Haliotrematoides spp. (Monogenoidea: Dactylogyridae) parasitizing Lutjanus guttatus (Lutjanidae) in two localities of the Pacific coast of Mexico, and their phylogenetic position within the Ancyrocephalinae through sequences of the 28S rRNA

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C., Km 2.5 Antigua carretera a Coatepec, 91070 Xalapa, Veracruz, Mexico" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Centro de Investigación en Alimentos y Desarrollo en Acuicultura y Manejo Ambiental, A. C., Unidad Mazatlán, Estero del Yugo s/n, 82000 Mazatlán, Sinaloa, Mexico" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Haliotrematoides spp. (Monogenoidea: Dactylogiridae) parasitando Lutjanus guttatus (Lutjanidae) en dos localidades de la costa pacífica de México y su posición filogenética dentro de Ancyrocephalinae a través de secuencias del 28S rRNA" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figures 12–15" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr12v15.jpeg" "Alto" => 801 "Ancho" => 1636 "Tamanyo" => 107911 ] ] "descripcion" => array:1 [ "en" => "Drawings of Haliotrematoides spinatus from Lutjanus guttatus found in Chamela Bay, Jalisco and Mazatlán, Sinaloa, Mexico. 12, dorsal anchor; 13, ventral anchor; 14, dorsal bar; 15, ventral bar. All measurements are in micrometers." ] ] ] "textoCompleto" => "IntroductionThe genus Lutjanus (Steindacher) (Lutjanidae), the most species-rich among the family Lutjanidae, contains 68 species distributed around the world (<a class="elsevierStyleCrossRef" href="#bib0015">Froese & Pauly, 2014</a>). These fish are commercially important for fisheries, and at least 20 species have been examined for monogeneans, since it is well-known the impact that these parasites may have on fish populations. Species of 4 genera of dactylogyrids have been found on the gills of snappers around the world, Euryhaliotrema<a class="elsevierStyleCrossRef" href="#bib0060">Kritsky and Boeger, 2002</a>, Haliotrema Johnston and Tiegs, 1922, Haliotrematoides<a class="elsevierStyleCrossRef" href="#bib0065">Kritsky, Tingbao & Yuan, 2009</a> and Tetrancistrum Goto and Kikuchi, 1917; 2 other genera, Euryhaliotrematoides Plaisance and Kritsky, 2004, and Aliatrema Plaisance and Kritsky, 2004 were recently considered as synonyms of Euryhaliotrema based on the morphology of their male copulatory organ (MCO) (<a class="elsevierStyleCrossRef" href="#bib0050">Kritsky, 2012</a>). In Mexico, 9 dactylogyrid species have been described from snappers, i.e. H. cornigerum (<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov, 1976</a>), H. gracilihamus (<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov, 1976</a>), H. heteracantha (<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov, 1976</a>), H. longihamus (<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov, 1976</a>), H. magnigastrohamus (<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov, 1976</a>), H. overstreeti Kritsky and Bullard in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al. (2009)</a> from Campeche Bay; H. guttati (<a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas, Fajer-Ávila & Lamothe-Argumedo, 2008</a>), E. perezponcei<a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas, Fajer-Ávila & Lamothe-Argumedo, 2008</a> from Mazatlán, Sinaloa and Cruz de Huanacaxtle, Nayarit, and E. mehen (<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jiménez, García-Gasca & Fajer-Ávila, 2012</a>) from Mazatlán, Sinaloa. The taxonomic status of some of these species of dactylogyrids has been unstable due to the lack of morphological details (mostly in haptoral hard parts and copulatory organ) in the original descriptions, although clarification has been gained after further taxonomic work conducted by several authors (e.g., <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al., 2009</a>).Recently, specimens of the spotted rose snapper Lutjanus guttatus (Steindachner) were collected in Chamela Bay, Jalisco and Mazatlán, Sinaloa, both on the Pacific coast of Mexico, as part of the study of the ectoparasites of fishes with commercial importance. From those fishes, specimens of dactylogyrids were collected from the gills. The objectives of this paper were to report the presence of 3 species of Haliotrematoides parasitizing the gills of spotted rose snappers, and to provide additional morphological information for each of them. In addition, we analyze the systematic position of these species (including E. perezponcei and E. mehen from Mazatlán) within the phylogeny of the Ancyrocephalinae, by using sequences of the 28S rRNA in the context of a wider phylogenetic analysis of dactylogyrids.Materials and methodsSpecimens of adult spotted rose snapper Lutjanus guttatus were sampled in 2010 in Mazatlán Bay, Sinaloa (23°18′44″N, 106°29′37″W) and from 2011 through 2012 in Chamela Bay, Jalisco (19°33′15″N, 105°06′45″W), in northwestern Mexico; fish were obtained from local fishermen who set nets in each locality, kept on ice once removed from the nets, and examined for gill parasites a few hours after capture. Gills were extracted, fixed and stored in 96% ethanol; parasites were excised from the host tissue using triangular, surgical, mounted needles (size 16, Barber of Sheffield, U.K.) and were prepared for morphological and molecular evaluation. For morphological comparison, type-specimens deposited at the National Museum of Natural History (NMNH), Smithsonian Institution, Washington, D.C. (formerly U.S. National Parasite Collection – USNPC), USA at the Colección Nacional de Helmintos (CNHE) and at the Colección de Parásitos de Peces del Noroeste de México (CPPNP) were studied as follows: H. guttati (USNPC 101370–101371; CNHE, Neotype 8460), H. plectridium (USNPC 101367–101369), H. spinatus (USNPC 101353–101355; CNHE 6464–6465).Morphological analysisThe haptor of each specimen was removed using a scalpel and air-dried on a glass slide; the corresponding body was transferred to a labeled Eppendorf tube containing 96% ethanol and stored at −20°C until required for molecular evaluation. Air-dried haptors were then subjected to a partial digestion using a proteinase K-base method (<a class="elsevierStyleCrossRef" href="#bib0025">García-Vásquez, Hansen, Cristison, Bron, & Shinn, 2011</a>). Some specimens were mounted (unstained) in Gray and Wess (<a class="elsevierStyleCrossRef" href="#bib0140">Vidal-Martínez, Aguirre-Macedo, Scholz, González-Solis, & Mendoza-Franco, 2001</a>) solution to clear the body tissue and visualize the haptoral hooks and copulatory complex. The haptoral armature and copulatory complex were studied using an immersion oil objective on an Olympus BX40 compound microscope. For comparisons, specimens were measured following <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al. (2009)</a>. When provided, measurements are presented in micrometers with the average followed by the range in parentheses. Specimens were deposited in the Colección Nacional de Helmintos from Mexico (CNHE) and in the U.S. National Parasite Collection (USNPC).DNA extraction and sequencingParasite bodies were digested overnight at 56°C in a solution containing 10mM Tris–HCl (pH 7.6), 20mM NaCl, 100mM Na2 EDTA (pH 8.0), 1% Sakozyl, and 0.1mg/ml proteinase K. Following digestion, DNA was extracted from the supernatant using DNAzol reagent (Molecular Research Center, Cincinnati, Ohio) according to the manufacturer's instructions. Some tissues were extracted using the DNeasy Tissue Kit (Qiagen, Valencia, California). A fragment of the 28S ribosomal gene was amplified using the polymerase chain reaction (PCR). The primers Ancy55F (5′-GAGATTAGCCCATCACCG AAG-3′) (<a class="elsevierStyleCrossRef" href="#bib0095">Plaisance, Littlewood, Olson, & Morand, 2005</a>) and LSU1200R (5′-GCATAGTTCACCATCTTTCGG-3′) (<a class="elsevierStyleCrossRef" href="#bib0075">Littlewood, Curini-Galletti, & Herniou, 2000</a>) were used to amplify (PCR) a LSU fragment; also, the internal primers Halio-F (5′-ACCCGCTGAATTTAAGCAT-3′) and Halio-R (5′-TGGTCCGTGTTTCAAGAC-3′) (<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jiménez et al., 2012</a>). The PCR (25μl) consisted of 2.5μl of 1μl of 10μM of each primer, 2.5μl of 10× buffer, 1.5μl of MgCl2 15mM, 0.5μl dNTP's 10mM, 1U of Taq DNA polymerase (Platinum Taq, Invitrogen Corporation, São Paulo, Brazil), 2μl of DNA template, and 13.675μl of water. The PCR cycling protocol included denaturation at 94°C for 2min, followed by 35 cycles of 94°C for 1min, annealing at 50–58°C depending on dactylogyrid species (E. perezponcei 50°C, E. mehen 55°C, H. guttati and H. spinatus 58°C, and H. plectridium 55°C) for 1min and final extension at 72°C for 1min.The reaction was performed in a MJ Research thermal cycler using a heated lid to reduce refluxing. Sequencing reactions were performed using an ABI Big Dye (Applied Biosystems, Boston, MA) terminator sequencing chemistry, and reaction products were separated and detected using an ABI 310 capillary DNA sequencer. Contigs were assembled and base calling differences resolved using Codoncode Aligner version 3.0.1 (Codoncode Corporation, Dedham, MA). All sequences were deposited in GenBank database.Alignments and phylogenentic analysesSequences obtained in the current study from 28S (D1–D3) were aligned along with other species of Dactylogyridae available in GenBank using Clustal W implemented in Mega 5 (<a class="elsevierStyleCrossRef" href="#bib0135">Tamura, Peterson, Peterson, Stecher, & Kumar, 2011</a>) and adjusted manually with the Mesquite 2.75 program (<a class="elsevierStyleCrossRef" href="#bib0080">Maddison & Maddison, 2011</a>). Maximum likelihood (ML) and Bayesian Inference (BI) analyses were performed (<a class="elsevierStyleCrossRef" href="#bib0040">Huelsenbeck & Ronquist, 2001</a>). The jModelTest software version 0.1.1 (<a class="elsevierStyleCrossRef" href="#bib0100">Posada, 2008</a>) was used to select the best model of evolution for our dataset. The model (GTR+I+G) was selected based on the Akaike information criteria. The ML tree was inferred using RAxML 7.0.4, for each dataset (<a class="elsevierStyleCrossRef" href="#bib0130">Stamatakis, 2006</a>). Maximum likelihood clade support was assessed by bootstrap resampling with 10,000 replicates. Additionally, Bayesian analyses were performed with the program MrBAYES version 3.1.2 (<a class="elsevierStyleCrossRef" href="#bib0040">Huelsenbeck & Ronquist, 2001</a>). The settings were 2 simultaneous runs with 4 Markov chains and 5 million MCMC generations, sampling every 200 generations, a heating parameter value of 0.2 and a ‘burnin’ of 10%. Numbers at the interior branches of the consensus tree represent posterior probabilities (PP). Trees were drawn using FigTree program version 1.3.1 (<a class="elsevierStyleCrossRef" href="#bib0105">Rambaut, 2006</a>). The genetic divergence among species (E. perezponcei, E. mehen, H. plectridium, H. guttati and H. spinatus) was estimated using uncorrected “p-distances” method with the program MEGA v. 5 (<a class="elsevierStyleCrossRef" href="#bib0135">Tamura et al., 2011</a>).ResultsThree species of Haliotrematoides were found parasitizing the gills of L. guttatus in Mazatlán, Sinaloa and Chamela Bay, Jalisco (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). The specimens collected in the present study were compared morphologically with type and voucher specimens, mainly in terms of haptoral hooks and male copulatory organ (MCO). The following species were found:<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Dactylogyridae Bychowsky, 1933Haliotrematoides<a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al., 2009</a>Haliotrematoides guttati (<a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas et al., 2008</a>)Taxonomic summarySite: gills.Type host and locality: Lutjanus guttatus (Steindachner), Pacific Coast off Mazatlán, Sinaloa, Mexico (23°29′N, 106°36′W).Host and localities: Chamela Bay, Jalisco, Mexico (19°31′49″N, 105°04′55″W). Mazatlán, Sinaloa (23°13′10″N, 106°26′05″W).Previous records: Cruz de Huanacaxtle, Nayarit, Mexico (20°44′N, 105°22′W); Taboga Island, Panama (8°49′N, 79°34′W); Perlas Archipielago, Panama (8°22′N, 79°01′W).Specimens deposited: CPPNP 7293, 5 vouchers (from the type locality), 4 vouchers CNHE 8354 and 1 voucher USNPC 106930 (from Chamela).DNA reference sequence: