Heterochromatin characterization and ribosomal gene location in two monotypic genera of bloodsucker bugs (Cimicidae, Heteroptera) with holokinetic chromosomes and achiasmatic male meiosis

Abstract

Members of the family Cimicidae (Heteroptera: Cimicomorpha) are temporary bloodsuckers on birds and bats as primary hosts and humans as secondary hosts. Acanthocrios furnarii (2n=12=10+XY, male) and Psitticimex uritui (2n=31=28+X1X2Y, male) are two monotypic genera of the subfamily Haematosiphoninae, which have achiasmatic male meiosis of collochore type. Here, we examined chromatin organization and constitution of cimicid holokinetic chromosomes by determining the amount, composition and distribution of constitutive heterochromatin, and number and location of nucleolus organizer regions (NORs) in both species. Results showed that these two bloodsucker bugs possess high heterochromatin content and have an achiasmatic male meiosis, in which three regions can be differentiated in each autosomal bivalent: (i) terminal heterochromatic regions in repulsion; (ii) a central region, where the homologous chromosomes are located parallel but without contact between them; and (iii) small areas within the central region, where collochores are detected. Acanthocrios furnarii presented a single NOR on an autosomal pair, whereas P. uritui presented two NORs, one on an autosomal pair and the other on a sex chromosome. All NORs were found to be associated with CMA3 bright bands, indicating that the whole rDNA repeating unit is rich in G+C base pairs. Based on the variations in the diploid autosomal number, the presence of simple and multiple sex chromosome systems, and the number and location of 18S rDNA loci in the two Cimicidae species studied, we might infer that rDNA clusters and genome are highly dynamic among the representatives of this family.

Karyotype diversity among predatory Reduviidae (Heteroptera)

“…Many of these chromosome variations have been associated with chromosomal rearrangements such as fusion and fragmentation (Ueshima 1979, Papeschi and Bidau 1985, Papeschi 1988, 1994, Rebagliati et al 2001, Bressa et al 2002, Papeschi and Bressa 2006, Poggio et al 2007, 2009, 2014, Grozeva et al 2010, Chirino et al 2013, Chirino and Bressa 2014). Although these arguments have been proposed considering the occurrence of rearrangements, there is not much evidence of these changes in Heteroptera.…”

“…Due to the lack of phylogenetic analyses as well as the absence of chromosome markers for most heteropterans, the evolutionary direction for certain rearrangements is very speculative, especially in heteropteran predators. However, there are sporadic examples where chromosome rearrangements can be supposed, as observed in Cosmoclopius nigroannulatus , where numerical diversity is clearly linked to the fragmentation of sex chromosomes (Papeschi 1994, 1996, Poggio et al 2007, 2013a, 2014). …”

“…The variation in the content and distribution of heterochromatin in autosomes and sex chromosomes is well documented in heteropteran species, and occurs mainly in the terminal chromosomal regions (Grozeva and Nokkala 2002, Bressa et al 2005, Panzera et al 2010, Grozeva et al 2010, Chirino et al 2013, Suman and Kaur 2013, Poggio et al 2014, Bardella et al 2014a). This common feature was observed only in Montina confusa among the predator species studied here.…”

“…The 18S rDNA locus is the principal marker on chromosomes of Nepomorpha, Pentatomomorpha and Cimicomorpha (González-García et al 1996, Papeschi et al 2003, Cattani et al 2004, Cattani and Papeschi 2004, Dias de Campos Severi-Aguiar and Azeredo-Oliveira 2005, Severi-Aguiar et al 2006, Morielle-Souza and Azeredo-Oliveira 2007, Bressa et al 2008, 2009, Grozeva et al 2010, 2011, Poggio et al 2011, 2013a, 2014, Panzera et al 2012, Chirino et al 2013a, Bardella et al 2013). Of the 36 species of Pentatomomorpha studied until now, the rDNA loci are preferably located in autosomes with only four species with rDNA loci on the sex chromosomes (González-García et al 1996, Bressa et al 2009, Grozeva et al 2011, Bardella et al 2013).…”

Comparison of different cytogenetic methods and tissue suitability for the study of chromosomes in Cimex lectularius (Heteroptera, Cimicidae)

“…This genus is characterised by possession of the all-important heteropteran cytogenetic features: holokinetic chromosomes (e.g. Wolf et al 1997, Mola and Papeschi 2006, Guerra et al 2010, Poggio et al 2014, achiasmatic male meiosis of collochore type (Nokkala and Nokkala 1983, Nokkala and Grozeva 2000, Grozeva and Nokkala 2002, Ituarte and Papeschi 2004, Grozeva et al 2008, Poggio et al 2009, postreductional inverted male sex chromosome meiosis (Viera et al 2009, and the diffuse stage (Kuznetsova and Maryańska-Nadahowska 2000, Bressa et al 2002b, Rebagliati et al 2005, Lanzone and Souza 2006. However the cytogenetic research on Cimex species is difficult because of some other chromosome characteristics, such as the small size, high morphological similarity and superspiralization during almost the whole period of chromosomal division (e.g.…”