Skip to main content
SpringerLink
Log in

Coevolution between Contracaecum (Nematoda, Anisakidae) and Austrolebias (Cyprinodontiformes, Rivulidae) host-parasite complex from SW Atlantic coastal basins

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In recent years, molecular studies in host-parasite interactions in terms of coevolution have become important. Larvae (L3) of two species of Contracaecum were found parasitizing species of Rivulidae in the Atlantic coastal basins from Uruguay. The aim of this study is to determine the patterns of differentiation of this host-parasite complex in order to clarify possible coevolutionary events in such interaction throughout phylogeographic approach using both nuclear and mitochondrial molecular markers (internal transcribed spacers (ITS) and cytochrome oxidase subunit 1 (cox-1)). Based on both markers, intraspecific variation in Contracaecum species was lower than 2 %, while interspecific variation was greater than 10 %. Both species of Contracaecum constitute monophyletic groups. Contracaecum resulted in a paraphyletic genus when incorporating other Contracaecum species and closely related nematode sequences from GenBank. ITS regions showed that Contracaecum sp. 1 is more closely related to other species of the same genus than with their counterparts from Atlantic coastal basins in Uruguay. Haplotype network for both markers corroborate the existence of two distinct taxa. While ITS pairwise FST comparisons and the indirect estimate of gene flow confirm the existence of two distinct Contracaecum species, mitochondrial gene detected low levels of migrants between some of the populations from both species. Our results suggest that coevolution in this host-parasite complex species is plausible. Parasite cladogenetic events occur almost simultaneously with the separation of the hypothetical ancestors of each species complex of Austrolebias during Pliocene. Additionally, the two lineages of Contracaecum colonize differently the species within each of the Austrolebias complexes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Auto Contr AC 19:716–723

    Article  Google Scholar 

  • Amato LH (1986) Seis especies nuevas del género Cynolebias Steindachner, 1876 de Uruguay y Paraguay (Cyprinodontiformes, Rivulidae). Comun Zool Mus Hist Nat Montev 1:1–27

    Google Scholar 

  • Avise JC (1994) Molecular markers: natural history and evolution. Chapman and Hall Bernardi G, Powers DA, New York

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  PubMed  CAS  Google Scholar 

  • Blouin MS, Yowell CA, Courtney CH, Dame JB (1998) Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Mol Biol Evol 15:1719–1727

    Article  PubMed  CAS  Google Scholar 

  • Blouin MS, Liu J, Berry RE (1999) Life cycle variation and the genetic structure of nematode populations. Heredity 83:253–259

    Article  PubMed  CAS  Google Scholar 

  • Brooks DJ, McLennan D (1991) Neotropical freshwater stingrays and their parasites: a tale of two oceans. In: Parascript. Parasites and the language of evolution. Smithsonian Institution Press, Washington, p 57–69

  • Brooks DR, Thorson TB, Mayes MA (1981) Freshwater stingrays and their helminth parasites: testing hypotheses of evolution and coevolution. In: Funk VA, Brooks DR (eds) Advances in cladistics. Proceedings of the Willi Henning Society. New York Botanical Garden, New York, pp 147–175

    Google Scholar 

  • Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A 76:1967–1971

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cavallero S, Nadler SA, Paggi L, Barros NB, 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. Parasitol Res 108:781–792. doi:10.1007/s00436-010-2226-y

    Article  PubMed  Google Scholar 

  • Costa W (2006) The South American annual killifish genus Austrolebias (Teleostei: Cyprinodontiformes: Rivulidae): phylogenetic relationships, descriptive morphology and taxonomic revision. Zootaxa 1213:1–162

    Google Scholar 

  • Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257. doi:10.1111/j.1365-294X.2005.02587.x

    Article  PubMed  CAS  Google Scholar 

  • D’ Amelio S, Cavallero S, Dronen NO, Barros NB, Paggi L (2012) Two new species of Contracaecum Railliet y Henry, 1912 (Nematoda: Anisakidae), C. fagerholmi n. sp. and C. rudolphii F from the brown pelican Pelecanus occidentalis in the northern Gulf of Mexico. Syst Parasitol 81:1–16. doi:10.1007/s11230-011-9323-x

    Article  Google Scholar 

  • Desdevises Y (2007) Cophylogeny: insights from fish-parasite systems. Parassitologia 49:125–128

