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Aphid–Buchnera–Ant symbiosis; or why are aphids rare in the tropics and very rare further south?

Published online by Cambridge University Press:  09 January 2018

Evgeny Perkovsky  and
Piotr Wegierek
Evgeny Perkovsky*
Affiliation:
Schmalhausen Institute of Zoology, National Academy of Sciences of Ukraine, ul. Bogdana Khmel'nitskogo 15, Kiev 01601, Ukraine. Email: perkovsk@gmail.com
Piotr Wegierek
Affiliation:
Department of Zoology, University of Silesia, Bankowa 9, 40-007 Katowice, Poland. Email: piotr.wegierek@us.edu.pl
*
*Corresponding author
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Abstract

At least since the Cretaceous Terrestrial Revolution, the geographical distribution of aphids, particularly in the Northern Hemisphere, has been strongly affected by the low thermal tolerance of their obligatory bacterial symbiont, Buchnera aphidicola, which was why the aphids switched to obligate parthenogenesis in low latitudes. Hormaphidids and greenideids penetrated into the tropics only after the Oligocene strengthening of climate seasonality, and specialisations of the tropical representatives of these families did not allow them to spread further south (in the case of cerataphidines), or only allowed in few cases (in the case of greenideids).

Aphids suffered from the Mesozoic–Cenozoic boundary extinction event much more strongly than other insects. The extinction was roughly coincidental with the establishment of the tight symbiosis of aphids with formicine and dolichoderine ants, which was accompanied by the flourishing of all three groups.

In the Cretaceous, all of the representatives of extant and subfamilies occupied positions that were subordinate to Armaniinae and Sphecomyrminae. Prior to large ant colonies evolving their efficient ant–aphid mutualism, the aphids remained unprotected before the growing ant predation. The origin of the aphid trophobiosis with large colonies of Formicinae and Dolichoderinae has resulted in the steep decline of aphids left beyond that ant–aphid symbiotic network. By at least the basal Eocene (unlike the Late Cretaceous), ant proportions in the entomofauna increased sharply, and evident dominants emerged. Even now, aphid milkers from small colonies (hundreds of specimens) never protect their symbionts, and homopteran-tending ants are more likely to be dominant, with large colonies of 104–105 workers.

The mutualistic ant–aphid system failed to cross the tropical belt during the Cenozoic because of Buchnera's low heat tolerance. As a result, the native southern temperate aphid fauna consists now of seven genera only, five of which are Late Cretaceous relicts. Some of them had relatives in Late Cretaceous amber of the Northern Hemisphere.

Keywords

AphidoideaBuchnera aphidicolacoevolutionFormicidaegeographical and geological distribution
Type
Articles
Information
Earth and Environmental Science Transactions of The Royal Society of Edinburgh , Volume 107 , Issue 2-3: Fossil Insects, Arthropods and Amber , June 2016 , pp. 297 - 310
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Copyright © The Royal Society of Edinburgh 2018 

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References

6. References

Agarwala, B. K. & Dixon, A. F. G. 1986. Population trends of Cervaphis schouteniae on Microcos paniculata and its relevance to the paucity of aphid species in India. Indian Biologist 18, 37–39.Google Scholar
Archibald, S. B., Johnson, K. R., Mathewes, R. W. & Greenwood, D. R. 2011. Intercontinental dispersal of giant thermophilic ants across the Arctic during early Eocene hyperthermals. Proceedings of the Royal Society B 278, 3679–88.10.1098/rspb.2011.0729Google Scholar
