Abstract
The morphologically uniform suborder Cyphophthalmi represents a basal group of harvestmen (Opiliones). As such, it plays an important role in the reconstruction of the karyotype evolution within this arachnid order. The cytogenetic analysis of 6 representatives of the suborder Cyphophthalmi, namely Miopsalis sp. (2n = 30; Stylocellidae), Austropurcellia arcticosa (Cantrell, 1980) (2n = 30; Pettalidae), Parapurcellia amatola de Bivort & Giribet, 2010 (2n = 32; Pettalidae), Paramiopsalis aff. ramulosus Juberthie, 1962 (2n = 28; Sironidae), Cyphophthalmus duricorius Joseph, 1868 (2n = 24; Sironidae), and Siro carpaticus Rafalski, 1956 (2n = 52; Sironidae) was performed. Fluorescence in situ hybridization with 18S rDNA probe was used to analyze the distribution of major ribosomal RNA genes in harvestmen. We confront the obtained cytogenetic data with current hypotheses on cyphophthalmid phylogeny to reconstruct their karyotype evolution. We conclude that the ancestral karyotype of harvestmen consisted of 2n = 30 elements with 1 chromosome pair bearing terminal rDNA clusters. The rDNA locus was multiplicated in the evolution of Cyphophthalmi. However, decreases as well as increases in the number of chromosomes have been detected in the karyotype evolution of Cyphophthalmi. Our data thus reveal unexpected diversity in cyphophthalmid karyotypes.
References
1.
Adilardi RS, Ojanguren Affilastro AA, Martí DA, Mola LM: Cytogenetic analysis on geographically distant parthenogenetic populations of Tityus trivittatus Kraepelin, 1898 (Scorpiones, Buthidae): karyotype, constitutive heterochromatin and rDNA localization. Comp Cytogenet 8:81-92 (2014).
2.
Adilardi RS, Ojanguren Affilastro AA, Mattoni CI, Mola LM: Male and female meiosis in the mountain scorpion Zabius fuscus (Scorpiones, Buthidae): heterochromatin, rDNA and TTAGG telomeric repeats. Genetica 143:393-401 (2015).
3.
Araujo D, Rheims CA, Brescovit AD, Cella DM: Extreme degree of chromosome number variability in species of the spider genus Scytodes (Araneae, Haplogynae, Scytodidae). J Zool Syst Evol Res 46:89-95 (2008).
4.
Boyer SL, Clouse RM, Benavides LR, Sharma P, Schwendinger PJ, et al: Biogeography of the world: a case study from cyphophthalmid Opiliones, a globally distributed group of arachnids. J Biogeogr 34:2070-2085 (2007).
5.
Cabral de Mello DC, Moura RC, Martins C: Cytogenetic mapping of rRNAs and histone H3 genes in 14 species of Dichotomius (Coleoptera, Scarabaeidae, Scarabaeinae) beetles. Cytogenet Genome Res 134:127-135 (2011).
6.
de Bivort BL, Giribet G: A systematic revision of the South African Pettalidae (Arachnida: Opiliones: Cyphophthalmi) based on a combined analysis of discrete and continuous morphological characters with the description of seven new species. Invertebrate Systematics 24:371-406 (2010).
7.
Dolejš P, Kořínková T, Musilová J, Opatová V, Kubcová L, et al: Karyotypes of central European spiders of the genera Arctosa, Tricca, and Xerolycosa (Araneae: Lycosidae). Eur J Entomol 108:1-16 (2011).
8.
Dreszer TB, Rada T, Giribet G: Cyphophthalmus solentiensis sp. nov. (Cyphophthalmi, Sironidae), a new endogean mite harvestmen species from Croatia, with an application of confocal laser microscopy to illustrate genitalia in Opiliones. Breviora 543:1-15 (2015).
9.
Dunlop JA: Geological history and phylogeny of Chelicerata. Arthropod Struct Dev 39:124-142 (2010).
10.
Faria R, Navarro A: Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25:660-669 (2010).
11.
