Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T07:52:47.445Z Has data issue: false hasContentIssue false

New cytogenetic data on Caryophyllaeus laticeps and Paracaryophyllaeus gotoi, parasites of evolutionary interest

Published online by Cambridge University Press:  10 May 2022

Martina Orosová*
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovakia
Anna Marková
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovakia
František Marec
Affiliation:
Biology Centre of the Czech Academy of Sciences, Institute of Entomology, Branišovská 31, 370 05 České Budějovice, Czech Republic
Daniel Barčák
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovakia
Timea Brázová
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovakia
Mikuláš Oros*
Affiliation:
Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovakia
*
Author for correspondence: Martina Orosová, E-mail: orosm@saske.sk
Author for correspondence: Martina Orosová, E-mail: orosm@saske.sk

Abstract

Caryophyllideans are intestinal parasites of freshwater fishes, occupying a basal position among the ‘true’ tapeworms. We performed detailed cytogenetic analyses of the well-known caryophyllidean species Caryophyllaeus laticeps. For comparison, we also examined for the first time the chromosomes of Paracaryophyllaeus gotoi, a specific parasite of loaches in China. Both species showed a diploid chromosome number of 2n = 20, n = 10m. Chromomycin A3 (CMA3)/diamidino-2-phenylindole (DAPI) staining performed for the first time in the class Cestoda revealed CMA3+/DAPI bands in the pericentromeric regions of the short arms of chromosome pair no. 7 in the karyotype of C. laticeps. Fluorescence in situ hybridization with the 18S rDNA probe confirmed the presence of a single cluster of major rDNA near the centromere on a pair of small chromosomes in both species. These findings support the hypothesis that the ancestral state in the family Caryophyllaeidae is a single interstitial cluster of major rDNA genes and thus one nucleolar organizer region per haploid genome. Our results, which we presented together with literature data plotted on a phylogenetic tree, show stability of caryophyllidean karyotypes at the genus level, but showed differences between genera without a clear phylogenetic signal. The data allowed us to at least formulate a hypothesis about the ancestral haploid chromosome number of n = 10 for the family Caryophyllaeidae and possibly for the sister family Capingentidae. In addition, we compared two populations of C. laticeps from water bodies with different levels of polychlorinated biphenyl contamination, showing a slightly increased incidence of chromosomal abnormalities at the contaminated site.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bajer, A (1959) Change of length and volume of mitotic chromosomes in living cells. Hereditas 45, 579596.CrossRefGoogle Scholar
Barčák, D, Oros, M, Hanzelová, V and Scholz, T (2017) A synoptic review of Caryophyllaeus Gmelin, 1790 (Cestoda: Caryophyllidea), parasites of cyprinid fishes. Folia Parasitologica 64, 027.CrossRefGoogle Scholar
Bazsalovicsová, E, Kráľová-Hromadová, I, Brabec, J, Hanzelová, V, Oros, M and Scholz, T (2014) Conflict between morphology and molecular data: a case of the genus Caryophyllaeus (Cestoda, Caryophyllidea), monozoic tapeworm of cyprinid fishes. Folia Parasitologica 61, 346352.CrossRefGoogle Scholar
Bombarová, M and Špakulová, M (2015) New chromosome characteristics of the monozoic tapeworm Caryophyllaeus laticeps (Cestoda, Caryophyllidea). Helminthologia 52, 336340.CrossRefGoogle Scholar
