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European species of the aphid genus Eulachnus Del Guercio, 1909 (Hemiptera: Aphididae: Lachninae): revision and molecular phylogeny

MARIUSZ KANTURSKI, ŁUKASZ KAJTOCH, KARINA WIECZOREK

Abstract


The aphid genus Eulachnus in Europe is revised to include 12 species, using an integrative taxonomy approach, based on morphometric, molecular and biological traits. Fundatrix, apterous and alate viviparous female of a new species–Eulachnus stekolshchikovi Kanturski sp. nov. are described. Neotypes are designated for E. agilis, E. brevipilosus and E. nigricola. Lectotypes are designated for E. alticola, E. cembrae, E. rileyi and E. tuberculostemmatus. New synonyms are proposed: E. abameleki syn. nov. (= Cinara pini), E. cretaceus syn. nov. (= E. agilis), E. tauricus syn. nov. (= E. rileyi), E. pallidus syn. nov. (= E. tuberculostemmatus). Eulachnus mingazzinii (near Cinara piniphila) and E. nigrofasciatus (near C. brauni) are regarded as incertae sedis. Full species status is given for E. garganicus stat. nov. and E. ibericus stat. nov. Apterous viviparous female of E. cembrae; apterous and alate viviparous females of remaining species are redescribed. Sexual morphs of E. agilis, E. alticola, E. cembrae, E. intermedius, E. nigricola, E. rileyi and oviparous female of E. tuberculostemmatus are fully redescribed and figured for the first time. Fundatrices of E. agilis, E. brevipilosus, E. cembrae, E. rileyi and E. tuberculostemmatus, sexuales of E. brevipilosus and the alate male of E. tuberculostemmatus are described and figured. A new host plant–Pinus cembra for E. brevipilosus is reported, and this species is recorded for the first time from Czech Republic. Eulachnus tuberculostemmatus is reported for the first time from Croatia. Phylogenetic studies, based on the COI and ITS2 molecular markers, are provided to visualize and discuss the relationships within the European species. COI barcodes are provided for seven species.

 


Keywords


Hemiptera, aphids, COI, ITS2, morphological description, Eulachnini, molecular analysis, Palaearctic, Pinus spp., SEM

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References


Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215 (3), 403–10.
https://doi.org/10.1016/S0022-2836(05)80360-2

Baker, A.C. (1920) Generic classification of the hemipterous Aphididae. U.S. Department of Agriculture Bulletins, 826, 1–109.
https://doi.org/10.5962/bhl.title.108795

Binazzi, A. (1978) Contributi alla conoscenza degli afidi delle conifere. I. Le specie del genn. Cinara Curt., Schizolachnus Mordv., Cedrobium Remaud. ed Eulachnus d. Gu. presenti in Italia (Homoptera: Aphidoidea: Lachnidae). Redia, 61, 291–400.

Binazzi, A. (1983a) Contributi alla conoscenza degli afidi delle conifere. V. I Lacnidi del pino d'Aleppo con la descrizione di tre sottospecie nuove (Homoptera Aphidoidea Lachnidae). Redia, LXVI, 97–130.

Binazzi, A. (1983b) Contributi alla conoscenza degli afidi delle conifere. VI. Una nuova specie di Eulachnus appartenente al gruppo agilis e considerazioni sulle entità affini (Homoptera Aphidoidea Lachnidae). Redia, LXVI, 195–214.

Binazzi, A. (1989) Contributi alla conoscenza degli afidi delle conifere. X. Una nuova specie di Eulachnus del pino mugo e chiave per gli Eulacnini noti di tale conifera (Homoptera Aphidoidea Lachnidae). Redia, LXXII, 169–193.

Binazzi, A. (1990) Contributions to the knowledge of the conifer aphid fauna. XI. Taxonomical notes on some European pine living species of Cinara with reference to the Italian fauna (Homoptera Aphidoidea Lachnidae). Redia, LXXIII, 137–148.

Binazzi, A. (1996) Key to the alate viviparous females of the species of Eulachnus Del Guercio occurring in Italy (Aphididae Lachninae). Redia, LXXIX, Appendice, 1–6.

