Molecular evidence and additional morphological characters to distinguish Ornithodoros brodyi and Ornithodoros yumatensis (Ixodida: Argasidae) in their different developmental stages
-
Carmen Guzmán-Cornejo
, Luis García-Prieto
, Andrea Rebollo-Hernández , José M. Venzal , Santiago Nava and Sokani Sánchez-Montes
Abstract
Ornithodoros brodyi and Ornithodoros yumatensis are two species distributed in the Americas and associated with bats and caves. Both species have similar morphology, and the diagnostic traits of adults have not been detailed or illustrated accurately. In this study, the independence of both species is validated on the basis of molecular evidence (using partial sequences of 16S rDNA gene), and the morphological differences between them (dentition of the hypostome and traits of individual mammillae) are confirmed through light and scanning electron microscopy. In addition to the above characteristics, we observed other traits that may serve to differentiate both species: dorsal setae are short and thick in O. yumatensis and are thin and moderate in size in O. brodyi. We also observed a conspicuous hood in O. brodyi, which was absent in O. yumatensis. Another characteristic observed is a line of setae, near the end of Tarsi II-IV, which in O. brodyi is formed by less than five setae and in O. yumatensis by more than five. The main morphological difference between larvae of the 2 species is the number of ventral setae [9 (4 circumanal pairs) in O. brodyi and 8 (3 circumanal pairs) in O. yumatensis]. The genetic divergence in 16S rDNA sequences between these two species ranges from 9.7 to 10.6%.
Acknowledgments
We thank Laura Del Castillo Martínez for her assistance in mounting process; Silvia Espinosa Matias for preparing the scanning electron micrographs; Laura Márquez for processing samples for sequencing; Anabel Bieler Antolin for editing our photomicrographs and SEM images; Lorenza Beati for the loan of specimens from the USNTC and for allowing the use of collection facilities; Livia León Paniagua for hosts identification; Griselda Montiel-Parra, Gerardo Contreras, Josue López; Ali Lira, Martin Cabrera, Luis Darci Verde for field assistance during our biospeleological expeditions; Gerardo Rivas for statistical advice. This study was supported by the Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, Universidad Nacional Autónoma de México (PAPIIT-UNAM No. IN214114). This manuscript was edited for proper English language by American Journal Experts editors (certificate 896F-44F5-47C5-D61C-701C).
References
Apanaskevich D., Oliver Jr. 2014. Life cycles and Natural History of Ticks. In. Sonenshine D.E., Roe R.M. (Eds) Biology of Ticks. N.Y. Oxford University Press. 59–73Search in Google Scholar
Cooley R.A., Kohls G.M. 1941. Three New Species of Ornithodoros (Acarina: Ixodoidea). Public Health Reports, 56, 587–594. 10.2307/4583666Search in Google Scholar
Cooley R.A., Kohls G.M. 1944. The Argasidae of North America, Central America and Cuba. The American Midland Naturalist. Monograph No. 1, pp.15210.4269/ajtmh.1945.s1-25.1.TMs1-250010071aSearch in Google Scholar
Clifford C.M., Kohls G.M., Sonenshine D.E. 1964. The systematic of the subfamily Ornithodorinae (Acarina: Argasidae). I. The genera and subgenera. Annals of the Entomological Society of America, 57, 429–437. 10.1093/aesa/57.4.429Search in Google Scholar
Dooley T., Bristol J., Canaris A. 1976. Ectoparasites from Bats in Extreme West Texas and South-Central New Mexico. Journal of Mammalogy, 57, 189–191. 10.2307/1379530Search in Google Scholar
Estrada-Peña A., Venzal J.M., Kocan K. M., Tramuta C., Tomassone L., de la Fuente J., Labruna M. 2008. Observations on Antricola Ticks: Small Nymphs Feed on Mammalian Hosts and Have a Salivary Gland Structure Similar to Ixodid Ticks. Journal of Parasitology, 94, 953–955. 10.1645/GE-1371.1Search in Google Scholar PubMed
