B chromosomes in Sternorrhyncha (Hemiptera, Insecta)

Review on B Chromosomes Cytogenet Genome Res 106:210-214 (2004) DOI: 10.1159/000079289

B chromosomes in Sternorrhyncha (Hemiptera, Insecta) A. Maryańska-Nadachowska Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków (Poland)

Abstract. In the hemipteroid insects of the suborder Sternorrhyncha, B chromosomes are relatively common in comparison with other suborders of Hemiptera. However, the occurrence of supernumerary chromosomes is restricted, in most cases, to several genera or closely related species. At least in some species of Psylloidea with the XY sex determination system, a mitotically stable B chromosome integrated into an

Introduction

B chromosomes, also known as supernumerary or accessory chromosomes, occur in many plants and animals (White, 1973; Jones and Rees, 1982). B chromosomes are considered as selfish and parasitic genetic elements and do not follow Mendelian laws of inheritance. Many of them show a high transmission rate in meiosis and/or mitosis leading to their accumulation, which favours their increase in frequency and the establishment of B chromosome polymorphisms in natural populations (Camacho et al., 2000). A large number of recent studies have confirmed that B chromosomes are relatively frequent in insects. They have been described predominantly in intensively cytogenetically studied taxonomic groups. However, Bs are not present in all individuals or populations studied and thus they could have been overlooked in chromosome counts of some species. The hemipteroid insects (Hemiptera), which are divided into true bugs (Heteroptera), Coleorhyncha, Fulgoromorpha,

Received l 7 Seplember 2003; manuscript accepted 29 January 2004. Reąucst rcprints trom: Dr. A. Maryańska-Nadachowska Instilute of Systematicsand Evolution of Animals Polish Academy of Sciences, Stawkowska 17, 31-016 Kraków (Poland) telephonc: +48-12-422-7006: fax: +48-12-422-4294 e-mail: maryanska^isez.pan.krakow.pl

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achiasmatic segregation system with the X, and became fixed as a Y chromosome. In some Aphidoidea with a multiple X system of sex determination, B chromosomes appear to be in fact non-functional X chromosomes. Supernumerary chromosomes thus probably play an important role in the evolution of sex determination systems in Sternorrhyncha. Copyright ©2004 S. KargerAG, Basel

Cicadomorpha, and Sternorrhyncha (Sorensen et al., 1995), belong to groups relatively well-studied karyologically. The suborder Sternorrhyncha comprises four clearly distinguished superfamilies: whiteflies (Aleyrodoidea), jumping plant-lice (Psylloidea), aphids (Aphidoidea), and scale insects (Coccoidea) (Zrzavy, 1990; Klimaszewski and Wojciechowski, 1992). Chromosome numbers of whiteflies have been described for only four species (Blackman and Cahill, 1998). Karyotypes of jumping plant-lice are known for more than 150 species (Maryańska-Nadachowska, 2002). Basic chromosome sets of aphids and scale insects, which comprise many agricultural and forest pests, have been described for morę than 800 species (Kuznetsova and Shaposhnikov, 1973; Blackman, 1980a, b, 1986, 1990) and almost 400 species (Nur, 1980; Nur et al., 1987; Moharana, 1990), respectively. B chromosomes in Sternorrhyncha

The frequency distribution of supernumerary chromosomes in particular superfamilies is random (Table 1). Only one species that carries B chromosomes has been described in Aleyrodoidea (Thomsen, 1927). In Psylloidea, accessory chromosomes are not as rare and have been found in nine species (Matcharashvili and Kuznetsova, 1997; Kuznetsova et al., 1997; Maryańska-Nadachowska, 1999; Nokkala et al., 2000; Maryańska-Nadachowska et al., Acccssible online at: www.karger.com/cgr

