р. 38–49. doi: 10.1159000357056

35. Gloag R., Ding G.L., Christie J.R., Buchmann G., Beekman M., Oldroyd B.P. An invasive social insect overcomes genetic load at the sex locus. Nature Ecology & Evolution. 2016. V.1. doi: 10.1038s41559-016-0011

36. Gotoh H., Zinna R.A., Warren I., DeNieu M., Niimi T., Dworkin I., Emlen D.J., Miura T., Lavine L.C. Identification and functional analyses of sex determination genes in the sexually dimorphic stag beetle Cyclommatus metallifer. BMC Genomics. 2016. P.17. doi: 10.1186s12864–016–2522–8

37. Graham P., Penn J.K., Schedl P. Masters change, slaves remain. Bioessays. 2003. V. 25. P. 1–4.

38. Gu H., Dorn S. Mating system and sex allocation in the gregarious parasitoid Cotesia glomerata. Anim Behav. 2003. V.66 (2). P. 259– 264. doi: 10.1006/anbe.2003.2185

39. Harpur B.A., Sobhani M., Zayed A. A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera. The Netherlands Entomological Society Entomologia Experimentalis et Applicata. 2012. P.1–9. doi: 10.1111j.1570–7458.2012.01306.x

40. Hasselmann M., Fondrk M.K., Page R.E., Beye M. Fine scale mapping in the sex locus region of the honey bee (Apis mellifera). Insect Molecular Biology. 2001. V. 10(6). P. 605–608. doi: 10.1046/j.0962–1075.2001.00300.x

41. Hasselmann M., Gempe T., Schiott M., Nunes–Silva C.G., Otte M., Beye M. Evidence for the evolutionary nascence of a novel sex determination pathway in honey bees. Nature. 2008a. V. 454. P. 519 – 523. doi: 10.1038nature07052

42. Hasselmann M., Vekemans X., Pflugfelder J. Evidence for convergent nucleotide evolution and high allelic turnover rates at the complementary sex determiner gene of Western and Asian honeybees Mol. Biol. Evol. 2008b. V. 25 (4). P. 696–708. doi:10.1093molbevmsn011

43. Hasselmann M., Lechner S., Schulte C., Beye M. Origin of a function by tandem gene duplication limits the evolutionary capability of its sister copy. Proc Natl Acad Sci USA. 2010. V. 107 (30). Р. 13378–13383. doi: 10.1073/pnas.1005617107

44. Heimpel G.E., de Boer J.G. Sex determination in the Hymenoptera. Annu. Rev. Entomol. 2008. V. 53. P. 209–230. doi: 10.1146annurev.ento.53.103106.093441

45. Heraty J.M., Darling D.C. Fossil Eucharitidae and Perilampidae (Hymenoptera: Chalcidoidea) from Baltic Amber. Zootaxa. 2009. V.2306. P.1 – 16.

46. Hodgkin J. The remarkable ubiquity of DM domain factors as regulators of sexual phenotype: ancestry or aptitude? Genes Dev. 2002. V. 16. P. 2322–2326

47. Hu S., Dilcher D.L., Jarzen D.M., Taylor D.W. Early steps of angiosperm–pollinator coevolution. Proc Natl Acad Sci USA. 2008. V. 10 (1). Р. 240–245. doi: 10.1073 pnas.0707989105

48. Kellner K., Seal J.N., Heinze J. Sex at the margins: parthenogenesis vs. facultative and obligate sex in a Neotropical ant. J Evol Biol. 2013. V. 26 (1). P. 108 – 117. doi: 10.1111jeb.12025

49. Koch V., Nissen I., Schmitt B.D., Beye M. Independent evolutionary origin of fem paralogous genes and complementary sex determination in hymenopteran insects. PLOS ONE. 2014. V. 9. P. 11. doi: 10.1371journal.pone.0091883

50. Koukidou M., Alphey L. Practical applications of insects' sexual development for pest control Sex Dev. 2014. V. 8 (13). P. 127 – 136.doi: 10.1159000357203