Forman M, Nguyen P, Hula V, Král J: Sex chromosome pairing and extensive NOR polymorphism in Wadicosa fidelis (Araneae: Lycosidae). Cytogenet Genome Res 141:43-49 (2013).
12.
Fuková I, Nguyen P, Marec F: Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome 48:1083-1092 (2005).
13.
Giribet G, Edgecombe GD, Wheeler WC, Babbitt C: Phylogeny and systematic position of Opiliones: a combined analysis of chelicerate relationships using morphological and molecular data. Cladistics 18:5-70 (2002).
14.
Giribet G, Vogt L, González AP, Sharma P, Kury AB: A multilocus approach to harvestman (Arachnida: Opiliones) phylogeny with emphasis on biogeography and the systematics of Laniatores. Cladistics 26:408-437 (2010).
15.
Giribet G, Sharma PP, Benavides LR, Boyer SL, Clouse RM, et al: Evolutionary and biogeographical history of an ancient and global group of arachnids (Arachnida: Opiliones: Cyphophthalmi) with a new taxonomic arrangement. Biol J Linn Soc 105:92-130 (2012).
16.
Goldman AS, Lichten M: The efficiency of meiotic recombination between dispersed sequences in Saccharomyces cerevisiae depends upon their chromosomal location. Genetics 144:43-55 (1996).
17.
Gorlov IP, Tsurusaki N: Analysis of the phenotypic effects of B chromosomes in a natural population of Metagagrella tenuipes (Arachnida: Opiliones). Heredity 84:209-217 (2000a).
18.
Gorlov IP, Tsurusaki N: Morphology and meiotic/mitotic behavior of B chromosomes in a Japanese harvestman, Metagagrella tenuipes (Arachnida: Opiliones): no evidence for B accumulation mechanisms. Zool Sci 17:349-355 (2000b).
19.
Grzywacz B, Maryanska-Nadachowska A, Chobanov DP, Karamysheva T, Warchalowska-Sliwa E: Comparative analysis of the location of rDNA in the Palaearctic bushcricket genus Isophya (Orthoptera: Tettigoniidae: Phaneropterinae). Eur J Entomol 108:509-517 (2011).
20.
Hedin M, Tsurusaki N, Macías-Ordóñez R, Shultz JW: Molecular systematics of sclerosomatid harvestmen (Opiliones, Phalangioidea, Sclerosomatidae): geography is better than taxonomy in predicting phylogeny. Mol Phylogenet Evol 62:224-236 (2012).
21.
Imai HT, Marayama T, Gojobori YI, Crozier RH: Theoretical bases for karyotype evolution. 1. The minimum-interaction hypothesis. Am Nat 128:900-920 (1986).
22.
Juberthie C: Nombres chromosomiques chez les Sironidae, Trogulidae, Ischyropsalidae, Phalangiidae (Opiliones). CR Acad Sci Paris 242:2860-2862 (1956).
23.
Juberthie C: Étude des opilions cyphophthalmes Stylocellinae du Portugal: description de Paramiopsalis ramulosus gen. n., sp. n. Bull Mus Natl Hist Nat Paris 34:267-275 (1962).
24.
Král J: Evolution of multiple sex chromosomes in the spider genus Malthonica (Araneae: Agelenidae) indicates unique structure of the spider sex chromosome systems. Chromosome Res 15:863-879 (2007).
25.
Král J, Musilová J, Šťáhlavský F, Řezáč M, Zübeyde A, et al: Evolution of the karyotype and sex chromosome systems in basal clades of araneomorph spiders (Araneae: Araneomorphae). Chromosome Res 14:859-880 (2006).
26.
Král J, Kováč L, Šťáhlavský F, Lonský P, Luptáčik P: The first karyotype study in palpigrades, a primitive order of arachnids (Arachnida: Palpigradi). Genetica 134:79-87 (2008).
27.
Král J, Kořínková T, Forman M, Krkavcová L: Insights into the meiotic behavior and evolution of multiple sex chromosome systems in spiders. Cytogenet Genome Res 133:43-66 (2011).
28.