the 856bp ribosomal DNA sequence of the LSU (D1-D3) is deposited in GenBank under accession numbers <a href="ncbi-n:HQ615993">HQ615993</a> (from Mazatlán) and <a href="ncbi-n:KC663673">KC663673</a>–KC663674 (from Chamela Bay).RemarksFive specimens of this species were found in Chamela bay, Jalisco and 10 were found in Mazatlán, Sinaloa, Mexico, corresponding with the genus description provided by Kritsky and Mendoza-Franco (<a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al., 2009</a>). This species was originally described as H. guttati as a parasite of L. guttatus from Mazatlán by <a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas et al. (2008)</a>. In 2009, Kritsky et al. found 2 specimens from the gills of snappers in Panama, and based on the comparison of their specimens with the original description, and their examination of the paratype and 2 voucher specimens (Harold W. Manter Laboratory, University of Nebraska-Lincoln, HWML, 48570, 48571) transferred the species to the genus Haliotrematoides. Following <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al. (2009)</a> recommendation for the need of a re-description of this species, we studied in further detail our specimens and those deposited in museum collections (neotype, CNHE, and vouchers from the USNPC from Panama), and herein we provide the following details of some morphological traits: dorsal anchor with a well-developed membrane 12 (11–15) long, showing some striations on the surface of the curvature to the point; in the mid portion of perforation on the anchors base, a small heel is observed (not observed in specimens from Panama), a long inner root, no developed outer root (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Ventral anchor with both roots well developed, inner root 14 (12–16.5) long and ending pointed, longer than the outer root which is 6.5 (6–8) long and rounded (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 2</a>). Dorsal bar delicate, round in the middle, with a small knob, square ends where anchor attaches (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 3</a>). V-shaped ventral bar 41 (38.5–44) wide, but in description made by <a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas et al. (2008)</a> is described as “W-shaped”, this was not observed in the type specimens that were studied (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 4</a>). Hooks with terminal depressed thumb directed to point, point opened and beyond thumb (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 5</a>). MCO tubular-shaped forming a spiral, conical base with the anterior part narrower than the base, and bearing a long whip heading to the anterior part of the body (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 6</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>Chamela Bay represents a new geographical record for this species.Haliotrematoides plectridium Kritsky & Mendoza-Franco, 2009Taxonomic summarySite: gills.Type host and locality: Lutjanus guttatus (Steindachner), off Taboga Island, Panama (8°49′N, 79°34′W).Host and localities: Lutjanus guttatus (Steinadachner), Chamela Bay, Jalisco, Mexico (19°31′49″N, 105°04′55″W), and Mazatlán, Sinaloa, Mexico (23°13′10″N, 106°26′05″W).Previous records: Perlas Archipielago, Panama (8°22′N, 79°01′W).Specimens deposited: CNHE 7292, 2 vouchers (from Mazatlán); CNHE 8353, 4 vouchers (from Chamela Bay).DNA reference sequence: the 856bp ribosomal DNA sequence of the LSU (D1–D3) is deposited in GenBank under accession number <a href="ncbi-n:HQ615994">HQ615994</a>, <a href="ncbi-n:KC713622">KC713622</a> (from Mazatlán). No sequences were obtained from Chamela Bay, Mexico (10 specimens were prepared for molecular analysis but fail to amplify).RemarksA total of 10 specimens were found in Mazatlán, Sinaloa and 19 in Chamela Bay, Jalisco. Our specimens are in agreement with the original description of Kritsky and Mendoza-Franco (2009) in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al. (2009)</a> from Taboga Island, and from Perlas Archipelago, both in Panama. Records from Mazatlán and Chamela represent new geographical records for this species. We observed in our specimens the following taxonomic traits, some of them slightly different from specimens from Panama: a membrane-like structure in the inner root of dorsal anchor, 8 (6–12.5) long, no outer root developed (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 7</a>). Ventral anchor with a depressed inner root, with the inner root longer than the outer root, 11 (8–17) long (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 8</a>). Dorsal bar 41 (36.5–46) wide, thin and concave while in the Panama specimens the bar is smaller, 35 (31–37) wide (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 9</a>). Ventral bar concave, 43 (40–47) wide, with 2 subterminal pockets in the anterior margin (convex in specimens from Panama) (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 10</a>). The MCO possess a filament at the end, finishing bulged in our specimens (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 11</a>), while this structure was not observed in Panama specimens.<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Haliotrematoides spinatus Kritsky & Mendoza-Franco, 2009Taxonomic summarySite: gills.Type host and locality: Lutjanus guttatus (Steindachner), off Taboga Island, Panama (8°49′N, 79°34′W)Host and localities: Chamela Bay, Jalisco, Mexico (19°31′49”N, 105°04′55”W), and Mazatlán, Sinaloa, México (23°29′N, 106°36′W).Previous records: Perlas Archipielago, Panama (8°22′N, 79°01′W).Specimens deposited: CNHE 7291 and CNHE 7546, 4 vouchers (from Mazatlán) and CNHE 8355, 4 vouchers, 2 vouchers USNPC 106934–106935 (from Chamela Bay).DNA reference sequence: the 856bp ribosomal DNA sequence of the LSU (D1–D3) is deposited in GenBank under accession numbers <a href="ncbi-n:HQ615995">HQ615995</a>, KC713623–KC713627 (from Mazatlán) and KC663675–KC663678 (from Chamela Bay).RemarksA total of 10 worms of this species were found in Mazatlán, Sinaloa and 11 from Chamela Bay, Jalisco. The specimens collected in the present study, conform to the description