Baranov, V. A., Andersen, T. & Perkovsky, E. E. 2015. Orthoclads from Eocene Amber from Sakhalin (Diptera: Chironomidae, Orthocladiinae). Insect Systematics & Evolution 46(4), 359–78.Google Scholar
Blackman, R. L. & Eastop, V. 2006. Aphids on World's herbaceous plants and shrubs. Chichester: Wiley. Available: http://www.aphidsonworldsplants.infoGoogle Scholar
Blakey, R. 2011. Global Paleogeography (accessed 15.12.14.). http://cpgeosystems.com/paleomaps.html.Google Scholar
Bodenheimer, F. S. & Swirski, E. 1957. The Aphidoidea of the Middle East. Jerusalem: Weizmann Science Press. 378 pp.Google Scholar
Braendle, C., Miura, T., Bickel, R., Shingleton, A. W., Kambhampati, S. & Stern, D. L. 2003. Developmental origin and evolution of bacteriocytes in the aphid – Buchnera symbiosis. PLoS Biology 1, 70–76.Google Scholar
Buchner, P. 1965. Endosymbiosis of animals with plant microorganisms. New York: John Wiley. 909 pp.Google Scholar
Burke, G, Fiehn, O. & Moran, N. 2010. Effects of facultative symbionts and heat stress on the metabolome of pea aphids. The ISME Journal: Multidisciplinary Journal of Microbial Ecology 4, 242–52.10.1038/ismej.2009.114Google Scholar
Charles, H. & Ishikawa, H. 1999. Physical and Genetic Map of the Genome of Buchnera, the Primary Endosymbiont of the Pea Aphid Acyrthosiphon pisum. Journal of Molecular Evolution 48, 142–50.10.1007/PL00006452Google Scholar
Chen, Ch.-Y., Lai, Ch.-Y. & Kuo, M.-H. 2009. Temperature effect on the growth of Buchnera endosymbiont in Aphis craccivora (Hemiptera: Aphididae). Symbiosis 49, 53–59.10.1007/s13199-009-0011-4Google Scholar
Chen, D.-Q., Montllor, C. B. & Purcell, A. H. 2000. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomologia Experimentalis et Applicata 95, 315–23.Google Scholar
Cholodkovsky, N. 1899. Aphidologische Mitteilungen. Zoologischer Anzeiger 22(602), 468–77.Google Scholar
Coiffard, C., Gomez, B., Daviero-Gomez, V. & Dilcher, D. L. 2012. Rise to dominance of angiosperm pioneers in European Cretaceous environments. Proceedings of the National Academy of Sciences of the United States of America 109, 20955e20959.Google Scholar
Davies, T. J., Barraclough, T. G., Chase, M. W., Soltis, P. S., Soltis, D. E. & Savolainen, V. 2004. Darwin's abominable mystery: insights from a supertree of the angiosperms. Proceedings of the National Academy of Sciences of the United States of America 101, 1904–09.10.1073/pnas.0308127100Google Scholar
Dedryver, Ch.-A., Hulle, M., Le Gallic, J.-F., Caillaud, M. C. & Simon, J. C. 2001. Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae. Oecologia 128, 379–88.10.1007/s004420100674Google Scholar
del Guercio, G. 1909. Contribuzione alla conoscenza dei Lacnidi Italiani. Morphologia, sistematica, biologia generale e loro importanza economica. Redia 5, 173–243.Google Scholar
Depa, Ł., Mróz, E. & Szawaryn, K. 2012. Molecular identity of Stomaphis quercus (Hemiptera: Aphidoidea: Lachnidae) and description of a new species. European Journal of Entomology 109(3), 435–44.Google Scholar
Depa, Ł., Kanturski, M., Junkiert, Ł. & Wieczorek, K. 2015. Giant females vs. dwarfish males of the genus Stomaphis Walker (Hemiptera: Aphididae) – an aphid example of the ongoing course to permanent parthenogenesis? Arthropod Systematics and Phylogeny 73(1), 19–40.Google Scholar
Dilcher, D. 2000. Toward a new synthesis: major evolutionary trends in angiosperm fossil record. Proceedings of the National Academy of Sciences of the United States of America 97, 7030–36.10.1073/pnas.97.13.7030Google Scholar
Dixon, A. F. G. 1985. Aphid ecology an Optimization Approach. Glasgow: Blackie and Sons. 157 pp.Google Scholar
Dixon, A. F. G. 1987. The way of life of aphids: host specificity, speciation and distribution. In Minks, A. K. & Harrewijn, P. (eds) Aphids their biology, natural enemies and control, 197–207. Amsterdam: Elsevier Science Publishers. xx+450 pp.Google Scholar
