Ivalú M Ávila Herrera1, Jiří Král2, Markéta Pastuchová3, Martin Forman3, Jana Musilová3,4, Tereza Kořínková3,5, František Šťáhlavský6, Magda Zrzavá7,8, Petr Nguyen7,8, Pavel Just3,6, Charles R Haddad9, Matyáš Hiřman6, Martina Koubová3, David Sadílek3,6, Bernhard A Huber10. 1. Laboratory of Arachnid Cytogenetics, Department of Genetics and Microbiology, Faculty of Science, Charles University, Viničná 5, 128 44, Prague 2, Czech Republic. avilai@natur.cuni.cz. 2. Laboratory of Arachnid Cytogenetics, Department of Genetics and Microbiology, Faculty of Science, Charles University, Viničná 5, 128 44, Prague 2, Czech Republic. spider@natur.cuni.cz. 3. Laboratory of Arachnid Cytogenetics, Department of Genetics and Microbiology, Faculty of Science, Charles University, Viničná 5, 128 44, Prague 2, Czech Republic. 4. Research Team of Plant Stress Biology and Biotechnology, Division of Crop Genetics and Breeding, Crop Research Institute, Drnovská 507/73, 161 00, Prague 6, Czech Republic. 5. , Prague 1, Czech Republic. 6. Invertebrate Zoology Unit, Department of Zoology, Faculty of Science, Charles University, Viničná 7, 128 44, Prague 2, Czech Republic. 7. Laboratory of Molecular Cytogenetics, Department of Molecular Biology and Genetics, Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic. 8. Laboratory of Molecular Cytogenetics, Department of Molecular Biology and Genetics, Institute of Entomology, Biology Centre CAS, Branišovská 31, 370 05, České Budějovice, Czech Republic. 9. Research Group of Arachnid Systematics and Ecology, Department of Zoology and Entomology, Faculty of Natural and Agricultural Sciences, University of the Free State, P.O. Box 339, Bloemfontein, 9300, Republic of South Africa. 10. Arachnida Section, Alexander Koenig Zoological Research Museum, Adenauerallee 160, 53113, Bonn, Germany.
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.
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.
Authors: Ivalú M Ávila Herrera; Jiří Král; Markéta Pastuchová; Martin Forman; Jana Musilová; Tereza Kořínková; František Šťáhlavský; Magda Zrzavá; Petr Nguyen; Pavel Just; Charles R Haddad; Matyáš Hiřman; Martina Koubová; David Sadílek; Bernhard A Huber Journal: BMC Ecol Evol Date: 2021-05-21
Authors: Milan Řezáč; Steven Tessler; Petr Heneberg; Ivalú Macarena Ávila Herrera; Nela Gloríková; Martin Forman; Veronika Řezáčová; Jiří Král Journal: PLoS One Date: 2022-07-07 Impact factor: 3.752