Естественная история циклического партеногенеза тлей (Homoptera: Aphidinea)

И.А. Гаврилов-Зимин

Труды Зоологического института РАН, 2024, 328(4): 595–621 · https://doi.org/10.31610/trudyzin/2024.328.4.595

Резюме

В статье предлагается и аргументируется гипотеза о возникновении циклического партеногенеза у тлей как следствии их исторически исходного обитания в закрытых стробилоподобных галлах на хвойных деревьях. Вскрытие галлов сильно растянуто во времени, что препятствует нормальной панмиксии и создаёт селективное преимущество для партеногенетического размножения. Миграция тлей на вторичные кормовые растения, на которых никогда не образуется закрытых галлов, партеногенетическое размножение на этих растениях и последующее одновременное возвращение «ремигрантов» на основное кормовое растение позволяют синхронизировать развитие обоеполого поколения и добиться массовой панмиксии лишь в конце жизненного цикла, совпадающего с летним окончанием роста побегов или осенним завершением вегетационного периода в целом. В связи с тем, что развитие обоеполого поколения всегда происходит во второй половине года, когда условия для питания тлей на древесных растениях становятся неблагоприятными, то понятным оказываются мелкие размеры половых особей и их сниженная плодовитость (часто всего одно яйцо на самку), в сравнении с партеногенетическими поколениями первой половины года. Эволюционный переход тлей с хвойных на покрытосеменные растения в меловом периоде попутно означал возможность развития в более просторных галлах, вмещающих несколько последовательных партеногенетических поколений, переход к живорождению и телескопической эмбрионизации, существенно ускоряющей смену поколений. Утрату яйцеклада у филлоксер и, гипотетически, произошедших от них афидоидных тлей можно объяснить исходной жизнью в галлах, где откладка яиц не требует специальных приспособлений. Эволюционный переход от яйцекладности партеногенетических поколений к живорождению произошёл, вероятно, у предков современных эриосоматид (Eriosomatidae), о чём свидетельствуют плезиоморфные черты репродуктивной биологии последних.

Ключевые слова

адельгиды, галлы, однополое размножение, пемфигиды, филлоксеры, хермесы, эволюция

Поступила в редакцию 15 июля 2024 г. · Принята в печать 30 октября 2024 г. · Опубликована онлайн 5 декабря 2024 г.

Литература

Annand P.N. 1928. A contribution toward a monograph of the Adelginae (Phylloxeridae) of North America. Stanford University Publications (Biological Sciences), 6(1): 1–146.

Aoki S. and Kurosu U. 2010. A Review of the biology of Cerataphidini (Hemiptera, Aphididae, Hormaphidinae), focusing mainly on their life cycles, gall formation, and soldiers. Psyche, 380351: 1–34. https://doi.org/10.1155/2010/380351

Baker H. 1935. Phylloxera devastatrix Perg. on pecans. Journal of Economic Entomology, 28(4): 681–685. https://doi.org/10.1093/jee/28.4.681

Blackman R.L. 1987. Reproduction, cytogenetics and development. In: A.K. Minks and P. Harrewijn (Eds). Aphids. Their biology, natural enemies and control. Volume A. Elsevier, Amsterdam, Oxford, New York, Tokyo: 163–195.

Blackman R.L. and Hales D.F. 1986. Behaviour of the X chromosomes during growth and maturation of parthenogenetic eggs of Amphorophora tuberculata (Homoptera, Aphididae), in relation to sex determination. Chromosoma, 94: 59–64. https://doi.org/10.1007/bf00293530

Cholodkowski N.A. 1915. Chermeses, injuring coniferous trees. M. Merkushev Publisher, Petrograd, 90 p. [In Russian].

Cock M.J.W., Shaw R.H. and Blackman R.L. 2010. On the biology of Ceratopemphigus zehntneri Schouteden (Hemiptera: Aphididae), a gall-forming aphid on Ligustrum robustum subsp. Walkeri (Oleaceae), in Sri Lanka. Zootaxa, 2614: 46–52. https://doi.org/10.11646/zootaxa.2614.1.4

Csóka G., Stone G.N. and Melika G. 2005. Biology, ecology, and evolution of gall-inducing Cynipidae. In: A. Raman, C.W. Schaefer and T.M. Withers (Eds). Biology, Ecology, and Evolution of Gall-Inducing Arthropods. Science Publishers, Enfield, Plymouth: 573–642.