Brázová, T, Miklisová, D, Barčák, D, Uhrovič, D, Šalamún, P, Orosová, M and Oros, M (2021) Hazardous pollutants in the environment: fish host–parasite interactions and bioaccumulation of polychlorinated biphenyls. Environmental Pollution 291, 118175.CrossRefGoogle ScholarPubMed
Chuiko, GM, Tillitt, DE, Zajicek, JL, Flerov, BA, Stepanova, VM, Zhelnin, YY and Podgornaya, VA (2007) Chemical contamination of the Rybinsk reservoir, northwest Russia: relationship between live polychlorinated biphenyls (PCB) content and health indicators in bream (Abramis brama). Chemosphere 67, 527536.CrossRefGoogle Scholar
Doanh, PN, Shinohara, A, Horii, Y, Yahiro, S, Habe, S, Vannavong, N, Strobel, M, Nakamura, S and Nawa, S (2009) Morphological differences and molecular similarities between Paragonimus bangkokensis and P. harinasutai. Parasitology Research 105, 429439.CrossRefGoogle Scholar
Dobigny, G, Ozouf-Costaz, C, Bonillo, C and Volobuev, V (2002) ‘Ag-NORs’ are not always true NORs: new evidence in mammals. Cytogenetic and Genome Research 98, 7577.CrossRefGoogle Scholar
Grey, AJ (1979) A Comparative Study of the Chromosomes of Twenty Species of Caryophyllidean Tapeworms (Dissertation). College of Arts and Sciences, Department of Biology, State University of New York, Albany, USA, p. 214.Google Scholar
Grey, AJ and Mackiewicz, JS (1974) Chromosomes of the caryophyllidean tapeworm Glaridacris laruei. Experimental Parasitology 36, 159166.CrossRefGoogle ScholarPubMed
Grey, AJ and Mackiewicz, JS (1980) Chromosomes of the caryophyllidean cestodes: diploidy, triploidy and parthenogenesis in Glaridacris catostomi. International Journal of Parasitology 10, 397407.CrossRefGoogle Scholar
Hanzelová, V, Oros, M, Barčák, D, Miklisová, D, Kirin, D and Scholz, T (2015) Morphological polymorphism in tapeworms: redescription of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea) and characterisation of its morphotypes from different fish hosts. Systematic Parasitology 90, 177190.CrossRefGoogle ScholarPubMed
Hooper, DM and Price, PD (2017) Chromosomal inversion differences correlate with range overlap in passerine birds. Nature Ecology & Evolution 1, 15261534.CrossRefGoogle ScholarPubMed
Kato, A, Albert, PS, Vega, JM and Birchler, JA (2006) Sensitive fluorescence in situ hybridization signal detection in maize using directly labeled probes produced by high concentration DNA polymerase nick translation. Biotechnic and Histochemistry 81, 7178.CrossRefGoogle ScholarPubMed
Kozlovskaya, VI and German, AV (1997) Polychlorinated biphenyls and polycyclic aromatic hydrocarbons in ecosystem of Rybinsk reservoir. Water Resources 24, 563569 (in Russian).Google Scholar
Kráľová-Hromadová, I, Štefka, J, Špakulová, M, Orosová, M, Bombarová, M, Hanzelová, V, Bazsalovicsová, E and Scholz, T (2010) Intraindividual ITS1 and ITS2 ribosomal sequence variation linked with multiple rDNA loci: a case of triploid Atractolytocestus huronensis, the monozoic cestode of common carp. International Journal for Parasitology 40, 175181.CrossRefGoogle Scholar
Levan, A, Fredga, K and Sandberg, A (1964) Nomenclature for centromere position on chromosomes. Hereditas 52, 201220.CrossRefGoogle Scholar
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of the Platyhelminthes. London: Taylor and Francis, pp. 262278.Google Scholar
Motomura, I (1929) On the early development of monozoic cestode, Archigetes appendicularis, including the oogenesis and fertilisation. Annotationes Zoologicae Japonenses 12, 109129.Google Scholar
Naseeb, S, Carter, Z, Minnis, D, Donaldson, I, Zeef, L and Delneri, D (2016) Widespread impact of chromosomal inversions on gene expression uncovers robustness via phenotypic buffering. Molecular Biology and Evolution 33, 16791696.CrossRefGoogle ScholarPubMed