Binazzi, A. & Mier Durante, P. (1997) Una nueva subspecie espa˜nola de Eulachnus. E. mediterraneus ibericus ssp. n. (Aphididae: Lachninae). Boletín de la Asociación española de Entomología, 21 (3–4), 69–78.

Blackman, R.L. & Eastop, V.F. (1994) Aphids on the World’s Trees: An Identification and Information Guide. CAB International, Wallingford, 987 pp.

Blackman, R.L. & Eastop, V.F. (2016) Aphids on the World’s Plants. An Identification and Information Guide. Available from: http://www.aphidson-worldsplants.info/ (accessed 15 January 2016)

Bozhko, M. (1961) Novyy rod i novy vid tley (Homoptera: Aphidoidea) s yuga Ukrainy, Moldovy i Predkavkazie. Trudy Wsyesayusnego Entomologyckyego Oshchestva, 48, 5–37.

Börner, C. (1940) Neue Blattläuse aus Mitteleuropa. Privately published, Namburg (Saale), 4 pp.

Börner, C. (1950) Neue europäische Blattlausarten. Privately published, Namburg (Saale), 18 pp.

Carter, C.I. & Maslen, N.R. (1982) Conifer lachnids. Bulletin of Forrestry Commision London, No. 58, 1–75.

Chen, R., Favret, C., Jiang, L., Wang, Z. & Qiao, G. (2016) An aphid lineage maintains a bark–feeding niche while switching to and diversifying on conifers. Cladistics, 32 (5), 555–572.
https://doi.org/10.1111/cla.12141

Coeur d’acier, A., Cruaud, A., Artige, E., Genson, G., Clamens, A.-L., Pierre, E., Hudaverdian, S., Simon, J.-C., Jousselin, E. & Rasplus, J.-Y. (2014) DNA Barcoding and the Associated PhylAphidB@se Website for the Identification of European Aphids (Insecta: Hemiptera: Aphididae). PloS ONE, 9 (6), e97620.
https://doi.org/10.1371/journal.pone.0097620

von Dohlen, C.D., Kurosu, U. & Aoki, S. (2002). Phylogenetics and evolution of the eastern Asian-eastern North American disjunct aphid tribe, Hormaphidini (Hemiptera: Aphididae). Molecular Phylogenetics and Evolution, 23 (2), 257–267. https://doi.org/10.1016/s1055-7903(02)00025-8

Eastop, V.F. (1972). A taxonomic review of the species of Cinara Curtis occurring in Britain (Hemiptera Homoptera Aphididae). Bulletin of The British Museum (Natural History), Entomology, 27, 104–186.

Eastop, V.F. & Hille Ris Lambers, D. (1976) Survey of the World's Aphids. W. Junk, The Hague, 573 pp.

Favret, C. (2016) Aphid Species File. Version 5.0/5.0. Available from: http://Aphid.SpeciesFile.org/ (accessed 5 January 2016)

Favret, C. & Voegtlin, D. (2004a) A Revision of the Cinara Species (Hemiptera: Aphididae) of the United States Pinyon Pines. Annals of the Entomological Society of America, 97 (6), 1165–1197.
https://doi.org/10.1603/0013-8746(2004)097[1165:arotcs]2.0.co;2

Favret, C. & Voegtlin, D. (2004b) Speciation by host–switching in pinyon Cinara (Insecta: Hemiptera: Aphididae). Molecular Phylogenetics and Evolution, 32 (1), 139–51.
https://doi.org/10.1016/j.ympev.2003.12.005

Ferguson, J.W.H. (2002) On the use of genetic divergence for identifying species. Biological Journal of the Linnean Society, 75, 509–516.
https://doi.org/10.1046/j.1095-8312.2002.00042.x

Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

Foottit, R.G., Maw, H.E.L., von Dohlen, C.D. & Herbert, D.N. (2008) Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Molecular Ecology Resources, 8, 1189–1201.
https://doi.org/10.1111/j.1755-0998.2008.02297.x

del Guercio, G. (1909) Contribuzione alla conoscenza dei Lacnidi Italiani. Morfologia, systematica, biologia generale e loro importanza economica. Redia, V, 315–359.

