Acessibilidade / Reportar erro
Articles • Mem. Inst. Oswaldo Cruz 108 (3) • May 2013 • https://doi.org/10.1590/S0074-02762013000300017   copy

Chromosomal divergence and evolutionary inferences in Rhodniini based on the chromosomal location of ribosomal genes

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

In this study, we used fluorescence in situ hybridisation to determine the chromosomal location of 45S rDNA clusters in 10 species of the tribe Rhodniini (Hemiptera: Reduviidae: Triatominae). The results showed striking inter and intraspecific variability, with the location of the rDNA clusters restricted to sex chromosomes with two patterns: either on one (X chromosome) or both sex chromosomes (X and Y chromosomes). This variation occurs within a genus that has an unchanging diploid chromosome number (2n = 22, including 20 autosomes and 2 sex chromosomes) and a similar chromosome size and genomic DNA content, reflecting a genome dynamic not revealed by these chromosome traits. The rDNA variation in closely related species and the intraspecific polymorphism in Rhodnius ecuadoriensis suggested that the chromosomal position of rDNA clusters might be a useful marker to identify recently diverged species or populations. We discuss the ancestral position of ribosomal genes in the tribe Rhodniini and the possible mechanisms involved in the variation of the rDNA clusters, including the loss of rDNA loci on the Y chromosome, transposition and ectopic pairing. The last two processes involve chromosomal exchanges between both sex chromosomes, in contrast to the widely accepted idea that the achiasmatic sex chromosomes of Heteroptera do not interchange sequences.

chromosomal evolution; Chagas disease vectors; Triatominae; holocentric chromosomes; rDNA variability

The subfamily Triatominae (Hemiptera: Reduviidae) currently comprises 142 species of blood-sucking insects, assembled in five-six tribes and 15-19 genera (Galvão et al. 2003, Schofield & Galvão 2009, Rosa et al. 2012). The Rhodniini tribe is the second largest and includes two genera: Rhodnius (18 species) and Psammolestes (3 species). Although the phylogenetic origin of many triatomine tribes and genera remains problematic (Hwang & Weirauch 2012), the Rhodniini tribe is considered monophyletic, comprising two groups, namely the robustus and pictipes lineages, with the Psammoles-tes genus integrating the robustus lineage (Monteiro et al. 2000, 2002). Rhodniini species display different degrees of synanthropic behaviour from sylvatic to highly domestic (Abad-Franch et al. 2009). The domestic species are of great medical interest for their role as vectors of Chagas disease, particularly Rhodnius prolixus in Venezuela and Colombia (and also in parts of Central America) (Hashimoto & Schofield 2012), Rhodnius pal-lescens in Panama, Colombia, Costa Rica and Nicaragua (Calzada et al. 2010), Rhodnius ecuadoriensis in Ecuador and northern Peru (Cuba Cuba et al. 2002), Rhodnius stali in Bolivia (Matias et al. 2003) and several species in the Amazon Region (Aguilar et al. 2007).

As in other Heteroptera, the Triatominae possess holocentric chromosomes characterised by a diffuse or non-localised centromere (Hughes-Schrader & Schrader 1961). The main source of karyotype variation in this subfamily involves changes in chromosome number, differences in C-heterochromatin (such as the number, size and location of C-blocks) and genomic DNA content (Panzera et al. 2007, 2010). However, Rhodniini karyotypes seem to be highly conserved, with no known variations either in the number of autosomes (20) or sex mechanism (XY in males, XX in females). In addition, Rhodniini species exhibit chromosomes of similar size and possess the lowest genomic DNA content of all the triatomines (Panzera et al. 2007). Only a few Rhodniini species present C-heterochromatin (Rhodnius colombiensis, Rhodnius nasutus, R. pallescens and Rhodnius pictipes) (Dujardin et al. 2002), with only one of these species exhibiting C-band polymorphisms (Gómez-Palacio et al. 2008, 2012).

Several authors have applied fluorescence in situ hybridisation (FISH) using rDNA probes to reveal chromosomal changes in the holocentric chromosomes of Heteroptera (Kuznetsova et al. 2011). Previous studies in Triatominae have demonstrated that the 45S rDNA clusters show remarkable variation in their chromosomal location, particularly in the genus Triatoma (Panzera et al. 2012).

