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ISSN 0373-5680 Rev. Soc. Entomol. Argent. 66 (3-4): 81-89, 2007 81

New contributions to the study of Corixoidea: cytogenetic characterization of three species of from Argentina and the plausible mechanisms of karyotype evolution within

BRESSA, María José and Alba Graciela PAPESCHI

Laboratorio de Citogenética y Evolución, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria. Pabellón 2, C1428EGA, Ciudad Autónoma de Buenos Aires, Argentina; e-mail: [email protected]

Nuevas contribuciones al estudio de Corixoidea: caracterización citogenética de tres especies de Sigara de Argentina y los posibles mecanismos de evolución del cariotipo en Nepomorpha

„ RESUMEN. Los estudios citogenéticos en contribuyen al análisis de las tendencias evolutivas en el taxón. Los Heteroptera se caracterizan por poseer cromosomas holocinéticos, diferentes sistemas de cromosomas sexuales y un par de cromosomas m en algunas especies. En este trabajo describimos el cariotipo y la meiosis masculina de Sigara denseconscripta (Breddin), S. chrostowskii Jaczewski y S. rubyae (Hungerford). Las tres especies tienen un número diploide de 24, con un par de cromosomas m y un sistema de cromosomas sexuales XY/XX. Con estos resultados son 30 las especies de Corixoidea estudiadas citogenéticamente y el cariotipo modal de la superfamilia es 2n= 20+2m+XY en machos. La información citogenética disponible hasta el presente en Heteroptera nos permite sugerir que la presencia de cromosomas m y cromosomas sexuales XY/XX, serían caracteres plesiomórficos para Nepomorpha. La ausencia de cromosomas m en especies de Nepoidea y Ochteroidea, y los sistemas de cromosomas sexuales X0 y Xn0 (en machos) en especies de Corixoidea, Naucoroidea y Nepoidea, serían caracteres derivados que habrían surgido evolutivamente más tarde.

PALABRAS CLAVE. Citogenética. Heteroptera. Cromosomas holocinéticos. Meiosis. Cromosomas m.

„ ABSTRACT. Cytogenetic studies in Heteroptera contribute to the analysis of evolutionary trends within the group. Heteroptera are characterized by the possession of holokinetic chromosomes, different sex chromosome mechanisms and a pair of m chromosomes in some species. In the present work, the male karyotype and meiosis in Sigara denseconscripta (Breddin), S. chrostowskii Jaczewski, and S. rubyae (Hungerford) are described. The three species share a diploid chromosome number of 2n= 24 with a pair of m chromosomes and an XY/XX sex

Recibido: 22-V-2007; aceptado: 10-VII-2007 82 Rev. Soc. Entomol. Argent. 66 (3-4): 81-89, 2007

chromosome system. With this study the chromosome number of 30 species of Corixoidea are known and the modal karyotype is 2n= 20+2m+XY in males. The available cytogenetic information in Heteroptera led us to suggest that the presence of a pair of m chromosomes and an XY/XX sex chromosome system could be considered as plesiomorphic for Nepomorpha. The absence of m chromosomes in species of Ochteroidea and Nepoidea, and the sex chromosome systems

X0 and Xn0 (male) in species of Corixoidea, Naucoroidea, and Nepoidea should be considered as derived characters, which arose later in evolution.

KEY WORDS. Cytogenetics. Heteroptera. Holokinetic chromosomes. Meiosis. m chromosomes.

