Insights into the Meiotic Behavior and Evolution of Multiple Sex Chromosome Systems in Spiders

Abstract

A characteristic feature of spider karyotypes is the predominance of unusual multiple X chromosomes. To elucidate the evolution of spider sex chromosomes, their meiotic behavior was analyzed in 2 major clades of opisthothele spiders, namely, the entelegyne araneomorphs and the mygalomorphs. Our data support the predominance of X₁X₂0 systems in entelegynes, while rare X₁X₂X₃X₄0 systems were revealed in the tuberculote mygalomorphs. The spider species studied exhibited a considerable diversity of achiasmate sex chromosome pairing in male meiosis. The end-to-end pairing of sex chromosomes found in mygalomorphs was gradually replaced by the parallel attachment of sex chromosomes in entelegynes. The observed association of male X univalents with a centrosome at the first meiotic division may ensure the univalents’ segregation. Spider meiotic sex chromosomes also showed other unique traits, namely, association with a chromosome pair in males and inactivation in females. Analysis of these traits supports the hypothesis that the multiple X chromosomes of spiders originated by duplications. In contrast to the homogametic sex of other animals, the homologous sex chromosomes of spider females were already paired at premeiotic interphase and were inactivated until prophase I. Furthermore, the sex chromosome pairs exhibited an end-to-end association during these stages. We suggest that the specific behavior of the female sex chromosomes may have evolved to avoid the negative effects of duplicated X chromosomes on female meiosis. The chromosome ends that ensure the association of sex chromosome pairs during meiosis may contain information for discriminating between homologous and homeologous X chromosomes and thus act to promote homologous pairing. The meiotic behavior of 4 X chromosome pairs in mygalomorph females, namely, the formation of 2 associations, each composed of 2 pairs with similar structure, suggests that the mygalomorph X₁X₂X₃X₄0 system originated by the duplication of the X₁X₂0 system via nondisjunctions or polyploidization.

Chromosomal characteristics of a Brazilian whip spider (Amblypygi) and evolutionary relationships with other arachnid orders

“…The number and location of NORs were only established, for example, in approximately 30 species of Araneae (Král et al, 2006;Král, 2007;Oliveira et al, 2007;Rodríguez-Gil et al, 2007;Araujo et al, 2008;Stávale et al, 2010Stávale et al, , 2011Dolejš et al, 2011;Král et al, 2011), 17 species of Scorpiones (Schneider et al, 2009a,b;Schneider and Cella, 2010), 3 species of Opiliones (Gorlov and Tsurusaki, 2000;Oliveira et al, 2006;Schneider et al, 2008;Mattos et al, 2013), and two species of Palpigradi (Král et al, 2008). In almost all these species, the NORs were only identified through the use of silver impregnation; however, in an overview of the NOR distribution in Coleoptera, Schneider et al (2007) showed that the results were usually coincident when the chromosomes were examined with both silver impregnation and FISH technique.…”

Sex Chromosome Pairing and Extensive NOR Polymorphism in <b><i>Wadicosa fidelis</i></b> (Araneae: Lycosidae)

“…The sex chromosomes of lycosids were reported to initially pair in parallel. During late prophase I, pairing was restricted to centromeric regions [Král et al, 2011]. In W. fidelis , the centromeric pairing of X univalents persists until metaphase II, which is a unique feature for entelegynes.…”

“…Although X chromosome pairing in lycosids is usually restricted to prophase I, it can continue during metaphase and anaphase I in some species [Dolejš et al, 2011;Král et al, 2011]. The sex chromosomes of lycosids were reported to initially pair in parallel.…”

“…Remarkably, haplogyne araneomorphs often exhibit sex chromosome-linked NORs [Král et al, 2006;Oliveira et al, 2007]. This NOR location has also been found in some entelegynes [Král et al, 2011;Paula-Neto, 2011].…”

“…The modes of sex chromosome pairing during male meiosis are diverse in spiders. Sex chromosomes show parallel attachment or endto-end pairing at both ends [Král et al, 2011].…”