Cumming M.E.P. 1962. The biology of Pineus similis (Gill.) (Homoptera: Phylloxeridae) on Spruce. The Canadian Entomologist, 94(4): 395–408. https://doi.org/10.4039/Ent94395-4

Danzig Е.М. 1993. Suborder Coccinea. Families Phoenicococcidae и Diaspididae. Nauka, St. Petersburg, 453 p. (Fauna of Russia and neighbouring countries. New series, No. 144). [In Russian].

Danzig E.M. and Gavrilov-Zimin I.A. 2014. Palaearctic mealybugs (Homoptera: Coccinea: Pseudococcidae). Part 1. Subfamily Phenacoccinae. ZIN RAS, St. Petersburg, 678 p. (Fauna of Russia and neighbouring countries. New series, No. 148).

Danzig E.M. and Gavrilov-Zimin I.A. 2015. Palaearctic mealybugs (Homoptera: Coccinea: Pseudococcidae). Part 1. Subfamily Phenacoccinae. ZIN RAS, St. Petersburg, 619 p. (Fauna of Russia and neighbouring countries. New series, No. 149).

Davis G.K. 2012. Cyclical parthenogenesis and viviparity in aphids as evolutionary novelties. Journal of Experimental Zoology. (B, Molecular and Developmental Evolution), 318(6): 448–59. https://doi.org/10.1002/jez.b.22441

Dixon A.F.G. 1987. Evolution and adaptive significance of cyclical parthenogenesis in aphids. In: A.K. Minks and P. Harrewijn (Eds). Aphids. Their biology, natural enemies and control. Vol. A. Elsevier, Amsterdam, Oxford, New York, Tokyo: 289–297.

Favret C., Havill N.P., Miller G.L., Sano M. and Victor B. 2015. Catalog of the adelgids of the world (Hemiptera, Adelgidae). ZooKeys, 534: 35–54. https://doi.org/10.3897/zookeys.534.6456

Felsenstein J. 1974. The evolutionary advantage of recombination. Genetics, 78(2): 737–56. https://doi.org/10.1093/genetics/78.2.737

Gavrilov I.A. 2007. A catalogue of chromosomal numbers and genetic systems of scale insects (Homoptera: Coccinea) of the world. Israel Journal of Entomology, 37: 1–45.

Gavrilov-Zimin I.A. 2018. Ontogenesis, morphology and classification of archaeococcids (Homoptera: Coccinea: Orthezioidea). Supplementum 2 to Zoosystematica Rossica. ZIN RAS, St.-Petersburg. 260 p. https://doi.org/10.31610/zsr/2018.supl.2.1

Gavrilov-Zimin I.A. 2021. Aberrant ontogeneses and life cycles in Paraneoptera. Comparative Cytogenetics, 15(3): 253–277. https://doi.org/10.3897/compcytogen.v15.i3.70362

Gavrilov-Zimin I.A. 2022. Development of theoretical views on viviparity. Biological Bulletin Reviews, 12: 570–595. https://doi.org/10.1134/S2079086422060032

Gavrilov-Zimin I.A. 2023. Ancient reproductive modes and criteria of multicellularity. Comparative Cytogenetics, 17: 195–238. https://doi.org/10.3897/compcytogen.17.109671

Gavrilov-Zimin I.A. 2024. The concept of evolutional embryonization/desembryonization of ontogeneses. Uspehi Sovremennoi Biologii, 144 (In press). [In Russian].