Guglielmino, A., Kajtoch, Ł., Maryańska-Nadachowska, A., Lis, A. & Bückle, Ch. (2014) Italian neo–endemism in a widespread group of leafhoppers insects: A revision of the Eupteryx aurata group (Auchenorrhyncha: Cicadellidae: Typhlocybinae) using morphology, ecology and genetics. Zoologischer Anzeiger, 253, 283–308.
https://doi.org/10.1016/j.jcz.2014.01.002

Hall, T.A. (1999) BioEdit: a user–friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, London, 41, 95–98.

Hebert, P.D.N., Cywinska, A., Ball, S.L. & De Waard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270 (1512), 313–321.
https://doi.org/10.1098/rspb.2002.2218

Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America, 101, 14812–14817.
https://doi.org/10.1073/pnas.0406166101

Hebert, P.D.N. & Gregory, T.R. (2005) The promise of DNA barcoding for taxonomy. Systematic Biology, 54 (5), 852–859.
https://doi.org/10.1080/10635150500354886

Heie, O.E. (1995) The Aphidoidea of Fennoscandia and Denmark VI. Aphidinae. Part 3 of Macrosiphini and Lachnidae. Fauna entomologica scandinavica, 31, 1–222.

Heinze, K. (1962) Pflanzenschädliche Blattlausarten der Familien Lachnidae, Adelgidae und Phylloxeridae, eine systematisch–faunistische Studie. Deutsche Entomologische Zeitschrift, 9 (I/II), 143–227.

Hollingsworth, P.M. (2007) DNA Barcoding: Potential Users. Genomics, Society and Policy, 3 (2), 44–474.
https://doi.org/10.1186/1746-5354-3-2-44

Huelsenbeck, J.P. & Ronquis, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.
https://doi.org/10.1093/bioinformatics/17.8.754

Huelsenbeck, J.P., Ronquist, F., Nielsen, R. & Bollback, J.P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310–2314. https://doi.org/10.1126/science.1065889

Jousselin, E., Cruaud, A., Genson, G., Chevenet, F., Foottit, R.G. & Coeur d'acier, A. (2013) Is ecological speciation a major trend in aphids? Insights from a molecular phylogeny of the conifer–feeding genus Cinara. Frontiers in Zoology, 10 (56), 1–8. https://doi.org/10.1186/1742-9994-10-56

Kaltenbach, J.H. (1843) Monographie der Familien der Pflanzenläuse (Phytophthires) I. Teil. Die Blatt-und Erdläuse (Aphidina et Hyponomeutes). Aachen, Roschütz, 233 pp. https://doi.org/10.5962/bhl.title.51483

Kanturski, M. & Wieczorek, K. (2012) Metody zbioru i preparowania mszyc (Hemiptera: Aphidoidea) w badaniach faunistycznych, taksonomicznych i molekularnych. Młodzi Naukowcy dla Polskiej Nauki VIII. Nauki Przyrodnicze, V, 137–143.

Kanturski, M. & Wieczorek, K. (2014a) Systematic position of Eulachnus cembrae Börner with description of hitherto unknown sexual morphs of E. pumilae Inouye (Hemiptera, Aphididae, Lachninae). Deutsche Entomologische Zeitschrift, 61 (2), 123–132. https://doi.org/10.3897/dez.61.8048

Kanturski, M. & Wieczorek, K. (2014b) Nowe stanowiska rzadko spotykanych mszyc z rodzaju Eulachnus Del Guercio, 1909 (Hemiptera: Aphididae: Lachninae) w Południowej Polsce. Wiadomości Entomologiczne, 33 (1), 15–20.

Kanturski, M., Karcz, J. & Wieczorek, K. (2015) Morphology of the European species of the aphid genus Eulachnus (Hemiptera: Aphididae: Lachninae)—A SEM comparative and integrative study. Micron, 76, 23–36.
https://doi.org/10.1016/j.micron.2015.05.004

Kanturski, M., Bugaj–Nawrocka, A. & Wieczorek, K. (2016) Pine pest aphids of the genus Eulachnus (Hemiptera: Aphididae: Lachninae). How far can their range extend? Agricultural and Forest Entomology, 18 (4), 398–408.
https://doi.org/10.1111/afe.12171

Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
https://doi.org/10.1093/molbev/mst010