51. Lechner S., Ferretti L., Schöning C., Kinuthia W., Willemsen D., Hasselmann M. Nucleotide variability at its limit? Insights into the number and evolutionary dynamics of the sex–determining specificities of the honey bee Apis mellifera. Mol Biol Evol. 2014. V. 29. doi:10.1093molbevmst207

52. Ledon–Rettig C.C., Zattara E.E., Moczek A.P. Asymmetric interactions between doublesex and tissue– and sex–specific target genes mediate sexual dimorphism in beetles. Nat Commun.2017.V.8.doi: 10.1038ncomms14593

53. Liu G., Wu Q., Li J., Zhang G., Wan F. RNAi–mediated knock–down of transformer and transformer2 to generate male–only progeny in the oriental fruit fly, Bactrocera dorsalis. (Hendel) PloS One. 2015. V. 10 (6). doi: 10.1371journal.pone.0128892

54. Liu Z.Y., Wang Z.L., Wu X.B., Zeng Z.J Csd alleles in the red dwarf honey bee (Apis florea, Hymenoptera: Apidae) show exceptionally high nucleotide diversity. Insect Sci. 2011. V. 18. P. 645–651. doi:10.1111j.1744-7917.2011.01437.x

55. Liu Z.Y., Wang Z.L., Yan W.Y., Wu X.B., Zeng Z.J., Huang Z.Y. The sex determination gene shows no founder effect in the giant honey bee, Apis dorsata. PLoS One. 2012. V.7. e34436. doi:10.1371journal.pone.0034436

56. Ma W.J., Pannebakker B.A., van de Zande L., Schwander T., Wertheim B., Beukeboom L.W. Diploid males support a twostep mechanism of endosymbiont–induced thelytoky in a parasitoid wasp. BMC Evol. Biol. 2015. V. 15. P. 84. doi: 10.1186s12862–015–0370–9

57. Masuko K. Thelytokous parthenogenesis in the ant Myrmecina nipponica (Hymenoptera: Formicidae). Zoolog Sci. 2014. V. 31(9). P. 5826. doi:10.2108zs140050

58. Matsuda M., Nagahama Y., Shinomiya A., Sato T., Matsuda C., Kobayashi T., Morrey C.E., Shibata N., Asakawa S., Shimizu N., Hori H., Hamaguchi S., Sakaizumi M. DMY is a Y–specific DM–domain gene required for male development in the medaka fish. Nature. 2002. V. 417. P. 559–563.

59. Mine S., Sumitani M., Aoki F., Hatakeyama M., Suzuki M.G. Identification and functional characterization of the sex–determining gene doublesex in the sawfly, Athalia rosae (Hymenoptera: Tenthredinidae). Appl Entomol Zool. 2017. V. 52(3). P. 497-509. doi: 10.1007s13355–017–0502–3

60. Miyakawa M.O., Mikheyev A.S. QTL mapping of sex determination loci supports an ancient pathway in ants and honey bees. PLoS Genetics. 2015. V. 11(11). e1005656. doi:10.1371journal.pgen.1005656

61. Miyakawa M.O., Tsuchida K., Miyakawa H. The doublesex gene integrates multi–locus complementary sex determination signals in the Japanese ant, Vollenhovia emeryi. Insect Biochem Mol Biol. 2018. V. 94. P. 42 – 49. doi: 10.1016j.ibmb.2018.01.006

62. Nagaraju J., Gopinath G., Sharma V., Shukla J.N. Lepidopteran sex determination: a cascade of surprises. Sex Dev. 2014. V. 8 (1–3). P. 104–112. doi: 10.1159000357483

63. Naito T., Ishikawa M., Nishimoto Y. Two–locus multiple–allele sex determination in the rose sawfly Arge nigrinodosa. Presented at 3rd Int. Hymenopt. Congr., Canberra, Aust. 2000.