INTRODUCTION superfamily and 26 genera, with the large and widespread Sigara Fabricius being Corixoidea is the largest nepomorphan divided into many subgenera (Bachmann, group and their members are commonly 1981; Schuh & Slater, 1995). The called water boatmen. They occur worldwide cosmopolitan genus Sigara comprises in various types of stable and temporary, approximately 70 species in America, continental and insular, fresh and saline distributed from Canada to southern waters (Bachmann, 1981; Schaefer & Panizzi, Argentina in Santa Cruz province and the 2000). Corixids have a high dispersal Malvinas Islands (Bachmann, 1981; Morrone potential, which allows them to utilize et al., 2004). Micronectidae includes two various available habitats (Jannson, 1986). genera: Kirkaldy distributed in the Most of them fly very well, and they are the Old World and Australia, and Tenagobia typical invaders of water bodies, Bergroth distributed from Mexico to central including newly developed ones (Bachmann, Argentina in Buenos Aires province 1981; Schaefer & Panizzi, 2000). Corixids (Bachmann, 1981; Morrone et al., 2004). represent one of the most important True bugs, the Heteroptera, have many predators; they can feed on algal cells, cytogenetic characteristics that make them filamentous blue-greens, diatoms, unique among most insect groups: the microscopic protozoans and rotifers, small possession of chromosomes without a invertebrates, fish eggs and detritus primary constriction, the centromere, namely (Bachmann, 1981; Schaefer & Panizzi, 2000). holokinetic chromosomes; a pair of «m Various corixid species are incidental or chromosomes» in 16 families, belonging to obligatory predators on mosquito larvae in four infraorders; a different meiotic behaviour various regions of the world (Reynolds, 1975; for autosomes and sex chromosomes; and a Reynolds & Scudder, 1987a, b) and may be mean chiasma frequency of only one chiasma important control agents of mosquitoes. They per bivalent (Ueshima, 1979; Nokkala, 1986; can even be of significant importance for the Papeschi & Bressa, 2006). As a rule, development of some young stages of fish, autosomal bivalents are chiasmatic while the as food in small water bodies (Rask, 1983). sex chromosomes and m chromosomes are However, Corixids can be pests of fish achiasmatic. The m chromosomes are culture; some species are facultative predators generally of small size and show allocycly of fish eggs and larvae (Schaefer & Panizzi, with respect to both the autosomes and the 2000). sex chromosomes during male meiosis; they The superfamily Corixoidea comprises are usually unpaired and thus achiasmatic about 400 species, which are included in during early meiotic prophase (Ueshima, and Micronectidae. The former 1979; Papeschi & Bressa, 2006). contains the majority of known species of the The pattern of meiosis in the Heteroptera BRESSA, M. J. and A. G. PAPESCHI. Karyotype evolution in Corixoidea 83

Table I. Diploid chromosome number in species of Corixoidea (previous data cited in Ituarte & Papeschi, 2003, 2004 are included for comparisons)

Taxa 2n n

Corixidae Cymatinae Cymatia borsdorffi (Sahlberg) 26 (XY) -

Corixinae

Arctocorisa carinata (Sahlberg) 24 (XY) 10A+m+XY A. germari (Fieber) 24 (XY) - concinna (Fieber) 24 (XY) - C. praeusta (Fieber) 24 (XY) 10A+m+XY C. wollastoni (Douglas & Scott) 24 (XY) 10A+m+XY dentipes (Thomson) 24 (XY) 10A+m+XY C. punctata (Illiger) 24 (XY) - cavifrons (Thomson) 24 (XY) - castanea (Thomson) 24 (XY) - H. linnaei (Fieber) 24 (XY) 10A+m+XY H. sahlbergi (Fieber) 24 (XY) 10A+m+XY Krizousacorixa femorata (Guérin) 24 (XY) 10A+m+XY Sigara denseconscripta (Breddin)* 24 (XY) 10A+m+XY S. chrowstoskii Jaczewski* 24 (XY) 10A+m+XY S. distincta (Fieber) 24 (XY) 10A+m+XY S. dorsalis (Leach) 24 (XY) - S. falleni (Fieber) 24 (XY) 10A+m+XY S. fossarum (Leach) 24 (XY) 10A+m+XY S. lateralis (Leach) 24 (XY) - S. nigrolineata (Fieber) 24 (XY) 10A+m+XY S. platensis Bachmann 24 (XY) 10A+m+XY S. rubyae (Hungerford)* 24 (XY) 10A+m+XY S. scotti (Douglas & Scott) 24 (XY) - S. semistriata (Fieber) 24 (XY) 10A+m+XY S. striata (Linnaeus) 24 (XY) 10A+m+XY S. sp 24 (XY) - verticalis (Fieber) 24 (XY) -