Lagos, D.M., Voegtlin, D.J., Coeur d’acier, A. & Giordano, R. (2014) Aphis (Hemiptera: Aphididae) species groups found in the Midwestern United States and their contribution to the phylogenetic knowledge of the genus. Insect Science, 21, 374–391.
https://doi.org/10.1111/1744-7917.12089

Lee, Y., Lee, W., Lee, S. & Kim, H. (2015) A cryptic species of Aphis gossypii (Hemiptera: Aphididae) complex revealed by genetic divergence and different host plant association. Bulletin of Entomological Research, 105, 40–51.
https://doi.org/10.1017/s0007485314000704

Lee, Y., Lee, W., Kanturski, M., Foottit, R.G., Akimoto, S.-I. & Lee, S. (2017) Cryptic diversity of the subfamily Calaphidinae (Hemiptera: Aphididae) revealed by comprehensive DNA barcoding. PLoSONE, 12 (4), e0176582.
https://doi.org/10.1371/journal.pone.0176582

Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.
https://doi.org/10.1093/bioinformatics/btp187

Mamontova, V.A. (1968) Noviye vidy Aphidinea (Homoptera) v stepyakh Ukrainy. Vestnik Zoolgy, 2, 33–45.

Mamontova, V.A. (1972) Fauna Ukrainy. Tly—Lachnidae. Fauna Ukrainy, 20 (7), 80–89.

Mamontova, V.A. (2011) Tablycy dlya opredelenyya tley semeystwa Lachnidae (Homoptera, Aphidoidea, Lachnidae) fauny Vostocchnoy Evropy i sopredelnych territoriy. Ukrainsky Entomologichny Zhurnal, 2 (3), 3–39.

Mamontova, V.A. (2012) Tly semeystva Lyachnid (Homoptera, Aphidoidea, Lachnidae) Fauny Vostochnoy Evropy y Sopredelnych Terrytoryy. Nacyonalnaya Akademia Nauk Ukrainy, Naukowa Dumka, Kiw, 390 pp.

Massimino Cocuzza, G.E. & Cavalieri, V. (2014) Identification of aphids of Aphis frangulae-group living on Lamiaceae species through DNA barcode. Molecular Ecology Resources, 14, 447–457.
https://doi.org/10.1111/1755-0998.12199

Massimino Cocuzza, G.E., Di Silvestro, S., Giordano, R. & Carmelo Rapisarda, C. (2015) Congruence between cytochrome oxidase I (COI) and morphological data in Anuraphis spp. (Hemiptera, Aphididae) with a comparison between the utility of the 5’ barcode and 3’ COI regions. Zookeys, 529, 123–144.

Meyer, C.P. & Paulay, G. (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biology, 3 (12), e422.
https://doi.org/10.1371/journal.pbio.0030422

Miller, G.L., Jensen, A.S., Metz, M.A. & Parmenter, R.R. (2014) A new species of Atheroides Haliday (Hemiptera, Aphididae) native to North America. Zookeys, 452, 35–50. https://doi.org/10.3897/zookeys.452.8089

Moritz, C. & Cicero, C. (2004) DNA Barcoding: Promise and Pitfalls. PLoS Biology, 2 (10), e354.
https://doi.org/10.1371/journal.pbio.0020354

Mróz, E., Trela, J. & Depa, Ł. (2015) Taxonomic analysis of Lachnus pallipes/longirostris–roboris complex (Hemiptera, Aphididae, Lachninae), with the redescription of sexual morphs and new synonymy. Zoologischer Anzeiger, 254, 51–61. https://doi.org/10.1016/j.jcz.2014.11.002

Nieto Nafría, J.M., Mier Durante, M.P., Binazzi, A. & Pérez Hidalgo, N. (2002) Hemiptera, Aphididae II. Fauna Iberica, 19, 1–350.

Normark, B.B. (2000) Molecular systematics and evolution of the aphid family Lachnidae. Molecular Phylogenetic and Evolution, 14 (1), 131–140. https://doi.org/10.1006/mpev.1999.0699

Nylander, J.A.A. (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala.

Ortiz-Rivas, B. & 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, 305–317.

