Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-22T09:08:46.990Z Has data issue: false hasContentIssue false
  • English
  • Français

Novel polymorphic microsatellite loci in Anisakis pegreffii and A. simplex (s. s.) (Nematoda: Anisakidae): implications for species recognition and population genetic analysis

Published online by Cambridge University Press:  28 June 2019

Simonetta Mattiucci Open the ORCID record for Simonetta Mattiucci [Opens in a new window] ,
Eleonora Bello ,
Michela Paoletti ,
Steve C. Webb ,
Juan T. Timi ,
Arne Levsen ,
Paolo Cipriani  and
Giuseppe Nascetti
Simonetta Mattiucci*
Affiliation:
Department of Public Health and Infectious Diseases, Section of Parasitology, “Sapienza -University of Rome”, Laboratory affiliated to “Istituto Pasteur Italia-Fondazione Cenci Bolognetti, Italy” P.le Aldo Moro, 5 00185 Rome, Italy
Eleonora Bello
Affiliation:
Department of Ecological and Biological Sciences, Tuscia University, Viale dell'Università s/n 01100 Viterbo, Italy
Michela Paoletti
Affiliation:
Department of Ecological and Biological Sciences, Tuscia University, Viale dell'Università s/n 01100 Viterbo, Italy
Steve C. Webb
Affiliation:
Cawthron Institute, Nelson, New Zealand
Juan T. Timi
Affiliation:
Instituto de Investigaciones Marinas y Costeras, Universidad Nacional de Mar del Plata-CONICET, Mar del Plata, Argentina
Arne Levsen
Affiliation:
Institute of Marine Research, Bergen, Norway
Paolo Cipriani
Affiliation:
Institute of Marine Research, Bergen, Norway
Giuseppe Nascetti
Affiliation:
Department of Ecological and Biological Sciences, Tuscia University, Viale dell'Università s/n 01100 Viterbo, Italy
*
Author for correspondence: Simonetta Mattiucci, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The species of Anisakis constitute one of the most widespread groups of ascaridoid nematodes in the marine ecosystem. Three closely related taxa are recognised in the A. simplex (s. l.) complex, i.e. A. pegreffii, A. simplex (s. s.) and A. berlandi. They are distributed in populations of their intermediate/paratenic (fish and squids) and definitive (cetaceans) hosts. A panel of seven microsatellite loci (Anisl 05784, Anisl 08059, Anisl 00875, Anisl 07132, Anisl 00314, Anisl 10535 and Anisl 00185), were developed and validated on a total of N = 943 specimens of A. pegreffii and A. simplex (s. s.), collected in fish and cetacean hosts from allopatric areas within the range of distribution of these parasite species. In addition, the locus Anisl 7, previously detected in those Anisakis spp., was investigated. The parasites were first identified by sequence analysis of the EF1 α-1 nDNA. The panel of the microsatellites loci here developed have allowed to: (i) detect diagnostic microsatellite loci between the two species; (ii) identify specimens of the two species A. pegreffii, A. simplex (s. s.) in a multi-marker nuclear genotyping approach; (iii) discover two sex-linked loci in both Anisakis species and (iv) estimate levels of genetic differentiation at both the inter- and intra-specific level.

Keywords

Anisakis pegreffiiAnisakis simplex (s. s.)EF1 α-1 nDNAmicrosatellitesnuclear markerspopulation geneticssex-linked loci
Type
Research Article
Information
Parasitology , Volume 146 , Issue 11 , September 2019 , pp. 1387 - 1403
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

