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Morphometrical and molecular evidence suggests cryptic diversity among hookworms (Nematoda: Uncinaria) that parasitize pinnipeds from the south-eastern Pacific coasts

Published online by Cambridge University Press:  15 November 2018

M.T. González
Affiliation:
Instituto de Ciencias Naturales Alexander von Humboldt, Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta, Angamos 601-Antofagasta, Chile
Z. López
Affiliation:
Instituto de Ciencias Naturales Alexander von Humboldt, Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta, Angamos 601-Antofagasta, Chile Programa Doctorado en Ciencias m/Ecología y Evolución, Universidad de Chile, Av. Las Palmeras, Santiago, Chile
J.J. Nuñez
Affiliation:
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Casilla 567, Valdivia, Chile
K.I. Calderón-Mayo
Affiliation:
Programa Magíster en Ecología de Sistemas Acuáticos, Facultad de Ciencias del Mar y Recursos Biológicos, Universidad de Antofagasta, Angamos 601-Antofagasta, Chile
C. Ramírez
Affiliation:
Depto de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, Chile
D. Morgades
Affiliation:
Facultad de Veterinaria, Universidad de la República, Av. Alberto Lasplaces 1550, CP 11400, Montevideo, Uruguay
H. Katz
Affiliation:
Facultad de Veterinaria, Universidad de la República, Av. Alberto Lasplaces 1550, CP 11400, Montevideo, Uruguay
M. George-Nascimento
Affiliation:
Facultad de Ciencias, Universidad Católica de la Ssma Concepción, Concepción, Chile
H. Pavés
Affiliation:
Departamento de Ciencias Biológicas, Facultad de Ciencias, Universidad Santo Tomás, Los Carrera 753, Osorno, Chile
Corresponding
E-mail address:

Abstract

Hookworms of the genus Uncinaria parasitize pinniped pups in various locations worldwide. Four species have been described, two of which parasitize pinniped pups in the southern hemisphere: Uncinaria hamiltoni parasitizes Otaria flavescens and Arctocephalus australis from the South American coast, and Uncinaria sanguinis parasitizes Neophoca cinerea from the Australian coast. However, their geographical ranges and host specificity are unknown. Uncinaria spp. are morphologically similar, but molecular analyses have allowed the recognition of new species in the genus Uncinaria. We used nuclear genetic markers (internal transcribed spacer (ITS) and large subunit (LSU) rDNA) and a mitochondrial genetic marker (cytochrome c oxidase subunit I (COI)) to evaluate the phylogenetic relationships of Uncinaria spp. parasitizing A. australis and O. flavescens from South American coasts (Atlantic and Pacific coasts). We compared our sequences with published Uncinaria sequences. A Generalized Mixed Yule Coalescent (GMYC) analysis was also used to delimit species, and principal component analysis was used to compare morphometry among Uncinaria specimens. Parasites were sampled from A. australis from Peru (12°S), southern Chile (42°S), and the Uruguayan coast, and from O. flavescens from northern Chile (24°S) and the Uruguayan coast. Morphometric differences were observed between Uncinaria specimens from both South American coasts and between Uncinaria specimens from A. australis in Peru and southern Chile. Phylogenetic and GMYC analyses suggest that south-eastern Pacific otariid species harbour U. hamiltoni and an undescribed putative species of Uncinaria. However, more samples from A. australis and O. flavescens are necessary to understand the phylogenetic patterns of Uncinaria spp. across the South Pacific.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2018 