Micronectidae Micronecta poweri (Douglas & Scott) 24 (XY) - Tenagobia fuscata (Stål) 30 (XY) 14+XY

* present contribution 84 Rev. Soc. Entomol. Argent. 66 (3-4): 81-89, 2007

varies between species, particularly for the & Scott) and Tenagobia fuscata (Stål), have behaviour of the sex chromosomes and the been cytogenetically analyzed (Table I) m chromosomes. During the early prophase, (Southwood & Leston, 1959; Ituarte & the sex chromosomes X and Y are positively Papeschi, 2004). While M. poweri has the heteropycnotic and remain in this condition modal chromosome number of Corixidae until diakinesis. By late diakinesis, the X and (2n= 24), T. fuscata presents many interesting Y chromosomes are separated from each cytogenetic features, such as achiasmatic other, become isopycnotic and each is male meiosis. Besides, both species are composed of two sister chromatids (Ueshima, characterized by the absence of an m 1979; Papeschi & Bressa, 2006). chromosome pair. Within Corixidae, nine The autosomal bivalents segregate genera and 25 species belonging to the reductionally during the first meiotic division subfamilies Cymatinae (Cymatia borsdorfii and equationally during the second division. (Sahlberg)) and (24 species) have The achiasmatic m chromosomes associate been cytogenetically analyzed (Table I) at late diakinesis end-to-end, through the so- (Ituarte & Papeschi, 2004). All species of called «touch-and-go pairing»; they form a Corixinae show a diploid chromosome pseudobivalent, which segregates number of 24, with a pair of m chromosomes reductionally at anaphase I, and divides and an XY/XX sex chromosome system (male/ equationally at the second meiotic division. female), while C. borsdorfii has 2n= 26= On the other hand, sex chromosomes behave 24+XY (Ueshima, 1979). Sigara platensis as univalents in male meiosis I; they divide Bachmann was the only cytogenetically equationally at anaphase I, associate at described species inhabiting Argentina. It meiosis II through the touch-and-go pairing possesses the diploid chromosome number and segregate reductionally at anaphase II of 24 (2n= 20+2m+XY/XX, male/female) and (Ueshima, 1979; Manna, 1984; Papeschi & all the specimens analyzed showed from one Bressa, 2007). to three supernumerary chromosomes (Ituarte In all heteropteran species, the autosomes & Papeschi, 2003). tend to form a ring on the periphery of the In the present study, male karyotype and spindle at both meiotic metaphases, with the meiotic behaviour of Sigara denseconscripta sex chromosomes lying side by side in the (Breddin), S. chrostowskii Jaczewski, and S. centre of the ring. Usually, when m rubyae (Hungerford) from the National Park chromosomes are present, the X and Y form Pre-Delta (Entre Ríos province, Argentina) are part of the ring of the autosomal bivalents at described. The cytogenetic results are first metaphase, and the m pseudobivalent discussed at the superfamily level, and lies in its centre. At second metaphase, both evolutionary trends within Nepomorpha are the X-Y pseudobivalent and the m proposed. chromosome lie in the centre of a ring formed by the autosomes (Ueshima, 1979). This arrangement at the metaphase plates has been MATERIAL AND METHODS recorded in the Corixidae (Peters & Kleba, 1971), the (Ueshima & Ashlock, All adult males of Sigara denseconscripta, 1980), and the Stenocephalidae (Lewis & S. chrostowskii and S. rubyae were collected Scudder, 1958). in the National Park Pre-Delta (Entre Ríos Previous cytogenetic studies on 27 species province, Argentina). Immediately after their of Corixoidea have shown a noticeable capture, all specimens were fixed in ethanol: karyotypic uniformity with a diploid chloroform: glacial acetic acid (6:3:1) and the chromosome number of 24, a pair of m gonads were dissected under a binocular chromosomes, and an XY/XX sex stereoscopic microscope and kept in 70% chromosome system (male/female) (Table I) ethanol at 4°C. Slides were made by the (Ueshima, 1979; Ituarte & Papeschi, 2003, squash technique in ferric acetic 2004). Up to these days only two species of haematoxylin following conventional Micronectidae, Micronecta poweri (Douglas procedures. BRESSA, M. J. and A. G. PAPESCHI. Karyotype evolution in Corixoidea 85

