Evolutionary pattern of karyotypes and meiosis in pholcid spiders (Araneae: Pholcidae): implications for reconstructing chromosome evolution of araneomorph spiders

Abstract

Background Despite progress in genomic analysis of spiders, their chromosome evolution is not satisfactorily understood. Most information on spider chromosomes concerns the most diversified clade, entelegyne araneomorphs. Other clades are far less studied. Our study focused on haplogyne araneomorphs, which are remarkable for their unusual sex chromosome systems and for the co-evolution of sex chromosomes and nucleolus organizer regions (NORs); some haplogynes exhibit holokinetic chromosomes. To trace the karyotype evolution of haplogynes on the family level, we analysed the number and morphology of chromosomes, sex chromosomes, NORs, and meiosis in pholcids, which are among the most diverse haplogyne families. The evolution of spider NORs is largely unknown. Results Our study is based on an extensive set of species representing all major pholcid clades. Pholcids exhibit a low 2n and predominance of biarmed chromosomes, which are typical haplogyne features. Sex chromosomes and NOR patterns of pholcids are diversified. We revealed six sex chromosome systems in pholcids (X0, XY, X1X20, X1X2X30, X1X2Y, and X1X2X3X4Y). The number of NOR loci ranges from one to nine. In some clades, NORs are also found on sex chromosomes. Conclusions The evolution of cytogenetic characters was largely derived from character mapping on a recently published molecular phylogeny of the family. Based on an extensive set of species and mapping of their characters, numerous conclusions regarding the karyotype evolution of pholcids and spiders can be drawn. Our results suggest frequent autosome–autosome and autosome–sex chromosome rearrangements during pholcid evolution. Such events have previously been attributed to the reproductive isolation of species. The peculiar X1X2Y system is probably ancestral for haplogynes. Chromosomes of the X1X2Y system differ considerably in their pattern of evolution. In some pholcid clades, the X1X2Y system has transformed into the X1X20 or XY systems, and subsequently into the X0 system. The X1X2X30 system of Smeringopus pallidus probably arose from the X1X20 system by an X chromosome fission. The X1X2X3X4Y system of Kambiwa probably evolved from the X1X2Y system by integration of a chromosome pair. Nucleolus organizer regions have frequently expanded on sex chromosomes, most probably by ectopic recombination. Our data suggest the involvement of sex chromosome-linked NORs in achiasmatic pairing.

Evolutionary Dynamics of Autopolyploids in Natural Populations: The Case of Turnera Sidoides Complex

“…The supposed stability of number and localization of NORs in spiders has knocked down with the increase of cytogenetic studies. In an analysis of NORs in 30 Pholcidae spiders, Ávila Herrera et al (2021) revealed a great diversity of number of this site, which can occur in autosomes and/or X sex chromosome. The results obtained herein using FISH with rDNA probe only in three Sicarius species revealed the presence of ribosomal cistrons in autosomes (S. ornatus and S. tropicus) and X 1 sex chromosome (S. cariri).…”

Insights into the Karyotype Evolution of Charinidae, the Early-Diverging Clade of Whip Spiders (Arachnida: Amblypygi)

“…Mapping of this cluster often revealed a single NOR site, which is probably an ancestral pattern in arachnids [36]. The number of NOR/rDNA loci has increased in some arachnid clades during their evolution [76,77,81,87]. In haplogyne spiders, these loci are also frequently placed on sex chromosomes [77,90].…”

“…The major rDNA cluster (45S rDNA) is by far the most utilized molecular chromosomal marker across diverse eukaryotic organisms, and especially in non-model groups [72][73][74]. The major rDNA cluster visualized either by 18S or 28S rDNA probes has already been localized in some spiders [36,46,73,[75][76][77], scorpions [45,76,[78][79][80][81][82], pseudoscorpions [83], harvestmen [84][85][86][87], ticks [73,88,89], and an amblypygid [18]. Mapping of this cluster often revealed a single NOR site, which is probably an ancestral pattern in arachnids [36].…”

“…The number of NOR/rDNA loci has increased in some arachnid clades during their evolution [76,77,81,87]. In haplogyne spiders, these loci are also frequently placed on sex chromosomes [77,90]. When stable distribution patterns for rDNA loci within a certain lineage are used as markers in the phylogenetic context, they may largely contribute to the interpretation of possible karyotype rearrangements (e.g., [84]).…”

Atypus karschi Dönitz, 1887 (Araneae: Atypidae): An Asian purse-web spider established in Pennsylvania, USA

“…snetsingeri to compare with other Atypus species, along with observations on habitat associations and natural history. Data on karyotype [e.g., 27 , 28 ] and genetic barcode are frequently used to reconstruct phylogeny and evolutionary history of taxa including spiders.…”