Karyotype differentiation and male meiosis in European clades of the spider genus Pholcus (Araneae, Pholcidae).

Haplogyne araneomorphs are a diverse spider clade. Their karyotypes are usually predominated by biarmed (i.e., metacentric and submetacentric) chromosomes and have a specific sex chromosome system, X1X2Y. These features are probably ancestral for haplogynes. Nucleolus organizer regions (NORs) spread frequently from autosomes to sex chromosomes in these spiders. This study focuses on pholcids (Pholcidae), a highly diverse haplogyne family. Despite considerable recent progress in pholcid cytogenetics, knowledge on many clades remains insufficient including the most species-rich pholcid genus, Pholcus Walckenaer, 1805. To characterize the karyotype differentiation of Pholcus in Europe, we compared karyotypes, sex chromosomes, NORs, and male meiosis of seven species [P.alticeps Spassky, 1932; P.creticus Senglet, 1971; P.dentatus Wunderlich, 1995; P.fuerteventurensis Wunderlich, 1992; P.phalangioides (Fuesslin, 1775); P.opilionoides (Schrank, 1781); P.silvai Wunderlich, 1995] representing the dominant species groups in this region. The species studied show several features ancestral for Pholcus, namely the 2n♂ = 25, the X1X2Y system, and a karyotype predominated by biarmed chromosomes. Most taxa have a large acrocentric NOR-bearing pair, which evolved from a biarmed pair by a pericentric inversion. In some lineages, the acrocentric pair reverted to biarmed. Closely related species often differ in the morphology of some chromosome pairs, probably resulting from pericentric inversions and/or translocations. Such rearrangements have been implicated in the formation of reproductive barriers. While the X1 and Y chromosomes retain their ancestral metacentric morphology, the X2 chromosome shows a derived (acrocentric or subtelocentric) morphology. Pairing of this element is usually modified during male meiosis. NOR patterns are very diverse. The ancestral karyotype of Pholcus contained five or six terminal NORs including three X chromosome-linked loci. The number of NORs has been frequently reduced during evolution. In the Macaronesian clade, there is only a single NOR-bearing pair. Sex chromosome-linked NORs are lost in Madeiran species and in P.creticus. Our study revealed two cytotypes in the synanthropic species P.phalangioides (Madeiran and Czech), which differ by their NOR pattern and chromosome morphology. In the Czech cytotype, the large acrocentric pair was transformed into a biarmed pair by pericentric inversion.

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

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.