New Cytogenetic Data on Nabidae (Heteroptera: Cimicomorpha), with a Discussion of Karyotype Variation and Meiotic Patterns, and Their Taxonomic Significance
Total Page：16
File Type：pdf, Size：1020Kb
Eur. J. Entomol. 101: 205–210, 2004 ISSN 1210-5759 New cytogenetic data on Nabidae (Heteroptera: Cimicomorpha), with a discussion of karyotype variation and meiotic patterns, and their taxonomic significance VALENTINA G. KUZNETSOVA1, SNEJANA GROZEVA2 and SEPPO NOKKALA3 1Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1, 199034 St. Petersburg, Russia; e-mail: [email protected] 2 Institute of Zoology, Bulgarian Academy of Sciences, blvd Tsar Osvoboditel 1, 1000 Sofia, Bulgaria; e-mail: [email protected] 3Laboratory of Genetics, Department of Biology, University of Turku, 20014 Turku, Finland; e-mail: [email protected] Key words. Heteroptera, Nabidae, karyotypes, meiosis, evolution, taxonomy, phylogeny Abstract. As a part of ongoing cytogenetic studies on the bug family Nabidae (Heteroptera), the karyotypes and meiotic patterns of male Nabis (Aspilaspis) viridulus Spinola, 1837, N. (A.) indicus (Stål, 1873) (subfamily Nabinae) and Prostemma guttula (Fabricius, 1787) (subfamily Prostemmatinae) are described. N. viridulus and N. indicus differ from P. guttula in their chromosome numbers, which are 2n = 32 + XY and 2n = 26 + XY, respectively, and behaviour of the sex chromosomes in male meiosis, which, respectively, show “distance pairing” and “touch- and-go pairing” in spermatocyte metaphase II. The karyotype of 2n = 34 and “touch-and-go pairing” are considered to be plesiomor- phic characters in Nabidae. The evolutionary mechanisms that might underlie different chromosome numbers, the taxonomic significance of karyotype variation and the distribution of meiotic patterns in the family, are discussed. INTRODUCTION Here, as a part of ongoing cytogenetic studies on Nabidae (Nokkala & Nokkala, 1984; Kuznetsova & Nabidae (damsel bugs) are predators with a world wide MaryaĔska-Nadachowska, 2000; Grozeva & Nokkala, distribution. Taxonomically, the family belongs to the 2003; Grozeva et al., 2004), we present information on superfamily Cimicoidea, infraorder Cimicomorpha. the karyotypes and male meiotic patterns in another three Nabidae include approximately 400 species in about 20 nabid species: Nabis (Aspilaspis) viridulus Spinola, 1837, genera and four subfamilies (Kerzhner, 1981, 1996). N. (A.) indicus (Stål, 1873) (subfamily Nabinae, tribe There are chromosome data for 24 species and 5 genera Nabini) and Prostemma guttula (Fabricius, 1787) (sub- of the subfamilies Nabinae and Prostemmatinae family Prostemmatinae, tribe Prostemmatini). The ances- (Ueshima, 1979; Kuznetsova & MaryaĔska-Nadachow- tral karyotype and male meiotic pattern of Nabidae are ska, 2000 and references therein). All these species have suggested. The evolutionary mechanisms that might have an XY sex-determining system, but different chromosome resulted in the different chromosome numbers, the taxo- numbers of 2n = 18, 34, 38; 26–28 in Pagasa fusca nomic significance of the variation in karyotype and the (Stein, 1857), and several values in the range of 18 to 40 distribution of meiotic patterns in the family, are dis- in different populations of Himacerus apterus (Fabricius, cussed. 1798). Owing to the statistical predominance of 2n = 18 (16 + XY) this karyotype was proposed as the modal and MATERIAL AND METHODS ancestral one for the family (Leston, 1957; Ueshima, Males of Nabis (Aspilaspis) viridulus (7) and N. (A.) indicus 1979; Thomas, 1996; Kuznetsova & MaryaĔska- (6) were collected in Israel; males of Prostemma guttula (4) Nadachowska, 2000). The other karyotypes are thought to were collected in Bulgaria. They were fixed in the field in 3 : 1 be derivates, with 2n = 32 + XY, showing doubling of the ethanol-acetic acid mixture. autosome number compared with 2n = 16 + XY (the phe- Males of all three species had 7 follicles per testis. Testicular nomenon known as “pseudopolyploidy” after Battaglia, follicles were dissected and squashed under a coverslip in a drop 1956, or ”autosomal polyploidy” after Kuznetsova & of 45% acetic acid. The coverslips were removed after freezing with dry ice; slides were dehydrated in freshly prepared 3 : 1 MaryaĔska-Nadachowska, 2000) as originated by a poly- fixative for 20 min and air-dried. ploidy (Thomas, 1996). For staining, the Feulgen-Giemsa procedure of Grozeva & The meiotic behaviour of the sex chromosomes in the Nokkala (1996) was applied as follows: slides were immersed in Nabidae species is reported to differ from that observed in 1 N HCl at room temperature for 20 min, hydrolysed in 1N HCl other Heteropteran species as they show “distance at 60°C for 8 min and stained with Schiff’s reagent for 20 min. pairing” at the second male meiotic division instead of the Slides were thoroughly rinsed with