    PubMed  CAS  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. doi:10.1186/1471-2148-7-214

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dzido J, Kijewska A, Rokicki J (2012) Selected mitochondrial genes as species markers of the Arctic Contracaecum osculatum complex. J Helminthol 86:252–258. doi:10.1017/S0022149X11000332

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed Central  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed Central  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed Central  PubMed  CAS  Google Scholar 

  • García G (2006) Multiple simultaneous speciation in killifishes of the Cynolebias adloffi species complex (Cyprinodontiformes, Rivulidae) from phylogeography and chromosome data. J Zool Syst Evol Res 44:75–87. doi:10.1111/j.1439-0469.2005.00346.x

    Article  Google Scholar 

  • García G, Scvortzoff E, Máspoli M, Vaz Ferreira R (1993) Analysis of karyotypic evolution in natural population of Cynolebias (Pisces: Cyprinodontiformes, Rivulidae) using banding techniques. Cytologia 58:85–94

    Article  Google Scholar 

  • García G, Wlasiuk G, Lessa EP (2000) High levels of mitochondrial cytochrome b divergence and phylogenetic relationships in the annual killifishes of the genus Cynolebias (Cyprinodontiformes, Rivulidae). Zool J Linn Soc-Lond 129:93–110

    Article  Google Scholar 

  • García G, Lalanne AI, Aguirre G, Cappeta M (2001) Chromosome evolution in the anual killfish genus Cynolebias and mitocondrial analysis. Chromosome Res 9:437–448

    Article  PubMed  Google Scholar 

  • García G, Alvarez-Valin F, Gomez N (2002) Mitochondrial genes: signals and noise in the phylogenetic reconstruction of the annual killifish genus Cynolebias (Cyprinodontiformes, Rivulidae). Biol J Linn Soc 76:49–59

    Google Scholar 

  • García G, Claramunt S, Lalanne AI (2004) Genetic differentiation among annual fishes of the genus Cynolebias (Cyprinodontiformes, Rivuluidae) in a Biosphere Reserve site from Uruguay. Environ Biol Fish 70:247–256

    Article  Google Scholar 

  • García G, Loureiro M, Berois N, Arezo MJ, Casanova G, Clivio G, Olivera A (2009) Pattern of differentiation in the annual killifish genus Austrolebias (Cyprinodontiformes: Rivulidae) from a biosphere reserve site in South America: a multidisciplinary approach. Biol J Linn Soc 98:620–235

    Article  Google Scholar 

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010

    Article  PubMed  CAS  Google Scholar 

  • Harpending HC (1994) Signature of ancient population growth in a low resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    PubMed  CAS  Google Scholar 

  • Hasan A, Suguri S, Fujimoto C, Itaki R, Harada M, Kawabata M, Bugoro H, Albino B (2008) Genetic diversity in two sibling species of the Anopheles punctulatus group of mosquitoes on Guadalcanal in the Solomon Islands. BMC Evol Biol 8:318. doi:10.1186/1471-2148-8-318

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  PubMed  CAS  Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192

    Article  Google Scholar 

  • Hoberg EP, Brooks DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. J Biogeogr 35:1533–1550. doi:10.1111/j.1365-2699.2008.01951.x

    Article  Google Scholar 

  • Holmes DS, Bonner J (1973) Preparation, molecular weight, base composition, and secondary structure of giant nuclear ribonucleic acid. Biochemistry 12:2330–2338

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Crandall KA (1997) Phylogeny estimation and hypothesis testing using maximum likelihood. Annu Rev Ecol Syst 28:437–466

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738

    PubMed Central  PubMed  CAS  Google Scholar 

  • Klimpel S, Kleinertz S, Reinhold H, Rückert S (2007) Genetic variability in Hysterothylacium aduncum, a raphidascarid nematode isolated from sprat (Sprattus sprattus) of different geographical areas of the northeastern Atlantic. Parasitol Res 101:1425–1430. doi:10.1007/s00436-007-0662-0

    Article  PubMed  Google Scholar 

  • Kuusela J, Holopainen R, Meinila M, Anttila P, Koski P, Ziętara M, Veselov A, Primmer C, Lumme J (2009) Clonal structure of salmon parasite Gyrodactylus salaris on a coevolutionary gradient on Fennoscandian salmon (Salmo salar). Ann Zool Fenn 46:21–33