The aim of this study was to determine whether the Rhodniini genus displays karyotype homogeneity, which involves the chromosomal position of active genes, such as ribosomal genes. We used FISH to analyse the chromosomal location of 45S rDNA clusters in the robustus and pictipes lineages and performed population ana-lyses of the most important vector species (R. prolixus, R. pallescens and R. ecuadoriensis). The data obtained using this marker correlated with the evolutionary relationships established using molecular analyses.

MATERIALS AND METHODS

Materials - We studied the chromosomal location of 45S rDNA clusters in 10 Rhodnius species representing the two phylogenetic groups of the genus (Abad-Franch et al. 2009, Schofield & Galvão 2009): the robustus lineage (Rhodnius milesi, R. nasutus, Rhodnius neglectus, Rhodnius neivai, R. prolixus and Rhodnius robustus) and pictipes lineage (R. ecuadoriensis, R. pallescens, R. pictipes and R. stali). At least two male individuals were analysed for each species and individuals collected from natural populations were used when possible (Table). For the species analysed at the population level, at least three individuals were studied per location (Table). For R. prolixus, we studied specimens from additional localities to complement our previous results (Panzera et al. 2012). For R. ecuadoriensis, we studied populations from different countries, i.e., Peru and Ecuador. For R. pallescens, we included new populations from Colombia and Panama, representing the two evolutionary groups of the species recognised by morphometric, molecular and cytogenetic differences, as reported by Gómez-Palacio et al. (2008, 2012) (Table).

Thumbnail
TABLE
Geographical origin and available data on 45S rDNA chromosomal location in Rhodniini species obtained by fluorescent in situ hybridization

FISH - The FISH assays were conducted using squashed gonad preparations that had previously been fixed in 3:1 ethanol:acetic acid, as described by Panzera et al. (2012). A DNA plasmid harbouring an 807-bp region of the 18S rDNA gene of Triatoma infestans (accession Y18750) was used as a probe; the probe was labelled using the Nick Translation System (Invitrogen, Carlsbad, California, USA) with Cy3-dUTP (GE Healthcare, Life Sciences, Oregon, USA). The slides were mounted using Vectashield H-100 (Vector Laboratories, Inc, Burlingame, California, USA) containing 2 µg/mL 4',6-diamidino-2-phenylindole.

Microscopy and imaging - The slides were analysed using a Nikon Eclipse 80i epifluorescence microscope. The images were obtained with a Nikon DS-5Mc-U2 digital, cooled camera using Nikon Nis Elements 3.1 Advanced Research software and processed with Adobe Photoshop(r) software. At least 30 meiotic metaphases (I or II) or diplotene stages were studied for each individual.

RESULTS

The mapping results are summarised in Table and are discriminated by species and populations; previous reports on rDNA cluster location in Rhodniini are also included. The 45S rDNA clusters have one or two chromosome loci per haploid genome, showing two chromosome location patterns: either on both sex chromosomes (X and Y chromosomes) or only on the X chromosome (Figs 1, 2). In all cases, the hybridisation signals were located in a terminal or subterminal chromosomal position. In all the species (except R. stali) carrying two 45S rDNA loci, great differences in the signal intensities were observed and the intensity for the Y chromosome was reduced. Both chromosomal location patterns were observed in each phylogenetic group, as described below.

Fig. 1
tribe Rhodniini: robustus lineage. Interspecific variability in the chromosome location of the 45S rDNA by fluorescent in situ hybridization in male meiotic cells. All species have the same diploid chromosome number: 2n = 22 chromosomes (20 autosomes plus XY in males). The rDNA signals are located either on both sex chromosomes (A-C) or just on one sex chromosome (X chromosome) (D-F). A: Rhodnius neivai, metaphase II; B: Rhodnius neglectus, metaphase II; C: Rhodnius milesi, metaphase I; D: Rhodnius nasutus, metaphase II; E: Rhodnius robustus, diplotene; F: Rhodnius prolixus, metaphase II. Bar = 10 µm

Fig. 2
tribe Rhodniini: pictipes lineage. Interspecific and intraspecific variability in the chromosome location of the 45S rDNA by fluorescent in situ hybridization in male meiotic cells. All species have the same diploid chromosome number: 2n = 22 chromosomes (20 autosomes plus XY in males). The rDNA signals are located on both sex chromosomes (A-D) and only in one sex chromosome (X chromosome) (E). A: Rhodniuspictipes, metaphase II; B: Rhodnius stali, metaphase II; C: Rhodnius pallescens, metaphase II, D: Rhodnius ecuadoriensis from Ecuador, metaphase II; E: Rhodnius ecuadoriensis from Peru, metaphase I. Bar = 10 ìm.

