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Comparative Analysis of Germ Cells and DNA of the Genus Amblyomma: Adding New Data on Amblyomma Maculatum and Amblyomma Ovale Species (Acari: Ixodidae)

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Comparative Analysis of Germ Cells and DNA of the Genus Amblyomma: Adding New Data on Amblyomma Maculatum and Amblyomma Ovale Species (Acari: Ixodidae) Parasitol Res (2017) 116:2883–2892 DOI 10.1007/s00436-017-5592-x ORIGINAL PAPER Comparative analysis of germ cells and DNA of the genus Amblyomma: adding new data on Amblyomma maculatum and Amblyomma ovale species (Acari: Ixodidae) Fredy Arvey Rivera-Páez1,2 & Bruno Rodrigues Sampieri3 & Marcelo Bahia Labruna4 & Renata da Silva Matos1 & Thiago Fernandes Martins4 & Maria Izabel Camargo-Mathias1 Received: 9 May 2017 /Accepted: 10 August 2017 /Published online: 18 August 2017 # Springer-Verlag GmbH Germany 2017 Abstract Among tick species, members of the subfamily (mitochondrial) molecular markers were used to study the genet- Amblyomminae have received special attention, since they serve ic relationships of the species. The results show that the tick male as vectors for pathogens such as Rickettsia spp. and display reproductive system and its germ cells contain useful candidate cryptic species complexes that make their taxonomical classifi- characters for taxonomical analyses of Ixodida. cation challenging. Amblyomma ovale, Amblyomma maculatum, and other species of the genus Amblyomma have shown a long Keywords Cryptic species . Spermiotaxonomy . Ticks . history of taxonomic controversies. Spermiotaxonomy has Histology . Molecular markers proved to be a valuable tool in the solution of systematic con- flicts in Metazoa that can aid molecular and external morpholog- ical analyses in ticks and, overall, provide more robust analyses Introduction and results. With this in mind, this study included histological analyses of the reproductive system of the species A. ovale and Tick (Ixodidae) systematics has been discussed for decades, A. maculatum, as well as the description of morphohistological and periodically, the phylogeny of several groups is revisited characters of the male reproductive system of ticks of the genus through new analytical tools. Among the most known tick Amblyomma, in order to evaluate these characters within the subfamilies, Amblyomminae has received special attention, current clustering proposals. In addition, 16S rDNA and COI since it harbors cryptic species that, until recently, were con- sidered polymorphic by authors that followed the analyses of Hoogstraal and Aeschlimann (1982). Some important revi- The original version of this article was revised: The data in Table 3 were sions have been made using molecular and biogeographical misaligned. Correct table alignment is presented here. phylogeny techniques such as those developed by Black and * Maria Izabel Camargo-Mathias Piesman (1994), Burger et al. (2012), Beati et al. (2013), and [email protected] Nava et al. (2014), which confirmed the polyphyletic origin of the subfamily, its current distribution in the American conti- 1 Departamento de Biologia, Instituto de Biociências, UNESP - nent, and the real taxonomic status of some species of medical Universidade Estadual Paulista, Avenida 24-A, 1515, Bairro Bela and veterinarian importance, such as the Amblyomma Vista, Rio Claro, SP CEP13506-900, Brazil cajennense sensu lato complex. 2 Grupo de Investigación GEBIOME, Departamento de Ciencias The Amblyomma maculatum group includes the following Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad de species: A. maculatum (Koch, 1844); Amblyomma neumanni Caldas, Calle 65 No. 26-10 Apartado Aéreo 275 Manizales, Caldas, Colombia (Ribaga, 1902); Amblyomma parvitarsum (Neumann, 1901); Amblyomma tigrinum (Koch, 1844); and Amblyomma triste 3 Universidade Estadual de Campinas, Museu de Zoologia, R. Charles Darwin s/n, cidade universitária, Campinas, SP, Brazil (Koch, 1844) (Camicas et al. 1998). Camicas et al. (1998) clustered them within the Amblyomma ovale group that in- 4 Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São cludes A. ovale and Amblyomma aureolatum, in the revisited Paulo-USP, Av. Prof. Orlando Marques de Paiva, 87, CEP version of the subgenus Anastosiella, originally proposed by 05508-000, Cidade Universitária, São Paulo, SP, Brazil Santos Dias (1963). 