Dixon, A. F. G. 1998. Aphid ecology an Optimization Approach. 2nd Edition. London: Chapman and Hall. 300 pp.Google Scholar
Dixon, A. F. G., Kindlmann, P., Lepš, J. & Holman, J. 1987. Why there so few species of aphids, especially in the tropics. American Naturalist 129, 580–92.Google Scholar
Dixon, A. F. G., Holman, J. & Thieme, T. 1998. Sex and size in aphids. In Nieto Nafría, J. M. & Dixon, A. F. G. (eds) Aphids in Natural and Managed Ecosystems, 173–78. León, Spain: Universidad de León, Secretariado de Publicaciones. 688 pp.Google Scholar
Dlussky, G. M. 1981. [Miocene ants (Hymenoptera, Formicidae) of the USSR]. Trudy Paleontologicheskogo Instituta Akademii Nauk SSSR 183, 64–83. [In Russian.]Google Scholar
Dlussky, G. M. 1983. [A new family of Upper Cretaceous Hymenoptera: an “intermediate link” between ants and Scolioidea.] Paleontologicheskii Zhurnal 3, 65–78. [In Russian. English translation: Paleontological Journal 17(3), 63–76.]Google Scholar
Dlussky, G. M. & Rasnitsyn, A. P. 2003. Ants (Hymenoptera: Formicidae) of Formation Green River and some other Middle Eocene deposits of North America. Russian Entomological Journal 11, 411–36.Google Scholar
Dlussky, G. M. & Rasnitsyn, A. P. 2007. [Paleontological record and stages of ant evolution.] Uspehi Sovremennoi Biologii 127(2), 118–34. [In Russian.]Google Scholar
Douglas, A. E. 2006. Phloem-sap feeding by animals: problems and solutions. Journal of Experimental Botany 57(4), 747–54.10.1093/jxb/erj067Google Scholar
Drinnan, A. N. & Chambers, T. C. 1986. Flora of the Lower Cretaceous Koonwarra Fossil Bed (Korumburra Group), South Gippsland, Victoria. Memoirs of the Association of Australasian Palaeontologists 3, 1–77.Google Scholar
Dunbar, H. E., Wilson, A. C. C., Ferguson, N. R. & Moran, N. A. 2007. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biology 5(5), e96.10.1371/journal.pbio.0050096Google Scholar
Durak, R. & Durak, T. 2015. Redescription of males of the aphid species Cinara (Cupressobium) tujafilina and Cinara (Cupressobium) cupressi (Hemiptera, Lachninae). Zootaxa 4032(2), 209–14.10.11646/zootaxa.4032.2.7Google Scholar
Eisner, T. & Wilson, E. O. 1952. The Morphology of the Proventriculus of a Formicine Ant. Psyche 59(2), 47–60.10.1155/1952/14806Google Scholar
Evans, G. A. 2008. The whiteflies (Hemiptera: Aleyrodidae) of the World and their host plants and natural enemies. Version 2008-09-23. http://www.sel.barc.usda.gov.591/WF/world-whitefly-catalog.pdf. Accessed 14 October 2014.Google Scholar
Feder, M. E. & Hofmann, G. E. 1999. Heat-shock proteins, molecular chaperones, and the stress response: Evolutionary and ecological physiology. Annual Review of Physiology 61, 243–82.Google Scholar
Fukatsu, T., Aoki, S., Kurosu, U. & Ishikawa, H. 1994. Phylogeny of Cerataphidini Aphids Revealed by Their Symbiotic Microorganisms and Basic Structure of Their Galls: Implications for Host–Symbiont Coevolution and Evolution of Sterile Soldier Castes. Zoological Science 11, 613–23.Google Scholar
Funk, D. J., Wernegreen, J. J. & Moran, N. A. 2001. Intraspecific variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics 157(2), 477–89.Google Scholar
García Morales, M., Denno, B. D., Miller, D. R., Miller, G. L., Ben-Dov, Y. & Hardy, N. B. 2016. ScaleNet: A literature-based model of scale insect biology and systematics. Database. doi: 10.1093/database/bav118. http://scalenet.info.Google Scholar
Gavrilov-Zimin, I. A., Stekolshchikov, A. V. & Gautam, D. C. 2015. General trends of chromosomal evolution in Aphidococca (Insecta, Homoptera, Aphidinea+Coccinea). Comparative Cytogenetics 9(3), 335–422.Google Scholar