Robustus lineage - In R. neivai, R. neglectus and R. milesi, the rDNA clusters were located on both sex chromosomes (Fig. 1A, B, C, respectively), whereas the rDNA signal was detected on the X chromosome in R. nasutus and R. robustus (Fig. 1D, E). The R. prolixus population analyses did not reveal variability in the individuals from the new localities studied, with all presenting rDNA clusters on the X chromosome (Fig. 1F).

Pictipes lineage - In R. pictipes and R. stali, the rDNA clusters were located on the X and Y sex chromosomes (Fig. 2A, B, respectively). The same pattern was observed for R. pallescens among the individuals from the four populations studied, with the rDNA clusters located on the X and Y sex chromosomes, even in specimens with different amounts of C-heterochromatin (Fig. 2C). However, we observed striking intraspecific variability in R. ecuadoriensis. The population from Ecuador showed ribosomal genes located on both sex chromosomes (Fig. 2D), whereas the hybridisation signal was detected only on the X chromosome in the Peruvian population (Fig. 2E).

DISCUSSION

Interspecific variability of the 45S rDNA cluster location - Based on the FISH analyses performed on 13 Rhodniini species to date, eight of which are described for the first time in the present study, one or two 45S rDNA loci per haploid genome were observed. Two localisation patterns were revealed: either on both sex chromosomes (X and Y chromosomes) (8 species) or only on the X chromosome (4 species), with one species presenting both patterns (R. ecuadoriensis) (Figs 1, 2, Table). The number of rDNA loci was consistent with other Triatominae species, with the detection of up to two loci (see Panzera et al. 2012 for a review). In the Triatomini tribe, or within the genus Triatoma, the ribosomal genes showed four different chromosomal positions, including autosomes bearing 45S rDNA (Panzera et al. 2012). The Rhodniini tribe showed far less variability (rDNA loci restricted to the sex chromosomes), which might reflect their monophyletic origin, in contrast to the putative polyphyletic origin of the genus Triatoma (Hypsa et al. 2002, Hwang & Weirauch 2012). However, the Rhodniini variation in the ribosomal cluster position occurred despite their karyotype homogeneity, reflecting a genome dynamic that is not revealed by other chromosome traits. Different authors have proposed that changes in C-heterochromatin could affect the position and number of rDNA loci in several insect groups (Hirai et al. 1996, Criniti et al. 2005, Roy et al. 2005, Oliveira et al. 2010). Nevertheless, the position of rDNA loci in Rhodniini species and other triatomines does not appear to be associated with the presence, absence and/or variations in the amount of autosomal constitutive heterochromatin (i.e., R. pallescens) (Table).

Intraspecific variation of rDNA chromosomal location - Population studies were performed on the three Rhodnius species which serve as the main vectors of Chagas disease (Table). No intraspecific variation was revealed in the R. prolixus and R. pallescens populations. The uniformity of the ribosomal gene location in R. prolixus, including the sylvatic and domestic populations, was consistent with the molecular studies indicating low variability in this species (Monteiro et al. 2003). In R. pallescens, the two evolutionary groups with morphometric and genetic divergence (Gómez-Palacio et al. 2008, 2012) also presented the same rDNA chromosome location. However, for R. ecuadoriensis, we detected striking differences in the rDNA location between the individuals from Peru and Ecuador (Fig. 2E, F). Molecular comparisons with mitochondrial sequences (cytochrome b) also showed markedly divergent haplotypes in the populations from these countries, suggesting that these populations represent discrete groups or incipient species (Abad-Franch et al. 2003, Abad-Franch & Monteiro 2005). Considering that both populations show different affinities for domestic and sylvatic habitats (Grijalva et al. 2012), their identification as distinct genetic groups has important epidemiological consequences for vector control programmes (Abad-Franch et al. 2001). Further FISH studies with other Peruvian and Ecuadore-an populations from different habitats and experimental crosses among them are crucial to determine whether the observed genetic variations reflect intraspecific polymorphisms or involve different species.