    Article  Google Scholar 

  • Li AX, D’Amelio S, Paggi L, He F, Gasser RB, Lun ZR, Abollo E, Turchetto M, Zhu XQ (2005) Genetic evidence for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) and the validity of Contracaecum septentrionale (Kreis, 1955) (Nematoda: Anisakidae). Parasitol Res 96:361–366. doi:10.1007/s00436-005-1366-y

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187

    Article  PubMed  CAS  Google Scholar 

  • Liedloff A (1999) Mantel nonparametric test calculator for Windows. Version 2.0. Distributed by the author, School of Natural Resource Science, Queensland University of Technology, Brisbane, Australia

  • Lin RQ, Liu GH, Zhang Y, D’Amelio S, Zhou DH, Yuan ZG, Zou FC, Song HQ, Zhu XQ (2012) Contracaecum rudolphii B: gene content, arrangement and composition of its complete mitochondrial genome compared with Anisakis simplex s.l. Exp Parasitol 130:135–140. doi:10.1016/j.exppara.2011.11.003

    Article  PubMed  CAS  Google Scholar 

  • Loureiro M, de Sá R (1996) External morphology of the chorion of the annual fishes Cynolebias (Cyprinodontiformes: Rivulidae). Copeia 1016–1022

  • Loureiro M, Duarte A, Zarucki M (2011) A new species of Austrolebias Costa (Cyprinodontiformes: Rivulidae) from northeastern Uruguay, with comments on distribution patterns. Neotrop Ichthyol 9:335–342

    Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    PubMed  CAS  Google Scholar 

  • Mattiucci S (2006) Parasites as biological tags in population studies of demersal and pelagic fish species. Parassitologia 48:23–25

    PubMed  CAS  Google Scholar 

  • Mattiucci S, Nascetti G (2008) Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasit 66:47–148. doi:10.1016/S0065-308X(08)00202-9

    Article  Google Scholar 

  • Mattiucci S, Paoletti M, Olivero-Verbel J, Baldiris R, Arroyo-Salgado B, Garbin L, Navone G, Nascetti G (2008) Contracaecum bioccai n. sp. from the brown pelican Pelecanus occidentalis (L.) in Colombia (Nematoda: Anisakidae): morphology, molecular evidence and its genetic relationship with congeners from fish-eating birds. Syst Parasitol 69:101–121. doi:10.1051/parasite/2008153408

    Article  PubMed  Google Scholar 

  • Medrano JF, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43

    PubMed  CAS  Google Scholar 

  • Molnar R, Bartelmes G, Dinkelacker I, Witte H, Sommer R (2011) Mutation rates and intraspecific divergence of the mitochondrial genome of Pristionchus pacificus. Mol Biol Evol 28:2317–2326. doi:10.1093/molbev/msr057

    Article  PubMed  CAS  Google Scholar 

  • Nadler S, Hudspeth DSS (2000) Phylogeny of the ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. J Parasitol 86:380–393

    Article  PubMed  CAS  Google Scholar 

  • Nadler SA, D'Amelio S, Fagerholm HP, Berland B, Paggi L (2000) Phylogenetic relationships among species of Contracaecum Railliet & Henry, 1912 and Phocascaris Host, 1932 (Nematoda: Ascaridoidea) based on nuclear rDNA sequence data. Parasitology 121:455–463

    Article  PubMed  CAS  Google Scholar 

  • Nadler S, D`Amelio S, Murray D, Paggi L, Siu S, Sakanari JA (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from Northern Pacific marine mammals. J Parasitol 91:1413–1429

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  • Palumbi S, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu

  • Pardo CS, Mejía K, Navarro Y, Atencio V (2007) Prevalencia y abundancia de Contracaecum sp. en rubio Salminus affinis en el Río Sinú y San Jorge: descripción morfológica. Revista MVZ Córdoba 12:887–896

    Google Scholar 

  • Pontes T, D’Amelio S, Costa G, Paggi L (2005) Molecular characterization of larval anisakid nematodes from marine fishes of Madeira by a PCR-based approach, with evidence for a new species. J Parasitol 91:1430–1434

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Presa P, Pardo B, Martínez P, Bernatchez L (2002) Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Mol Biol Evol 19:2161–2175