Gavrilov-Zimin I.A. and Danzig E.M. 2012. Taxonomic position of the genus Puto Signoret (Homoptera: Coccinea: Pseudococcidae) and separation of higher taxa in Coccinea. Zoosystematica Rossica, 22(1): 97–111. https://doi.org/10.31610/zsr/2012.21.1.97

Gavrilov-Zimin I.A., Grozeva S.M., Gapon D.A., Kurochkin A.S., Trencheva K.G. and Kuznetsova V.G. 2021. Introduction to the study of chromosomal and reproductive patterns in Paraneoptera. Comparative Cytogenetics, 15(3): 217–238. https://doi.org/10.3897/compcytogen.v15.i3.69718

Gavrilov-Zimin I.A., Stekolshikov A.V. and Gautam D.C. 2015. General trends of chromosomal evolution in Aphidococca (Insecta, Homoptera, Aphidinea + Coccinea). Comparative Cytogenetics, 9(3): 335–422. https://doi.org/10.3897/CompCytogen.v9i3.4930

Gokhman V.E. and Kuznetsova V.G. 2017. Parthenogenesis in Hexapoda: holometabolous insects. Journal of Zoological Systematics and Evolutionary Research, 2018, 56: 23–34. https://doi.org/10.1111/jzs.12183

Grassi B. 1912. Contribute alia conoscenza delle Fillosserini ed in particolare delta Fillosera della Vite. Tipografica nazionale di G. Bertero EC, Rome, 456 p.

Hales D.F., Tomiuk J., Wöhrmann K. and Sunnucks P. 1997. Evolutionary and genetic aspects of aphid biology: a review. European Journal of Entomology, 94: 1–55.

Han L., Zhao Y., Zhao M., Sun J., Sun B. and Wang X. 2023. New fossil evidence suggests that angiosperms flourished in the middle Jurassic. Life, 13(3, 819): 1–12. https://doi.org/10.3390/life13030819

Havelka J., Danilov J. and Rakauskas R. 2019. Aphids of the family Adelgidae in Lithuania: distribution, host specificity and molecular (mitochondrial COI and nuclear EF-1α) diversity. Biologia, 2020, 75: 1155–1167. https://doi.org/10.2478/s11756-019-00365-1

Havill N.P. and Foottit R.G. 2007. Biology and evolution of Adelgidae. Annual Review of Entomology, 52: 325–349. https://doi.org/10.1146/annurev.ento.52.110405.091303

Havill N.P., Griffin B.P., Andersen J.C., Foottit R.G., Justesen M.J., Caccone A., D'Amico V. and Elkinton J.S. 2020. Species delimitation and invasion history of the balsam woolly adelgid, Adelges (Dreyfusia) piceae (Hemiptera: Aphidoidea: Adelgidae), species complex. Systematic Entomology, 46: 186–204. https://doi.org/10.1111/syen.12456

Heie O.E. 1987. Palaeontology and phylogeny. In: A.K. Minks and P. Harrewijn (Eds). Aphids. Their Biology, Natural Enemies and Control. Elsevier, Amsterdam: 367–391.

Heie O.E. and Wegierek P. 2009. A classification of the Aphidomorpha (Hemiptera: Sternorrhyncha) under consideration of the fossil taxa. Redia, 92: 69–72.

Hille Ris Lambers D. 1950. An apparently unrecorded mode of reproduction in Aphididae. Proceedings of 8th International Congress of Entomology, Stockholm, p. 235.

Hood G.R., Zhang L., Topper L., Brandão-Dias P.E.P., Del Pino G.A., Comerford M.S. and Egan S.P. 2018. "Closing the life cycle" of Andricus quercuslanigera (Hymenoptera: Cynipidae). Annals of the Entomological Society of America, 111(3): 103–113. https://doi.org/10.1093/aesa/say005

Ivanova-Kazas O.M. 1977. Asexual reproduction of animals. Leningrad University, Leningrad, 240 p. [In Russian].

Ivanova-Kazas O.M. 1981. Comparative embryology of invertebrates. Part 6. Atelocerata. Nauka, Moscow, 207 p. [In Russian].

Ivanova-Kazas O.M. 1995. Evolutionary embryology of animals. Nauka, St. Petersburg, 565 p. [In Russian].

