The neo-X and neo-Y sex chromosomes of Dysdercus albofasciatus represent a unique model for the study of early stages of sex chromosome evolution since they retained the ability to pair and recombine, in contrast to sex chromosomes in most Heteroptera. Here we examined structure, molecular differentiation, and meiotic behaviour of the D. albofasciatus neo-sex chromosomes. Two related species with the ancestral X0 system, D. chaquensis and D. ruficollis, were used for a comparison. In D. albofasciatus, 2 nucleolar organizer regions (NORs) were identified on the neo-X chromosome using fluorescence in situ hybridization (FISH) with an rDNA probe, whereas a single NOR was found on an autosomal pair in the other 2 species. Genomic in situ hybridization (GISH) differentiated a part of the original X in the neo-X chromosome but not the neo-Y chromosome. The same segment of the neo-X chromosome was identified by Zoo-FISH with a chromosome painting probe derived from the X chromosome of D. ruficollis, indicating that this part is conserved between the species. Immunostaining against the cohesin subunit SMC3 revealed that only terminal regions of the D. albofasciatus neo-Xneo-Y bivalent pair and form a synaptonemal complex, which is in keeping with the occurrence of terminal chiasmata, whereas the interstitial region forms a large loop indicating the absence of homology. These results support the hypothesis that the neo-X chromosome evolved by insertion of the original X chromosome into 1 NOR-bearing autosome in an ancestor carrying the X0 system. As a consequence, the homologue of this NOR-autosome became the neo-Y chromosome. A subsequent inversion followed by transposition of the NOR located on the neo-Y onto the neo-X chromosome resulted in the present neo-sex chromosome system in D. albofasciatus.

Keywords:
Chromosome painting, Evolution, GISH, NOR, Ribosomal DNA, Sex chromosomes, Synaptonemal complex, Zoo-FISH
1.
Arnheim N, Krystal M, Schmickel R, Wilson G, Ryder O, et al: Molecular evidence for genetic exchange among ribosomal genes on non-homologous chromosomes in man and apes. Proc Nat Acad Sci USA 77:7323–7327 (1980).
2.
Ayling LJ, Griffin DK: The evolution of sex chromosomes. Cytogenet Genome Res 99:125–140 (2002).
3.
Bachtrog D: A dynamic view of sex chromosome evolution. Curr Opin Genet Dev 16:578–585 (2006).
4.
Bedo DG: Karyotypic and chromosome banding studies of the potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera, Gelechiidae). Can J Genet Cytol 26:141–145 (1984).
5.
Bergero R, Charlesworth D: The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24:95–102 (2009).
6.
Bressa MJ, Papeschi AG, Mola LM, Larramendy ML: Meiotic studies in Dysdercus Guérin Méneville 1831 (Heteroptera: Pyrrhocoridae). I. Neo-XY in Dysdercus albofasciatus Berg 1878, a new sex chromosome determining system in Heteroptera. Chromosome Res 7:503–508 (1999).
7.
Bressa MJ, Fumagalli E, Ituarte S, Frassa MV, Larramendy ML: Meiotic studies in Dysdercus Guérin Méneville 1831 (Heteroptera: Pyrrhocoridae). II. Evidence on variations of the diffuse stage between wild and laboratory-inbred populations of Dysdercus chaquensis Freiberg, 1948. Hereditas 137:125–131 (2002).
8.
Bressa MJ, Papeschi AG, Fumagalli E, van Doesburg PH, Larramendy M: Cytogenetic and nucleolar meiotic cycle analyses in Dysdercus imitator Blote, 1931 (Heteroptera, Pyrrhocoridae) from Argentina. Folia Biol 51:135–141 (2003).
9.
Bressa MJ, Larramendy M, Papeschi AG: Heterochromatin characterization in five species of Heteroptera. Genetica 124:307–317 (2005).
10.