64. Narendra U., Zhu L., Li B., Wilken J., Weiss M.A. Sex–specific gene regulation. The Doublesex DM motif is a bipartite DNA–binding domain. J. Biol Chem. 2002. V.277 (45). Р. 43463–43473. doi 10.1074jbc.M204616200

65. Nguyen T.M., Bressac C., Chevrier C. Heat stress affects male reproduction in a parasitoid wasp. J Insect Physiol. 2013. V. 59 (3). P. 248–254. doi:10.1016j.jinsphys.2012.12.001

66. Nissen I., Müller M., Beye M. The Am–tra2 gene is an essential regulator of female splice regulation at two levels of the sex determination hierarchy of the honeybee. Genetics. 2012. V. 192. P. 1015–1026. doi: 10.1534genetics.112.143925

67. Normark B.B. The evolution of alternative genetic systems in insects. Annu. Rev. Entomol. 2003. V. 48. P. 397–423.

68. Nugnes F., Gebiola M., Monti M.M., Gualtieri L., Giorgini M., Wang J., Bernardo U. Genetic diversity of the invasive gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) and of its Rickettsia endosymbiont, and associated sex–ratio differences. PLoS One. 2015. V. 10(5). e0124660. doi:10.1371journal.pone.0124660

69. Oliveira D.C., Werren J.H., Verhulst E.C., Giebel J.D., Kamping A., Beukeboom L.W., van de Zande L. Identification and characterization of the doublesex gene of Nasonia. Insect Mol Biol. 2009. V. 18 (3). P. 315 – 324. doi: 10.1111j.1365–2583.2009.00874.x

70. Paladino L.C., Muntaabski I., Lanzavecchia S., Bagousse–Pinguet Y.L., Viscarret M., Juri M., Fueyo–Sanchez L., Papeschi A., Cladera J., Bressa M.J. Complementary sex determination in the parasitic wasp Diachasmimorpha longicaudata. PLoS One. 2015. 17p. doi:10.1371journal.pone.0119619

71. Pearcy M., Hardy O., Aron S. Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity (Edinb). 2006.V. 96 (5). P. 377 – 382. doi: 10.1038sj.hdy.6800813

72. Peters R.S., Krogmann L., Mayer C., Carlo P., Thomas S., Shanlin L., Xin Z., Torsten W., Rust J., Misof B., Niehuis O. Evolutionary History of the Hymenoptera. Current Biology. 2017. V.27 P.1013–1018. doi:10.1016j.cub.2017.01.027

73. Price D.C., Egizi A., Fonseca D.M. The ubiquity and ancestry of insect doublesex. Scientific Reports. 2015. V. 5. 13068. doi: 10.1038srep13068

74. Rabeling C., Kronauer D.J. Thelytokous parthenogenesis in eusocial Hymenoptera. Annu Rev Entomol. 2013. V. 58. P.273 – 292.

75. Rabeling C., Lino-Neto J., Cappellari S.C., DosSantos I.A., Mueller U.G., Bacci M. Thelytokous parthenogenesis in the fungus-gardening ant Mycocepurus smithii (Hymenoptera: Formicidae). PLoS One. 2009. V. 4. e6781. doi: 10.1371/journal.pone.0006781

76. Ravary F., Jaisson P. Absence of individual sterility in thelytokous colonies of the ant Cerapachys biroi Forel (Formicidae, Cerapachyinae). Insectes Sociaux. 2004. V. 51. P. 67–73. doi:10.1007s00040-003-0724-y

77. Ronquist F., Klopfstein S., Vilhelmsen L., Schulmeister S., Murray D.L., Rasnitsyn A.P. A total–evidence approach to dating with fossils, applied to the early radiation of the Hymenoptera. Syst. Biol. 2012. V. 61. P. 973–999.