Gannon W.L., Sikes, R. S. 2007. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 88, 809–82310.1644/06-MAMM-F-185R1.1Search in Google Scholar
Hall T.A. 1999. Bioedit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98Search in Google Scholar
Jones E.K., Clifford C.M., Keirans J.E., Kohls G.M. 1972. The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the Western Hemisphere. Brigham Young University Science Bulletin, Biological Series, 17, 1–40Search in Google Scholar
Kohls G.M., Sonenshine D.E., Clifford C.M. 1965. The systematics of the subfamily Ornithodorinae (Acarina: Argasidae). II. Identification of the larvae of the Western Hemisphere and description of three new species. Annals of the Entomological Society of America, 58, 331–36410.1093/aesa/58.3.331Search in Google Scholar PubMed
Matheson R. 1935. Three new species of ticks, Ornithodoros (Acarina: Ixodoidea). Journal of Parasitology, 21, 347–353. 10.2307/4583666Search in Google Scholar
Norris D.E., Klompen J.S.H., Keirans J.E., Black W.C. 4th. 1996. Population genetics of Ixodes scapularis (Acari: Ixodidae) based on mitochondrial 16S and 12S genes. Journal of Medical Entomology, 33, 78–89. 10.1093/jmedent/33.1.78Search in Google Scholar PubMed
Pence D.B., Knoxjones J., Knipping P.A. 1981. Acari of Antillean bats (Chiroptera). Journal of Medical Entomology, 18, 353– 354. 10.1093/jmedent/18.4.353Search in Google Scholar
STATSOFT, INC. 2009. Statistica V.8. Tulsa, Oklahoma, USASearch in 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. Molecular Biology and Evolution. 10.1093/molbev/msr121Search in Google Scholar
Thompson J.D., Higgins D., Gibson T.J. 1994. CLUSTAL W: improving the sensivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680. 10.1093/nar/22.22.4673Search in Google Scholar
Trout R.T., Steelman C.D., Szalanski A.L. 2009. Population genetics and phylogeography of Ixodes scapularis from canine and deer in Arkansas. Southwestern Entomologist, 34, 273–287. 10.3958/059.034.0308Search in Google Scholar
Venzal J.M., Nava S., Terassini F.A., Ogrzewalska M., Camargo L.M.A., Labruna M.B. 2013. Ornithodoros peropteryx (Acari: Argasidae) in Bolivia: an argasid tick with a single nymphal stage. Experimental and Applied Acarology, 61, 231–241. 10.1007/s10493-013-9689-3Search in Google Scholar
Villegas-Guzman G.A., López-González C., Vargas M. 2005. Ectoparasites associated to two species of Corynorhinus (Chiroptera: Vespertilionidae) from Guanaceví Mining Region, Durango, Mexico. Journal of Medical Entomology, 42, 125– 127. 10.1603/0022-2585(2005)042[0125:EATTSO]2.0.CO;2Search in Google Scholar
Wackerly D., Mendenhall W., Scheaffer R.L. 2014. Mathematical Statistics with Applications. Cengage Learning, Boston, pp. 944Search in Google Scholar
© 2017 W. Stefański Institute of Parasitology, PAS
Articles in the same Issue
- Review
- Pseudopecoelus mccauleyi n. sp. and Podocotyle sp. (Digenea: Opecoelidae) from the deep waters off Oregon and British Columbia with an updated key to the species of Pseudopecoelus von Wicklen, 1946 and checklist of parasites from Lycodes cortezianus (Perciformes: Zoarcidae)
- New record of Steinernema arenarium (Artyukhovsky) (Rhabditida: Steinernematidae) from Ukraine and a note on its distribution
- Isolation and molecular characterization of a Naegleria strain from a recreational water fountain in Tenerife, Canary Islands, Spain
- PCR denaturing gradient gel electrophoresis as a useful method to identify of intestinal bacteria flora in Haemaphysalis flava ticks
- Three new species of Pharygodonidae (Nematoda: Oxyuridea) in Laudakia tuberculata (Squamata: Agamidae) from Dehradun, Uttarakhand, India
- Amoebicidal activity of α-bisabolol, the main sesquiterpene in chamomile (Matricaria recutita L.) essential oil against the trophozoite stage of Acanthamoeba castellani Neff
- A new species of Oochoristica (Cyclophyllidea: Linstowiidae) from non-native Mediterranean geckos, Hemidactylus turcicus (Sauria: Gekkonidae), from Texas, USA