2884 Parasitol Res (2017) 116:2883–2892 The taxa A. maculatum, A. triste, and A. tigrinum were Ibagué (04° 23′ 50″ N, 75° 8′ 12″ W) in the department of described as valid species by Koch (1844), based on adult Tolima, Andean region of Colombia. The ticks were taxonom- specimens from the USA, Uruguay, and Brazil, respectively. ically identified based on their external morphology, using a However, Neumann (1899) considered that these three taxa light microscope (Leica M205C stereomicroscope), following belonged to a single species, namely A. maculatum, which Aragão and da Fonseca (1961), Jones et al. (1972), and was adopted by subsequent authors, until the study of Kohls Estrada-Peña et al. (2005). In addition, specimens from each (1956), who revalidated the three species based on morpho- species were prepared for scanning electron microscopy logical characters. Since then, although considered to be sep- (SEM) (Hitachi Scanning Electron Microscope model arate species, the identification of these tick species has been TM3000), according to the techniques described by Corwin controversial, in particular the distinction between et al. (1979). A. maculatum and A. triste (Estrada-Peña et al. 2005; Following the morphological identification, a molecular Guglielmone et al. 2013; Lado 2015; Mendoza Uribe and assessment was performed for the species A. ovale and Chavez Chorocco 2004; Mertins et al. 2010). Lado (2015), A. maculatum, as well as for the species analyzed in terms of based on different mitochondrial and nuclear molecular their reproductive system by Sampieri et al. (2014, 2016a, b), markers, suggests that A. triste should be synonymized with being these: A. aureolatum, A. triste,andAmblyomma A. maculatum. sculptum (Berlese, 1888) (Ixodidae, Amblyomminae). The On the other hand, Amblyomma aureolatum (Pallas, 1772) species Rhipicephalus sanguineus s.l. (tropical linage) and and Amblyomma ovale (Koch, 1844) have been described as Ornithodoros rostratus (Aragão, 1911) were used as the Bovale^ complex by Aragão and da Fonseca (1961). These outgroups I and II, respectively. In the same way, the repro- authors redescribed the male and female of both tick species, ductive system of A. ovale and A. maculatum (Colombia) discussed the systematics, and convincingly supported the use were processed and analyzed by histological techniques as of the name A. aureolatum and A. ovale (Guglielmone et al. described in Sampieri et al. (2016a, b). 2003). Specimens of each species, A. aureolatum, A. triste, Against this backdrop, this study aimed to reanalyze the A. sculptum, A. ovale, A. maculatum,andRhipicephalus systematics and phylogenetic positions of representatives of sanguineus s.l., were individually processed for the molecular Amblyominnae subfamily, including the species A. ovale and analyses. For this purpose, DNA was extracted using the A. maculatum collected in Colombia, adding new data related DNeasy Blood and Tissue Kit (Qiagen), following the manu- to their reproductive system and germ cell morphology given facturer’s protocol, and tested by two PCR protocols, one the association of this species with epidemiological issues and targeting the mitochondrial cytochrome c oxidase subunit I public health in North and South America (Ferrari et al. 2012; (COI) gene and the other the 16S rDNA gene. For the COI Guglielmone et al. 2003;Ladoetal.2015;Navaetal.2008). gene PCR, we used primers LCO1490 (F) 5-GGTCAACA Furthermore, this study compiled the results obtained until AATCATAAAGATATTGG-3 and HCO2198 (R) 5- now, based on the descriptions by Sampieri et al. (2014, TAAACTTCAGGGTGACCAAAAAATCA-3 (Folmer et al. 2016a, b), on the anatomy and morphology of the male tick 1994). For the 16S rDNA gene, we used primers F 5′-CTGC reproductive system, mainly the genus Amblyomma with oc- TCAATGATTTTTTAAATTGCTGTGG-3′ and R 5′-CCGG currence in Brazil and Colombia. TCTGAACTCAGATCAAGT-3′ (Norris et al. 1996). In addi- A list of useful characters in taxonomic analyses was ob- tion to the Amblyomma species used for the morphological tained from the results generated in these studies adding the studies, the species A. cajennense s.s. (Brazil) and A. mixtum new data obtained here which were contrasted with the mo- (Colombia) were also amplified, as representatives of the lecular data generated from the analysis of the mtDNA COI Bcajennense^ complex. and 16S rDNA gene sequences, in order to confirm if the male The PCR products were visualized on horizontal 1% aga- reproductive system and its germ cells are a source of candi- rose gels with 1X TBE pH 8.0 running buffer at 110 V/50 mA, date characters for tick systematics. stained with SYBR Safe® dye and photo-documented on a GelDoc-It®2310 Imager (UVP). The PCR products were pu- rified with the QIAquick PCR Purification Kit (Qiagen®), Materials and methods according to the manufacturer’s instructions, and sent to Macrogen Inc. (South Korea) for DNA sequencing. The se- Study species and molecular evaluation quenced fragments were analyzed and edited using Geneious Trial v8.14 (Drummond et al. 2009) and Sequencher 4.1 During the months of August 2014, January and August 2015, (Gene Codes Corporation, Ann Arbor, Michigan, USA). In and May 2016, ticks of the species A. ovale and A. maculatum addition, the sequences were searched by MegaBlast against were directly collected from dogs (Canis familiaris) in the the public databases and deposited in Genbank and Barcode of municipalities of Saldaña
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