Cattani MV, Papeschi AG: Nucleolus organizing regions and semi-persistent nucleolus during meiosis in Spartocera fusca (Thurnberg) (Coreidae, Heteroptera). Hereditas 140:105–111 (2004).
11.
Cattani MV, Greizerstein EJ, Papeschi AG: Male meiotic behaviour and nucleolus organizing regions in Camptischium clavipes (Fabr.) (Coreidae, Heteroptera) analyzed by fluorescent banding andin situ hybridization. Caryologia 57:267–273 (2004).
12.
Charlesworth D, Charlesworth BW, Marais G: Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128 (2005).
13.
Chickering AM: An unusual complex in Lethocerus. Anat Rec 37:156 (1927).
14.
Chickering AM, Bacorn B: Spermatogenesis in the Belostomatidae. IV. Multiple chromosomes in Lethocerus. Pap Mich Acad Sci 17:529–533 (1933).
15.
Criniti A, Simonazzi G, Cassanelli S, Ferrari M, Bizzaro D, et al: Distribution of heterochromatin and rDNA on the holocentric chromosomes of the aphids Dysaphis plantaginea and Melanaphis pyraria (Hemiptera: Aphididae). Eur J Entomol 106:153–157 (2009).
16.
Flores SV, Evans AL, McAllister BF: Independent origins of new sex-linked chromosomes in the melanica and robusta species groups of Drosophila. BMC Evol Biol 8:33 (2008).
17.
Franco M, Bressa MJ, Papeschi AG: Karyotype and male meiosis in Spartocera batatas (Fabricius) and meiotic behaviour of multiple sex chromosomes in Coreidae, Heteroptera. Eur J Entomol 103:9–16 (2006).
18.
Fuková I, Nguyen P, Marec F: Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome 48:1083–1092 (2005).
19.
Fuková I, Traut W, Vítková M, Nguyen P, Kubíčková S, et al: Probing the W chromosome of the codling moth, Cydia pomonella, with sequences from microdissected sex chromatin. Chromosoma 116:135–145 (2007).
20.
Gokhman VE, Kuznetsova V: Comparative insect karyology: current state and applications. Entomol Rev 86:352–368 (2006).
21.
Haaf T, Schmid M: An early stage of ZW/ZZ sex chromosome differentiation in Poecilia sphenops var. melanistica (Poeciliidae, Cyprinodontiformes). Chromosoma 89:37–41 (1984).
22.
Henking H: Untersuchungen über die ersten Entwicklungsvorgänge in den Eiern der Insekten. II. Über Spermatogenese und deren Beziehung zur Eientwicklung bei Pyrrhocoris apterus L. Z wiss Zool 51:685–736 (1891).
23.
Iturra P, Veloso A: Further evidence for early sex chromosome differentiation of Anuran species. Genetica 78:25–31 (1989).
24.
Jacobs DH: The evolution of a neo-XY1Y2 sex chromosome system by autosome-sex chromosome fusion in Dundocoris nodulicarinus Jacobs (Heteroptera: Aradidae: Carventinae). Chromosome Res 12:175–191 (2004).
25.
Jande SS: An analysis of the chromosomes in the four species of the family Belostomatidae (Heteroptera, Cryptocerata). Res Bull (N.S.) Panjab Univ 10:25–34 (1959).
26.
Jones KW, Singh L: Snakes and the evolution of sex chromosomes. Trends Genet 1:55–61 (1985).
27.
Kejnovsky E, Hobza R, Cermak T, Kubat Z, Vyskot B: The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity 102:533–541 (2009).
28.
Kubickova S, Cernohorska H, Musilova P, Rubes J: The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Chromosome Res 10:571–577 (2002).
29.
Lockwood APM: ‘Ringer’ solutions and some notes on the physiological basis of their ionic composition. Comp Biochem Physiol 2:241–289 (1961).
30.