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References

Baylis, HA (1933) A new species of the nematode genus Uncinaria from a sea-lion, with some observations on related species. Parasitology 25, 308316.CrossRefGoogle Scholar
Berta, A and Churchill, M (2012) Pinniped taxonomy, review of currently recognized species and subspecies, and evidence used for their description. Mammal Review 42, 207234.CrossRefGoogle Scholar
Bouckaert, R et al. (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10(4), e1003537.CrossRefGoogle ScholarPubMed
Castinel, A et al. (2006) First report and characterization of adult Uncinaria spp. in New Zealand sea lion (Phocarctos hookeri) pups from the Auckland Islands, New Zealand. Parasitology Research 98, 304309.CrossRefGoogle ScholarPubMed
Catalano, S et al. (2015) Morphological variability and molecular identification of Uncinaria spp. Nematoda Ancylostomatidae from grizzly and black bears: new species or phenotypic plasticity? Journal of Parasitology 101, 182192.CrossRefGoogle ScholarPubMed
Chilton, NB et al. (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Molecular Phylogenetic Evolution 40, 118128.CrossRefGoogle ScholarPubMed
Dailey, MD and Hill, BL (1970) A survey of metazoan parasites infecting the California (Zalophus californianus) and Steller (Eumetopias jubatus) sea lion. Bulletin of the Southern California Academy of Sciences 69, 126132.Google Scholar
Darriba, D et al. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Efron, B (1982) The jackknife, the bootstrap and other resampling plans. Monograph. 38, 196.Google Scholar
Filatov, DA (2002) Proseq software for preparation and evolutionary analysis of DNA sequence datasets. Molecular Ecology Notes 2, 621624.CrossRefGoogle Scholar
George-Nascimento, M, Lima, M and Ortiz, E (1992) A case of parasite mediated competition? Phenotypic differentiation among hookworms Uncinaria sp. (Nematoda: Ancylostomatidae) in sympatric and allopatric populations of South American sea lions Otaria byronia and fur seals Arctocephalus australis (Carnivora: Otariidae). Marine Biology 112, 527533.CrossRefGoogle Scholar
Hall, TA (1999) BioEdit a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Halnet, B, Schmidt, A and Bolek, M (2015) Cryptic species of hairworm parasites revealed by molecular data and crowdsourcing of specimen collections. Molecular Phylogenetic and Evolution 82, 211218.Google Scholar
Haynes, BT et al. (2014) Unexpected absence of genetic separation of a highly diverse population of hookworms from geographically isolated hosts. Infection, Genetic and Evolution 28, 192200.CrossRefGoogle ScholarPubMed
Hu, M et al. (2002) Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase subunit 1 reveals significant substructuring in hookworm populations. Electrophoresis 23, 2734.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Huelsenbeck, JP et al. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 23102314.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.CrossRefGoogle ScholarPubMed
Kuzmina, T and Kuzmin, Y (2015) Description of Uncinaria lyonsi n. sp. Nematoda Ancylostomatidae from the California sea lion Zalophus californianus Lesson (Carnivora Otariidae). Systematic Parasitology 902, 165176.CrossRefGoogle Scholar
Li, WLS and Drummond, AJ (2012) Model averaging and Bayes factor calculation of relaxed molecular clocks in Bayesian phylogenetics. Molecular Biology and Evolution 29, 751761.CrossRefGoogle ScholarPubMed
Lucio-Forster, A et al. (2012) Morphological differentiation of eggs of Ancylostoma caninum, Ancylostoma tubaeforme, and Ancylostoma braziliense from dogs and cats in the United States. Journal of Parasitology 98, 10411044.CrossRefGoogle ScholarPubMed
Marcus, AD et al. (2014) Uncinaria sanguinis sp. n. Nematoda Ancylostomatidae from the endangered Australian sea lion Neophoca cinerea (Carnivora Otariidae). Folia Parasitologica 61, 255265.CrossRefGoogle Scholar
Monaghan, MT et al. (2009) Accelerated species inventory on Madagascar using coalescent based models of species delineation. Systematic Biology 58, 298311.CrossRefGoogle ScholarPubMed