Král J, Kořínková T, Krkavcová L, Musilová J, Forman M, et al: Evolution of karyotype, sex chromosomes, and meiosis in mygalomorph spiders (Araneae: Mygalomorphae). Biol J Linn Soc 109:377-408 (2013).
29.
Levan AK, Fredga K, Sandberg AA: Nomenclature for centromeric position on chromosomes. Hereditas 5:201-220 (1964).
30.
Mattos VF, Cella DM, Carvalho LS, Candido DM, Schneider MC: High chromosome variability and the presence of multivalent associations in buthid scorpions. Chromosome Res 21:121-136 (2013).
31.
Mattos VF, Carvalho LS, Cella DM, Schneider MC: Location of 45S ribosomal genes in mitotic and meiotic chromosomes of buthid scorpions. Zool Sci 31:603-607 (2014).
32.
Mieczkowski PA, Lemoine FJ, Petes TD: Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair 5:1010-1020 (2006).
33.
Murienne J, Giribet G: The Iberian Peninsula: ancient history of a hot spot of mite harvestmen (Arachnida: Opiliones: Cyphophthalmi: Sironidae) diversity. Zool J Linn Soc 156:785-800 (2009).
34.
Murienne J, Karaman I, Giribet G: Explosive evolution of an ancient group of Cyphophthalmi (Arachnida: Opiliones) in the Balkan Peninsula. J Biogeogr 37:90-102 (2010).
35.
Nguyen P, Sahara K, Yoshido A, Marec F: Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera). Genetica 138:343-354 (2010).
36.
Oliveira RM, Zacaro AA, Gnaspini P, Cella DM: Cytogenetics of three Brazilian Goniosoma species: a new record for diploid number in Laniatores (Opiliones, Gonyleptidae, Goniosomatinae). J Arachnol 34:435-443 (2006).
37.
Oliveira RM, de Jesus AC, Brescovit AD, Cella DM: Chromosomes of Crossopriza lyoni (Blackwall 1867), intraindividual numerical chromosome variation in Physocyclus globosus (Taczanowski 1874), and the distribution pattern of NORs (Araneomorphae, Haplogynae, Pholcidae). J Arachnol 35:293-306 (2007).
38.
Panzera Y, Pita S, Ferreiro MJ, Ferrandis I, Lages C, et al: High dynamics of rDNA cluster location in kissing bug holocentric chromosomes (Triatominae, Heteroptera). Cytogenet Genome Res 138:56-67 (2012).
39.
Paula-Neto E, Araujo D, Carvalho LS, Cella DM, Schneider MC: Chromosomal characteristics of a Brazilian whip spider (Amblypygi) and evolutionary relationships with other arachnid orders. Genet Mol Res 12:3726-3734 (2013).
40.
Pinto-da-Rocha R, Machado G, Giribet G (eds): Harvestmen: The Biology of Opiliones (Harvard University Press, Cambridge 2007).
41.
Rodríguez-Gil SG, Merani MS, Scioscia CL, Mola LM: Cytogenetics in three species of Polybetes Simon 1897 from Argentina (Araneae, Sparassidae) I. Karyotype and chromosome banding pattern. J Arachnol 35:227-237 (2007).
42.
Sadílek D, Nguyen P, Koç H, Kovařík F, Yağmur EA, et al: Molecular cytogenetics of Androctonus scorpions: an oasis of calm in the turbulent karyotype evolution of the diverse family Buthidae. Biol J Linn Soc 115:69-76 (2015).
43.
Sakamoto Y, Zacaro AA: LEVAN, an ImageJ plugin for morphological cytogenetic analysis of mitotic and meiotic chromosomes (2009). http://rsbweb.nih.gov/ij/plugins/levan/levan.html.
44.
Schneider CA, Rasband WS, Eliceiri KW: NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675 (2012).
45.
Schneider MC, Cella DM: Karyotype conservation in 2 populations of the parthenogenetic scorpion Tityus serrulatus (Buthidae): rDNA and its associated heterochromatin are concentrated on only one chromosome. J Hered 101:491-496 (2010).