Klymiuk A.A. and Stockey R.A. 2012. A lower Cretaceous (Valanginian) seed cone provides the earliest fossil record for Picea (Pinaceae). American Journal of Botany, 99: 1069–1082. https://doi.org/10.3732/ajb.1100568

Kranz B.D., Schwarz M.P., Morris D.C. and Crespi B.J. 2002. Life history of Kladothrips ellobus and Oncothrips rodwayi: insight into the origin and loss of soldiers in gall-inducing thrips. Ecological Entomology, 27: 49–57. https://doi.org/10.1046/j.1365-2311.2002.0380a.x

Kuznetsova V.G., Gavrilov-Zimin I.A., Grozeva S.M. and Golub N.V. 2021. Comparative analysis of chromosome numbers and sex chromosome systems in Paraneoptera (Insecta). Comparative Cytogenetics, 15(3): 279–327. https://doi.org/10.3897/CompCytogen.v15.i3.71866

Mamontova V.A. 1991. Suborder Aphidinea – Aphids. In: E.N. Savchenko (Ed.). Gall-inducing insects of agricultural and wild plants of European part of USSR. Homoptera, Lepidoptera, Coleoptera, Heteroptera. Naukova Dumka, Kiev: 46–123. [In Russian].

Mamontova V.A. 2008. Evolution, phylogenesis, system of the aphid family lachnidae (Homoptera: Aphidoidea). Naukova Dumka, Kiev, 207 p. [In Russian].

Mamontova V.A. 2012. Aphids of the family Lachnidae (Homoptera: Aphidoidea) of the fauna of Eastern Europe and neighboring territories. Naukova Dumka, Kiev, 390 p. [In Russian].

Marchal P. 1913. Contribution à l’étude de la biologie des Chermes. Annales des Scienses Naturelles (Zoologie), 18: 153–385.

Moran N.A. 1992. The evolution of aphid life cycles. Annual Review of Entomology, 37: 321–348. https://doi.org/10.1146/annurev.en.37.010192.001541

Mordwilko A. 1901. On the biology and morphology of aphids (fam. Aphididae Pass.). M. Stasyulevich Publisher, St. Petersburg, 947 p. [In Russian].

Noordam D. 2004. Aphids of Java. Part V: Aphidini. Zoologische Verhandelingen, 346: 7–206.

Orlando E. 1974. Sex determination in Megoura viciae Bukton (Homoptera Aphididae). Monitore Zoologico Italiano, 8(1–2): 61–70.

Ortiz-Rivas B. and Martínez-Torres D. 2010. Combination of molecular data support the existence of three main lineages in the phylogeny of aphids (Hemiptera: Aphididae) and the basal position of the subfamily Lachninae. Molecular Phylogenetics and Evolution, 55(1): 305–317. https://doi.org/10.1016/j.ympev.2009.12.005

Ostrovsky A.N., Lidgard S., Gordon D.P., Schwaha T., Genikhovich G. and Ereskovsky A.V. 2016. Matrotrophy and placentation in invertebrates: a new paradigm. Biological Reviews, 91: 673–711. https://doi.org/10.1111/brv.12189

Otto S.P. 2009. The evolutionary enigma of sex. American Naturalist, 174 (Suppl. 1): S1–S14. https://doi.org/10.1086/599084

Ozaki K. 2000. Insect-plant interactions among gall size determinants of adelgids. Ecological Entomology, 25: 452–459. https://doi.org/10.1046/j.1365-2311.2000.00281.x

Pergande T. 1904. North American Phylloxerinae affecting Hicoria (Carya) and other trees. Proceedings of Davenport Academia of Sciences, 9: 185–273. https://doi.org/10.5962/bhl.title.54119

Perotti M., Young D. and Braig H. 2016. The ghost sex-life of the paedogenetic beetle Micromalthus debilis. Scientific Reports, 6: 27364. https://doi.org/10.1038/srep27364

Popova A.A. 1967. The types of aphid adaptations to feeding on their host plants. Nauka, Leningrad, 291 p. [In Russian].

Qiao G.X., Zhang G.X. and Cao Y. 2001. The genus Neophyllaphis Takahashi (Homoptera: Aphididae) from China with description of one new species. Oriental Insects, 35(1): 91–96. https://doi.org/10.1080/00305316.2001.10417290

Raske A.G. and Hudson A.C. 1964. The development of Pineus strobi (Hartig) (Adelginae, Phylloxeridae) on white pine and black spruce. The Canadian Entomologist, 96(4): 599–616. https://doi.org/10.4039/Ent96599-4

Rohfritsch O. 1992. Patterns in gall development. In: J.D. Shorthouse and O. Rohfritsch (Eds). Biology of insect-induced galls. Oxford University Press, Oxford, NY: 60–86. [Cited after Tabuchi et al. 2009]

Shaposhnikov G.Ch. 1964. Suborder Aphidinea – Aphids. In: G.Ya. Bei-Bienko (Ed.). Keys to the insects of European part of USSR. Vol. 1. Nauka, Moscow–Leningrad: 489–616. [In Russian].