Intraspecific variation of rDNA cluster location is fairly common in plants (Pedrosa et al. 2006), is rare in such vertebrates as amphibians (Andronico et al. 1985) and fish (Castro et al. 2001), but is unusual in insects, with only one case reported in species with holocentric chromosomes (Panzera et al. 2012). In Orthoptera and Coleoptera (Cabrero et al. 2003a, b, Cabral-de-Mello et al. 2011b, respectively), intraspecific variation involves a polymorphism in the number of chromosomes that harbour ribosomal clusters. With regard to holocentric chromosomes, the variation recently described in T. infestans populations involves the complete transfer of the rDNA locus from an autosomal position to the X chromosome (Panzera et al. 2012). The polymorphism in R. ecuadoriensis described here is similar to that observed in Orthoptera and Coleoptera because it also represents a variation in the number of chromosomes carrying ribosomal genes (Fig. 2D, E). The intraspecific polymorphisms in the ribosomal cluster position in these two Triatominae species suggests that this character varies at a faster rate than that observed in other insects groups, particularly those with holocentric chromosomes.

Taxonomic and evolutionary features - According to the FISH results obtained for the 46 triatomine species studied to date, the ribosomal gene chromosomal location is a species-specific characteristic (Panzera et al. 2012, this paper). Both cases of intraspecific variation detected in triatomines reflect recent divergence processes, which could lead to incipient speciation (R. ecuadoriensis) or a marked population differentiation (T. infestans). In addition, closely related species, such as R. colombiensis and R. pallescens (Abad-Franch & Monteiro 2005), can be differentiated using this marker (Table), suggesting that the 45S chromosomal localisation of the ribosomal clusters could be an appropriate marker for the recognition and detection of recently diverged species or populations. FISH analyses of R. robustus (Monteiro et al. 2003) and/or Triatoma sordida (Noireau et al. 1999) cryptic species could help to test this hypothesis.

The determination of the chromosomal location of rDNA clusters is important to understanding karyotypic evolution in different insect taxa (Hirai et al. 1996, Roy et al. 2005, Cabrero & Camacho 2008, Oliveira et al. 2010), including lepidopteran species, which, similar to Heteroptera, also possess holocentric chromosomes (Nguyen et al. 2010). In several closely related species of Triatominae, such as the protracta and dispar complexes within the genus Triatoma, or in all Panstrongylus species, the chromosomal location of rDNA clusters is an evolutionarily conserved cytogenetic trait and closely related species display the same chromosomal positions (Panzera et al. 2012). However, this character is not evolutionarily conserved in the Rhodniini tribe, as each of the two genetic lineages shows both patterns of chromosomal location (Table).

Considering the monophyletic origin of the Rhodniini tribe, we can hypothesise which of the two ribosomal genes locations is the ancestral form. Given the number of Rhodnius species with ribosomal loci on both sex chromosomes (8/13 species), we suggest that this pattern represents the primitive form; thus, species with rDNA clusters only on the X chromosome could reflect a loss of the Y chromosome ribosomal locus. In support of this idea, Rhodnius domesticus and R. neivai, which are considered to be ancient isolated species, present the X-Y pattern (Abad-Franch & Monteiro 2007). Additional evidence for the X-Y pattern as the ancestral location is provided by the variation observed in the present study for the R. ecuadoriensis populations from Peru. These populations exhibit rDNA clusters only on the X chromosome (Fig. 2F) and are believed to have derived from ancestral populations in central Ecuador (Abad-Franch et al. 2001, 2009, Grijalva et al. 2005), which show ribosomal genes on both sex chromosomes (Fig. 2E). An ancestral configuration of rDNA loci on both sex chromosomes has also been suggested in other insects, such as melanogaster group, whereby some species have also subsequently lost the ribosomal genes located on the Y chromosome (Roy et al. 2005).