provided by Kritsky and Mendoza-Franco (2009) in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al. (2009)</a>. The finding of this species in L. guttatus from Mazatlán and Chamela represent new geographical records. Our specimens show a delicate and short membrane in the outer root of the dorsal anchor, possessing a straight and relatively long point 24 (23–26) long, and a straight shaft (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 12</a>), meanwhile in the specimens from Panama the point is 21 long, and shaft is slightly curved, but differences might be due to intraspecific morphological variation. Ventral anchor with inner root small in our specimens, while in those from Panama the inner root is larger (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 13</a>). Dorsal bar slightly curved with short spine-like projections, anteriorly directed on each end, while specimens from Panama have 2 angled base dorsal bar (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 14</a>). The specimens of the present study possess a straight ventral bar, with 2 submedial pockets along the anterior margin and subterminal anterior notches (dorsal view), with a triangular ridge at the mid-portion of the anterior margin (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 15</a>), however in specimens from Panama this was not apparent.<elsevierMultimedia ident="fig0015"></elsevierMultimedia>Systematic position and genetic divergence of Haliotrematoides spp.A total of 16 sequences were generated for the 3 species of Haliotrematoides recorded in this study: H. guttati (3 specimens), H. plectridium (2 specimens) and H. spinatus (11 specimens); additionally, 13 specimens of other 2 species of dactylogyrids were also sequenced: E. mehen (5), and E. perezponcei (8). The phylogenetic tree inferred from maximum likelihood analysis is shown in <a class="elsevierStyleCrossRef" href="#fig0020">Fig. 16</a>. The maximum likelihood tree (−ln likelihood=32,275.20) is presented, as the topology obtained from ML analysis was similar to the consensus tree of the Bayesian analysis. Likewise, the values of posterior probabilities are presented in the ML tree for comparison. The intra and interspecific genetic divergence (uncorrected P-distances) of species collected from snappers in Chamela Bay and Mazatlán is shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>. Euryhaliotrema and Haliotrematoides are not sister groups, and genetic divergence between genera varied from 20.5 to 24.2. The 3 species of Haliotrematoides differ in a range that varied from 4.8% between H. guttati and H. spinatus, and 17.3% between H. plectridium and H. spinatus. Intraspecific variation is very low, with the exception of that found among isolates of H. guttati (6%) and H. spinatus (8%). This intraspecific variation and the tree topology may indicate that these 2 species could represent a species complex. In the first case, the 3 isolates of H. guttati are not monophyletic, although this relationship is supported by low bootstrap and posterior probability values. Instead, the isolates of H. spinatus conform a monophyletic clade, although 2 subclades are formed, each with high support values (99/1) (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 16</a>). Even though this could represent a case for the existence of cryptic species, since morphological characters distinguishing those groups are not observed, the inclusion of other molecular markers and a larger sample size is necessary to test the hypothesis of a species complex.<elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia>Species of the genus Haliotrematoides herein studied are nested within the Ancyrocephalinae sensu lato (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 16</a>). Sequences of 2 species of Haliotrema described as parasites of Sciaenops ocellatus L. (Sciaenidae) in China (one of them H. schenzhenensis, Wang, Lui, & Zhou, 2003), are nested as the sister group of H. plectridium, a relationship highly supported by bootstrap and posterior probability values. We were unable to confirm the taxonomic determination of that species since we had no access to museum specimens. This is what the DNA sequence data suggest, however this need to be taken with caution, because it is possible that the species from China may actually belong to the genus Haliotrematoides, but this needs to be determined when type-specimens are studied.DiscussionIn this study new geographical records of 3 species of Haliotrematoides are presented, and a few details of the morphology of these species are given to complete their taxonomic description. In addition, the specimens collected were sequenced and new data was generated for the 28S rRNA gene, establishing sister-group relationships of the genus within the Ancyrocephalinae sensu lato. Genetic divergence values indicate that the species H. guttati and H. spinatus potentially represent a species complex. Unfortunately, we found no characters that allowed us to distinguish the specimens on morphological grounds. However, since we used in this study only 1 molecular marker, we took a conservative position and we decided to only recognize the potential existence of 2 cryptic species. These results need to be further corroborated by using at least another molecular marker such as cox1, which is more variable and may be more precise in identifying genetic lineages corresponding with separate species, and also it has been proven to be useful in achieving comprehensive species descriptions that facilitate reliable species diagnostics and rapid assessment of biodiversity, as in the case of species in the genus Gyrodactylus von Nordmann, 1832 (<a class="elsevierStyleCrossRef" href="#bib0035">Hansen, Bakke, & Bachmann, 2007</a>).A single molecular marker has been used in previous studies on monogenoids when characterizing new species or describing genetic divergence; some studies used either a ribosomal marker (such as internal transcribed spacers) (<a class="elsevierStyleCrossRef" href="#bib0045">Huyse & Volckaert, 2002</a>), or a mitochondrial gene such as cox1 (<a class="elsevierStyleCrossRef" href="#bib0030">Hansen, Bachmann, & Bakke, 