Hales, D. F. 1989. The chromosomes of Schoutedenia lutea (Homoptera, Aphidoidea, Greenideinae), with an account of meiosis in the male. Chromosoma 98, 295–300.Google Scholar
Hales, D. F., Tomiuk, J., Wörhmann, K. & Sunnucks, P. 1997. Evolutionary and genetic aspects of aphid biology: a review. European Journal of Entomology 94, 1–55.Google Scholar
Hardy, N. B., Peterson, D. A. & Dohlen, C. D. 2015. The evolution of life cycle complexity in aphids: ecological optimization, or historical constraint? Evolution 69, 1423–32.10.1111/evo.12643Google Scholar
Harris, M. 1766. The Aurelian, or Natural History of English Insects; namely Moths and Butterflies. Together with the Plants on which they feed. A faithful Account of their respective Changes; their usual Haunts when in the winged State; and their standard names, as given and established by the worthy and ingenious Society of Aurelians. Drawn, engraved and coloured, from the natural subjects themselves. By Moses Harris, Secretary to the Aurelian Society. London: printed for the author. 92 pp; 44 col. pics.Google Scholar
Heie, O. E. 1967. Studies on fossil aphids (Homoptera: Aphidoidea), especially in the Copenhagen collection of fossils in Baltic amber. Spolia zoologica Musei Hauniensis 26, 1–274.Google Scholar
Heie, O. E. 1980. The Aphidoidea (Hemiptera) of Fennoscandia and Danmark. I General Part. The Families Mindaridae, Hormaphididae, Thelaxidae, Anoecidae and Pemphigidae. Fauna Entomologica Scandinavica 9, 1–236.Google Scholar
Heie, O. E. 1994. Why are there so few aphid species in the temperate areas of the southern hemisphere? European Journal of Entomology 91, 127–33.Google Scholar
Heie, O. E. 2009. Aphid mysteries not yet solved (Hemiptera: Aphidomorpha). Aphids and Other Hemipterous Insects 15, 31–48.Google Scholar
Heie, O. E. & Pike, E. M. 1992. New aphids in Cretaceous amber from Alberta (Insecta, Homoptera). Canadian Entomologist 124(6), 1027–53.10.4039/Ent1241027-6Google Scholar
Heie, O. E. & Wegierek, P. 2009. A classification of the Aphidomorpha (Hemiptera Sternorrhyncha) under consideration of the fossil taxa. Redia 92, 69–77.Google Scholar
Heie, O. E. & Wegierek, P. 2011. A list of fossil aphids (Hemiptera, Sternorrhyncha, Aphidomorpha). Monographs of the Upper Silesian Museum 6. 82 pp.Google Scholar
Herman, A. B., Akhmetiev, M. A., Kodrul, T. M., Moiseeva, M. G. & Yakovleva, A. I. 2009. Flora development in Northeastern Asia and Northern Alaska during the Cretaceous-Paleogene transitional epoch. Stratigraphy and Geological Correlation 17(1), 79–97.Google Scholar
Ivanov, V. D., Melnitsky, S. I. & Perkovsky, E. E. 2016. [Caddisflies from Cenozoic resins of Europe.] Paleontologicheskii Zhurnal 5, 33–61. [In Russian. English translation: Paleontological Journal 50(5), 485–93.]Google Scholar
Johnson, K. R. 2002. Megaflora of the Hell Creek and lower Fort Union Formations in the western Dakotas: vegetational response to climate change, the Cretaceous–Tertiary boundary event, and rapid marine transgression. Geological Society of America, Special Paper 361, 329–91.Google Scholar
Kania, I. & Wegierek, P. 2008. Palaeoaphididae (Hemiptera, Sternorrhyncha) from Lower Cretaceous Baissa deposits. Morphology and Classification. Kraków: Instytut Systematyki i Ewolucji Zwierząt Polskiej Akademii Nauk. 133 pp.Google Scholar
Kawada, K. 1987. Polymorphism and morph determination. In Minks, A. K. & Harrewijn, P. (eds) Aphids their biology, natural enemies and control, 255–68. Amsterdam: Elsevier Science Publishers. 384 pp.Google Scholar
Khramov, A. V., Liu, Q., Zhang, H. & Jarzembowski, E. A. 2016. Early green lacewings (Insecta: Neuroptera: Chrysopidae) from the Jurassic of China and Kazakhstan. Papers in Palaeontology 2(1), 25–39.Google Scholar