Manna GK: Chromosomes in evolution in Heteroptera; in Sharma AK, Sharma A (eds): Chromosomes in Evolution of Eukaryotic Groups, Vol II, pp 189–225 (CRC Press, Boca Raton 1984).
31.
Marec F: Synaptonemal complex in insects. Int J Insect Morphol Embryol 25:205–233 (1996).
32.
Messthaler H, Traut W: Phases of sex chromosomes inactivation in Oncopeltus fasciatus and Pyrrhocoris apterus (Insecta, Heteroptera). Caryologia 28:501–510 (1975).
33.
Mola LM, Papeschi AG: Citogenética de Dysdercus chaquensis (Heteroptera: Pyrrhocoridae). Rev Soc Entomol Argent 56:20 (1997).
34.
Moses MJ, Poorman PA, Roderick TH, Davisson MT: Synaptonemal complex analysis of mouse chromosomal rearrangements IV. Synapsis and synaptic adjustment in two paracentric inversions. Chromosoma 84:457–474 (1982).
35.
Nanda I, Schartl M, Feichtinger J, Epplen JT, Schmid M: Early stages of sex chromosome differentiation in fish as analysed by simple repetitive DNA sequences. Chromosoma 101:301–310 (1992).
36.
Nokkala S, Nokkala C: Chromosomes in two bug species of Hebrus (Hebridae, Heteroptera). The occurrence of neo-XY sex chromosome system in Heteroptera. Caryologia 52:27–30 (1999).
37.
Panzera F, Perez R, Panzera Y, Alvarez F, Scvortzoff E, et al: Karyotype evolution in holocentric chromosomes of three related species of triatomines (Hemiptera-Reduviidae). Chromosome Res 3:143–150 (1995).
38.
Papeschi AG: C-banding and DNA content in three species of Belostoma (Heteroptera) with large differences in chromosome size and number. Genetica 76:43–51 (1988).
39.
Papeschi AG: DNA content and heterochromatin variation in species of Belostoma (Heteroptera, Belostomatidae). Hereditas 115:109–114 (1991).
40.
Papeschi AG, Bressa MJ: Evolutionary cytogenetics in Heteroptera. J Biol Res 5:3–21 (2006).
41.
Papeschi AG, Mola LM, Bressa MJ, Greizerstein EJ, Lia V, et al: Behaviour of ring bivalents in holokinetic systems: alternative sites of spindle attachment in Pachylis argentinus and Nezara viridula (Heteroptera). Chromosome Res 11:725–733 (2003).
42.
Pigozzi MI, Solari AJ: Differential immunolocalization of a putative Rec8p in meiotic autosomes and sex chromosomes of triatomine bugs. Chromosoma 112:38–47 (2003).
43.
Piza SdT: Cromossômios de Dysdercus (Hemiptera-Pyrrhocoridae). An Esc Sup Agric ‘Luiz de Queiroz’ 4:209–216 (1947a).
44.
Piza SdT: Comportamento dos cromossômios sexuais de Dysdercus mendesi na segunda divisão dos espermatócitos. Bragantia 7:269–271 (1947b).
45.
Piza SdT: Interpretacão do typo sexual de ‘Dysdercus mendesi’ Bloete (Hemiptera Pyrrhocoridae). Genet Iber 3:107–112 (1951).
46.
Ray-Chaudhuri SP, Manna GK: A new type of segregation of the sex chromosomes in the meiotic divisions of the cotton stainer Dysdercus koenigii (Fabr.). J Genet 51:191–197 (1952).
47.
Rebagliati P, Papeschi AG, Mola LM: Meiosis and fluorescent banding in Edessa meditabunda and E. rufomarginata (Heteroptera: Pentatomidae: Edessinae). Eur J Entomol 100:11–18 (2003).
48.
Roy V, Monti-Dedieu L, Chaminade N, Siljak-Yakovlev S, Aulard S, et al: Evolution of the chromosomal location of rDNA genes in two Drosophila species subgroups: ananassae and melanogaster. Heredity 94:388–395 (2005).