46.
Schneider MC, Zacaro AA, Oliveira RM, Gnaspini P, Cella DM: Conventional and ultrastructural analyses of the chromosomes of Discocyrtus pectinifemur (Opiliones, Laniatores, Gonyleptidae). J Zool Syst Evol Res 47:203-207 (2008).
47.
Schneider MC, Zacaro AA, Pinto-da-Rocha R, Candido DM, Cella DM: A comparative cytogenetic analysis of Bothriuridae species and overview of the chromosome data of Scorpiones. J Hered 100:545-555 (2009a).
48.
Schneider MC, Zacaro AA, Pinto-da-Rocha R, Candido DM, Cella DM: Complex meiotic configuration of the holocentric chromosomes: the intriguing case of the scorpion Tityus bahiensis. Chromosome Res 17:883-898 (2009b).
49.
Schönhofer AL, McCormack M, Tsurusaki N, Martens J, Hedin M: Molecular phylogeny of the harvestmen genus Sabacon (Arachnida: Opiliones: Dyspnoi) reveals multiple Eocene-Oligocene intercontinental dispersal events in the Holarctic. Mol Phylogenet Evol 66:303-315 (2013).
50.
Šťáhlavský F, Král J: Karyotype analysis and achiasmatic meiosis in pseudoscorpions of the family Chthoniidae (Arachnida: Pseudoscorpiones). Hereditas 140:49-60 (2004).
51.
Šťáhlavský F, Král J, Harvey MS, Haddad CR: A karyotype study on the pseudoscorpion families Geogarypidae, Garypinidae and Olpiidae (Arachnida: Pseudoscorpiones). Eur J Entomol 103:277-289 (2006).
52.
Šťáhlavský F, Boyer SL, Harvey MS, Giribet G: First cytogenetic study of a member of the harvestman family Pettalidae (Opiliones: Cyphophthalmi). Aust J Entomol 51:299-302 (2012).
53.
Stávale LM, Schneider MC, Araujo D, Brescovit AD, Cella DM: Chromosomes of Theridiidae spiders (Entelegynae): interspecific karyotype diversity in Argyrodes and diploid number intraspecific variability in Nesticodes rufipes. Genet Mol Biol 33:663-668 (2010).
54.
Stávale LM, Schneider MC, Brescovit AD, Cella DM: Chromosomal characteristics and karyotype evolution of Oxyopidae spiders (Araneae, Entelegynae). Genet Mol Res 10:752-763 (2011).
55.
Traut W: Pachytene mapping in the female silkworm Bombyx mori L. (Lepidoptera). Chromosoma 58:275-284 (1976).
56.
Tsurusaki N: Geographic variation of chromosomes in Sabacon makinoi Suzuki (Arachnida, Opiliones, Sabaconidae). Bull Biogeogr Soc Jpn 44:111-116 (1989).
57.
Tsurusaki N: Geographic variation of the number of B chromosomes in Metagagrella tenuipes (Opiliones, Phalangiidae, Gagrellinae). Mem Queensl Mus 33:659-665 (1993).
58.
Tsurusaki N: Cytogenetics; in Pinto-da-Rocha R, Machdo G, Giribet G (eds): Harvestmen: The Biology of Opiliones, pp 266-279 (Harvard University Press, Cambridge 2007).
59.
Tsurusaki N, Cokendolpher J: Chromosomes of sixteen species of harvestman (Arachnida, Opiliones, Caddidae and Phalangiidae). J Arachnol 18:151-166 (1990).
60.
Tsurusaki N, Murakami M, Shimokawa K: Geographic variation of chromosomes in the Japanese harvestman, Gagrellopsis nodulifera, with special reference to a hybrid zone in western Honshu. Zool Sci 8:265-275 (1991).
61.
Tsurusaki N, Svojanovská H, Schöenhofer A, Šťáhlavský F: The harvestmen cytogenetic database, version 2.5. http://www.arthropodacytogenetics.bio.br/index.html (last accessed March 3, 2016).
© 2016 S. Karger AG, Basel
2016
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.