Table 1. Species of Sternorrhyncha with B chromosomes

Taxa

Number of chromosomes 2n

References

♂26 + BB

Thomsen, 1927

♂12+XO+B ♂12+XO+BB ♂ 12+XO+BBB ♂ 14+XO+B ♂ 24+XO+B ♂24+XO+B ♂ 24+XO+B ♂24+XO+B ♂24+XO+B

Matcharashvili and Kuznetsova, 1997 Maryańska-Nadachowska, 1999

♂24+XY+B ♂24+XO+B

Kuznetsova et al., 1997 Kuznetsova et al., 1997

♂4+XlX20+B ♂4+X,X20+BB ♂2+XiX20+B ♂2+X1X20+BB ♂14+X,X20+BBB ♂ 14+X,X20+BBBB ♂4+X,X20+BBB ♂4+XO+BB ♂4+X,X20+B

Blackman, 1976

♀ I O + 1-8B

Nur, 1962b, 1966a, b, 1969; Nur and Brett, 1987, 1988 Nur et al., 1987

Aleyrodoidea Aleurodes proletella Psylloidea Psyllidae Rhinocola aceris Baeopelma foersteri Cacopsylla crataegi Cacopsvlla hippophaes Cacopsvlla nehulosa Cacopsylla peregrina Psylla ledi Triozidae Bactericera curvatinervis Trioza apicalis Aphidoidea Euceraphis betulae Euceraphis punctipennis Euceraphis mucida Euceraphis sp. no. 1 Euceraphis sp. no. 2 Euceraphis sp. no. 3 Coccoidea Pseudoccocus affinis (obscurus) Antonina pertiosa

2001). B chromosomes occur, at low frequency, in natural populations of Psyllidae and Triozidae (most B-carrying individuals harboured only one supernumerary chromosome). The most interesting and unique example of B chromosome occurrence and behaviour in Psylloidea is Rhinocola aceris, where four types of supernumeraries (B 1 , B2, B3, B4) were described (Maryańska-Nadachowska, 1999; Nokkala et al., 2000) (Figs. 1-15). This widely distributed, Palaearctic species shows a basic karyotype consisting of 10 autosomes and the X chromosome in males (Maryańska-Nadachowska et al., 1992), and demonstrates a high tolerance to the presence of supernumerary chromosomes. Among eight populations studied from Finland, Russia, Poland and Georgia, seven carried mitotically stable B chromosomes (Nokkala et al., 2000; Table 1). A stable frequency of supernumerary chromosomes is often found for several years, but, in R. aceris, intrapopulation differences in B frequency were observed between samples collected in several years. This probably indicates that B chromosome frequencies in R. aceris depend not only on a high degree of tolerance to additional elements in the chromosome set, but also on other factors. B chromosomes are mitotically stable and segregate quite regularly from the X chromosome. Their behaviour during mitotic prophase and metaphase I suggests that their regular segregation probably results from the incorporation of B chromosomes into achiasmate segregation mechanisms with the X chromosome in the place occupied by the Y chromosome in species with an XY sex determination system. Similar B chromosome behaviour was observed in Cacopsylla peregrina (Kuznetsova et al., 1997) and C. crataegi (Matcharashvili and Kuznetsova, 1997). Additional data from Fin-

♀ 24 + BB

Nokkala et al., 2000 Matcharashvili and Kuznetsova, 1997 Maryanska-Nadachowska et al., 2001 Kuznetsova et al., 1997 Kuznetsova et al., 1997 Kuznetsova et al., 1997

Blackman, 1976 Blackman, 1988 Blackman, 1988 Blackman, 1988 Blackman, 1988

land (Turku), Poland (Warsaw) and Bulgaria (Sofia) confirmed that the extra univalent chromosome segregating from the X in C. peregrina was present in all males. The mitotic stability and the segregation pattern of the B from the X in meiosis, traced in all stages, were highly regular. The meiotic X and B chromosomes, which appear as univalents during meiotic prophase, associate at metaphase I on the basis of the achiasmatic segregation mechanisms. Segregating univalents associate and show "touch and go" pairing at early metaphase I, and segregate from each other at anaphase I. All characteristics of supernumerary chromosome in C. peregrina, originally identified as a B chromosome (Kuznetsova et al., 1997), suggest that this extra chromosome has to be referred to as an achiasmatic Y chromosome (Nokkala et al., 2003) (Fig. 16). If this scenario is true then Y chromosomes present in Heteropsylla cubana might also have arisen from B chromosomes (Maryańska-Nadachowska et al., 1996). This interpretation is paralleled by the hypothesis that the Y chromosome in Drosophila evolved from a specialized B chromosome instead of a degenerated homologue of the X chromosome (Hackstein et al., 1996; Carvalho, 2002). In Aphidoidea, supernumerary chromosomes have been reported in several species of the genus Euceraphis feeding on various species of birch trees (Betula species). In Euceraphis, with a multiple X chromosome system, the mechanism of appearance and role of B chromosomes seem to be different (Blackman 1976, 1988). Although traditionally viewed and still widely accepted as derived from autosomes, B chromosomes can originate in a number of ways (Camacho et al., 2000). Most of the Euceraphis species have one or more supernumerary chromosomes, similar to the X, but showing greater stability in