    Article  PubMed  CAS  Google Scholar 

  • Railliet A, Henry A (1912) Quelques nématodes parasites des reptiles. B Soc Pathol Exot 5:251–259

    Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer v.1.5. Retrieved March 1, 2014, from http://beast.bio.ed.aC.uk/Tracer

  • Ramos-Onsins SE, Rozas J (2002) Statistical propierties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501

    Article  PubMed  CAS  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rohde K (1982) Host-parasite interactions. In: Ecology of marine parasites. University of Queensland Press, St Lucia, pp 72–103

  • Ross LG, Ross B (2008) Anaesthetic and sedative techniques for aquatic animals, 3rd edn. Blackwell, Oxford, UK, p 228

    Book  Google Scholar 

  • Shamsi S, Eisenbarth A, Saptarshi S, Beveridge I, Gasser RB, Lopata AL (2011) Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters. Parasitol Res 108:927–934. doi:10.1007/s00436-010-2134-1

    Article  PubMed  Google Scholar 

  • Sprechman P (1980) Paleoecología, paleogeografía y estratigrafía de la región costera del Uruguay durante el Neógeno y Cuaternario. Actas II Congreso Argentino de Paleontología y Bioestratigrafía, y I Congreso Latinoamericano de Paleontología. Buenos Aires, pp 237–256

  • Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (* and other methods). Sinauer, Sunderland

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed Central  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math Life Sci (American Mathematical Society) 17:57–86

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Traversa D, Kuzmina T, Kharchenko VA, Iorio R, Klei TR, Otranto D (2008) Haplotypic variability within the mitochondrial gene encoding for the cytochrome c oxidase 1 (cox1) of Cylicocyclus nassatus (Nematoda, Strongylida): evidence for an affiliation between parasitic populations and domestic and wild equid hosts. Vet Parasitol 156:241–247. doi:10.1016/j.vetpar.2008.05.031

    Article  PubMed  CAS  Google Scholar 

  • Vaz-Ferreira R, Sierra B (1972) Los géneros de Cyprinodontidae de aguas temporales sudamericanas. Bol Soc Zool Uruguay 2:36–42

    Google Scholar 

  • Vaz-ferreira R, Sierra B (1973) Caracteres etológicos genéricos y específicos en los peces del género Cynolebias Steindachner 1876. Bol Soc Zool Uruguay 2:22–35

    Google Scholar 

  • Vidal Martínez VM, Aguirre ML, Scholz T, González DE, Mendoza EF (2002) Atlas de los helmintos parásitos de cíclidos de México. Instituto Politécnico Nacional, México, p 182

    Google Scholar 

  • Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genom Proteome Bioinforma 8:77–80. doi:10.1016/S1672-0229(10)60008-3

    Article  CAS  Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research received financial support from the Initiation Research Project from CSIC_UdelaR (Comisión Sectorial de Investigación Científica) and from post-graduate fellowship of C. Delgado Agencia Nacional de Investigación e Innovación (ANII) of Uruguay. We thank V. Gutiérrez and N. Ríos for their contributions during the field work. We are also very grateful to the following colleagues: M. Loureiro, A. Duarte, S. Serra, C. Passos, and N. Papa for kindly providing additional annual fish specimens from different collecting sites and to O. Volonterio, R.Ponce de León, and J.M. Caspeta-Mandujano for their help in the nematode identification. The authors are also grateful to the Japanese government for the donation of equipment. The research of G.G. was also supported by SNI (ANII).

Author information

Authors and Affiliations

  1. Sección Genética Evolutiva, Facultad de Ciencias, UdelaR, Iguá 4225, 11400, Montevideo, Uruguay

    Cecilia Delgado & Graciela García

Authors
  1. Cecilia Delgado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Graciela García
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cecilia Delgado.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Appendix S1

(DOC 88 kb)

Appendix S2

(DOC 39 kb)

Appendix S3

(DOC 178 kb)

Appendix S4

(DOC 41 kb)

Appendix S5

(DOC 168 kb)

Appendix S6

(DOC 72 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Delgado, C., García, G. Coevolution between Contracaecum (Nematoda, Anisakidae) and Austrolebias (Cyprinodontiformes, Rivulidae) host-parasite complex from SW Atlantic coastal basins. Parasitol Res 114, 913–927 (2015). https://doi.org/10.1007/s00436-014-4257-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4257-2

Keywords

Search

Navigation