78. Ross L., Davies N.G., Gardner A. How to make a haploid male. Evolution Letters. 2019. V. 3 (2). P. 173-184. doi:10.1002evl3.107

79. Roth A., Vleurinck C., Netschitailo O., Bauer V., Otte M., Kaftanoglu O., Page R. E., Beye M. A genetic switch for worker nutrition-mediated traits in honeybees. PLoS Biol. 2019. V. 17(3). e3000171. https:doi.org10.1371journal.pbio.3000171

80. Saccone G., Salvemini M., Polito L.C. The transformer gene of Ceratitis capitata: a paradigm for a conserved epigenetic master regulator of sex determination in insects. Genetica. 2011. V. 139(1). P. 99-111. doi: 10.1007s10709-010-9503-7

81. Sanchez L. Sex–determining mechanisms in insects. Int. J. Dev. Biol. 2008. V.52. P.837 – 856. doi: 10.1387ijdb.072396ls

82. Sawanth S.K., Gopinath G., Sambrani N., Arunkumar K.P. The autoregulatory loop: A common mechanism of regulation of key sex determining genes in insects. J. Biosci. 2016. V. 41(2). P. 283 – 294.

83. Schneider M.V., Driessen G., Beukeboom L.W., Boll R., van Eunen K., Selzner A., Talsma J., Lapchin L. Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera). Heredity. 2003. V. 90. P. 260–267.

84. Schurko A.M. To “Bee or not to bee” male or female? An educational primer for use with “The Am–tra2 gene is an essential regulator of female splice regulation at two levels of the sex determination hierarchy of the honeybee”. Genetics. 2013. V. 193 (4). P. 1019–1023. doi: 10.1534genetics.113.150417

85. Shukla J.N., Nagaraju J. Doublesex: a conserved downstream gene controlled by diverse upstream regulators. Journal of Genetics. 2010. V. 89 (3). P. 341–356.

86. Shukla J.N., Palli S.R. Sex determination in beetles: production of all male progeny by parental RNAi knockdown of transformer. Sci Rep. 2012. V. 2 (602). doi:10.1038srep00602

87. Stahlhut J.K., Cowan D.P. Inbreeding in a natural population of Euodynerus foraminatus (Hymenoptera: Vespidae), a solitary wasp with single‐locus complementary sex determination. Molecular Ecology. 2004. V.13. P.631– 638. doi: 10.1046j.1365-294X.2004.02090.x

88. Sun D., Guo Z., Liu Y., Zhang Y. Progress and prospects of CRISPR/Cas systems in insects and other arthropods. Front Physiol. 2017. V. 8. P. 608. doi: 10.3389fphys.2017.00608

89. Tanaka A., Aoki F., Suzuki M.G. Conserved domains in the transformer protein act complementary to regulate sex-specific splicing of its own pre-mRNA. Sex Dev. 2018. V. 12 (4). P. 180-190. doi: 10.1159000489444

90. Tarpy D.R., Delaney D.A., Seeley T.D. Mating Frequencies of Honey Bee Queens (Apis mellifera L.) in a Population of Feral Colonies in the Northeastern United States. PLoS One. 2015. V. 10 (3). e0118734. doi: 10.1371journal.pone.0118734

91. Tram U., Fredrick K., Werren J.H., Sulliva W. Paternal chromosome segregation during the first mitotic division determines Wolbachia–induced cytoplasmic incompatibility phenotype. Journal of Cell Science. 2006. V.119. P.3655– 3663. doi:10.1242jcs.03095

92. Trukhina A.V., Lukina N.A., Wackerow–Kouzova N.D., Smirnov A.F. The variety of vertebrate mechanisms of sex determination. Biomed Res Int. 2013. V. 2013 (587460). doi: 10.11552013587460

93. Tsutsui Y., Maeto K., Hamaguchi K., Isaki Y., Takami Y., Naito T., Miura K. Apomictic parthenogenesis in a parasitoid wasp Meteorus pulchricornis, uncommon in the haplodiploid order Hymenoptera. Bull. Entomol. Res. 2014. V. 104 (3). P.307–313. doi: 10.1017S0007485314000017

94. van de Zande L., Verhulst E.C. Genomic imprinting and maternal effect genes in haplodiploid sex determination. Sex Dev. 2014. V. 8. P. 74–82. doi: 10.11590003571

95. van Wilgenburg E., Driessen G., Beukeboom L.W. Single locus complementary sex determination in Hymenoptera: an "unintelligent" design? Frontiers in Zoology. 2006. V. 3(1). doi: 10.1186/1742-9994-3-1

96. Vavre F., de Jong J.H., Stouthamer R. Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae. Heredity (Edinb). 2004. V. 93 (6). P. 5926.