Nadler, SA et al. (2000) Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: hypothesis testing supplants verification. Journal of Parasitology 86, 10991106.CrossRefGoogle ScholarPubMed
Nadler, SA et al. (2013) Molecular systematics of pinniped hookworms (Nematoda: Uncinaria): species delimitation host associations and host-induced morphometric variation. International Journal for Parasitology 43, 11191132.CrossRefGoogle ScholarPubMed
Nyakatura, K and Bininda-Emonds, ORP (2012) Updating the evolutionary history of Carnivora (Mammalia): a new species-level supertree complete with divergence time estimates. BMC Biology 10, 12.CrossRefGoogle ScholarPubMed
Nylander, JA et al. (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology 53, 4767.CrossRefGoogle ScholarPubMed
Oliveira, LR et al. (2008) Morphological and genetic evidence for two evolutionarily significant units ESUS in the South American fur seal Arctocephalus australis. Conservation Genetics 9, 14511466.CrossRefGoogle Scholar
Oliveira, LR and Brownell, RL Jr (2014) Taxonomic status of two subspecies of South American fur seals Arctocephalus australis australis vs. A. a. gracilis. Marine Mammal Science 30, 12581263.CrossRefGoogle Scholar
Pavés, H (2008) Conducta Reproductiva, Mortalidad Neonatal y Tendencia Poblacional De Una Agrupación Reproductiva Del Lobo Fino Austral (Arctocephalus australis, Zimmermann, 1783) en La Isla Guafo, Chiloé, Chile. PhD thesis. Mención sistemática y Ecología, Facultad de Ciencias. Universidad Austral de Chile.CrossRefGoogle Scholar
Pavés, H et al. (2016) Breeding season of the South American fur seal (Arctocephalus australis gracilis): new data to establish independent evolutionary histories. Revista de Biologia Marina y Oceanografia 51, 241253.CrossRefGoogle Scholar
Pons, J et al. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595609.CrossRefGoogle ScholarPubMed
Powell, JR et al. (2011) Evolutionary criteria outperform operational approaches in producing ecologically relevant fungal species inventories. Molecular Ecology 20, 655666.CrossRefGoogle ScholarPubMed
Ramos, P et al. (2013) Morphometric and molecular characterization of the species of Uncinaria Frölich 1789 (Nematoda) parasitic in the Australian fur seal Arctocephalus pusillus doriferus (Schreber) with notes on hookworms in three other pinniped hosts. Systematic Parasitology 85, 6578.CrossRefGoogle ScholarPubMed
Seguel, M and Gottdenker, N (2017) The diversity and impact of hookworm infections in wildlife. International Journal for Parasitology: Parasites and Wildlife 6, 177194.Google ScholarPubMed
Sepúlveda, F and González, MT (2014) Molecular and morphological analyses reveal that the pathogen Benedenia seriolae (Monogenea: Capsalidae) is a complex species: implications for yellowtail Seriola spp. aquaculture. Aquaculture 418–419, 94100.CrossRefGoogle Scholar
Silvestro, D and Michalak, I (2012) raxmlGUI: a graphical front-end for RAxML. Organisms Diversity & Evolution 12, 335337.CrossRefGoogle Scholar
Struck, T et al. (2018) Finding evolutionary processes hidden in cryptic species. Trends in Ecology & Evolution 33, 153163.CrossRefGoogle ScholarPubMed
Swofford, DL (2001) PAUP*. Phylogenetic Anaylsis Using Parsimony (*and Other Methods). 4th ed. Sunderland, MA: Sinauer Associates.Google Scholar
Túnez, JI et al. (2013) The role of Pleistocene glaciations in shaping the genetic structure of South American fur seals (Arctocephalus australis). New Zealand Journal of Marine Freshwater Research 47, 139152.CrossRefGoogle Scholar
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Morphometrical and molecular evidence suggests cryptic diversity among hookworms (Nematoda: Uncinaria) that parasitize pinnipeds from the south-eastern Pacific coasts
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Morphometrical and molecular evidence suggests cryptic diversity among hookworms (Nematoda: Uncinaria) that parasitize pinnipeds from the south-eastern Pacific coasts
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