Nevertheless, the alternative hypothesis, i.e., an ancestral location of the ribosomal genes on the X chromosome, should not be excluded, considering that a significant excess of gene movement from the X chromosome has been demonstrated in most species with the XY sex system (see Pease & Hahn 2012 for a review). This hypothesis would imply either a partial transfer of ribosomal genes from the X to the Y chromosome, as mediated through the transposition of mobile elements (Schubert & Wobus 1985) or chromosomal rearrangements promoted through ectopic recombination (homologous recombination between repetitive sequences of non-homologous chromosomes) (Hanson et al. 1996). In almost all of the Rhodniini species described in this paper (Figs 1, 2), the Y chromosome ribosomal signal was less intense than that observed for the X chromosome, indicating that the ribosomal cluster copy number is significantly lower on the Y chromosome. This low copy number supports the mechanism proposed by Dubcovsky and Dvorak (1995), which implies the dispersion of a single rDNA copy and the successive amplification of the copy number, suggesting an ancestral location of ribosomal genes on the X chromosome. In many organisms, rDNA clusters behave as mobile genetic elements due to the presence of transposable elements adjacent to the ribosomal genes (Schubert & Wobus 1985, Zhang et al. 2008). Several transposable elements have been described in Triatominae (Gilbert et al. 2010), including a non-long terminal repeat retrotransposon inserted inside the 28S rDNA sequence of R. prolixus (Jakubczak et al. 1991). Thus, we can envisage an rDNA cluster with associated transposable elements moving through genomes, as previously postulated for other insects (Cabrero & Camacho 2008, Nguyen et al. 2010, Cabral-de-Mello et al. 2011a). Such species as T. infestans and R. ecuadoriensis, which are polymorphic for the location of rDNA, would be excellent models for the identification of transposable elements and the ana-lysis of their dispersal mechanisms.

Ectopic recombination and rDNA transposition indicate a heterologous association between sex chromosomes. As a rule, heteropteran sex chromosomes are considered asynaptic and achiasmatic during meiotic division and do not form synaptonemal complexes (Solari 1979, Ueshima 1979, Pigozzi & Solari 2003). In all triatomine species, sex chromosomes are intimately associated from early meiotic prophase until diakinesis, forming a positive heteropycnotic body (Panzera et al. 2010). This close spatial proximity between sex chromosomes is an essential prerequisite for ectopic recombination and rDNA transposition. Thus, the existence of ribosomal loci on two sex chromosomes in 13 triatomine species from four different genera (Rhodnius, Psammolestes, Eratyrus and Triatoma) (Panzera et al. 2012, this paper) suggests that chromosomal exchanges between achiasmatic sex chromosomes are more common than previously suspected, at least in this insect group.

Moreover, regardless of which ribosomal gene location is ancestral, the inter and intraspecific rDNA variation in Rhodniini indicates that rDNA transposition is independent of taxonomic units. Furthermore, the variation suggests that the three proposed mechanisms of rDNA change, i.e., the loss of rDNA loci on the Y chromosome, rDNA transposition and ectopic pairing between both sex chromosomes, could have occurred several times during the karyotypic evolution of the Rhodniini tribe.

ACKNOWLEDGEMENTS

To Christopher J Schofield (LSHTM, London, UK), for valuable comments on the paper, and Aldo Valente (IEC, Pará, Brazil) and Franklin Vargas (Univ. Nacional de Trujillo, Peru), for supplying triatomine material.