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

Baldwin, RE, Rew, MB, Johansson, ML, Banks, MA and Jacobson, KC (2011) Population structure of three species of Anisakis nematodes recovered from Pacific sardines (Sardinops sagax) distributed throughout the California Current System. Journal of Parasitology 97, 545–554. doi.org/10.1645/GE-2690.1.Google Scholar
Betson, M, Halstead, FD, Nejsum, P, Imison, E, Khamis, IS, Sousa-Figueiredo, JC, Rollinson, D and Stothard, JR (2011) A molecular epidemiological investigation of Ascaris on Unguja, Zanzibar using isoenyzme analysis, DNA barcoding and microsatellite DNA profiling. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 370–379. doi.org/10.1016/j.trstmh.2011.04.009.Google Scholar
Blažeković, K, Pleić, IL, Đuras, M, Gomerčić, T and Mladineo, I (2015) Three Anisakis spp. isolated from toothed whales stranded along the eastern Adriatic Sea coast. International Journal for Parasitology 45, 17–31. doi.org/10.1016/j.ijpara.2014.07.012.Google Scholar
Buchmann, K and Mehrdana, F (2016) Effects of anisakid nematodes Anisakis simplex (s. l.), Pseudoterranova decipiens (s. l.) and Contracaecum osculatum (s. l.) on fish and consumer health. Food and Waterborne Parasitology 4, 13–22. doi.org/10.1016/j.fawpar.2016.07.003.Google Scholar
Cavallero, S, Nadler, SA, Paggi, L, Barros, NB and D'Amelio, S (2011) Molecular characterization and phylogeny of anisakid nematodes from cetaceans from southeastern Atlantic coasts of USA, Gulf of Mexico and Caribbean Sea. Parasitology Research 108, 781–792.Google Scholar
Chai, JY, Murrell, KD and Lymbery, AJ (2005) Fish-borne parasitic zoonoses: status and issues. International Journal for Parasitology 35, 1233–1254. doi.org/10.1016/j.ijpara.2005.07.013.Google Scholar
Cole, R and Viney, M (2018) The population genetics of parasitic nematodes of wild animals. Parasites & Vectors 11, 590. doi.org/10.1186/s13071-081-3137-5.Google Scholar
Criscione, CD and Blouin, MS (2007) Parasite phylogeographycal congruence with salmon host evolutionarily significant units: implications for salmon conservation. Molecular Ecology 16, 993–1005.Google Scholar
Criscione, CD, Cooper, B and Blouin, MS (2006) Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology 87, 823–827.Google Scholar
Criscione, CD, Anderson, JD, Raby, K, Sudimack, D, Subedi, J, Rai, DR, Upadhayay, RP, Jha, B, Williams-Blangero, S and Anderson, TJ (2007) Microsatellite markers for the human nematode parasite Ascaris lumbricoides: development and assessment of utility. Journal of Parasitology 93, 704–708. doi.org/10.1645/GE-1058R.1.Google Scholar
D'Amelio, S, Mathiopoulos, KD, Santos, CP, Pugachev, ON, Webb, SC, Picanḉo, M and Paggi, L (2000) Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (nematoda: Ascaridoidea) defined by polymerase chain reaction-based restriction fragment length polymorphism. International Journal for Parasitology 30, 223–226. doi.org/10.1016/S0020-7519(99)00178-2.Google Scholar
Evanno, G, Regnaut, S and Goudet, J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620. doi.org/10.1111/j.1365-294X.2005.02553.x.Google Scholar
Excoffier, L and Lischer, HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567. doi.org/10.1111/j.1755-0998.2010.02847.x.Google Scholar
Felsenstein, J (1993) PHYLIP: Phylogeny Inference Package. Seattle, WA: University of Washington.Google Scholar
Glenn, TC, Lance, ST, McKee, AM, Webster, BL, Emery, AM, Zerlotini, A, Oliveira, G, Rollinson, D and Faircloth, BC (2013) Significant variance in genetic diversity among populations of Schistosoma haematobium detected using microsatellite DNA loci from a genome-wide database. Parasites and Vectors 6, 300. doi.org/10.1186/1756-3305-6-300.Google Scholar
González, AF, Gracia, J, Miniño, I, Romón, J, Larsson, C, Maroto, J, Regueira, M and Pascual, S (2018) Approach to reduce the zoonotic parasite load in fish stocks: when science meets technology. Fisheries Research 202, 140–148. doi.org/10.1016/j.fishres.2017.08.016.Google Scholar
Goudet, J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485–486.Google Scholar
Greeff, JM, Reid, K, Gagjee, JR, Clift, SJ and de Waal, PJ (2018) Population genetic structure of the parasitic nematode Spirocerca lupi in South Africa. Veterinary Parasitology 258, 64–69. doi.org/10.1016/vet.par.2018.06.007.Google Scholar
Grillo, V, Jackson, F and Gilleard, JS (2006) Characterisation of Teladorsagia circumcincta microsatellites and their development as population genetic markers. Molecular and Biochemical Parasitology 148, 181–189. doi.org/10.1016/j.molbiopara.2006.03.014.Google Scholar