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Figs. 1-15. Various B chromosome types in Rhinocola aceris (Psylloidea, Hemiptera) in meiotic prophase and metaphase I. Slides were stained with the C-banding method. Figs. l, 5, 10, 12, 13 and 14 correspond to figures 2b, 4b, 7b, 5b, 5d and 5c in Maryańska-Nadachowska (1999), respectively.

size and number than typical B chromosomes. A multiple X system in Aphidoidea probably arises simply from X0 by fissions of the single original X chromosome into two or more parts (Blackman, 1995). However, the multiple X system has probably little or no significance in molecular genetic basis of

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sex determination. The behaviour of additional chromosomes with the functional X is apparent. The smaller Bs vary somewhat in size and could have derived from larger ones by, for example, deletion. The larger Bs are similar to the X chromosomes. Almost all species of Euceraphis have at least one of

Fig. 16. The Y chromosome, originated from the B chromosome, in Cacopsylaperegrina with the achiasmatic XY sex determination system. The slide was stained using the Feulgen-Giemsa method.

these extra chromosomes. The relationship of these B chromosomes with the functional X chromosomes is obvious. In Euceraphis, supernumerary chromosomes are stable elements in the chromosomal set and selection that provides stability of B chromosome numbers is probably based on the development of a balanced system of their accumulation and elimination. B chromosomes are in fact non-functional X chromosomes and seem

References Blackman RL: Cytogenetics of two species of Euceraphis (Homoptera, Aphididae). Chromosoma 56: 393408(1976). Blackman RL: Chromosome numbers in the Aphididae and their taxonomic significance. Syst Ent 5:7-25 (1980a). Blackman RL: Chromosomes and parthenogenesis in aphids, in Blackman RL, Hewitt GM, Ashburner M (eds): Insect Cytogenetics. Symp R Ent Soc London 10:133-148(1980b). Blackman RL: The chromosomes of Japanese Aphididae (Homoptera) with notes on the cytological work of Orihay Shinji. Cytologia 51:59-83 (1986). Blackman RL: Stability of a multiple X chromosome system and associated B chromosomes in birch aphids (Euceraphis spp., Homoptera: Aphididae). Chromosoma 96:318-324 (1988). Blackman RL: The chromosomes of Lachnidae. Acta Phytopat Entom Hung 25:273-282 (l990). Blackman RL: Sex determination in insects, in: Leather SR, Hardie J (eds): Insect Reproduction, pp 57-94 (CRC Press, Boca Raton 1995). Blackman RL, Cahill M: The karyotype of Bemisia tabaci (Hemiptera: Aleyrodidae). Buli Entom Res 88:213-215(1998). Camacho JPM, Sharbel TF, Beukeboom LW: B-chromosome evolution. Phil Trans R Soc Lond B 355:163-178(2000).

to derive from X chromosomes rather than from other elements of the chromosomal set. In Euceraphis, the number of B chromosomes varies not only between species, but also between populations within species as in the case of Euceraphis betulae, E. punctipennis and E. mucida (Blackman, 1976, 1988). Two other aphid genera Symydobius and Clethrobius, closely related to Euceraphis, also show the presence of additional chromosomal elements interpreted as a non-functional X. In Coccoidea, a peculiar and unstable system of B chromosomes was found in the mealybug Pseudoccocus affinis (= obscurus) (Nur, 1962a, b, 1966a, b). In this species the rate of transmission and accumulation of supernumeraries is high through male meiosis, and up to eight accessory chromosomes can be present in some specimens. These Bs reduce the fitness of P. affinis individuals and are maintained because of meiotic drive. One of the first demonstrations of the existence of A chromosome genes being able to suppress B chromosome drive was reported in this species (Nur and Brett, 198-5, 1987, 1988). B chromosomes have also been described in two other species of coccids: Nautococcus schraderae (Hughes-Schrader, 1942 in Nur, 1962b) and Antoninapertiosa (Nur et al, 1987). In other suborders within Hemiptera, supernumerary chromosomes have been found only sporadically in spite of the fact that a large number of species have been karyotyped. For instance in Cicadomorpha, where karyotypes of morę than 580 species arę known, B chromosomes were described only in three species belonging to three genera (Kirillova and Kuznetsova, 1990). In Heteroptera, accessory chromosomes arę even less freąuent (see e.g. Muramoto, 1973; Mola and Papeschi, 1993).

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