Koch, C. L. 1857. Die Pflanzenläuse Aphiden getreu nach dem Leben abgebildet und beschrieben. Nürnberg: J. L. Lotzbeck. 335 pp.Google Scholar
Kodrul, T. M. 1999. Paleogenovaja fitostratigraphija Juzhnogo Sakhalina. [.] Transactions of GIN RAS 519, 1–150. [In Russian.]Google Scholar
Kononova, E. L. 1976. [Extinct aphid families (Homoptera, Aphidinea) of the Late Cretaceous.] Paleontologicheskii Zhurnal 3, 117–26. [In Russian. English translation: Paleontological Journal 10(3), 352–60.]Google Scholar
Kononova, E. L. 1977. [New species of aphids (Homoptera, Aphidinea) from the Upper Cretaceous deposits of the Taimyr.] Entomologicheskoe Obozrenie 56(3), 588–600. [In Russian.]Google Scholar
Kurosu, U., Buranapanichpan, S. & Aoki, S. 2006. Astegopteryx spinocephala (Hemiptera: Aphididae), a new aphid species producing sterile soldiers that guard eggs laid in their gall. Entomological Science 9, 181–90.10.1111/j.1479-8298.2006.00165.xGoogle Scholar
LaPolla, J. S., Dlussky, G. M. & Perrichot, V. 2013. Ants and the Fossil Record. Annual Review of Entomology 58, 609–30.Google Scholar
LaPolla, J. S. & Greenwalt, D. E. 2015. Fossil Ants (Hymenoptera: Formicidae) of the Middle Eocene Kishenehn Formation. Sociobiology 62(2), 163–74.10.13102/sociobiology.v62i2.163-174Google Scholar
Lichtenstein, J. 1882. Coccus lataniae=Boisduvalia lataniae=Cerataphis lataniae. Annales de la Société Entomologique de France 2, XVI.Google Scholar
Linnaeus, C. 1758. Systema naturae per regna tria naturae secundum classes,ordines, genera, species, cum characteribus, differentiis, synonymis, locis, 10th ed., vol. 1. Holmiae: Impensis Laurentii Salvii. 824 pp.Google Scholar
Ma, C.-S., Hau, B. & Poehling, H.-M. 2004. The effects of heat stress on the survival of the rose grain aphid, Metopolophium dirhodum (Hemiptera: Aphididae). European Journal of Entomology 101, 327–31.Google Scholar
Magallon, S. & Castillo, A. 2009. Angiosperm diversification through time. American Journal of Botany 96, 349–65.Google Scholar
Martin, S. K., Skidmore, L. I. & Stilwell, J. D. 2016. A first record of Cretaceous aphids (Hemiptera, Sternorrhyncha, Aphidomorpha) in Australia, from the Lower Cretaceous Koonwarra Fossil Bed, Victoria. Zootaxa 4137, 95–107.Google Scholar
Martinez-Torres, D., Buades, C., Latorre, A & Moya, A. 2001. Molecular Systematics of Aphids and Their Primary Endosymbionts. Molecular Phylogenetics and Evolution 20(3), 437– 49.Google Scholar
McDonald, M. J., Rice, D. P. & Desai, M. M. 2016. Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531, 233–36.10.1038/nature17143Google Scholar
Michalik, A., Szklarzewicz, T., Jankowska, W. & Wieczorek, K. 2014. Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): ultrastructure, distribution and transovarial transmission. European Journal of Entomology 111(1), 91–104.Google Scholar
Montllor, C. B., Maxmen, A. & Purcell, A. H. 2002. Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entomology 27(2), 189–95.Google Scholar
Moran, N. A. 1992. The evolution of life cycles in aphids. Annual Review of Entomology 37, 321–48.Google Scholar
Moran, N. A., Munson, M. A., Baumann, P. & Ishikawa, H. 1993. A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proceedings of the Royal Society, London B 253, 167–71.Google Scholar
Moran, N. A., McCutcheon, J. P. & Nakabachi, A. 2008. Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165–90.Google Scholar
Moran, N. A. & Baumann, P. 1994. Phylogenetics of cytoplasmically inherited micro-organisms of arthropods. Trends in Ecology & Evolution 9, 15–20.Google Scholar
Moran, N. A. & Yun, Y. 2015. Experimental replacement of an obligate insect symbiont. Proceedings of the National Academy of Sciences of the United States of America 112(7), 2093–96.10.1073/pnas.1420037112Google Scholar