distilled water, then re- orthodox “touch-and-go pairing” (Nokkala & Nokkala, hydrated in Sorensen’s phosphate buffer for 10 min and stained 1984; Kuznetsova & MaryaĔska-Nadachowska, 2000). with 2% Giemsa solution in the same buffer for 15–20 min. When appropriately stained, slides were rinsed briefly with dis- 205 Fig. 1. a–d – male meiotic chromosomes of Nabis (Aspilaspis) viridulus, 2n = 34 (32 + XY): a – metaphase I; b – metaphase II; polar view; c – metaphase II, equatorial view; d – anaphase II / telophase II transition, two daughter plates; e, f – male meiotic chro- mosomes of Nabis (Aspilaspis) indicus, 2n = 34 (32 + XY): e – prometaphase I; f – metaphase II, equatorial view; g–i – male mei- otic chromosomes of Prostemma guttula, 2n = 28 (26 + XY): g – metaphase I; h – metaphase II, polar view; i – metaphase II / anaphase II transition, equatorial view. Scale = 10 µm tilled water, air dried and mounted in Entellan (Merck, Darm- somes (Fig. 1b). When viewed from the pole, MII plates stadt, Germany). were “radial” with the sex chromosomes lying in the Chromosome spreads were analysed using an Olympus BH 2 centre of the ring formed by the autosomes. The sex chro- light microscope with an OM-4 camera. mosomes were spaced separately from each other without RESULTS any visible links between them. Viewed from the side, the sex chromosomes showed a bipolar co-orientation, the so- The meiotic karyotypes of N. viridulus and N. indicus called “distance pairing”. The sex chromosomes moved are similar. At first metaphase (MI) in both species the towards the poles ahead of the autosomes (Figs 1c, f). spermatocytes have 16 autosomal bivalents plus X and During AII, they segregated resulting in spermatocyte II Y-chromosomes, indicating a diploid karyotype of 2n = nuclei with 16 autosomes plus an X or a Y chromosome 32 + XY (Figs 1a, e). Bivalents were of a gradually (Fig. 1d). decreasing size. The X was the largest and the Y was one In P. guttula, spermatocyte MI had 13 autosomal biva- of the medium-sized chromosomes. lents plus X and Y chromosomes, consequently male dip- In the bivalents, the homologues were aligned in par- loid karyotype was defined as 2n = 26 + XY (Fig. 1g). allel with no chiasmata between them. As in the great All bivalents were achiasmatic and graded in size. The X majority of Heteroptera (Ueshima, 1979), the first divi- was the largest and the Y a medium-sized chromosome. sion was reductional for the autosomal bivalents, whereas MII plates were “radial” with the sex chromosomes lying the sex chromosomes underwent equational separation in in centre of the ring formed by the autosomes (Fig. 1h). anaphase I (AI) and segregation in AII (postreduction). At this stage, the sex chromosomes formed a pseudo- Each MII cell therefore contained both X and Y chromo- bivalent by so-called “end-to-end” pairing, or more prop- 206 TABLE 1. Chromosome numbers of Nabidae.* 1861, N. (A.) viridulus and N. (A.) indicus; N. NN Taxa 2n (Halonabis) sareptanus Dohrn, 1862; Himacerus (Aptus) NABINAE mirmicoides (O. Costa, 1834). Although a population of 1. NABINI 18 the latter species from Caucasus shows some chromo- Nabis (s.str.) punctatus Costa, 1847 some number polymorphism (2n = 34–38) (Kuznetsova & 2. N. (s.str.) brevis Scholtz, 1847 18 MaryaĔska-Nadachowska, 2000), the 2n = 34 karyotype, 3. N. (s.str.) ericetorum Scholtz, 1847 18 4. N. (s.str.) ferus (Linnaeus, 1758) 18 initially reported from England (Leston, 1957), was 5. N. (s.str.) pseudoferus Remane, 1949 18 recently confirmed for populations of this species from 6. N. (s.str.) meridionalis Kerzhner, 1963 18 Germany and the North Caucasus, Russia (Grozeva et al., 7. N. (s.str.) rugosus (Linnaeus, 1758) 18 2004). The same chromosome number polymorphism (2n 8. N. (s.str.) stenoferus Hsiao, 1964 18 = 34–38) was reported for H. (Aptus) maracandicus 9. N. (Tropiconabis) kinbergii Reuter, 1872 18 (Reuter, 1890) in Kazakhstan (Kuznetsova & MaryaĔska- 10. N. (Dolichonabis) limbatus Dahlbom, 1851 18 Nadachowska, 2000), however, a 2n = 38, without poly- 11. N. (Dolichonabis) tesquorum (Kerzhner, 1968) 18 morphism, was recorded for this species in Turkmenia 12. N. (Reduviolus) americoferus Carayon, 1961 18 (Schachow, 1932). We are inclined to believe that H. mir- 13. N. (Milu) reuteri Jakovlev, 1876 18 micoides and H. maracandicus have, respectively, 2n = 14. N. (Limnonabis) ussuriensis Kerzhner, 1962 18 15. N. (Limnonabis) lineatus Dahlbom, 1851 18 34 and 2n = 38 in their standard sets. An unusual range of 16. N. (Nabicula) flavomarginatus Scholtz, 1847 18 chromosome numbers was reported for a third Himacerus 17. N. (Aspilaspis) pallidus Fieber, 1861 34 species – H. (Himacerus) apterus, which has dissimilar 18. N. (Aspilaspis) viridulus Spinola, 1837** 34 chromosome numbers in different populations. Two 19. N. (Aspilaspis) indicus (Stal, 1873)** 34 European