REFERENCES

  • Abad-Franch F, Monteiro FA 2005. Molecular research and the control of Chagas disease vectors. An Acad Bras Cienc 77: 437-454.
  • Abad-Franch F, Monteiro FA 2007. Biogeography and evolution of Amazonian triatomines (Heteroptera: Reduviidae): implications for Chagas disease surveillance in humid forest ecoregions. Mem Inst Oswaldo Cruz 102 (Suppl. I): 57-70.
  • Abad-Franch F, Monteiro FA, Jaramillo NO, Gurgel-Gonçalves R, Dias FBS, Diotaiuti L 2009. Ecology, evolution and the long-term surveillance of vector-borne Chagas disease: a multi-scale appraisal of the tribe Rhodniini (Triatominae). Acta Trop 112: 159-177.
  • Abad-Franch F, Monteiro FA, Patterson JS, Miles MA 2003. Phylogenetic relationships among members of the Pacific Rhodnius lineage (Hemiptera: Reduviidae: Triatominae). Infect Genet Evol 2: 244-245.
  • Abad-Franch F, Paucar CA, Carpio CC, Cuba Cuba CA, Aguilar VHM, Miles MA 2001. Biogeography of Triatominae (Hemip-tera: Reduviidae) in Ecuador: implications for the design of control strategies. Mem Inst Oswaldo Cruz 96: 611-620.
  • Aguilar HM, Abad-Franch F, Dias JCP, Junqueira ACV, Coura JR 2007. Chagas disease in the Amazon Region. Mem Inst Oswaldo Cruz 102 (Suppl. I): 47-55.
  • Andronico F, De Lucchini S, Graziani F, Nardi I, Batistoni R, Barsacchi-Pilone G 1985. Molecular organization of ribosomal RNA genes clustered at variable chromosomal sites in Triturus vulgaris meridionalis (Amphibia, Urodela). J Mol Biol 186: 219-229.
  • Cabral-de-Mello DC, Moura RC, Martins C 2011a. Cytogenetic mapping of rRNAs and histone H3 genes in 14 species of Dichotomius (Coleoptera, Scarabaeidae, Scarabaeinae) beetles. Cytogenet Genome Res 134: 127-135.
  • Cabral-de-Mello DC, Oliveira SG, Moura RC, Martins C 2011b. Chromosomal organization of the 18S and 5S rRNAs and histone H3 genes in Scarabaeinae coleopterans: insights into the evolutionary dynamics of multigene families and heterochromatin. BMC Genet 12: 88.
  • Cabrero J, Bugrov A, Warchalowska-Sliwa E, López-León MD, Perfectti F, Camacho JP 2003a. Comparative FISH analysis in five species of Eyprepocnemidine grasshoppers. Heredity (Edinb) 90: 377-381.
  • Cabrero J, Camacho JPM 2008. Location and expression of ribosomal RNA genes in grasshoppers: abundance of silent and cryptic loci. Chromosome Res 16: 595-607.
  • Cabrero J, Perfectti F, Gómez R, Camacho JPM, López-León MD 2003b. Population variation in the A chromosome distribution of satellite DNA and ribosomal DNA in the grasshopper Eyprepocnemis plorans. Chromosome Res 11: 375-381.
  • Calzada JE, Pineda V, Garisto JD, Samudio F, Santamaría AM, Saldaña A 2010. Human trypanosomiasis in the eastern region of the Panama province: new endemic areas for Chagas disease. Am J Trop Med Hyg 82: 580-582.
  • Castro J, Rodríguez S, Pardo BG, Sánchez L, Martínez P 2001. Population analysis of an unusual NOR-site polymorphism in brown trout (Salmo trutta L.). Heredity (Edinb) 86: 291-302.
  • Criniti A, Simonazzi G, Cassanelli S, Ferrari M, Bizzaro D, Manicardi GC 2005. X-linked heterochromatin distribution in the holocentric chromosomes of the green apple aphid Aphis pomi. Genetica 124: 93-98.
  • Cuba Cuba CA, Abad-Franch F, Rodríguez JR, Vásquez FV, Velásquez LP, Miles MA 2002. The triatomines of northern Peru, with emphasis on the ecology and infection by trypanosomes of Rhodnius ecuadoriensis (Triatominae). Mem Inst Oswaldo Cruz 97: 175-183.
  • Dubcovsky J, Dvorak J 1995. Ribosomal RNA multigene loci: nomads of the Triticeae genomes. Genetics 140: 1367-1377.
  • Dujardin JP, Schofield CJ, Panzera F 2002. Los vectores de la enfermedad de Chagas, Académie Royale des Sciences D'Outre-Mer, Bruxelles, 189 pp.