Mordvilko, A. K. 1914. Insectes Hémiptères (Insecta Hemiptera). I. Aphidodea. Faune de la Russie et des pays limitrophes fondée principalement sur les collectionnes du Musée Zoologique de l'Académie Impériale des Sciences de Petrograd Livraison 1, I–CLXIV, 1–236, 1–9.Google Scholar
Nieto Nafría, J. M. & Favret, C. (eds). 2011. Register of 12 family-group and genus-group taxa of Aphidoidea (Hemiptera Sternorrhyncha). León, Spain: Universidad de León, Secretariado de Publicaciones. 465 pp.Google Scholar
Novgorodova, T. A. 2015. Organization of honeydew collection by foragers of different species of ants (Hymenoptera: Formicidae): Effect of colony size and species specificity. European Journal of Entomology 112(4), 688–97.10.14411/eje.2015.077Google Scholar
Offenberg, J. 2001. Balancing between mutualism and exploitation: the symbiotic interaction between Lasius ants and aphids. Behavioral Ecology & Sociobiology 49, 304–10.Google Scholar
Oliver, T. H., Leather, S. R. & Cook, J. M. 2008. Macroevolutionary patterns in the origin of mutualisms involving ants. Journal of Evolutionary Biology 21, 1597–1608.Google Scholar
Otto, S. P. 2009. The evolutionary enigma of sex. The American Naturalist 174, Suppl. 1, S1–S14.Google Scholar
Ouvrard, D. 2016. Psyl'list – The World Psylloidea Database. http://www.hemiptera-databases.com/psyllist - searched on 18 October 2016 doi:10.5519/0029634Google Scholar
Pérez-Brocal, V., Gil, R., Ramos, S., Lamelas, A., Postigo, M., Michelena, J. M., Silva, F. J., Moya, A. & Latorre, A. 2006. A small microbial genome: the end of a long symbiotic relationship? Science 314, 312–13.10.1126/science.1130441Google Scholar
Perkovsky, E. E. 2010. [Participation of Germaraphis aphids (Homoptera, Aphidinea) in weight fractions of the Rovno amber and their syninclusions with ants.] Vestnik zoologii 44(1), 55–62. [In Russian, with English Abstract.]Google Scholar
Perkovsky, E. E. 2011. Syninclusions of the Eocene winter ant Prenolepis henshei (Hymenoptera: Formicidae) and Germaraphis aphids (Hemiptera: Eriosomatidae) in Late Eocene Baltic and Rovno amber: some implications. Russian Entomological Journal 20(3), 303–13.10.15298/rusentj.20.3.15Google Scholar
Perkovsky, E. E. 2012. [On influence of latitudinal changes in summer temperatures on the Late Eocene aphids Germaraphis (Homoptera, Aphidoidea) and on their symbiotic relationships with ants.] Vestnik zoologii 46(1), 51–58. [In Russian, with English Abstract.]Google Scholar
Perkovsky, E. E., Rasnitsyn, A. P., Vlaskin, A. P. & Taraschuk, M. V. 2007. A comparative analysis of the Baltic and Rovno amber arthropod faunas: representative samples. African Invertebrates 48(1), 229–45.Google Scholar
Perkovsky, E. E., Zosimovich, V. Yu. & Vlaskin, A. P. 2010. Rovno amber. In Penney, D. (ed.) Biodiversity of Fossils in Amber from the Major World Deposits, 116–36. Manchester: Siri Scientific Press. 304 pp.Google Scholar
Perkovsky, E. E., Rasnitsyn, A. P., Vlaskin, A. P. & Rasnitsyn, S. P. 2012. [Contribution to the study of the structure of amber forest communities based on analysis of syninclusions in the Rovno Amber (Late Eocene of Ukraine).] Paleontologicheskii Zhurnal 3, 70–78. [In Russian. English translation: Paleontological Journal 46(3), 293–301.]Google Scholar
Perkovsky, E. E. & Makarkin, V. N. 2015. First confirmation of spongillaflies (Neuroptera: Sisyridae) from the Cretaceous. Cretaceous Research 56, 363–71.Google Scholar
Perkovsky, E. E. & Wegierek, P. 2015. [On causes of mass extinction of Late Cretaceous aphids.] Palaeontonology: Communities and crises, 22–24. Conference dedicated to the 70th anniversary (memory) of V. V. Zherikhin. Abstracts. Moscow: Borissiak Paleontological Institute of the Russian Academy of Sciences. [In Russian.]Google Scholar
