Advances in understanding the karyotype evolution of Tetrapulmonata and two other arachnid taxa, Ricinulei and Solifugae
Loading...
Date
Authors
Kral, Jiri
Sember, Alexandr
Divisova, Klara
Korinkova, Tereza
Reyes Lerma, Azucena C.
Avila Herrera, Ivalu M.
Forman, Martin
Stahlavsky, Frantisek
Musilova, Jana
Torres Kalme, Sabrina
Journal Title
Journal ISSN
Volume Title
Publisher
MDPI
Abstract
BACKGROUND/OBJECTIVES : Arachnids are a megadiverse arthropod group. The present study investigated the chromosomes of pedipalpid tetrapulmonates (orders Amblypygi, Thelyphonida, Schizomida) and two arachnid orders of uncertain phylogenetic placement, Ricinulei and Solifugae, to reconstruct their karyotype evolution. Except for amblypygids, the cytogenetics of these arachnid orders was almost unknown prior to the present study. METHODS : Chromosomes were investigated using methods of standard (Giemsa-stained preparations, banding techniques) and molecular cytogenetics (fluorescence in situ hybridization, comparative genomic hybridization). RESULTS AND CONCLUSIONS : New data for 38 species, combined with previously published data, suggest that ancestral arachnids possessed low to moderate 2n (22–40), monocentric chromosomes, one nucleolus organizer region (NOR), low levels of heterochromatin and recombinations, and no or homomorphic sex chromosomes. Karyotypes of Pedipalpi and Solifugae diversified via centric fusions, pericentric inversions, and changes in the pattern of NORs and, in solifuges, also through tandem fusions. Some solifuges display an enormous amount of constitutive heterochromatin and high NOR number. It is hypothesized that the common ancestor of amblypygids, thelyphonids, and spiders exhibited a homomorphic XY system, and that telomeric heterochromatin and NORs were involved in the evolution of amblypygid sex chromosomes. The new findings support the Cephalosomata clade (acariforms, palpigrades, and solifuges). Hypotheses concerning the origin of acariform holocentric chromosomes are presented. Unlike current phylogenetic hypotheses, the results suggest a sister relationship between Schizomida and a clade comprising other tetrapulmonates as well as a polyploidization in the common ancestor of the clade comprising Araneae, Amblypygi, and Thelyphonida.
Description
DATA AVAILABILITY STATEMENT : The original contributions presented in this study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author.
SUPPLEMENTARY MATERIAL : FIGURE S1. Amblypygi: Phrynichidae: Euphrynichus amanica, male karyotype. Based on two sister metaphases II (Giemsa staining). Scale bar = 10 μm. FIGURE S2. Amblypygi: Phrynichidae: Euphrynichus bacillifer (A) and Phrynichus ceylonicus (B), male karyotypes. Based on two sister metaphases II (Giemsa staining). Scale bars = 10 μm. FIGURE S3. Amblypygi: Phrynichidae: Damon medius, male, pattern of NORs (red). Metaphase II (FISH, DAPI staining). Note two submetacentric chromosomes (belonging to different chromosome pairs) bearing terminal NOR (arrowheads). Scale bar = 10 μm. FIGURE S4. Thelyphonida: Thelyphonidae: Hypoctoninae: Hypoctonus cf. gastrostictus (A) and Labochirus proboscideus (B), male karyotypes. Based on two sister metaphases II (Giemsa staining). Scale bars = 10 μm. FIGURE S5. Thelyphonida: Thelyphonidae: Hypoctoninae: Yekuana venezolensis, diploid set (A) and Mastigoproctinae: Uroproctus assamensis, haploid set (B), male karyotypes. In the haploid set, each chromosome pair is represented by one chromosome. Based on two sister metaphases II (A) or single metaphase II (B), stained by Giemsa. Scale bars = 10 μm. FIGURE S6. Thelyphonida: Thelyphonidae: Thelyphoninae: Ginosigma sp. (A) and Thelyphonus cf. linganus (B), male karyotypes. Based on two sister metaphases II (Giemsa staining). Scale bars = 10 μm. FIGURE S7. Ricinulei: Cryptocellus narino (A,C,D) and Ricinoides olounoua (B), male, pattern of NORs (red) and meiosis. (A) Pachytene, visualization of NORs (FISH, DAPI staining). One bivalent with subterminal NOR locus (arrowhead). (B) Mitotic metaphase, visualization of NORs (FISH, DAPI staining). Note small pair with subterminal NOR locus (arrowheads). (C) Diffuse stage (Giemsa staining). Bivalents exhibit enormous decondensation. (D) Metaphase I (Giemsa staining). Plate did not contain any heteromorphic bivalent. Note precocious segregation of chromosomes (arrows) of bivalent. Scale bars = 10 μm. FIGURE S8. Solifugae: females, association of homologous chromosomes throughout cell cycle (Giemsa staining). Letter pairs indicate putative homologs. (A) Gluvia dorsalis, early mitotic metaphase. (B) Paragaleodes pallidus, interphase nucleus containing haploid number (i.e., six) of blocks of CH. Scale bars = 10 μm. FIGURE S9. Solifugae: Eremobatidae (A) and Daesiidae (B), male karyotypes. Based on mitotic metaphase (Giemsa staining). (A) Eremobates pallipes karyotype with predominance of acrocentric pairs. Insets: NOR-bearing chromosomes from another mitotic metaphase (FISH, DAPI staining). Most of arm of metacentric pair no. 6 formed by NOR locus (red). (B) Gnosippus sp. karyotype with predominance of acrocentric chromosomes. Scale bars = 10 μm. TABLE S1. Material examined, including sex, instar, localities, and methods used. Abbreviations: C, C-banding; CGH, detection of sex chromosomes through CGH; F, fluorescent banding; fj, female juvenile; mj, male juvenile; j, juvenile, sex undetermined; NOR, NOR detection through FISH; S, standard evaluation of mitosis and meiosis (Giemsa-stained preparations); subad, subadult; T, telomeric repeat detection through FISH.
