Variation in Sperm Formation Patterns in Jumping Plant-Lice (Hemiptera: Psylloidea): a Light Microscopic Study
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PL-ISSN0015-5497(print),ISSN1734-9168(online) FoliaBiologica(Kraków),vol.62(2014),No4 Ó InstituteofSystematicsandEvolutionofAnimals,PAS,Kraków, 2014 doi:10.3409/fb62_4.321 VariationinSpermFormationPatternsinJumpingPlant-Lice (Hemiptera:Psylloidea): aLightMicroscopicStudy EugeniaS.LABINA,Anna MARYAÑSKA-NADACHOWSKA, Daniel BURCKHARDT, andValentinaG.KUZNETSOVA AcceptedOctober02,2014 LABINA E.S., MARYAÑSKA-NADACHOWSKA A., BURCKHARDT D., KUZNETSOVA V.G. 2014. Variation in sperm formation patterns in jumping plant-lice (Hemiptera: Psylloidea): a light microscopic study. Folia Biologica (Kraków) 62: 321-333. The patterns of sperm formation in sternorrhynchous jumping plant-lice are reviewed. To date information is available for 143 species belonging to 54 genera, 17 subfamilies and seven of the eight psylloid families (only Phacopteronidae is not represented). For the majority of the taxa (116 species, 39 genera, 10 subfamilies and the families Calophyidae, Carsidaridae and Liviidae) the data presented here is new and is based exclusively on studies using light microscopy. Five distinct patterns of chromatin reorganisation during metamorphosis of spermatids into spermatozoa are recognised, described and named here typesI-V.TypesIandIIIwerepreviouslyknown,typesII,IV andVaredescribedhereforthe firsttimeforjumpingplant-lice.ThemostwidespreadistypeIwhichisfoundineveryfamily representing the plesiomorphic condition of spermiogenesis in Psylloidea. Types III and V are autapomorphic for the Aphalarinae and Spondyliaspidinae, respectively. Type IV was found only in two genera of Euphyllurinae and may represent a synapomorphy. Type II occurs in several unrelated subfamilies and is interpreted as a homoplasy. The patterns of sperm formation are stable within most of the examined subfamilies and can be used, to a certain extent, to elucidate phylogenetic relationships within Psylloidea. Key words: Psyllids, Sternorrhyncha, spermiogenesis, evolution, systematics. Eugenia S. LABINA,ValentinaG.KUZNETSOVA, Department of Karyosystematics, Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034 Saint Petersburg, Russia. E-mails: [email protected], [email protected] Anna MARYAÑSKA-NADACHOWSKA, Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, S³awkowska 17, 31-016 Kraków, Poland. E-mail: [email protected] DanielBURCKHARDT, Naturhistorisches Museum, Augustinergasse 2, CH4001 Basel, Switzerland. E-mail: [email protected] Psyllids or jumping plant-lice (Sternorrhyncha: supported with the exception of their Aphalaridae, Psylloidea) are a relatively small group of hemip- Psyllidae, and Spondyliaspididae which were teraninsectswithabout3800describedandatleast shown to be polyphyletic (BURCKHARDT 1987a, b, as many undescribed species worldwide (BURCK- 1991,2005).BasedontheseresultsBURCKHARDT HARDT et al. 2014; D. BURCKHARDT, unpublished and OUVRARD (2012) published a revised classifi- data). WHITE and HODKINSON (1985), in their cation also comprising eight families of which five seminal paper on the systematics of psyllids based aresimilartothoseofWhiteandHodkinson(Calo- mostly on morphological characters of immatures, phyidae, Carsidaridae, Homotomidae, Phacop- introduced a classification with eight families teronidae, and Triozidae) but three are completely (Aphalaridae, Calophyidae, Carsidaridae, Homo- redefined (Aphalaridae, Liviidae, and Psyllidae). tomidae, Phacopteronidae, Psyllidae, Spondylias- Several attempts have been undertaken to study pididae and Triozidae). This classification was the systematics of Psylloidea using new characters, tested in the last three decades by several authors such as the number of seminal follicles (e.g. KLI- who investigated many taxa using morphological MASZEWSKI 1972; KLIMASZEWSKI et al. 1974; adult and immature as well as molecular characters. G£OWACKA et al. 1995; MARYAÑSKA-NADA- White and Hodkinson’s families were generally CHOWSKA et al. 2001a, b, c; KUZNETSOVA et al. 322 E.S.LABINA etal. 2012) and karyotypes (e.g. MARYAÑSKA-NADA- Material and Methods CHOWSKA 2002; LABINA et al. 2007). These char- acters were shown to be of some use in solving For nearly three decades, we have prepared hun- taxonomic problems at the suprageneric level. dreds of cytological preparations to study karyo- types and male meiosis of psyllids represented by Variation in sperm formation patterns within a wide taxonomic range (e.g. MARYAÑSKA-NADA- Psylloidea was investigated in a number of publi- CHOWSKA 2002; LABINA et al. 2007; KUZNETSOVA et al. 2012; NOKKALA et al. 2013). For this purpose, cations (LE MENN 1966a, b; KUZNETSOVA et al. adult males were fixed in Carnoy fixative (96% 1997; TIAN et