2003</a>). However, when the potential presence of cryptic species is recognized (<a class="elsevierStyleCrossRefs" href="#bib0085">Nadler & Pérez-Ponce de León, 2011; Pérez-Ponce de León & Nadler, 2010</a>), the use of several molecular markers in the context of a phylogenetic analysis, and the proper characterization of genetic divergence is highly recommended. This approach has been followed in some species of monogenoids by authors such as <a class="elsevierStyleCrossRef" href="#bib0150">Ziętara and Lumme (2003)</a> and <a class="elsevierStyleCrossRef" href="#bib0070">Kuusela, Ziętara, and Lumme (2008)</a>.The partial fragment of the 28S rRNA (D1-D3) gene has been widely used to investigate the phylogenetic relationships among some dactylogyrids (<a class="elsevierStyleCrossRefs" href="#bib0005">Blasco-Costa, Miguez-Lozano, Sarabeev, & Balbuena, 2012; Dang, Levsen, Shander, & Bristow, 2010; Plaisance et al., 2005; Šimková, Mat¿jusová, & Cunningham, 2006; Singh & Chaudhary, 2010, 2011</a>). Our results support the classification scheme proposed by <a class="elsevierStyleCrossRef" href="#bib0055">Kritsky and Boeger (1989)</a>, who described the polyphyletic and paraphyletic nature of this group of monogenoids. In our study, Ancyrocephalinae was also not recovered as a monophyletic group.As an additional result of our research, sequences of specimens of other ancyrocephalid monogeneans infecting the spotted rose snapper were obtained, particularly specimens of E. perezponcei that were collected from the gills of L. guttatus, a species previously described by <a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas et al. (2008)</a>, as well as specimens of E. mehen, a species described by <a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jiménez et al. (2012)</a>, both from Mazatlán. The taxonomic status of the genus Euryhaliotema has been also unstable. The genus was proposed by <a class="elsevierStyleCrossRef" href="#bib0060">Kritsky and Boeger (2002)</a> and, in a recent review of the genus by <a class="elsevierStyleCrossRef" href="#bib0050">Kritsky (2012)</a>, the author discovered that some specimens collected from snappers possessed a mixture of morphological features, and decided to include the species of Euryhaliotrematoides within the genus Euryhaliotrema. The species described by <a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jiménez et al. (2012)</a> as Euryhaliotrematoides mehen infecting L. guttatus from Mazatlán was then transferred to Euryhaliotrema by <a class="elsevierStyleCrossRef" href="#bib0050">Kritsky (2012)</a>. The molecular results we obtained herein confirm the proposal by <a class="elsevierStyleCrossRef" href="#bib0050">Kritsky (2012)</a> since E. perezponcei nests as the sister species of E. mehen. The presence of E. perezponcei as a parasite of L. guttatus in Chamela represents a new geographical record, and the fact that sequences of individuals of this species from Mazatlán and Chamela Bay are nearly identical may indicate that, irrespective of the geographical distance between localities, populations of the spotted rose snapper move along the Pacific coast of Mexico." "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:3 [ "identificador" => "xres548332" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec566149" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres548333" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec566150" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Materials and methods" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Morphological analysis" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "DNA extraction and sequencing" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Alignments and phylogenentic analyses" ] ] ] 6 => array:3 [ "identificador" => "sec0030" "titulo" => "Results" "secciones" => array:7 [ 0 => array:2 [ "identificador" => "sec0035" "titulo" => "Taxonomic summary" ] 1 => array:2 [ "identificador" => "sec0040" "titulo" => "Remarks" ] 2 => array:2 [ "identificador" => "sec0045" "titulo" => "Taxonomic summary" ] 3 => array:2 [ "identificador" => "sec0050" "titulo" => "Remarks" ] 4 => array:2 [ "identificador" => "sec0055" "titulo" => "Taxonomic summary" ] 5 => array:2 [ "identificador" => "sec0060" "titulo" => "Remarks" ] 6 => array:2 [ "identificador" => "sec0065" "titulo" => "Systematic position and genetic divergence of Haliotrematoides spp." ] ] ] 7 => array:2 [ "identificador" => "sec0070" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "xack185159" "titulo" => "Acknowledgments" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2014-08-20" "fechaAceptado" => "2015-02-03" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec566149" "palabras" => array:6 [ 0 => "Euryhaliotrema" 1 => "28S rRNA gene" 2 => "Cryptic species" 3 => "Mexico" 4 => "Monogenea" 5 => "Snapper" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec566150" "palabras" => array:6 [ 0 => "Euryhaliotrema" 1 => "28S rRNA" 2 => "Especies crípticas" 3 => "México" 4 => "Monogenea" 5 => "Pargo" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Specimens of wild populations of the spotted rose snapper, Lutjanus guttatus (Steindacher) were studied for monogenean parasites in 2 localities along the Mexican Pacific coast (Mazatlán, Sinaloa and Chamela Bay, Jalisco). Five species of dactylogyrids were found on the gills of their hosts: Haliotrematoides guttati (<a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas, Fajer-Ávila, & Lamothe-Argumedo, 2008</a>), H. plectridium Kristky and Mendoza-Franco in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky, Tingbao, & Yuan, 2009</a>, H. spinatus Kristky and Mendoza-Franco in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al. (2009)</a>, Euryhaliotrema perezponcei<a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas, Fajer-Ávila & Lamothe-Argumedo, 2008</a> and E. mehen (<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jiménez, García-Gasca, & Fajer-Avila, 2012</a>). Freshly collected specimens provided an opportunity to study and compare specimens from different localities in further detail and few morphological characters were added to the description of each species. Additionally, a fragment of 856bp of the 28S ribosomal RNA (D1–D3) was obtained for all the sampled monogeneans, and a phylogenetic analysis along with all available sequences of dactylogyrids was conducted to establish the systematic position of the species within the Ancyrocephalinae. Our results suggest that species of Haliotrema might be included in Haliotrematoides genus. In addition, the genetic divergence data suggest that H. guttati and H. spinatus may represent a species complex; however, this asseveration needs additional data." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "Se estudiaron los monogéneos que parasitan poblaciones silvestres de “pargos” o “huachinangos”, Lutjanus guttatus (Steindacher) en 2 localidades de la costa del Pacífico mexicano (Mazatlán, Sinaloa y Bahía de Chamela, Jalisco). Se recolectaron 5 especies de dactylogíridos de las branquias de sus hospederos: Haliotrematoides guttati (<a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas et al., 2008</a>), H. plectridium Kristky and Mendoza-Franco en <a class="elsevierStyleCrossRef" href="#bib0065">Kristky, Tingbao, and Yuan (2009)</a>, H. spinatus Kristky and Mendoza-Franco en <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al. (2009)</a>, Euryhaliotrema perezponcei<a class="elsevierStyleCrossRef" href="#bib0020">García-Vargas, Fajer-Ávila & Lamothe-Argumedo, 2008</a> and E. mehen (<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jiménez et al., 2012</a>). El material permitió observar la morfología en mayor detalle y comparar ejemplares de diferentes localidades aportando algunos caracteres morfológicos a la descripción de las especies. Se obtuvo la secuencia de un fragmento de 856bp del gen ribosomal 28S (dominios D1 a D3), de este modo se estableció la posición sistemática de éstas, en conjunto con las secuencias de otros dactylogíridos, dentro de la filogenia de los Ancyrocephalinae. Este análisis reveló que las especies de Haliotrema podrían incluirse en el género Haliotrematoides. Asimismo, los datos de divergencia genética sugieren que H. guttati y H. spinatus podrían representar un complejo de especies, aunque esto requiere ser verificado con datos adicionales." ] ] "NotaPie" => array:1 [ 0 => array:1 [ "nota" => "Peer Review under the responsibility of Universidad Nacional Autónoma de México." ] ] "multimedia" => array:6 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figures 1–6" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1v6.jpeg" "Alto" => 1597 "Ancho" => 1667 "Tamanyo" => 123757 ] ] "descripcion" => array:1 [ "en" => "Drawings of Haliotrematoides guttati from Lutjanus guttatus found in Chamela Bay, Jalisco and Mazatlán, Sinaloa, Mexico. 1, dorsal anchor; 2, ventral anchor; 3, dorsal bar; 4, ventral bar; 5, hook, male copulatory organ (MCO). All measurements are in micrometers." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figures 7–11" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr7v11.jpeg" "Alto" => 1186 "Ancho" => 1000 "Tamanyo" => 79450 ] ] "descripcion" => array:1 [ "en" => "Drawings of Haliotrematoides plectridium from Lutjanus guttatus found in Chamela Bay, Jalisco and Mazatlán, Sinaloa, Mexico. 7, dorsal anchor; 8, ventral anchor; 9, dorsal bar; 10, ventral bar; 11, male copulatory organ. All measurements are in micrometers." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figures 12–15" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr12v15.jpeg" "Alto" => 801 "Ancho" => 1636 "Tamanyo" => 107911 ] ] "descripcion" => array:1 [ "en" => "Drawings of Haliotrematoides spinatus from Lutjanus guttatus found in Chamela Bay, Jalisco and Mazatlán, Sinaloa, Mexico. 12, dorsal anchor; 13, ventral anchor; 14, dorsal bar; 15, ventral bar. All measurements are in micrometers." ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 16" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr16.jpeg" "Alto" => 4167 "Ancho" => 2689 "Tamanyo" => 1075360 ] ] "descripcion" => array:1 [ "en" => "Phylogenetic tree obtained through from maximum likelihood (ML) analysis based on the 28S sequences for selected dactylogyrid species, with some species of diplectanids used as outgroups." ] ] 4 => array:7 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Monogenean \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Locality \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">CNHE/USNPC \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">GenBank \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">Haliotrematoides guttati \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Chamela Bay \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8354/106930 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">KC663673–663674 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Mazatlán \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">7293/– \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">HQ615993 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">Haliotrematoides plectridium \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Chamela Bay \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8353/106931-106933 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">– \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Mazatlán \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">7292/– \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">HQ615994–KC713622 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">Haliotrematoides spinatus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Chamela Bay \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">8355/106934-106935 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">KC663675–KC663678 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Mazatlán \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">7291/– \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">HQ615995 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab885754.