SUPPLEMENTARY MATERIAL : FIGURE S1. Amblypygi: Phrynichidae: Euphrynichus amanica, male karyotype. Based on two sister metaphases II (Giemsa staining). Scale bar = 10 μm. FIGURE S2. Amblypygi: Phrynichidae: Euphrynichus bacillifer (A) and Phrynichus ceylonicus (B), male karyotypes. Based on two sister metaphases II (Giemsa staining). Scale bars = 10 μm. FIGURE S3. Amblypygi: Phrynichidae: Damon medius, male, pattern of NORs (red). Metaphase II (FISH, DAPI staining). Note two submetacentric chromosomes (belonging to different chromosome pairs) bearing terminal NOR (arrowheads). Scale bar = 10 μm. FIGURE S4. Thelyphonida: Thelyphonidae: Hypoctoninae: Hypoctonus cf. gastrostictus (A) and Labochirus proboscideus (B), male karyotypes. Based on two sister metaphases II (Giemsa staining). Scale bars = 10 μm. FIGURE S5. Thelyphonida: Thelyphonidae: Hypoctoninae: Yekuana venezolensis, diploid set (A) and Mastigoproctinae: Uroproctus assamensis, haploid set (B), male karyotypes. In the haploid set, each chromosome pair is represented by one chromosome. Based on two sister metaphases II (A) or single metaphase II (B), stained by Giemsa. Scale bars = 10 μm. FIGURE S6. Thelyphonida: Thelyphonidae: Thelyphoninae: Ginosigma sp. (A) and Thelyphonus cf. linganus (B), male karyotypes. Based on two sister metaphases II (Giemsa staining). Scale bars = 10 μm. FIGURE S7. Ricinulei: Cryptocellus narino (A,C,D) and Ricinoides olounoua (B), male, pattern of NORs (red) and meiosis. (A) Pachytene, visualization of NORs (FISH, DAPI staining). One bivalent with subterminal NOR locus (arrowhead). (B) Mitotic metaphase, visualization of NORs (FISH, DAPI staining). Note small pair with subterminal NOR locus (arrowheads). (C) Diffuse stage (Giemsa staining). Bivalents exhibit enormous decondensation. (D) Metaphase I (Giemsa staining). Plate did not contain any heteromorphic bivalent. Note precocious segregation of chromosomes (arrows) of bivalent. Scale bars = 10 μm. FIGURE S8. Solifugae: females, association of homologous chromosomes throughout cell cycle (Giemsa staining). Letter pairs indicate putative homologs. (A) Gluvia dorsalis, early mitotic metaphase. (B) Paragaleodes pallidus, interphase nucleus containing haploid number (i.e., six) of blocks of CH. Scale bars = 10 μm. FIGURE S9. Solifugae: Eremobatidae (A) and Daesiidae (B), male karyotypes. Based on mitotic metaphase (Giemsa staining). (A) Eremobates pallipes karyotype with predominance of acrocentric pairs. Insets: NOR-bearing chromosomes from another mitotic metaphase (FISH, DAPI staining). Most of arm of metacentric pair no. 6 formed by NOR locus (red). (B) Gnosippus sp. karyotype with predominance of acrocentric chromosomes. Scale bars = 10 μm. TABLE S1. Material examined, including sex, instar, localities, and methods used. Abbreviations: C, C-banding; CGH, detection of sex chromosomes through CGH; F, fluorescent banding; fj, female juvenile; mj, male juvenile; j, juvenile, sex undetermined; NOR, NOR detection through FISH; S, standard evaluation of mitosis and meiosis (Giemsa-stained preparations); subad, subadult; T, telomeric repeat detection through FISH.
Keywords
Heterochromatin, Holocentric, Nucleolus organizer region, Polyploidy, Sex chromosome, Solifuge, Somatic pairing, Ricinulei, Spiders (Araneae), Telomere, SDG-15: Life on land
Sustainable Development Goals
SDG-15:Life on land
Citation
Král, J.; Sember, A.; Divišová, K.; Korínková, T.; Reyes Lerma, A.C.; Ávila Herrera, I.M.;
Forman, M.; Št’áhlavský, F.; Musilová, J.; Torres Kalme, S.; et al. Advances in
Understanding the Karyotype Evolution of Tetrapulmonata and Two
Other Arachnid Taxa, Ricinulei and Solifugae. Genes 2025, 16, 207. https://doi.org/10.3390/genes16020207.