Fig. 1. Male meiosis of Sigara denseconscripta (a-f), S. chrostowskii (g) and S. rubyae (h, i). a) Pachytene; b) Diakinesis; c) Late Diakinesis; d) Metaphase I; e) Telophase I; f) Metaphase II; g) Metaphase I; h) Diakinesis with a pair of univalents (I); i) Metaphase I. Arrows point the sex chromosomes and arrowheads point the smallest autosomal bivalent. N= nucleolus; m= m chromosomes. Scale bar = 10 μm.

RESULTS chromosome as big as the medium-sized pair of autosomes. The Y chromosome is similar Sigara denseconscripta, S. chrostowskii, in size to the smallest autosomal pair in Sigara and S. rubyae possess a male diploid rubyae and S. chrostowskii, whereas it is chromosome number of 24 (2n= 20+2m+XY) smaller than the smallest bivalent in S. and a haploid chromosome number of 13 (n= denseconscripta. 10+m+XY) (Fig. 1). All of them present three At early meiotic prophase, the sex large, six medium-sized and one small pair chromosomes X and Y are positively of autosomes. The m chromosomes are the heteropycnotic and lie close to each other smallest of the complement and negatively (Fig. 1a). From pachytene to diplotene, a heteropycnotic. The sex chromosome system conspicuous nucleolus is observed associated is XY/XX (male/female), being the X with both sex chromosomes (Fig. 1a). At 86 Rev. Soc. Entomol. Argent. 66 (3-4): 81-89, 2007

Fig. 2. Distribution of male chromosome numbers, sex chromosome systems and presence/absence of m chromosomes in the families and superfamilies of Nepomorpha based on cytogenetic evidence.