Guardone, L, Armani, A, Nucera, D, Costanzo, F, Mattiucci, S and Bruschi, F (2018) Human anisakiasis in Italy: a retrospective epidemiological study over two decades. Parasité 25, 41.Google Scholar
Howe, KL, Bolt, BJ, Cain, S, Chan, J, Chen, WJ, Davis, P, Done, J, Down, T, Gao, S, Grove, C, Harris, TW, Kishore, R, Lee, R, Lomax, J, Li, Y, Muller, HM, Nakamura, C, Nuin, P, Paulini, M, Raciti, D, Schindelman, G, Stanley, E, Tuli, MA, Van Auken, K, Wang, D, Wang, X, Williams, G, Wright, A, Yook, K, Berriman, M, Kersey, P, Schedl, T, Stein, L and Sternberg, PW (2016) Wormbase 2016: expanding to enable helminth genomic research. Nucleic Acids Research 44, D774–D780. doi.org/10.1093/nar/gkv1217.Google Scholar
Johnson, PC, Webster, LM, Adam, A, Buckland, R, Dawson, DA and Keller, LF (2006) Abundant variation in microsatellites of the parasitic nematode Trichostrongylus tenuis and linkage to a tandem repeat. Molecular and Biochemical Parasitology 148, 210–218. doi.org/10.1016/j.molbiopara.2006.04.011.Google Scholar
Larkin, MA, Blackshields, G, Brown, NP, Chenna, R, McGettigan, PA, McWilliam, H, Valentin, F, Wallace, IM, Wilm, A, Lopez, R, Thompson, JD, Gibson, TJ and Higgins, DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics (Oxford, England) 23, 2947–2948.Google Scholar
Levsen, A, Svanevik, CS, Cipriani, P, Mattiucci, S, Gay, M, Hastiee, LC, Pierce, GJ, Bušelić, I, Mladineo, I, Karl, O, Ostermeyer, U, Buchmann, K, Højgaard, DP, González, AF and Pascual, S (2018) A survey of zoonotic nematodes of commercial key fish species from major European fishing grounds – introducing the FP7 PARASITE exposure assessment study. Fisheries Research 202, 4–21. doi.org/10.1016/j.fishres.2017.09.009.Google Scholar
Lowe, AJ, Jones, AE, Raybould, AF, Trick, M, Moule, CL and Edwards, KJ (2002) Transferability and genome specificity of a new set of microsatellite primers among Brassica species of the U triangle. Molecular Ecology Notes 2, 7–11.Google Scholar
Mattiucci, S and Nascetti, G (2007) Genetic diversity and infection levels of anisakid nematodes parasitic in fish and marine mammals from Boreal and Austral hemispheres. Veterinary Parasitology 148, 43–57. doi.org/10.1016/j.vetpar.2007.05.009.Google Scholar
Mattiucci, S and Nascetti, G (2008) Advances and trends in the molecular systematics of Anisakis nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Advances in Parasitology 66, 47–148. doi.org/10.1016/S0065-308X(08)00202-9.Google Scholar
Mattiucci, S, Nascetti, G, Cianchi, R, Paggi, L, Arduino, P, Margolis, L, Brattey, J, Webb, SC, D'Amelio, S, Orecchia, P and Bullini, L (1997) Genetic and ecological data on the Anisakis simplex complex with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). Journal of Parasitology 83, 401–416.Google Scholar
Mattiucci, S, Cipriani, P, Webb, SC, Paoletti, M, Marcer, F, Bellisario, B, Gibson, DI and Nascetti, G (2014) Genetic and morphological approaches distinguishing the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). Journal of Parasitology 15, 12–15. doi.org/10.1645/12-120.1.Google Scholar
Mattiucci, S, Acerra, V, Paoletti, M, Cipriani, P, Levsen, A, Webb, SC, Canestrelli, D and Nascetti, G (2016) No more time to stay ‘single’ in the detection of Anisakis pegreffii, A. simplex (s. s.) and hybridization events between them: a multi-marker nuclear genotyping approach. Parasitology 143, 998–1011. doi.org/10.1017/S0031182016000330.Google Scholar
Mattiucci, S, Paoletti, M, Colantoni, A, Carbone, A, Gaeta, R, Proietti, A, Frattaroli, S, Fazii, P, Bruschi, F and Nascetti, G (2017) Invasive anisakiasis by the parasite Anisakis pegreffii (Nematoda: Anisakidae): diagnosis by Real-time PCR hydrolysis probe system and Immunoblotting assay. BMC Infectious Diseases 17, 530. doi.org/10.1186/s12879-017-2633-0.Google Scholar
Mattiucci, S, Cipriani, P, Levsen, A, Paoletti, M and Nascetti, G (2018a) Molecular epidemiology of Anisakis and anisakiasis: an ecological and evolutionary road map. In Advances in Parasitology, 99, 93–263. doi.org/10.1016/bs.apar.2017.12.001.Google Scholar
Mattiucci, S, Giulietti, L, Paoletti, M, Cipriani, P, Gay, M, Levsen, A, Paoletti, M and Nascetti, G (2018b) Population genetic structure of the parasite Anisakis simplex (s. s.) collected in Clupea harengus L. from North East Atlantic fishing grounds. Fisheries Research 202, 103–111. doi.org/10.1016/j.fishres.2017.08.002.Google Scholar
