Sex-Linked Chromosome Heterozygosity in Males of Tityus confluens (Buthidae): A Clue about the Presence of Sex Chromosomes in Scorpions

Abstract

Scorpions of the genus Tityus show holokinetic chromosomes, achiasmatic male meiosis and an absence of heteromorphic sex chromosomes, like all Buthidae. In this work, we analysed the meiotic behaviour and chromosome rearrangements of a population of the scorpion Tityus confluens, characterising the cytotypes of males, females and embryos with different cytogenetic techniques. This revealed that all the females were structural homozygotes, while all the males were structural heterozygotes for different chromosome rearrangements. Four different cytotypes were described in males, which differed in chromosome number (2n = 5 and 2n = 6) and meiotic multivalent configurations (chains of four, five and six chromosomes). Based on a detailed mitotic and meiotic analysis, we propose a sequence of chromosome rearrangements that could give rise to each cytotype and in which fusions have played a major role. Based on the comparison of males, females and a brood of embryos, we also propose that the presence of multivalents in males and homologous pairs in females could be associated with the presence of cryptic sex chromosomes, with the male being the heterogametic sex. We propose that the ancestral karyotype of this species could have had homomorphic XY/XX (male/female) sex chromosomes and a fusion could have occurred between the Y chromosome and an autosome.

Insights into the origin of the high variability of multivalent-meiotic associations in holocentric chromosomes of Tityus (Archaeotityus) scorpions

“…Intraspecific variability in diploid number has been recorded in 40% of the 18 karyotyped Tityus species [ 42 , 69 ]. Similar to the species investigated herein, previous studies revealed variations at the inter- and intra-population levels and attributed differences in chromosome number to fission/fusion rearrangements [ 29 , 39 , 41 , 42 , 48 ]. In specimens of T .…”

“…Studies examining specific chromosomal regions in scorpions have increased significantly in recent years [ 29 , 39 – 42 , 48 , 83 – 87 ]. Data regarding the localization of NORs and rDNA has revealed remarkable stability, particularly in Tityus species, in which more than 80% of the species presented a similar pattern, i.e., NORs/rDNA in the terminal regions of two chromosomes.…”

“…confluens (2n = 5–6), Tityus curupi (2n = 32–31), T . obscurus (2n = 11–16) and Tityus uruguayensis (2n = 31) with holocentric chromosomes [ 40 – 42 , 48 ]. Thus, the telomeric chromosomal region is conserved despite extensive rearrangements.…”

“…In addition, the family Buthidae combines three unusual cytogenetic features: holocentric chromosomes, multivalent-meiotic associations and achiasmate meiosis in males [ 27 , 29 , 39 – 42 ]. Multivalent associations in meiosis have been observed in 50% of the species included in eight different buthid genera [ 27 , 29 , 39 – 48 ]. The numbers of chromosomes involved in these chains vary within a species, e.g., Isometrus maculatus (2n = 12) with multivalent of IV, VI and VIII chromosomes [ 43 – 45 ]; Lychas marmoreus (2n = 12–15) with seven bivalents (II) and chains consisting of the IV, VI, VIII, and X chromosomes [ 27 , 49 ]; Jaguajir agamemnon (2n = 28) with the 14II and chains of XXVIII chromosomes; and Jaguajir rochae (2n = 28) with VIII, X and IV+VIII chromosomes in the chains [ 29 ].…”

“…In buthid scorpions, heterozygous reciprocal translocations or fission/fusion rearrangements are hypothesized to be responsible for the origin of multi-chromosomal associations during meiosis I [ 27 , 29 , 39 – 42 , 48 ]. The mechanisms responsible for correct chromosome pairing and segregation of long chromosomal chains remain poorly characterized.…”