Perrichot, V., Wang, B. & Engel, M. S. 2016. Extreme Morphogenesis and Ecological Specialization among Cretaceous Basal Ants. Current Biology. http://dx.doi.org/10.1016/j.cub.2016.03.075Google Scholar
Poinar, G.O. Jr. & Brown, A. E. 2005. New Aphidoidea (Hemiptera: Sternorrhyncha) in Burmese amber. Proceedings of the Entomological Society of Washington 107, 835–45.Google Scholar
Ponomarenko, A. G. 1998. [Paleobiology of angiospermization.] Paleontologicheskii Zhurnal 4, 3–10. [In Russian. English translation: Paleontological Journal 32(4), 325–31.]Google Scholar
Popov, G. V. 2015. Syrphidae from the Cretaceous – refuted? 8th International Symposium on Syrphidae, Monschau, Germany 4–8 June 2015, Abstracts, 47.Google Scholar
Rasnitsyn, A. P., Bashkuev, A. S., Kopylov, D. S., Lukashevich, E. D, Ponomarenko, A. G., Popov, Yu. A., Rasnitsyn, D. A., Ryzhkova, O. V., Sidorchuk, E. A., Sukatsheva, I. D. & Vorontsov, D. D. 2016. Sequence and scale of changes in the terrestrial biota during the Cretaceous (based on materials from fossil resins). Cretaceous Research 61, 234–55.Google Scholar
Rasnitsyn, A. P. & Quicke, D. L. (eds) 2002. History of Insects. Dordrecht: Kluwer Academic Publishers. xii+517 pp.Google Scholar
Rayner, R. J., Bamford, M. K., Brothers, D. J., Dippenaar-Schoeman, A. S., Mckay, I. J., Oberprieler, R. G. & Waters, S. B. 1998 (1997). Cretaceous fossils from the Orapa diamond mine. Palaeontologica Africana 33, 55–65.Google Scholar
Rich, T. H., Rich, P. V., Wagstaff, B., McEwen-Mason, J., Douthitt, C. B. & Gregory, R. T. 1989. Early Cretaceous biota from the northern side of the Australo–Antarctic rift valley. Geological Society, London, Special Publications 47, 121–30.10.1144/GSL.SP.1989.047.01.10Google Scholar
Rosengren, R. & Sundström, L. 1987. The foraging system of a redwood ant colony (Formica s. str.) – collecting and defending food through an extended phenotype. Experientia Supplementum. 54, 117–37.Google Scholar
Rübsaamen, E. H. 1905. Beiträge zur Kenntnis Aussereuropäischer Zoocecidien. I, Gallen von Bismark Archipel. Marcellia 4, 5–25.Google Scholar
Russell, J. A. & Moran, N. A. 2006. Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society, London B 273, 603–10.10.1098/rspb.2005.3348Google Scholar
Rust, J. & Andersen, N. M. 1999. Giant ants from the Paleogene of Denmark, with a discussion of the fossil history and early evolution of ants (Hymenoptera: Formicidae). Zoological Journal of the Linnean Society 125, 331–48.Google Scholar
Sakata, H. 1995. Density-dependent predation of the ant Lasius niger (Hymenoptera: Formicidae) on two attended aphids Lachnus tropicalis and Myzocallis kuricola (Homoptera: Aphididae). Researches on Population Ecology 37, 159–64.Google Scholar
Scudder, S. H. 1877. The first discovered traces of fossil insects in the American Tertiaries. Geological Survey of Canada. Report of Progress 3, 741–62.Google Scholar
Shingleton, A. W., Stern, D. L. & Foster, W. A. 2005. The origin of a mutualism: a morphological trait promoting the evolution of ant-aphid mutualisms. Evolution 59(4), 921–26.10.1111/j.0014-3820.2005.tb01766.xGoogle Scholar
Simon, J. C., Rispe, C. & Sunnucks, P. 2002. Ecology and evolution of sex in aphids. Trends in Ecology & Evolution 17(1), 34–39.Google Scholar
Simon, J. C., Stoeckel, S. & Tagu, D. 2010. Evolutionary and functional insights into reproductive strategies of aphids. Comptes Rendus Biologies 333, 488–96.10.1016/j.crvi.2010.03.003Google Scholar
Simonet, P., Duport, G., Gaget, K., Weiss-Gayet, M., Colella, S., Febvay, G., Charles, H., Viñuelas, J., Heddi, A. & Calevro, F. 2016. Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis. Scientific Reports 6, 19967.Google Scholar