Pašek, V. (1953) Několik nových medovnic (Aphidoidea) z Československa. I. Zoologické Listy [Folia Zoologica et Entomologica], 2, 28–34

Pašek, V. (1954) Vošky našich lesných drevín, Homoptera: Aphidoidea. Vydavatelʹstvo Slovenskej akadémie vied, Bratyslava, 319 pp.

Pintera, A (1968) Aphids from the subtribe Schizolachnina (Homoptera: Lachnidae) in Middle Europe. Acta Entomologica Bohemoslavica, 65, 100–111.

Rambaut, A. & Drummond, A.J. (2003–2009) Tracer v1.4. Distributed by the Authors. http://beast.bio.ed.ac.uk/Trace (accessed 3 August 2014)

Rambaut, A. (2006) FigTree v. 1.3.1. Available from: http://tree.bio.ed.ac.uk/software/Fig.tree/. (accessed 3 August 2015)

Remaudière, G. & Remaudière M. (1997) Catalogue des Aphididae du Monde. INRA, Paris, 473 pp.

Rogers, J. & Gibbs, R.A. (2014) Comparative primate genomics: emerging patterns of genome content and dynamics. Nature Reviews Genetics, 15, 347–359. https://doi.org/10.1038/nrg3707

Sorensen, J.T. (1994) A revision of the aphid genus Essigella (Homoptera: Aphididae) its ecological associations with, and evolution on, Pinaceae hosts. Pan-Pacific Entomologist, 70, 1–102.

Swofford, D.L. (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland.

Szelegiewicz, H. (1978) Klucze do oznaczania owadów Polski. XVII, Homoptera, 5a, Mszyce–Aphidodea, 1, Lachnidae. Polskie Towarzystwo Entomologiczne, 107 pp.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
https://doi.org/10.1093/molbev/msr121

Theobald, F.V. (1915) African Aphididae. Part II. Bulletin of Entomological Research, 6, 103–153.
https://doi.org/10.1017/s0007485300044370

Tsuchida, T., Koga, R., Horikawa, M., Tsunoda, T., Maoka, T., Matsumoto, S., Simon, J.-C. & Fukatsu, T. (2010) Symbiotic bacterium modifies aphid body color. Science, 330 (6007), 1102–4.
https://doi.org/10.1126/science.1195463

White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Shinsky, J.J. & White, T.J. (Eds.), PCR - Protocols and Applications - A Laboratory Manual. Academic Press, Cambridge, pp. 315–322.
https://doi.org/10.1016/B978-0-12-372180-8.50042-1

Wieczorek, K. & Kajtoch, Ł. (2011) Relationships within Siphini (Hemiptera, Aphidoidea: Chaitophorinae) in light of molecular and morphological research. Systematic Entomology, 36, 164–174.
https://doi.org/10.1111/j.1365-3113.2010.00550.x

Wieczorek, K., Lachowska-Cierlik, D., Kajtoch, Ł. & Kanturski, M. (2017) The relationships within the Chaitophorinae and Drepanosiphinae (Hemiptera, Aphididae) inferred from molecular-based phylogeny and comprehensive morphological data. PLoS ONE, 12 (3), e0173608.
https://doi.org/10.1371/journal.pone.0173608

Wilson, H.F. (1911) Notes of the synonymy of the genera included in the tribe Lachnini. Annals of the Entomological Society of America, 4 (1), 51–54.
https://doi.org/10.1093/aesa/4.1.51

Zhang, H.C. & Qiao, G.X. (2007) Molecular phylogeny of Fordini (Hemiptera: Aphididae: Pemphiginae) inferred from nuclear gene EF–1α and mitochondrial gene COI. Bulletin of Entomological Research, 97, 379–386.
https://doi.org/10.1017/s0007485307005020

Zhang, H.C. & Qiao, G.X. (2008) Molecular phylogeny of Pemphiginae (Hemiptera: Aphididae) inferred from nuclear gene EF–1 α sequences. Bulletin of Entomological Research, 98, 499–507.
https://doi.org/10.1017/S0007485308005828

Zondag, R. (1983) Pine aphid (Eulachnus brevipilosus) in New Zaeland. Forest and Timber Insects in New Zealand, No. 55, 1–4. [revised 2009]




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