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Dactylogyrid species reported in the present study from the gills of Lutjanus guttatus from Chamela Bay, Jalisco and Mazatlán, Sinaloa, Mexico. CNHE-Coleccion Nacion de Helmintos, UNAM, México. USNPC – United States National Parasite Collection, USA." ] ] 5 => array:7 [ "identificador" => "tbl0010" "etiqueta" => "Table 2" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="" valign="top" scope="col" style="border-bottom: 2px solid black"> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">E. mehen \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">E. perezponcei \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">H. guttati \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">H. spinatus \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">H. plectridium \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">E. mehen \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0–0.05 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">13.6–15.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">20.5–22.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">21.5–24.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">22.25–22.8 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">E. perezponcei \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0–3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">20.7–23.9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">22.5–25.7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">24.3–25.7 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">H. guttati \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0–6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.8–10.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14.3–15.5 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">H. spinatus \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0–8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">13.6–17.3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="left" valign="top">H. plectridium \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="" valign="top"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab885753.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Uncorrected pairwise distances of the partial sequences of the 28S rRNA gene among species analyzed from Chamela Bay, Jalisco and Mazatlán, Sinaloa, Mexico. 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To Martín García Varela for his assistance with molecular analysis. This work was partly supported by PAPIIT IN204514 to GPPL. AGV thanks DGAPA-UNAM for a Postdoctoral scholarship." "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/18703453/0000008600000002/v2_201509041752/S1870345315000287/v2_201509041752/en/main.assets" "Apartado" => array:4 [ "identificador" => "41751" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Taxonomía y sistemática/ Taxonomy and systematics" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/18703453/0000008600000002/v2_201509041752/S1870345315000287/v2_201509041752/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1870345315000287?idApp=UINPBA00004N"]

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Taxonomy and systematics

Haliotrematoides spp. (Monogenoidea: Dactylogiridae) parasitando Lutjanus guttatus (Lutjanidae) en dos localidades de la costa pacífica de México y su posición filogenética dentro de Ancyrocephalinae a través de secuencias del 28S rRNA

Adriana García-Vásqueza,b,

Corresponding author

tocha76@hotmail.com

Corresponding author.

, Carlos Daniel Pinacho-Pinachoa, Lilia Catherine Soler-Jiménezc, Emma Josefina Fajer-Ávilac, Gerardo Pérez-Ponce de Leóna

a Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Apartado postal 70-153, Coyoacán, 04510 México, D.F., Mexico

b Red de Biología Evolutiva, Instituto de Ecología, A. C., Km 2.5 Antigua carretera a Coatepec, 91070 Xalapa, Veracruz, Mexico

c Centro de Investigación en Alimentos y Desarrollo en Acuicultura y Manejo Ambiental, A. C., Unidad Mazatlán, Estero del Yugo s/n, 82000 Mazatlán, Sinaloa, Mexico

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The genus <span class="elsevierStyleItalic">Lutjanus</span> &#40;Steindacher&#41; &#40;Lutjanidae&#41;&#44; the most species-rich among the family Lutjanidae&#44; contains 68 species distributed around the world &#40;<a class="elsevierStyleCrossRef" href="#bib0015">Froese &#38; Pauly&#44; 2014</a>&#41;&#46; These fish are commercially important for fisheries&#44; and at least 20 species have been examined for monogeneans&#44; since it is well-known the impact that these parasites may have on fish populations&#46; Species of 4 genera of dactylogyrids have been found on the gills of snappers around the world&#44; <span class="elsevierStyleItalic">Euryhaliotrema</span><a class="elsevierStyleCrossRef" href="#bib0060">Kritsky and Boeger&#44; 2002</a>&#44; <span class="elsevierStyleItalic">Haliotrema</span> Johnston and Tiegs&#44; 1922&#44; <span class="elsevierStyleItalic">Haliotrematoides</span><a class="elsevierStyleCrossRef" href="#bib0065">Kritsky&#44; Tingbao &#38; Yuan&#44; 2009</a> and <span class="elsevierStyleItalic">Tetrancistrum</span> Goto and Kikuchi&#44; 1917&#59; 2 other genera&#44; <span class="elsevierStyleItalic">Euryhaliotrematoides</span> Plaisance and Kritsky&#44; 2004&#44; and <span class="elsevierStyleItalic">Aliatrema</span> Plaisance and Kritsky&#44; 2004 were recently considered as synonyms of <span class="elsevierStyleItalic">Euryhaliotrema</span> based on the morphology of their male copulatory organ &#40;MCO&#41; &#40;<a class="elsevierStyleCrossRef" href="#bib0050">Kritsky&#44; 2012</a>&#41;&#46; In Mexico&#44; 9 dactylogyrid species have been described from snappers&#44; i&#46;e&#46; <span class="elsevierStyleItalic">H&#46; cornigerum</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov&#44; 1976</a>&#41;&#44; <span class="elsevierStyleItalic">H&#46; gracilihamus</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov&#44; 1976</a>&#41;&#44; <span class="elsevierStyleItalic">H&#46; heteracantha</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov&#44; 1976</a>&#41;&#44; <span class="elsevierStyleItalic">H&#46; longihamus</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov&#44; 1976</a>&#41;&#44; <span