Skaljac, M. 2016. Bacterial Symbionts of Aphids (Hemiptera: Aphididae). In Vilcinskas, A. (ed.) Biology and Ecology of Aphids, 100–26. Boka Raton: CRC Press. 282 pp.10.1201/b19967-6Google Scholar
Smith, J. M. & Maynard-Smith, J. 1978. The evolution of sex. Cambridge: University Press. 236 pp.Google Scholar
Sontag, E. 2003. Animal inclusions in a sample of unselected Baltic amber. Acta Zoologica Cracoviensia 46, 431–40.Google Scholar
Stadler, B. 1997. The relative importance of host plant, natural enemies and ants in the evolution of life-history characters of aphids. In Dettner, K., Bauer, G. & Vőlkl, W. (eds) Vertical food web interactions, 241–56. Berlin & Heidelberg: Springer-Verlag. xxii+390 pp.Google Scholar
Stadler, B. & Dixon, A. F. G. 2005. Ecology and evolution of aphid–ant interaction. Annual Review of Ecology Evolution and Systematics 36, 345–72.Google Scholar
Szwedo, J., Lapeyrie, J. & Nel, A. 2015. Rooting down the aphid's tree – the oldest record of the Aphidomorpha lineage from Palaeozoic (Insecta: Hemiptera). Systematic Entomology, 40(1), 207–13. doi: 10.1111/syen.12099Google Scholar
Tagu, D., Sabater-Muñoz, B. & Simon, J.-Ch. 2005. Deciphering reproductive polyphenism in aphids. Invertebrate Reproduction and Development 48, 71–80.Google Scholar
Takahashi, R. 1920. A new genus and species of aphid from Japan (Hem.). Canadian Entomologist 52(1), 19–20.Google Scholar
Tomiuk, J., Hales, D. F., Wőrhmann, K. & Morris, D. 1991. Genotypic variation and structure in Australian populations of the aphid Schoutedenia lutea. Hereditas 115, 17–23.Google Scholar
Unterman, B. M., Baumann, P. & McLean, D. L. 1989. Pea aphid symbiont relationships established by analysis of 16SrRNAs. Journal of Bacteriology 171, 2970–74.Google Scholar
van Ham, R. C. H. J., Kamerbeek, J., Palacios, C., Rausell, C., Abascal, F., Bastolla, U., Fernández, J. M., Jiménez, L., Postigo, M., Silva, F. J., Tamames, J., Viguera, E., Latorre, A., Valencia, A., Morán, F. & Moya, A. 2003. Reductive genome evolution in Buchnera aphidicola. Proceedings of the National Academy of Sciences of the United States of America 100(2), 581–86.10.1073/pnas.0235981100Google Scholar
Walker, F. 1870. Notes on aphides. The Zoologist, Second Series 5, 1996–2001.Google Scholar
Wang, H., Moore, M. J., Soltis, P. S., Bell, C. D., Brockington, S. F., Alexandre, R., Davis, C. C., Latvis, M., Manchester, S. R. & Soltis, D. E. 2009. Rosid radiation and the rapid rise of angiosperm-dominated forests. Proceedings of the National Academy of Sciences of the United States of America 106, 3853–58.Google Scholar
Watanabe, S, Murakami, T, Yoshimura, J, & Hasegawa, E. 2016. Color polymorphism in an aphid is maintained by attending ants. Science Advances 2(9), e1600606.10.1126/sciadv.1600606Google Scholar
Wegierek, P. & Mamontova, V. A. 1993. A new fossil species of the genus Stomaphis Walker (Aphidoidea: Lachnidae). Annals of the Upper Silesian Museum, Entomology Suppl. 1, 37–50.Google Scholar
Wieczorek, K., Kanturski, M. & Junkiert, L. 2013. The sexuales of giant black bark aphid, Pterochloroides persicae (Hemiptera, Aphidoidea: Lachninae). Zootaxa 3626, 94–98.Google Scholar
Wilcox, J. L., Dunbar, H. E., Wolfinger, R. D. & Moran, N. A. 2003. Consequences of reductive evolution for gene expression in an obligate endosymbiont. Molecular Microbiology 48, 1491–1500.Google Scholar
Wilson, E. O. & Hőlldobler, B. 2005. The rise of the ants: a phylogenetic and ecological explanation. Proceedings of the National Academy of Sciences of the United States of America 202, 7411–14.Google Scholar
Wőhrmann, K & Tomiuk, J. 1988. Life cycle strategies and genotypic variability in populations of aphids. Journal of Genetics 67(1), 43–52.10.1007/BF02927737Google Scholar