Caryologia. International Journal of Cytology, Cytosystematics and Cytogenetics 72(2): 91-95, 2019 Firenze University Press www.fupress.com/caryologiaCaryologia International Journal of Cytology, Cytosystematics and Cytogenetics ISSN 0008-7114 (print) | ISSN 2165-5391 (online) | DOI: 10.13128/cayologia-239 Citation: N.M. Travenzoli, I.C. de Oliveira Barbosa, G.A. Carvalho-Zilse, T.M.F. Salomão, D.M. Lopes (2019) Karyotypic description and repetitive DNA chromosome mapping of Melipo- na interrupta Latreille, 1811 (Hyme- noptera: Meliponini). Caryologia 72(2): 91-95. doi: 10.13128/cayologia-239 Published: December 5, 2019 Copyright: © 2019 N.M. Travenzoli, I.C. de Oliveira Barbosa, G.A. Carval- ho-Zilse, T.M.F. Salomão, D.M. Lopes. This is an open access, peer-reviewed article published by Firenze University Press (http://www.fupress.com/caryo- logia) and distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All rel- evant data are within the paper and its Supporting Information files. Competing Interests: The Author(s) declare(s) no conflict of interest. Karyotypic description and repetitive DNA chromosome mapping of Melipona interrupta Latreille, 1811 (Hymenoptera: Meliponini) Natália Martins Travenzoli1, Ingrid Cândido de Oliveira Barbosa2, Gislene Almeida Carvalho-Zilse2, Tânia Maria Fernandes Salomão3, Denilce Meneses Lopes1,* 1 Laboratório de Citogenética de Insetos, Departamento de Biologia Geral, Universidade Federal de Viçosa, CEP 36570-900, Viçosa, Minas Gerais, Brazil 2 Grupo de Pesquisas em Abelhas, Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia (INPA), CEP 69067-375, Manaus, Amazonas, Brazil 3 Laboratório de Biologia Molecular de Insetos, Departamento de Biologia Geral, Univer- sidade Federal de Viçosa, CEP 36570-900, Viçosa, Minas Gerais, Brazil *Corresponding author: denilce.lopes@ufv.br Abstract. Heterochromatic patterns in the genus Melipona vary among subgenera spe- cies. Melikerria is the only subgenus that presents species with different content of heterochromatin. Thus, the cytogenetic knowledge of other species of this subgenus is important for the understanding of karyotype evolution in Melipona. Here, we describe the karyotype of Melipona (Melikerria) interrupta based on the chromosomal hetero- chromatic patterns, AT and GC richness, mapping sequences of rDNA, microsatellites and telomeric regions. We observed 2n=18 chromosomes, with a high heterochromatin content rich in AT and euchromatic regions rich in GC base pairs. The high GC con- tent was observed at interstitial region near the junction of the stained euchromatin and heterochromatin of the first chromosomal pair, the same region marked for the rDNA 18S locus. Microsatellites hybridized only on euchromatin regions and the telo- meric probe on terminal regions of all chromosomes. Melipona (Melikerria) interrupta belongs to previous described heterochromatic Group II, suggesting there has been an increase in heterochromatin content in Melikerria. The M. quinquefasciata, belonging to the same subgenus as Melipona (Melikerria) interrupta, has low content of hetero- chromatin and appears to be evolving independently. So, the differences in the content heterochromatin, in the marker regions of CMA3 and the rDNA 18S locus in species of Melikerria is an important feature to be investigated further. Keywords. Cytogenetics, Fluorescence in situ Hybridization (FISH), Heterochromatin, Melikerria, Stingless bee. 1. INTRODUCTION Bees of the genus Melipona Illiger, 1806, are eusocial insects belonging to the Meliponini tribe and occur throughout the Neotropical region (Michener 2007; Camargo and Pedro 2013). This genus is represented by 73 species, 43 92 Natália Martins Travenzoli et al. of which can be found in Brazil (Camargo and Pedro 2013; Pedro 2014). Morphologically, the genus Melipona is grouped into four subgenera: Eomelipona, Meliker- ria, Melipona stricto sensu, and Michmelia (Camargo and Pedro 2013). The Melikerria, Melipona stricto sensu, and Michmelia subgenera are considered monophyl- etic, whereas Eomelipona is polyphyletic according to molecular phylogenies (Rasmussen and Cameron 2010; Ramírez et al. 2010). Cytogenetically, only 28 of all the Melipona species have had their karyotypes described. These species are characterized by a conserved diploid number of 2n = 18 chromosomes in females and n = 9 in males, except for M. seminigra merrilae and M. seminigra pernigra, with 2n = 22 (Francini et al. 2011). In addition, the pattern of heterochromatin distribution in some Melipona spe- cies differs from that observed in the majority of spe- cies in the Meliponini tribe (reviewed in Tavares et al. 2017; Cunha et al. 2018; Silva et al. 2018). The genus can be divided into two groups based on the pattern of dis- tribution and content of heterochromatin: Group I is composed of species with low heterochromatin content present only in the pericentromeric