- The ruby-crowned tanager Tachyphonus coronatus Vieillot, 1822 (Passeriformes: Thraupidae) as a new host for Isospora ramphoceli Berto, Flausino, Luz, Ferreira, Lopes, 2010 in Brazil
- Ecological implications of floods on the parasite communities of two freshwater catfishes in a Neotropical floodplain
- Morphological re-description of Electrotaenia malapteruri (Cestoda: Proteocephalidae) and Dujardinnascarismalapteruri (Nematoda: Heterocheilidae) infecting the Electric catfish Malapterurus electricus and heavy metal accumulation in host and parasites in relation to water and sediment analysis in Lake Manzala, North Delta, Egypt
- Disruption of egg production by triclabendazole-resistant Fasciola hepatica following treatment with a commercial preparation of myrrh (Mirazid)
- How does host ecology influence sampling effort in parasite diversity estimates? A case study using Neotropical freshwater fishes
- cDNA library construction of two human Demodexspecies
- Helminth (Cestoda, Nematoda) and coccidian (Apicomplexa: Eimeriidae) parasites of the eastern small-footed myotis, Myotis leibii (Chiroptera: Vespertilionidae) from Arkansas, with a description of a new species of Eimeria
- Molecular identification of Thelandros scleratus and Thelastoma icemi (Nematoda: Oxyruida) using mitochondrial cox 1 sequences
- First report on molecular evidence of Tylodelphys cerebralis (Diplostomulum cerebralis) Chakrabarti, 1968 (Digenea: Diplostomidae) from snakehead fish Channa punctata
- The role of domestic dogs in the transmission of zoonotic helminthes in a rural area of Mekong river basin
- The discovery of acanthocephalans parasitizing chaetognaths
- Redescription of Philometra margolisiMoravec, Vidal-Martínez et Aguirre-Macedo, 1995 (Nematoda: Philometridae), a gonad-infecting parasite of the red grouper Epinephelus morio (Serranidae) in the Gulf of Mexico
- Nematode parasites of the Chilean Flamingo, Phoenicopterus chilensis (Phoenicopteridae) from Central Argentina, with a description of a new species of Tetrameres (Tetrameridae)
- Molecular evidence and additional morphological characters to distinguish Ornithodoros brodyi and Ornithodoros yumatensis (Ixodida: Argasidae) in their different developmental stages
- Morphological description of Cosmocerca sp. (Nematoda: Cosmocerdidae) from the Mascarene grass frog Ptychadena cf. mascareniensis (Amphibia: Ptychadenidae). A light and scanning electron microscopic studies
- Detection of Echinococcus multilocularis DNA in fruit, vegetable, and mushroom samples collected in the non-endemic territory of the Pomerania province and comparison of the results with data from rural areas of the neighbouring highly endemic Warmia-Masuria province, Poland
- Toxoplasma gondii in backyard pigs: seroepidemiology and mouse bioassay
- Infection of the lesser spotted dogfish with Proleptus obtusus Dujardin, 1845 (Nematoda: Spirurida) reflects ontogenetic feeding behaviour and seasonal differences in prey availability
- A new species of the quill mite genus ChenophilaKethley, 1970 (Acariformes: Syringophilidae) from the Marbled Teal Marmaronetta angustirostris (Menetries) (Anseriformes: Anatidae) in Turkey
- Neuropathological lesions of clinical and sub clinical Coenurosis (Coenurus cerebralis) in organized goat farms in India
- Case Report
- Fatal aelurostrongylosis in a kitten in Serbia
Articles in the same Issue
- Review
- Pseudopecoelus mccauleyi n. sp. and Podocotyle sp. (Digenea: Opecoelidae) from the deep waters off Oregon and British Columbia with an updated key to the species of Pseudopecoelus von Wicklen, 1946 and checklist of parasites from Lycodes cortezianus (Perciformes: Zoarcidae)
- New record of Steinernema arenarium (Artyukhovsky) (Rhabditida: Steinernematidae) from Ukraine and a note on its distribution
- Isolation and molecular characterization of a Naegleria strain from a recreational water fountain in Tenerife, Canary Islands, Spain