97. Verhulst E.C., van de Zande L. Double nexus – Doublesex is the connecting element in sex determination. Briefings in Functional Genomics. 2015. P. 1–11. doi: 10.1093bfgpelv005

98. Verhulst E.C., van de Zande L. Insect sex determination: a cascade of mechanisms. Sex Dev. 2014. V. 8(13). P.56. doi: 10.1159000358405

99. Verhulst E.C., van de Zande L., Beukeboom L.W. Insect sex determination: it all evolves around transformer. Current Opinion in Genetics & Development. 2010b. V.20. P.376–383. doi:10.1016j.gde.2010.05.001

100.Verhulst E.C., Beukeboom L.W., van de Zande L. Maternal control of haplodiploid sex determination in the wasp Nasonia. Science. 2010a. 328. P. 620 – 623.

101.Wang H., Wang Z., Zeng Z., Wu X–B., Yan W–Y. Nucleotide diversity based on csd gene of the black giant honey bee, Apis laboriosa (Hymenoptera: Apidae). Eur. J. Entomol. 2013. V. 110(2). P.215–220. doi:10.14411eje.2013.095

102.Wang X.X., Qi L.D., Jiang R., Du Y–Z., Li Y–X. Incomplete removal of Wolbachia with tetracycline has two–edged reproductive effects in the thelytokous wasp Encarsia formosa (Hymenoptera: Aphelinidae). Sci Rep. 2017. V.7. P.440 – 414. doi:10.1038srep44014

103.Wang Z., Liu Z., Wu X., Yan W., Zeng Z. Polymorphism analysis of csd gene in six Apis mellifera subspecies. Mol Biol Rep. 2012. V. 39. P. 3067–3071. doi 10.1007s11033–011–1069–7

104.The Honeybee Genome Sequencing Consortium. Insights into social insects from the genome of the honeybee Apis mellifera. Nature. 2006. V. 443 (7114). P. 931–949. doi:10.1038nature05260

105.Werren J.H., Stouthamer R. PSR (paternal sex ratio) chromosomes: the ultimate selfish genetic elements. Genetica. 2003. V. 117 (1). P.85 – 101. doi:10.1023A:1022368700752

106.Whiting P.W. Multiple alleles in complementary sex determination of Habrobracon. Genetics. 1943. V. 24. P. 110–111.

107.Xu J., Chen S., Zeng B., James A.A., Tan A., Huang Y. Bombyx mori P–element somatic inhibitor (BmPSI) is a key auxiliary factor for silkworm male sex determination. PLoS Genet. 2017. V. 13 (1). e1006576. doi:10.1371journal.pgen.1006576

108.Zareba J., Blazej P., Laszkiewicz A., Sniezewski L., Majkowski M., Janik S., Cebrat M. Uneven distribution of complementary sex determiner (csd) alleles in Apis mellifera population. Scientific Reports. 2017. V.7. doi:10.1038s41598–017–02629–9

109.Zaviezo T., Retamal R., Urvois T., Fauvergue X., Blin A., Malausa T. Effects of inbreeding on a gregarious parasitoid wasp with complementary sex determination. Evol Appl. 2017. V. 11(2). P. 243–253. doi:10.1111eva.12537

110.Zhang W., Li B., Singh R., Narendra U., Zhu L., Weiss M.A. Regulation of sexual dimorphism: mutational and chemogenetic analysis of the doublesex DM domain. Mol. Cell Biol. 2006. V. 26 (2). P.535–547. doi: 10.1128/MCB.26.2.535-547.2006

Скачать pdf
наверх
eISSN: 2221-6197 DOI: 10.31301/2221-6197