Mladineo, I, Trumbić, Ž, Radonić, I, Vrbatović, A, Hrabar, J and Bušelić, I (2017) Anisakis simplex complex: ecological significance of recombinant genotypes in an allopatric area of the Adriatic Sea inferred by genome-derived simple sequence repeats. International Journal for Parasitology 47, 215–223. doi.org/10.1016/j.ijpara.2016.11.003.Google Scholar
Müller, F and Tobler, H (2000) Chromatin diminution in the parasitic nematodes Ascaris suum and Parascaris univalens. International Journal for Parasitology 30, 391–399. doi.org/10.1016/S0020-7519(99)00199-X.Google Scholar
Nascetti, G, Paggi, L, Orecchia, P, Smith, JW, Mattiucci, S and Bullini, L (1986) Electrophoretic studies on Anisakis simplex complex (Ascaridida: Anisakidae) from the Mediterranean and North East Atlantic. International Journal for Parasitology 16, 633–640. doi.org/10.1016/0020-7519(86)90032-9.Google Scholar
Nei, M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.Google Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MH, Szoecs, E and Wagner, H (2019) Vegan: Community Ecology Package. R package version 2.5-4.Google Scholar
Patrelle, C, Jouet, D, Lehrter, V and Ferté, H (2014) Development of 12 novel polymorphic microsatellite markers using a next generation sequencing approach for Spiculopteragia spiculoptera, a nematode parasite of deer. Molecular and Biochemical Parasitology 196, 122–125. doi.org/10.1016/j.molbiopara.2014.09.004.Google Scholar
Pritchard, JK, Stephens, M and Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Rabelo, ÉML, de Miranda, RRC, Furtado, LFV, Redondo, RAF, Tennessen, JA and Blouin, MS (2017) Development of new microsatellites for the hookworm Ancylostoma caninum and analysis of genetic diversity in Brazilian populations. Infection, Genetics and Evolution 51, 24–27. doi.org/10.1016/j.meegid.2017.03.008.Google Scholar
Redman, E, Packard, E, Grillo, V, Smith, J, Jackson, F and Gilleard, JS (2008) Microsatellite analysis reveals marked genetic differentiation between Haemonchus contortus laboratory isolates and provides a rapid system of genetic fingerprinting. International Journal for Parasitology 38, 111–122. doi.org/10.1016/j.ijpara.2007.06.008.Google Scholar
Reid, K, Hoareau, TB and Bloomer, P (2012) High-throughput microsatellite marker development in two sparid species and verification of their transferability in the family Sparidae. Molecular Ecology Resources 12, 740–752. doi.org/10.1111/j.1755-0998.2012.03138.x.Google Scholar
Rice, WR (1989) Analyzing tables of statistical tests. Evolution 43, 223–225. doi.org/10.1111/j.1558-5646.1989.tb04220.x.Google Scholar
Sambrook, J and Russell, DW (2001) Molecular cloning: a laboratory manual (3rd edition). Immunology 49, 895–909.Google Scholar
Selkoe, KA and Toonen, RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters 9, 615–629. doi.org/10.1111/j.1461-0248.2006.00889.x.Google Scholar
Swofford, DL and Selander, RBA (1997) BIOSYS 2. A Computer Program for the Analysis of Allelic Variation Genetics. Urbana, IL: University of Illinois.Google Scholar
Temperley, ND, Webster, LM, Adam, A, Keller, LF and Johnson, PC (2009) Cross-species utility of microsatellite markers in Trichostrongyloid nematodes. Journal of Parasitology 95, 487–489. doi.org/10.1645/GE-1624.1.Google Scholar
Umehara, A, Kawakami, Y, Araki, J and Uchida, A (2007) Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitology International 56, 211–215. doi.org/10.1016/j.parint.2007.02.005.Google Scholar
Valentini, A, Mattiucci, S, Bondanelli, P, Webb, SC, Mignucci-Giannone, A, Colom-Llavina, MM and Nascetti, G (2006) Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozyme data. Journal of Parasitology 92, 156–166. doi.org/10.1645/GE-3504.1.Google Scholar
Van Oosterhout, C, Hutchinson, WF, Wills, DP and Shipley, P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538. doi.org/10.1111/j.1471-8286.2004.00684.x.Google Scholar
Weir, BC and Cockerham, CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google Scholar
Zarlenga, DS, Hoberg, E, Rosenthal, B, Mattiucci, S and Nascetti, G (2014) Anthropogenics: human influence on global and genetic homogenization of parasite populations. Journal of Parasitology 100, 756–772. doi.org/10.1645/14-622.1.Google Scholar
Supplementary material: Image

Mattiucci et al. supplementary material

Figure S1

Download Mattiucci et al. supplementary material(Image)
Image 1.4 MB
Supplementary material: Image

Mattiucci et al. supplementary material

Figure S2

Download Mattiucci et al. supplementary material(Image)
Image 477.5 KB
Supplementary material: File

Mattiucci et al. supplementary material

Table S1

Download Mattiucci et al. supplementary material(File)
File 107 KB