Ogura, I (2004) Half-life of each dioxin and PCB congener in the human body. Organohalogen Compounds 66, 33293337.Google Scholar
Oros, M, Uhrovič, D and Scholz, T (2018) A new classification of Glaridacris Cooper, 1920 (Cestoda: Caryophyllidea), parasites of suckers (Catostomidae) in North America, including erection of Pseudoglaridacris n. gen. Journal of Parasitology 104, 6069.CrossRefGoogle ScholarPubMed
Orosová, M and Oros, M (2012) Classical and molecular cytogenetics of Khawia sinensis (Cestoda: Caryophyllidea), invasive parasite of carp, Cyprinus carpio. Parasitology Research 110, 19371944.CrossRefGoogle Scholar
Orosová, M and Špakulová, M (2018) Tapeworm chromosomes: their value in systematics with instructions for cytogenetic study. Folia Parasitologica 65, 001.CrossRefGoogle ScholarPubMed
Orosová, M, Kráľová-Hromadová, I, Bazsalovicsová, E and Špakulová, M (2010 a) Karyotype, chromosomal characteristics of multiple rDNA clusters and intragenomic variability of ribosomal ITS2 in Caryophyllaeides fennica (Cestoda). Parasitology International 59, 351357.CrossRefGoogle Scholar
Orosová, M, Marec, F, Oros, M, Xi, BW and Scholz, T (2010 b) A chromosome study and 18S rDNA in situ hybridization of Khawia saurogobii (Cestoda: Caryophyllidea). Parasitology Research 106, 587593.CrossRefGoogle Scholar
Orosová, M, Provazníková, I, Xi, BW and Oros, M (2019) Chromosomal study of Khawia abbottinae (Cestoda: Caryophyllidea): karyotype and localization of telomeric and ribosomal sequences after fluorescence in situ hybridization (FISH). Parasitology Research 118, 27892800.CrossRefGoogle Scholar
Orosová, M, Marková, A, Provazníková, I, Oros, M, Radačovská, A, Čadková, Z and Marec, F (2021) Molecular cytogenetic analysis of a triploid population of the human broad tapeworm, Dibothriocephalus latus (Diphyllobothriidea). Parasitology 148, 787797.CrossRefGoogle Scholar
Petkevičiūtė, R (1996) A chromosome study of Schistocephalus solidus (Muller, 1776) (Cestoda: Pseudophyllidea). Systematic Parasitology 33, 183186.CrossRefGoogle Scholar
Petkevičiūtė, R (2003) Comparative karyological analysis of three species of Bothriocephalus Rudolphi, 1808 (Cestoda: Pseudophyllidea). Parasitology Research 5, 358363.CrossRefGoogle Scholar
Petkevičiūtė, R and Bondarenko, SK (2001) Comparative karyological studies on the species of Eubothrium Nybelin, 1922 (Cestoda: Pseudophyllidea). Systematic Parasitology 50, 127134.CrossRefGoogle Scholar
Petkevičiūtė, R and Kuperman, BI (1992) Karyological investigation of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea). Folia Parasitologica 39, 115121.Google Scholar
Petkevičiūtė, R, Stunžėnas, V and Stanevičiūtė, G (2018) Comments on species divergence in the genus Sphaerium (Bivalvia) and phylogenetic affinities of Sphaerium nucleus and S. corneum var. mamillanum based on karyotypes and sequences of 16S and ITS1 rDNA. PLoS One 13, e0191427.CrossRefGoogle ScholarPubMed
Proffitt, MR and Jones, AW (1969) Chromosome analysis of Hymenolepis microstoma. Parasitology 25, 7284.Google ScholarPubMed
Rábová, M, Volker, M, Pelikánová, Š and Ráb, P (2015) Sequential chromosome bandings in fishes. In Ozouf-Costaz, C, Pisano, E, Foresti, F and Toledo, LFA (eds), Fish Cytogenetic Techniques, Ray-Fin Fishes and Chondrichthyans. Boca Raton, USA: CRC Press, pp. 6673.Google Scholar
Sahara, K, Marec, F and Traut, W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Research 76, 449460.CrossRefGoogle Scholar