al. 2007). LE MENN (1966a, b) was ethanol and glacial acetic acid, 3:1) and refriger- the first to observe the remarkable, so-called o ated at 5 C in the laboratory until slides were made. “binuclear” male germ cells by electron micros- Seminal follicles were extracted from adult speci- copyineightspeciesofHomotomidae(Homotoma mens and squashed on the slide. The preparations ficus), Psyllidae (Arytaina genistae, Cacopsylla were frozen using dry ice, the coverslips were re- visci, Chamaepsylla hartigii, Psylla alni, P. buxi) moved with a razor blade, and the preparations and Triozidae (Bactericera femoralis, Trioza urticae) were dehydrated in fresh Carnoy fixative for 20 min corresponding to “Type I” as defined below. and air dried. Then they were subjected either to Later, KUZNETSOVA et al. (1997) discovered by Schiff-Giemsa staining (GROZEVA &NOKKALA 1996) light microscopy a different, also unusual type of or to silver staining (HOWELL &BLACK 1980) or sperm formation in ten species of the genera to C-banding (SUMNER 1972), as the case required. Aphalara, Craspedolepta and Crastina (Aphalari- In our present study, the same cytological prepa- dae, Aphalarinae) corresponding to “Type III” as rations were used to study a post-meiotic phase of defined below. More recently, binuclear sperms spermatogenesis, i.e. spermiogenesis. By light mi- were reported for Acizzia jamatonica (Psyllidae) croscopy, we followed the progressive differentia- and Bharatiana septentrionalis (Calophyidae) tion of the spermatid components and changes in (TIAN et al. 2007) but the attribution to a particular chromatin organization during metamorphosis of sperm formation type is problematic. spermatids into spermatozoa in males of 125 spe- cies belonging to 51 genera and 16 subfamilies of In this paper we confirm the presence of the two the families Aphalaridae, Calophyidae, Carsidari- previously described types of sperm formation and dae, Homotomidae, Liviidae, Psyllidae, and add another three discovered by light microscopy Triozidae. Observation and literature data are in a wide taxonomical range of Psylloidea. Fur- summarised in Table 1. We follow the classifica- thermore, we plot the known types of sperm for- tion by BURCKHARDT and OUVRARD (2012). mationpatternsonacladogramreflectingthelatest Voucher preparations are deposited at the Depart- classification of Psylloidea by BURCKHARDT and ment of Experimental Zoology, Institute of Syste- OUVRARD (2012) and discuss the phylogenetic matics and Evolution of Animals PAS in Kraków, implications. Poland. Table 1 Species studied and types of spermiogenesis Type of Taxon spermio- Collecting data Indentification Reference genesis by Aphalaridae Aphalarinae binuclear ? ? LE MENN 1966a,b sperm Aphalara calthae (Linnaeus,1761) III Finland:near Turku – Caltha S.Nokkala KUZNETSOVA et al. palustre 1997 KUZNETSOVA et al. Aphalara exilis (WeberetMohr,1804) III Poland: Gorce Mts – Rumex sp. E. G³owacka 1997 Poland:west Beskidy Mts – Aphalaramaculipennis Löw,1886 III Polygonum sp. E. G³owacka presentpaper 1 Georgia:Kolkhida, Paliastomi KUZNETSOVA et al. Aphalara polygoni Foerster,1848 III Lake – Polygonum sp. A.Gegechkori 1997 Craspedolepta bulgarica Klimaszewski, Georgia:DavidGaredzhi– KUZNETSOVA et al. 1961 III Achillea sp. A.Gegechkori 1997 TypesofSpermiogenesisinPsylloidea 323 Table 1 cont. Russia: Primorsky Krai, Khasan- Craspedolepta flava (Kuwayama,1908) III sky District, near Kedrovaya Pad’ E.Labina presentpaper Reserve– Artemisia spp. Poland:KazimierzDolny– Craspedolepta flavipennis (Foerster, 1848) III Chrysanthemum sp. E. G³owacka presentpaper Russia: Primorsky Krai, Khasan- Craspedolepta kerzhneri Loginova, III skyDistrict,nearKedrovaya E.Labina presentpaper 1963 Pad’Reserve– Artemisia spp. Russia: Primorsky Krai, Khasan- Craspedoleptalatior Wagner,1944 III skyDistrict,nearKedrovaya E.Labina presentpaper Pad’Reserve– Artemisia spp. Russia: PrimorskyKrai, Craspedolepta lineolata Loginova,1962 III Vladivostok – Artemisia sp. E.Labina presentpaper Craspedolepta malachitica (Dahlbom, Poland: Mielnik– Artemisia KUZNETSOVA et al. 1851) III absinthium E. G³owacka 1997 Craspedolepta nebulosa (Zetterstedt, Poland: Gorce Mts – Chamerion KUZNETSOVA et al. 1828) III angustifolium E. G³owacka 1997 KUZNETSOVA et al. Craspedolepta nervosa (Foerster,1848) III Poland: Gorce Mts – Achillea sp. E. G³owacka 1997 KUZNETSOVA et al. Craspedolepta omissa Wagner,1944 III Poland: Gorce Mts – Artemisia sp. E. G³owacka 1997 MARYAÑSKA-NA Craspedoleptasonchi (Foerster,1848) III Finland – Leontodon autumnalis S.Nokkala DACHOWSKA et al. 2001c Craspedolepta subpunctata (Foerster, Poland: Gorce Mts – Chamerion KUZNETSOVA et al. 1848) III angustifolium E. G³owacka 1997 Russia: Primorsky Krai, Khasan- Craspedolepta terminata Loginova, skyDistrict,nearKedrovaya 1962 III Pad’