49.
Ruthmann A, Dahlberg R: Pairing and segregation of the sex chromosomes in X1X2-males of Dysdercus intermedius with a note on the kinetic organization of heteropteran chromosomes. Chromosoma 54:89–97 (1976).
50.
Sahara K, Marec F, Traut W: TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7:449–460 (1999).
51.
Schempp W, Schmid M: Chromosome banding in Amphibia. VI. BrdU-replication patterns in Anura and demonstration of XX/XY sex chromosomes in Rana esculenta. Chromosoma 83:697–710 (1981).
52.
Schrader F: The formation of tetrads and the meiotic mitoses in the male of Rhytidolomia senilis Say (Hemiptera, Heteroptera). J Morph 67:123–141 (1940).
53.
Schubert I: Chromosome evolution. Curr Opin Plant Biol 10:109–115 (2007).
54.
Schubert I, Wobus U: In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92:143–148 (1985).
55.
Solari AJ: Autosomal synaptonemal complexes and sex chromosomes without axes in Triatoma infestans (Reduviidae; Hemiptera). Chromosoma 72:225–240 (1979).
56.
Steinemann M, Steinemann S: Degenerating Y chromosome of Drosophila miranda: a trap for retrotransposons. Proc Natl Acad Sci USA 89:7591–7595 (1992).
57.
Steinemann M, Steinemann S: Enigma of Y chromosome degeneration: Neo-Y and Neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution. Genetica 102/103:409–420 (1998).
58.
Steinemann S, Steinemann M: Retroelements: tools for sex chromosome evolution. Cytogenet Genome Res 110:134–143 (2005).
59.
Suja JA, del Cerro AL, Page J, Rufas JS, Santos JL: Meiotic sister chromatid cohesion in holocentric sex chromosomes of three heteropteran species is maintained in absence of axial elements. Chromosoma 109:35–43 (2000).
60.
Toscani MA, Pigozzi MI, Bressa MJ, Papeschi AG: Synapsis with and without recombination in the male meiosis of the leaf-footed bug Holhymenia rubiginosa (Coreidae, Heteroptera). Genetica 132:173–178 (2008).
61.
Traut W: Pachytene mapping in the female silkworm Bombyx mori L. (Lepidoptera). Chromosoma 58:275–284 (1976).
62.
Traut W: Sex determination in the fly Megaselia scalaris, a model system for primary steps of sex chromosome evolution. Genetics 136:1097–1104 (1994).
63.
Traut W: The evolution of sex chromosomes in insects: differentiation of sex chromosomes in flies and moths. Eur J Entomol 96:227–235 (1999).
64.
Traut W, Sahara K, Otto TD, Marec F: Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma 108:173–180 (1999).
65.
Traut W, Sahara K, Marec F: Sex chromosomes and sex determination in Lepidoptera. Sex Dev 1:332–346 (2007).
66.
Ueshima N: Hemiptera II: Heteroptera; in John B (ed): Animal Cytogenetics, Vol 3: Insecta 6, pp V+117 (Gebrüder Borntraeger, Berlin-Stuttgart 1979).
67.
Vítková M, Fuková I, Kubíčková S, Marec F: Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosome Res 15:917–930 (2007).
68.
Volff JN, Nanda I, Schmid M, Schartl M: Governing sex determination in fish: Regulatory putsches and ephemeral dictators. Sex Dev 1:85–99 (2007).
69.
Vyskot B, Hobza R: Gender in plants: sex chromosomes are emerging from the fog. Trends Genet 20:432–438 (2004).
70.
Whiting MF: Phylogeny of the holometabolous insect orders: molecular evidence. Zoologica Scripta 31:3–15 (2002).
71.
Yoshido A, Marec F, Sahara K: Resolution of sex chromosome constitution by GISH and telomere-FISH in some species of Lepidoptera. Chromosoma 114:193–202 (2005).
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