regions, similar to that in the other Meliponini; and Group II comprised by species with a high heterochromatin content that covers large extensions of their chromosomes (Rocha and Pom- polo 1998; Rocha et al. 2002). From all the analyzed species, those belonging to the Eomelipona and Melipona stricto sensu subgenera present low levels of heterochromatin, whereas all those of the subgenus Michmelia have high levels of hetero- chromatin (Rocha and Pompolo 1998; Rocha et al. 2002; Rocha et al. 2003; Lopes et al. 2011; Cunha et al. 2018). However, Melikerria has only three species described cytogenetically that present the two patterns: Melipona fasciculata Smith, 1854 and Melipona grandis Guérin, 1844, with high content of heterochromatin and Melipo- na quinquefasciata Lepeletier, 1836 with a low content (Rocha et al. 2002; Rocha 2002; Lopes et al. 2011), mak- ing heterochromatic evolution in this group difficult to elucidate. Thus, cytogenetic studies with other species of the subgenus Melikerria are needed since they may help to elucidate the processes leading to the chromosomal alterations in the genus. The aim of this study was to characterize the kary- otype of Melipona (Melikerria) interrupta based on the heterochromatin distribution pattern and chromosomal regions rich in Guanine-Cytosine (GC) and Adenine- Thymine (AT) base pairs, as well as mapping the ribo- somal 18S DNA sites, the microsatellites GA(15), GAG(10), CAA(10), and CGG(10), and the regions containing telom- eric TTAGG(6) sequences. 2. MATERIAL AND METHODS Larvae of Melipona (Melikerria) interrupta were collected from three colonies in Itacoatiara, Amazo- nas, Brazil and kept in the Meliponary of the Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazônia, Brazil. Mitotic chromosomes were obtained from the larval brain ganglia at the last larval instar as described by Imai et al. (1988), and stained with Giem- sa. The heterochromatin regions were visualized by the C-band technique (Sumner 1972) and the DAPI and CMA3 fluorochromes were used according to Schweizer (1980). Fifteen individuals were used, with 10 meta- phases being analyzed on average for each slide. The images were obtained with an Olympus BX60 epifluores- cence microscope, using Olympus Q-Color3™ software Olympus® images. Fluorescent in situ Hybridization (FISH) was per- formed according to Pinkel et al. (1986), with modifi- cations: (metaphase chromosomes were denatured in 70%/2xSSC formamide at 75 °C for 5 min; the probes were hybridized with chromosomes in 20 µL of hybridi- zation mix and heated for 10 min at 85 o C). The 18S ribosomal DNA probe was labeled with digoxigenin- 11-dUTP (Roche Applied Science) and the signal was detected wit h anti-digoxigenin-rhodamine (Roche Applied Science). This probe was obtained by Poly- merase Chain Reaction (PCR) amplification, using the primers F1(5′-GTCATATGTTGTCTCAAAGA-3′) and 18SR1.1 (3′-TCTA ATTTTTTCA A AGTA A ACGC-5′) designed for the species Melipona quinquefasciata (Pereira 2006). The microsatellites GA(15), GAG(10), CAA(10), CGG(10), and TTAGG(6) were labeled directly with Cy3 in the 5′ regions (Sigma, St. Louis, MO, USA). The metaphase images were obtained with an Olympus BX53 microscope fitted with an Olympus DP73F cam- era, using the CellSens Imaging software. 3. RESULTS AND DISCUSSION The chromosome number observed in M. (Meliker- ria) interrupta was 2n = 18 (Fig. 1a) similar the number finding by Barbosa (2018), which does not differ from that reported by Kerr (1969, 1972). The C-band revealed a karyotype with high heterochromatin content (Fig. 1b), making visualization of the centromere difficult. Thus, we could not identify chromosome morphology to deter- mine the karyotype of this species. Based on the hetero- chromatic patterns, M. (Melikerria) interrupta can be classified as belonging to the group composed of species with more than 50% of heterochromatin in their chro- 93Karyotypic description and repetitive DNA chromosome mapping of Melipona interrupta mosomes, designated as Group II by Rocha and Pom- polo et al. (1998). The species M. (Melikerria) fasciculata and M. (Melikerria) grandis were classified as belonging to this group (Lopes et al. 2011; Andrade-Souza et al. 2018) as well as M. (Melikerria) interrupta. Unlike, M. (Melikerria) quinquefasciata has a low heterochroma- tin content (Rocha et al. 2007), indicating that the kar- yotype of M. quinquefasciata may be evolving indepen- dently or have been the karyotype plesiomorphic within the Melikerria. So, in this subgenus may have been an increase in the levels of heterochromatin in the karyo- type of the species. In fact, it has been, suggested that independent amplification of heterochromatin or dif- ferentiation in distinct Melipona subgenus (Piccoli et al. 2018). Staining with the base-specific fluorophores, DAPI and CMA3, indicated that the heterochromatic regions were DAPI+ (Fig. 1c) and the euchromatic regions were CMA3+. Stronger labeling with CMA3 was seen in the interstitial region near the euchromatin and heterochro- matin junction of the first chromosomal pair (Fig. 1d), coincident with the hybridization site of the 18S rDNA probe (Fig. 2a). Staining with DAPI has shown that het- erochromatin in eusocial bees is generally AT-rich (Brito et al. 2003; Rocha et al. 2003; Lopes et al. 2011; Godoy et al. 2013). This characteristic seems to be shared by Melipona species that contain either high or low levels of heterochromatin. Although the numbers of CMA3+ and rDNA mark- ers on a single pair of chromosomes are conserved traits in the genus (Cunha et al. 2018; Andrade-Souza et al. 2018), the chromosomal positions differ among spe- cies, even in those with a high heterochromatin content. According to the results of CMA3+ and rDNA probe, species with a low heterochromatin content exhibit- ed pericentromeric markings in the first chromosome pair, while Group II species showed terminal markings (reviewed in Cunha et al. 2018). Although M. (Meliker- ria) interrupta is classified as belonging to Group II, CMA3+ and rDNA markings were observed in the inter- stitial region of the first chromosomal pair. Melipo- na (Melikerria) fasciculata and M. (Melikerria) gran- dis, which belongs to the same subgenus, also showed CMA3+ markings in this region (Lopes et al. 2011; Andrade-Souza et al. 2018), different to that observed in the other species with high heterochromatin content (reviewed in Cunha et al. 2018). These results suggest that variation in the positions of GC rich regions and 18S rDNA sites may be results of divergent heterochro- matin evolutionary pathways in the Melipona as sug- gested by Cunha et al. (2018) and Picolli et al (2018). As the markings in other species of Group II is at the chro- mosome end, the occurrence of rearrangements, such as inversion, would result in a portion of heterochromatin at the ends of the chromosome. However, we did not find heterochromatin in these regions suggesting that the position of CMA3 and rDNA no result of chromo- some inversion events. The microsatellite probes GA(15), GAG(10), CAA(10), and CGG(10) labeled only euchromatin regions (Fig. 2b-e), while the telomeric probe TTAGG(6) showed staining in the terminal regions of the chromosomes of M. (Melikerria) interrupta (Fig. 2f ). This staining pat- tern in regions of euchromatin was also observed in the chromosomal mapping of Melipona scutellaris Latreille, 1811 using different repetitive DNA sequences (CA(15), GAC(10), and TAA(10)) (Piccoli et al. 2018). The TTAGG(6) labeling on the terminal regions of the chromosomes indicated the presence of the TTAGG sequence in the Fig. 1. Mitotic metaphase chromosomes of Melipona (Melikerria) interrupta stained with Giemsa (a), C- banding (b), DAPI (c), and CMA3 (d). Scale bar = 5 μm. Fig. 2. Patterns obtained in metaphase chromosomes of Melipona (Melikerria) interrupta with FISH using the following repetitive DNA probes: 18S (a), GA(15) (b), GAG(15) (c), CAA(10) (d), CGG(10) (e), and TTAGG(6) (f ). In blue: chromosomes stained with DAPI. In red: regions hybridized with probes. Scale bar = 5 μm. 94 Natália Martins Travenzoli et al. telomeric sites in the karyotype of M. (Melikerria) inter- rupta. Studies have shown that TTAGG (Sahara et al. 1999) and TCAGG (Mravinac et al. 2011) were observed in telomeres of several Hymenoptera species, including Apidae (Apis mellifera) (Meyne et al. 1995; Sahara et al. 1999) and Formicidae (Tapinoma nigerrimum, Myrmecia spp. and Acromyrmex striatus) (Meyne et al. 1995; Lorite et al. 2002; Frydrychová et al. 2004; Pereira et al. 2018). However, in many other Hymenoptera the TTAGG sequence was not observed in the telomeres of the chro- mosomes, suggesting that it has been lost and recovered in Apidae and Formicidae or that multiple losses of this region have occurred throughout the evolutionary histo- ry of the groups (Menezes et al. 2017). In this study, we report for the first time the telomeric sequence based on the FISH technique on a bee species of Meliponini tribe. This information added to the cytogenetic characteristics of Melipona already described in the literature may con- tribute to the understanding of karyotype evolution in these bees. We conclude that M. (Melikerria) interrupta is clas- sified as belonging to Group II based on heterochromatic patterns, which suggests an increase in the amount of heterochromatin in the subgenus Melikerria. It further suggests that karyotype the M. quinquefasciata be ple- siomorphic or this may be evolving independently in the group, and that the differences in the CMA3 and 18S marker regions interstitial, reported in the two species of Melikerria subgenus with high heterochromatin content, are an important feature to be further investigated. 5. 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