Šalgovičová, D and Zmetáková, Z (2006) Polychlorinated biphenyls in muscle tissue of freshwater fish in East Slovakia. Journal of Food and Nutrition Research 45, 171178.Google Scholar
Sandal, S, Yilmaz, B and Carpenter, DO (2008) Genotoxic effects of PCB 52 and PCB 77 on cultured human peripheral lymphocytes. Mutation Research 654, 8892.CrossRefGoogle ScholarPubMed
Scholz, T, Brabec, J, Kráľová-Hromadová, I, Oros, M, Bazsalovicsová, E, Ermolenko, A and Hanzelová, V (2011) Revision of Khawia spp. (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a key to their identification and molecular phylogeny. Folia Parasitologica 58, 197223.CrossRefGoogle Scholar
Scholz, T, Oros, M, Bazsalovicsová, E, Brabec, J, Waeschenbach, A, Xi, BW, Aydoğdu, A, Besprozvannykh, V, Shimazu, T, Králová-Hromadová, I and Littlewood, DTJ (2014) Molecular evidence of cryptic diversity in Paracaryophyllaeus (Cestoda: Caryophyllidea), parasites of loaches (Cobitidae) in Eurasia, including description of P. vladkae n. sp. Parasitology International 63, 841850.CrossRefGoogle ScholarPubMed
Scholz, T, Oros, M, Choudhury, A, Brabec, J and Waeschenbach, A (2015) New circumscription of freshwater fish parasites Monobothrium Diesing, 1863 and Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea) using morphological and molecular evidence. Journal of Parasitology 101, 2936.CrossRefGoogle ScholarPubMed
Scholz, T, Waeschenbach, A, Oros, M, Brabec, J and Littlewood, DTJ (2021) Phylogenetic reconstruction of early diverging tapeworms (Cestoda: Caryophyllidea) reveals ancient radiations in vertebrate hosts and biogeographic regions. International Journal for Parasitology 51, 263277.CrossRefGoogle ScholarPubMed
Špakulová, M, Orosová, M and Mackiewicz, JS (2011) Cytogenetics and chromosomes of the tapeworms (Platyhelmithes, Cestoda). Advances in Parasitology 74, 177230.CrossRefGoogle Scholar
Špakulová, M, Bombarová, M, Miklisová, D, Nechybová, S and Langrová, I (2019) How to become a successful invasive tapeworm: a case study of abandoned sexuality and exceptional chromosome diversification in the triploid carp parasite Atractolytocestus huronensis Anthony, 1958 (Caryophyllidea: Lytocestidae). Parasites & Vectors 12, 161.CrossRefGoogle Scholar
Sures, B, Nachev, M, Selbach, C and Marcogliese, DJ (2017) Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology’. Parasites & Vectors 10, 65.CrossRefGoogle ScholarPubMed
Vijayaraghavan, S and Subramanyam, S (1977) Chromosome number of the cestode Lytocestus indicus. Current Science 46, 312313.Google Scholar
Wellenreuther, M and Bernatchez, L (2018) Eco-evolutionary genomics of chromosomal inversions. Trends in Ecology & Evolution 33, 427440.CrossRefGoogle ScholarPubMed
Xi, BW, Barčák, D, Oros, M, Chen, K and Xie, J (2016) The occurrence of the common European fish cestode Caryophyllaeus laticeps (Pallas, 1781) in the river Irtysh, China: a morphological characterization and molecular data. Acta Parasitologica 61, 493499.CrossRefGoogle ScholarPubMed
Zrzavá, M, Hladová, I, Dalíková, M, Šíchová, J, Ounap, E, Kubíčková, S and Marec, F (2018) Sex chromosomes of the iconic moth Abraxas grossulariata (Lepidoptera, Geometridae) and its congener A. sylvata. Genes 9, 279.CrossRefGoogle ScholarPubMed
Supplementary material: Image

Orosová et al. supplementary material

Orosová et al. supplementary material 1

Download Orosová et al. supplementary material(Image)
Image 6.9 MB
Supplementary material: File

Orosová et al. supplementary material

Table S1

Download Orosová et al. supplementary material(File)
File 16.6 KB
Supplementary material: File

Orosová et al. supplementary material

Table S2

Download Orosová et al. supplementary material(File)
File 16.8 KB