diplotene-diakinesis, the X and Y univalents equationally (Fig. 1e). remain close to each other, while the m Second meiotic metaphase follows chromosomes are always separated and immediately after telophase I, without an negatively heteropycnotic. Autosomal interkinesis stage. At metaphase II, the X and bivalents generally present one chiasma Y chromosomes are associated forming a terminally located, but the three largest pseudobivalent (Fig. 1f). The autosomes and bivalents can show one chiasma at interstitial the sex pseudobivalent dispose at the position (Fig. 1b, d, h, i). From diakinesis equatorial plane forming a ring, and the m onwards, the m chromosomes begin to get chromosome lies in its centre. At anaphase closer and associate end-to-end to form a II, the X and Y segregate to opposite poles. pseudobivalent (pII) (Fig. 1b, c, h). At metaphase I, the m pseudobivalent lies in the centre of the ring formed by the autosomal DISCUSSION bivalents, and the X and Y univalents orientated side-by-side (Fig. 1d, f, i). At Heteroptera comprises eight infraorders, anaphase I the autosomal bivalents, as well and cytogenetic reports are unequally as the m pseudobivalent, divide reductionally distributed not only among these major while the sex chromosomes segregate groups, but also within them. At present, BRESSA, M. J. and A. G. PAPESCHI. Karyotype evolution in Corixoidea 87 approximately 1600 heteropteran species pair characteristic of Corixoidea could lose belonging to 46 families have been its particular meiotic behaviour and become cytogenetically analyzed. The male diploid a regular autosomal pair, contributing thus chromosome number of Heteroptera ranges to the increase in the diploid chromosome from 2n= 4 (Lethocerus sp., ) number of the species. to 80 (four species of Lopidea Uhler, ). Up to these days, 11 species of Sigara have Even though the most represented diploid been cytogenetically analyzed and only one number is 14 (460 species), 70% of the of them inhabits Argentina, namely Sigara species have diploid numbers between 12 to platensis Bachmann. Sigara platensis 34 chromosomes (Papeschi & Bressa, 2006). possesses the diploid chromosome number The study of karyotype evolution and the of 24 (2n= 20+2m+XY/XX, male/female), and mechanisms of chromosome change can all the specimens analyzed had from one to contribute to the understanding of the three supernumerary chromosomes (Ituarte evolution and taxonomic relationships & Papeschi, 2003). because the karyotypes are species-specific Sigara denseconscripta, S. rubyae, and S. characters. Discussions on karyotype chrostowskii show similarities in karyotype evolution in Heteroptera use the concept of (2n= 24= 20+2m+XY) and meiotic behaviour modal number, i.e., the commonest diploid to the species previously analyzed. From all number present in a group, such as family, these results, we suggest that Corixidae is a tribe or genera. The modal number is cytogenetically homogenous family, and an frequently considered as the ancestral one for ancestral karyotype of Corixoidea should be the group under analysis (Ueshima, 1979; 2n= 24= 20+2m+XY. Papeschi & Bressa, 2006). Concerning the chromosome Within Nepomorpha, 96 species have arrangements at the meiotic metaphase plates been cytogenetically characterized, and the in the three species of Sigara analyzed in families Belostomatidae and Corixidae have this paper, there is a deviation from the typical been the most extensively analyzed (27 and disposition described in Corixidae. During 25 species, respectively). So far, from the 27 metaphase II, the sex pseudobivalent disposes cytogenetically studied species of Corixoidea, at the equatorial plane forming part of the two belong to Micronectidae and the ring of autosomes, and only the m remaining 25 are included in Corixidae. chromosome lies in its centre. The Within the former, Micronecta poweri has the significance of this different pattern of modal chromosome number of Corixidae chromosome arrangement at metaphase (2n= 24), while Tengobia fuscata presents a plates remains obscure. higher diploid number (2n= 30) and an The m chromosomes in Heteroptera are achiasmatic male meiosis. Besides, both defined by their special meiotic behaviour: species are characterized by the absence of achiasmatic, and associated through a touch- an m chromosome pair (Ituarte & Papeschi, and-go pairing at first meiotic division. 2004; Papeschi & Bressa, 2007). However, nothing is known about the genetic On the other hand, all the species of information that the m chromosomes carry Corixidae show a diploid chromosome and their function in the genetic system of number of 24, with a pair of m chromosomes the species possessing them. The m and an XY/XX sex chromosome system (male/ chromosomes have been reported in 14 female), except Cymatia borsdorfii (2n= 26= heteropteran families, but are absent in 24+XY) (Ueshima, 1979; Ituarte & Papeschi, and (Papeschi 2003, 2004; Papeschi & Bressa, 2006). & Bressa, 2006, 2007). Considering that fusions and fragmentations From a cytogenetic point of view are the main mechanisms of karyotype Nepomorpha may be regarded as containing evolution in Heteroptera, the chromosome five groups: Nepoidea, Ochteroidea, number of C. borsdorfii could probably Naucoroidea, Corixoidea, and originate by the fragmentation of a pair of Notonectoidea. All of them with the only autosomes. Furthermore, the m chromosome exception Lethocerus sp. (Belostomatidae) 88 Rev. Soc. Entomol. Argent. 66 (3-4): 81-89, 2007

share a high diploid chromosome number chromosome systems X0 and Xn0 of the (Fig. 2). A total of 38 species analyzed from Corixoidea, Naucoroidea and Nepoidea most Nepoidea lack m chromosomes and show probably originated during the evolution both simple and multiple sex chromosome through the loss of the Y chromosome (X0)

systems (XY, XnY); the diploid number ranges and in some species fragmentation of the

between 4 and 46. In the second group, the original X chromosome (Xn0). On the other Ochteroidea, only one species has been hand, the m chromosomes had become lost studied; oculatus has 2n= at the origin of the superfamilies Nepoidea

