Complex meiotic configuration of the holocentric chromosomes: the intriguing case of the scorpion Tityus bahiensis

Abstract

Mitotic and meiotic chromosomes of Tityus bahiensis were investigated using light (LM) and transmission electron microscopy (TEM) to determine the chromosomal characteristics and disclose the mechanisms responsible for intraspecific variability in chromosome number and for the presence of complex chromosome association during meiosis. This species is endemic to Brazilian fauna and belongs to the family Buthidae, which is considered phylogenetically basal within the order Scorpiones. In the sample examined, four sympatric and distinct diploid numbers were observed: 2n = 5, 2n = 6, 2n = 9, and 2 = 10. The origin of this remarkable chromosome variability was attributed to chromosome fissions and/or fusions, considering that the decrease in chromosome number was concomitant with the increase in chromosome size and vice versa. The LM and TEM analyses showed the presence of chromosomes without localised centromere, the lack of chiasmata and recombination nodules in male meiosis, and two nucleolar organiser regions carrier chromosomes. Furthermore, male prophase I cells revealed multivalent chromosome associations and/or unsynapsed or distinctly associated chromosome regions (gaps, less-condensed chromatin, or loop-like structure) that were continuous with synapsed chromosome segments. All these data permitted us to suggest that the chromosomal rearrangements of T. bahiensis occurred in a heterozygous state. A combination of various factors, such as correct disjunction and balanced segregation of the chromosomes involved in complex meiotic pairing, system of achiasmate meiosis, holocentric nature of the chromosomes, population structure, and species dispersion patterns, could have contributed to the high level of chromosome rearrangements present in T. bahiensis.

Allele Sharing and Evidence for Sexuality in a Mitochondrial Clade of Bdelloid Rotifers

“…meiotic segregation and sexual reproduction might nevertheless occur is suggested by an atypical form of meiosis known in some species of the genus Oenothera and in certain other plants (Cleland 1972;Holsinger and Ellstrand 1984;Golczyk 2011;Rauwolf et al 2011;Golczyk et al 2014). In these plants and perhaps in some animals (Chinnappa and Victor 1979;Gross et al 2009;Schneider et al 2009), instead of synapsing side by side, chromosomes join end to end to form rings in which paternal and maternal chromosomes alternate. At first meiotic anaphase, maternal and paternal chromosomes segregate to opposite poles without genetic exchange except in telomeric regions, thereby keeping chromosomes of the same parentage together generation after generation as independently inherited units, known as Renner complexes ( Figure 5).…”

Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis

“…In general, holocentric clades do not show the predicted increase in karyotypic diversity (Panzera et al 1996;Gokhman and Kuznetsova 2006). In contrast, sedges (genus Carex), scale insects (genus Apiomorpha), and scorpions from the family Buthidae have extremely labile karyotypes (Cook 2000;Hipp 2007;Schneider et al 2009). Carex has inverted meiosis, and Buthidae have achiasmate meiosis (Davies 1956;Schneider et al 2009).…”

“…In contrast, sedges (genus Carex), scale insects (genus Apiomorpha), and scorpions from the family Buthidae have extremely labile karyotypes (Cook 2000;Hipp 2007;Schneider et al 2009). Carex has inverted meiosis, and Buthidae have achiasmate meiosis (Davies 1956;Schneider et al 2009). These features may have allowed karyotypes to change without compromising holocentric meiosis (Schneider et al 2009).…”

“…Carex has inverted meiosis, and Buthidae have achiasmate meiosis (Davies 1956;Schneider et al 2009). These features may have allowed karyotypes to change without compromising holocentric meiosis (Schneider et al 2009). The holocentric chromosome characteristic is also likely to affect the evolution of centromere DNA sequences and of the kinetochore proteins that bind to them.…”

Holocentric Chromosomes of <i>Luzula elegans</i> Are Characterized by a Longitudinal Centromere Groove, Chromosome Bending, and a Terminal Nucleolus Organizer Region

“…Strikingly, the terminal position of 45S rDNA was maintained in spite of the occurrence of multiple translocations [da Silva et al 2010]. Also many animals with holocentric chromosomes, for example the aphids Acyrthosiphon pisum [Bizzaro et al, 2000] and Schizaphis graminum [Mandrioli et al, 1999], the scorpion Tityus bahiensis [Schneider et al, 2009], the codling moth Cydia pomonella [Fukova et al, 2005], and the nematode C. elegans [Albertson, 1984], are characterized by terminal NOR-positions. Holocentric heteropterans seem to be an exception because they possess terminal and non-terminal 45S rDNA sites [Papeschi et al, 2003;Cattani and Papeschi, 2004;Rebagliati and Mola, 2010].…”