  • Galvão C, Carcavallo R, Rocha DS, Jurberg J 2003. A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution with nomenclatural and taxonomic notes. Zootaxa 202: 1-36.
  • Gilbert C, Schaack S, Pace II JK, Brindley PJ, Feschotte C 2010. A role for host-parasite interactions in the horizontal transfer of transposons across phyla. Nature 464: 1347-1350.
  • Gómez-Palacio A, Jaramillo-Ocampo N, Caro-Riaño H, Diaz S, Monteiro FA, Pérez R, Panzera F, Triana O 2012. Morphometric and molecular evidence of intraspecific biogeographical differentiation of Rhodnius pallescens (Hemiptera: Reduviidae: Rhodniini) from Colombia and Panama. Infect Genet Evol 12: 1975-1983.
  • Gómez-Palacio A, Jaramillo-Ocampo N, Triana-Chávez O, Saldaña A, Calzada J, Pérez R, Panzera F 2008. Chromosome variability in the Chagas disease vector Rhodnius pallescens (Hemiptera, Reduviidae, Rhodniini). Mem Inst Oswaldo Cruz 103: 160-164.
  • Grijalva MJ, Palomeque-Rodriguez FS, Costales JA, Davila S, Arcos-Teran L 2005. High household infestation rates by synanthropic vectors of Chagas disease in southern Ecuador. J Med Entomol 42: 68-74.
  • Grijalva MJ, Suarez-Davalos V, Villacis AG, Ocaña-Mayorga S, Dangles O 2012. Ecological factors related to the widespread distribution of sylvatic Rhodnius ecuadoriensis populations in southern Ecuador. Parasit Vectors 5: 17.
  • Hanson RE, Islam Faridi MN, Percival EA, Crane CF, Ji Y, McKnight TD, Stelly DM, Price HJ 1996. Distribution of 5S and 18S-28S rDNA loci in a tetraploid cotton (Gossypium hirsutum L) and its putative diploid ancestors. Chromosoma 105: 55-61.
  • Hashimoto K, Schofield CJ 2012. Elimination of Rhodnius prolixus in Central America. Parasit Vectors 5: 45.
  • Hirai H, Yamamoto MT, Taylor RW, Imai HT 1996. Genomic dispersion of 28S rDNA during karyotypic evolution in the ant genus Myrmecia (Formicidae). Chromosoma 105: 190-196.
  • Hughes-Schrader S, Schrader F 1961. The kinetochore of the Hemip-tera. Chromosoma 12: 327-350.
  • Hwang WS, Weirauch C 2012. Evolutionary history of assassin bugs (Insecta: Hemiptera: Reduviidae): insights from divergence dating and ancestral state reconstruction. PLoS ONE 7: e45523.
  • Hypsa V, Tietz D, Zrzavý J, Rego RO, Galvão C, Jurberg J 2002. Phylogeny and biogeography of Triatominae (Hemiptera, Reduviidae): molecular evidence of a New World origin of the Asiatic clade. Mol Phylogenet Evol 23: 447-457.
  • Jakubczak JL, Burke WD, Eickbush TH 1991. Retrotransposable elements RI and R2 interrupt the rRNA genes of most insects. Proc Natl Acad Sci USA 88: 3295-3299.
  • Kuznetsova VG, Grozeva SM, Nokkala S, Nokkala C 2011. Cytogenetics of the true bug infraorder Cimicomorpha (Hemiptera, Hete-roptera): a review. Zookeys 154: 31-70.
  • Matias A, De la Riva J, Martinez E, Torrez M, Dujardin JP 2003. Domiciliation process of Rhodnius stali (Hemiptera: Reduviidae) in Alto Beni, La Paz, Bolivia. Trop Med Int Health 8: 264-268.
  • Monteiro FA, Barrett TV, Fitzpatrick S, Cordón-Rosales C, Feliciangeli MD, Beard CB 2003. Molecular phylogeography of the Amazonian Chagas disease vectors Rhodnius prolixus and R. robustus. Mol Ecol 12: 997-1006.
  • Monteiro FA, Lazoski C, Noireau F, Solé-Cava AM 2002. Allozyme relationships among ten species of Rhodniini showing paraphyly of Rhodnius including Psammolestes. Med Vet Entomol 16: 83-90.
  • Monteiro FA, Wesson DM, Dotson EM, Schofield CJ, Beard CB 2000. Phylogeny and molecular taxonomy of the Rhodniini derived from mitochondrial and nuclear DNA sequences. Am J Trop Med Hyg 62: 460-465.
  • Morielle-Souza A, Azeredo-Oliveira MTV 2007. Differential characterization of holocentric chromosomes in triatomines (Hete-roptera, Triatominae) using different staining techniques and fluorescent in situ hybridization. Genet Mol Res 6: 713-720.