30+X1X2X3X4Y, and no m chromosomes have and Ochteroidea. Summarizing, both the X0

been recognized. In Naucoroidea, ten species and Xn0 systems in Corixoidea, Naucoroidea of are characterized by the and Nepoidea, and the absence of a pair of possession of a pair of m chromosomes and m chromosomes in Nepoidea and an X0 sex chromosome system. The diploid Ochteroidea should be considered as derived number varies from 20 to 51 in males. Within characters within Nepomorpha. Notonectoidea, the 17 species analyzed present m chromosomes, simple and multiple

sex chromosome systems (XY, X0, Xn0), and ACKNOWLEDGEMENTS a diploid number 2n= 23-26 (Ueshima, 1979; Manna, 1984; Papeschi & Bressa, 2006) (Fig. The authors wish to thank Dr. Axel O. 2). Bachmann for taxonomical identification of Taking into account the phylogenetic the specimens and his continuous relationships of families and superfamilies of encouragement for the study of aquatic Nepomorpha proposed by Rieger (1976) and heteropterans. The authors also thank Mahner (1993), the «primitive» superfamilies Administración de Parques Nacionales Nepoidea and Ochteroidea show both simple (Dirección de Conservación y Manejo). The and multiple sex chromosome systems (XY present study was supported by grants from

and XnY), and lack m chromosomes. The the Buenos Aires University (UBA) (X317) and Corixoidea and two other superfamilies, CONICET (PIP 5261). M. J. Bressa and A. Naucoroidea and Notonectoidea, present a Papeschi are members of the National pair of m chromosomes and show variable Council of Scientific and Technological

sex chromosome systems (XY, X0 and Xn0). Research (CONICET). Based on the presence of a Y chromosome in very primitive heteropteran species, Nokkala & Nokkala (1983, 1984) and LITERATURE CITED Grozeva & Nokkala (1996) suggested that the X0 system is a derived condition from the 1. BACHMANN, A. O. 1981. Insecta ancestral XY that is present in the majority of Corixidae. In: Ringuelet, R. A. (ed.), Fauna de agua dulce de la República Argentina, FECIC, the species cytogenetically analyzed. La Plata, pp. 270+plates I-XXXIV. Furthermore, from the finding of a pair of m 2. GROZEVA, S. & S. NOKKALA. 1996. Chromosomes chromosomes in three species of and their meiotic behavior in two families of the and two species of primitive infraorder (Heteroptera). Hereditas 125: 31-36. (Dispsocoromorpha), 3. ITUARTE, S. & A. G. PAPESCHI. 2003. Complemento Grozeva & Nokkala (1996) suggested that this cromosómico y comportamiento meiótico de pair of chromosomes might be included in Sigara platensis Bachmann, 1962 (Corixidae, the ancestral karyotype of the Heteroptera. Heteroptera). In: Huerta Grande, Córdoba, pp. 101. Under these hypotheses, and according to the 4. ITUARTE, S. & A. G. PAPESCHI. 2004. Achiasmatic available cytogenetic data of Nepomorpha, male meiosis in Tenagobia (Fuscagobia) fuscata we suggest that the presence of XY sex (Heteroptera, Corixoidea, Micronectidae). chromosome system and a pair of m Genetica 122: 199-206. 5. JANNSON, A. 1986. The Corixidae (Heteroptera) of chromosomes could be considered Europe and some adjacents regions. Acta plesiomorphic characters for this infraorder Entomol. Fenn. 47: 1-94. (Fig. 2). On the one hand, the sex BRESSA, M. J. and A. G. PAPESCHI. Karyotype evolution in Corixoidea 89

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