- PCR denaturing gradient gel electrophoresis as a useful method to identify of intestinal bacteria flora in Haemaphysalis flava ticks
- Three new species of Pharygodonidae (Nematoda: Oxyuridea) in Laudakia tuberculata (Squamata: Agamidae) from Dehradun, Uttarakhand, India
- Amoebicidal activity of α-bisabolol, the main sesquiterpene in chamomile (Matricaria recutita L.) essential oil against the trophozoite stage of Acanthamoeba castellani Neff
- A new species of Oochoristica (Cyclophyllidea: Linstowiidae) from non-native Mediterranean geckos, Hemidactylus turcicus (Sauria: Gekkonidae), from Texas, USA
- The ruby-crowned tanager Tachyphonus coronatus Vieillot, 1822 (Passeriformes: Thraupidae) as a new host for Isospora ramphoceli Berto, Flausino, Luz, Ferreira, Lopes, 2010 in Brazil
- Ecological implications of floods on the parasite communities of two freshwater catfishes in a Neotropical floodplain
- Morphological re-description of Electrotaenia malapteruri (Cestoda: Proteocephalidae) and Dujardinnascarismalapteruri (Nematoda: Heterocheilidae) infecting the Electric catfish Malapterurus electricus and heavy metal accumulation in host and parasites in relation to water and sediment analysis in Lake Manzala, North Delta, Egypt
- Disruption of egg production by triclabendazole-resistant Fasciola hepatica following treatment with a commercial preparation of myrrh (Mirazid)
- How does host ecology influence sampling effort in parasite diversity estimates? A case study using Neotropical freshwater fishes
- cDNA library construction of two human Demodexspecies
- Helminth (Cestoda, Nematoda) and coccidian (Apicomplexa: Eimeriidae) parasites of the eastern small-footed myotis, Myotis leibii (Chiroptera: Vespertilionidae) from Arkansas, with a description of a new species of Eimeria
- Molecular identification of Thelandros scleratus and Thelastoma icemi (Nematoda: Oxyruida) using mitochondrial cox 1 sequences
- First report on molecular evidence of Tylodelphys cerebralis (Diplostomulum cerebralis) Chakrabarti, 1968 (Digenea: Diplostomidae) from snakehead fish Channa punctata
- The role of domestic dogs in the transmission of zoonotic helminthes in a rural area of Mekong river basin
- The discovery of acanthocephalans parasitizing chaetognaths
- Redescription of Philometra margolisiMoravec, Vidal-Martínez et Aguirre-Macedo, 1995 (Nematoda: Philometridae), a gonad-infecting parasite of the red grouper Epinephelus morio (Serranidae) in the Gulf of Mexico
- Nematode parasites of the Chilean Flamingo, Phoenicopterus chilensis (Phoenicopteridae) from Central Argentina, with a description of a new species of Tetrameres (Tetrameridae)
- Molecular evidence and additional morphological characters to distinguish Ornithodoros brodyi and Ornithodoros yumatensis (Ixodida: Argasidae) in their different developmental stages
- Morphological description of Cosmocerca sp. (Nematoda: Cosmocerdidae) from the Mascarene grass frog Ptychadena cf. mascareniensis (Amphibia: Ptychadenidae). A light and scanning electron microscopic studies
- Detection of Echinococcus multilocularis DNA in fruit, vegetable, and mushroom samples collected in the non-endemic territory of the Pomerania province and comparison of the results with data from rural areas of the neighbouring highly endemic Warmia-Masuria province, Poland
- Toxoplasma gondii in backyard pigs: seroepidemiology and mouse bioassay
- Infection of the lesser spotted dogfish with Proleptus obtusus Dujardin, 1845 (Nematoda: Spirurida) reflects ontogenetic feeding behaviour and seasonal differences in prey availability
- A new species of the quill mite genus ChenophilaKethley, 1970 (Acariformes: Syringophilidae) from the Marbled Teal Marmaronetta angustirostris (Menetries) (Anseriformes: Anatidae) in Turkey
- Neuropathological lesions of clinical and sub clinical Coenurosis (Coenurus cerebralis) in organized goat farms in India
- Case Report
- Fatal aelurostrongylosis in a kitten in Serbia