Shaposhnikov G.Ch. 1979. Oligomerization, polymerization and organization of morphological structures in the evolution of aphids. Entomologicheskoe Obozrernie, 58: 718–741.

Shaposhnikov G.Ch. 1987. Evolutionary estimation of taxa. In: A.K. Minks and P. Harrewijn (Eds). Aphids. Their biology, natural enemies and control. Volume A. Elsevier, Amsterdam, Oxford, New York, Tokyo: 401–408.

Shcherbakov D.E. 2007. Extinct four-winged precoccids and the ancestry of scale insects and aphids (Hemiptera). Russian Entomological Journal, 16(1): 47–62.

Simon J.-Ch., Rispe C. and Sunnucks P. 2002. Ecology and evolution of sex in aphids. Trends in Ecology & Evolution. 17(1): 34–39. https://doi.org/10.1016/S0169-5347(01)02331-X

Smith J.M. 1978. The evolution of sex. Cambridge University Press, Cambridge. 242 p.

Steffan A.W. 1968. Evolution und Systematik der Adelgidae (Homoptera: Aphidina): Eine Verwandtschaftsanalyse auf vorwiegend ethologischer, zytologischer und karyologischer Grundlage. Zoologica, 115: 1–139. https://doi.org/10.1002/mmnd.4820280408

Stoetzel M.B. 1985a. Host alternation: a newly discovered attribute of the Phylloxeridae (Homoptera: Aphidoidea). Proceedings of Entomological Society of Washington, 87: 265–268.

Stoetzel M.B. 1985b. Pupiform larvae in the Phylloxeridae (Homoptera: Aphidoidea). Proceedings of Entomological Society of Washington, 87: 535–537.

Stone G.N., Schonrogge K., Atkinson R.J., Bellido D. and Pujade-Villar J. 2002. The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology, 47: 633–68. https://doi.org/10.1146/annurev.ento.47.091201.145247

Tabuchi K., Sano M. and Ozaki K. 2009. Delayed larval development without summer diapause in a galling adelgid (Hemiptera: Adelgidae). Annals of the Entomological Society of America, 102(3): 456–461. https://doi.org/10.1603/008.102.0315

Walton L. 1980. Gall formation and life history of Pineus floccus (Patch) (Homoptera: Aphidoidea) in Virginia. Virginia Journal of Science, 31: 55–60.

Wegierek P. 1992. Relationships within Aphidomorpha on the basis of thorax morphology. Wydawnictwo Uniwersytetu, Katowice, 106 p.

White M.J.D. 1973. Animal cytology and evolution. Cambridge University Press, Cambridge, 961 p.

Wilson A.C.C., Sunnucks P. and Hales D.F. 2003. Heritable genetic variation and potential for adaptive evolution in asexual aphids (Aphidoidea). Biological Journal of the Linnean Society, 79(1): 115–135. https://doi.org/10.1046/j.1095-8312.2003.00176.x

Wojciechowski W. 1992. Studies on the systematic system of aphids (Homoptera, Aphidinea). Uniwersytet Slaski, Katowice, 75 p.

Wool D. 2005. Gall-inducing aphids: biology, ecology, and evolution. In: A. Raman, C.W. Schaefer and T.M. Withers (Eds). Biology, ecology, and evolution of gall-inducing arthropods. Enfield, Science Publishers, 73–132.

Yan Sh., Wang W. and Shen J. 2020. Reproductive polyphenism and its advantages in aphids: switching between sexual and asexual reproduction. Journal of Integrative Agriculture, 19(6): 1447–1457. https://doi.org/10.1016/S2095-3119(19)62767-X

Zhang J.B., Li R.Q., Xiang X.G., Manchester S.R., Lin L., Wang W., Wen J. and Chen Z.D. 2013. Integrated fossil and molecular data reveal the biogeographic diversification of the eastern Asian-eastern North American disjunct hickory genus (Carya Nutt.). PLoS One, 8(7): e70449. https://doi.org/10.1371/journal.pone.0070449