  • Nguyen P, Sahara K, Yoshido A, Marec F 2010. Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera). Genetica 138: 343-354.
  • Noireau F, Zegarra M, Ordoñez J, Gutierrez T, Dujardin JP 1999. Genetic structure of Triatoma sordida (Hemiptera: Reduviidae) domestic populations from Bolivia: application on control interventions. Mem Inst Oswaldo Cruz 94: 347-351.
  • Oliveira SG, Moura RC, Silva AEB, Souza MJ 2010. Cytogenetic ana-lysis of two Coprophanaeus species (Scarabaeidae) revealing wide constitutive heterochromatin variability and the largest number of 45S rDNA sites among Coleoptera. Micron 41: 960-965.
  • Panzera F, Ferrandis I, Ramsey J, Salazar-Schettino PM, Cabrera M, Monroy C, Bargues MD, Mas-Coma S, O'Connor JE, Angulo V, Jaramillo N, Pérez R 2007. Genome size determination in Chagas disease transmitting bugs (Hemiptera-Triatominae) by flow cytometry. Am J Trop Med Hyg 76: 516-521.
  • Panzera F, Pérez R, Panzera Y, Ferrandis I, Ferreiro MJ, Calleros L 2010. Cytogenetics and genome evolution in the subfamily Triatominae (Hemiptera, Reduviidae). Cytogenet Genome Res 128: 77-87.
  • Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, Pérez R, Silva AE, Guerra M, Panzera F 2012. High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138: 56-67.
  • Pease JB, Hahn MW 2012. Sex chromosomes evolved from independent ancestral linkage groups in winged insects. Mol Biol Evol 29: 1645-1653.
  • Pedrosa HA, de Almeida CC, Mosiolek M, Blair MW, Schweizer D, Guerra M 2006. Extensive ribosomal DNA amplification during Andean common bean (Phaseolus vulgaris L.) evolution. Theor Appl Genet 112: 924-933.
  • Pigozzi MI, Solari AJ 2003. Differential immunolocalization of a putative Rec8p in meiotic autosomes and sex chromosomes of triatomine bugs. Chromosoma 112: 38-47.
  • Rosa JA, Rocha CS, Gardim S, Pinto MC, Mendonça VJ, Ferreira Fi-lho JCR, Costa de Carvalho EO, Camargo LMA, Oliveira J, Nascimento JD, Cilense M, Almeida CE 2012. Description of Rhodnius montenegrensis n. sp. (Hemiptera: Reduviidae: Triatominae) from the state of Rondônia, Brazil. Zootaxa 3478: 62-76.
  • Roy V, Monti-Dedieu L, Chaminade N, Siljak-Yakovlev S, Aulard S, Lemeunier F, Montchamp-Moreau C 2005. Evolution of the chromosomal location of rDNA genes in two Drosophila species subgroups: ananassae and melanogaster. Heredity (Edinb) 94: 388-395.
  • Schofield CJ, Galvão C 2009. Classification, evolution and species groups within the Triatominae. Acta Trop 110: 88-100.
  • Schubert I, Wobus U 1985. In situ hybridization confirms jumping nucleolus organizing regions in Allium. Chromosoma 92: 143-148.
  • Solari AJ 1979. Autosomal synaptonemal complexes and sex chromosomes without axes in Triatoma infestans (Reduviidae, Hemiptera). Chromosoma 72: 225-240.
  • Ueshima N 1979. Hemiptera II: Heteroptera. In Animal cytogenetics. Insecta, Vol. 3, Part 6, 2nd ed., Gebrüder Borntraeger, Berlin-Stuttgart, 117 pp.
  • Zhang X, Eickbush MT, Eickbush TH 2008. Role of recombination in the long-term retention of transposable elements in rRNA gene loci. Genetics 180: 1617-1626.
  • Financial support: CSIC-Udelar, PEDECIBA, ANII

Publication Dates

  • Publication in this collection
    May 2013

History

  • Received
    07 Nov 2012
  • Accepted
    07 Feb 2013
Instituto Oswaldo Cruz, Ministério da Saúde Av. Brasil, 4365 - Pavilhão Mourisco, Manguinhos, 21040-900 Rio de Janeiro RJ Brazil, Tel.: (55 21) 2562-1222, Fax: (55 21) 2562 1220 - Rio de Janeiro - RJ - Brazil
E-mail: memorias@fiocruz.br
Acompanhe os números deste periódico no seu leitor de RSS