class="elsevierStyleItalic">H&#46; magnigastrohamus</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0145">Zhukov&#44; 1976</a>&#41;&#44; <span class="elsevierStyleItalic">H&#46; overstreeti</span> Kritsky and Bullard in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46; &#40;2009&#41;</a> from Campeche Bay&#59; <span class="elsevierStyleItalic">H&#46; guttati</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas&#44; Fajer-&#193;vila &#38; Lamothe-Argumedo&#44; 2008</a>&#41;&#44; <span class="elsevierStyleItalic">E&#46; perezponcei</span><a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas&#44; Fajer-&#193;vila &#38; Lamothe-Argumedo&#44; 2008</a> from Mazatl&#225;n&#44; Sinaloa and Cruz de Huanacaxtle&#44; Nayarit&#44; and <span class="elsevierStyleItalic">E&#46; mehen</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jim&#233;nez&#44; Garc&#237;a-Gasca &#38; Fajer-&#193;vila&#44; 2012</a>&#41; from Mazatl&#225;n&#44; Sinaloa&#46; The taxonomic status of some of these species of dactylogyrids has been unstable due to the lack of morphological details &#40;mostly in haptoral hard parts and copulatory organ&#41; in the original descriptions&#44; although clarification has been gained after further taxonomic work conducted by several authors &#40;e&#46;g&#46;&#44; <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46;&#44; 2009</a>&#41;&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Recently&#44; specimens of the spotted rose snapper <span class="elsevierStyleItalic">Lutjanus guttatus</span> &#40;Steindachner&#41; were collected in Chamela Bay&#44; Jalisco and Mazatl&#225;n&#44; Sinaloa&#44; both on the Pacific coast of Mexico&#44; as part of the study of the ectoparasites of fishes with commercial importance&#46; From those fishes&#44; specimens of dactylogyrids were collected from the gills&#46; The objectives of this paper were to report the presence of 3 species of <span class="elsevierStyleItalic">Haliotrematoides</span> parasitizing the gills of spotted rose snappers&#44; and to provide additional morphological information for each of them&#46; In addition&#44; we analyze the systematic position of these species &#40;including <span class="elsevierStyleItalic">E&#46; perezponcei</span> and <span class="elsevierStyleItalic">E&#46; mehen</span> from Mazatl&#225;n&#41; within the phylogeny of the Ancyrocephalinae&#44; by using sequences of the 28S rRNA in the context of a wider phylogenetic analysis of dactylogyrids&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><p id="par0015" class="elsevierStylePara elsevierViewall">Specimens of adult spotted rose snapper <span class="elsevierStyleItalic">Lutjanus guttatus</span> were sampled in 2010 in Mazatl&#225;n Bay&#44; Sinaloa &#40;23&#176;18&#8242;44&#8243;<span class="elsevierStyleHsp" style=""></span>N&#44; 106&#176;29&#8242;37&#8243;<span class="elsevierStyleHsp" style=""></span>W&#41; and from 2011 through 2012 in Chamela Bay&#44; Jalisco &#40;19&#176;33&#8242;15&#8243;<span class="elsevierStyleHsp" style=""></span>N&#44; 105&#176;06&#8242;45&#8243;<span class="elsevierStyleHsp" style=""></span>W&#41;&#44; in northwestern Mexico&#59; fish were obtained from local fishermen who set nets in each locality&#44; kept on ice once removed from the nets&#44; and examined for gill parasites a few hours after capture&#46; Gills were extracted&#44; fixed and stored in 96&#37; ethanol&#59; parasites were excised from the host tissue using triangular&#44; surgical&#44; mounted needles &#40;size 16&#44; Barber of Sheffield&#44; U&#46;K&#46;&#41; and were prepared for morphological and molecular evaluation&#46; For morphological comparison&#44; type-specimens deposited at the National Museum of Natural History &#40;NMNH&#41;&#44; Smithsonian Institution&#44; Washington&#44; D&#46;C&#46; &#40;formerly U&#46;S&#46; National Parasite Collection &#8211; USNPC&#41;&#44; USA at the Colecci&#243;n Nacional de Helmintos &#40;CNHE&#41; and at the Colecci&#243;n de Par&#225;sitos de Peces del Noroeste de M&#233;xico &#40;CPPNP&#41; were studied as follows&#58; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span> &#40;USNPC 101370&#8211;101371&#59; CNHE&#44; Neotype 8460&#41;&#44; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">plectridium</span> &#40;USNPC 101367&#8211;101369&#41;&#44; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span> &#40;USNPC 101353&#8211;101355&#59; CNHE 6464&#8211;6465&#41;&#46;</p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Morphological analysis</span><p id="par0020" class="elsevierStylePara elsevierViewall">The haptor of each specimen was removed using a scalpel and air-dried on a glass slide&#59; the corresponding body was transferred to a labeled Eppendorf tube containing 96&#37; ethanol and stored at &#8722;20<span class="elsevierStyleHsp" style=""></span>&#176;C until required for molecular evaluation&#46; Air-dried haptors were then subjected to a partial digestion using a proteinase K-base method &#40;<a class="elsevierStyleCrossRef" href="#bib0025">Garc&#237;a-V&#225;squez&#44; Hansen&#44; Cristison&#44; Bron&#44; &#38; Shinn&#44; 2011</a>&#41;&#46; Some specimens were mounted &#40;unstained&#41; in Gray and Wess &#40;<a class="elsevierStyleCrossRef" href="#bib0140">Vidal-Mart&#237;nez&#44; Aguirre-Macedo&#44; Scholz&#44; Gonz&#225;lez-Solis&#44; &#38; Mendoza-Franco&#44; 2001</a>&#41; solution to clear the body tissue and visualize the haptoral hooks and copulatory complex&#46; The haptoral armature and copulatory complex were studied using an immersion oil objective on an Olympus BX40 compound microscope&#46; For comparisons&#44; specimens were measured following <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46; &#40;2009&#41;</a>&#46; When provided&#44; measurements are presented in micrometers with the average followed by the range in parentheses&#46; Specimens were deposited in the Colecci&#243;n Nacional de Helmintos from Mexico &#40;CNHE&#41; and in the U&#46;S&#46; National Parasite Collection &#40;USNPC&#41;&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">DNA extraction and sequencing</span><p id="par0025" class="elsevierStylePara elsevierViewall">Parasite bodies were digested overnight at 56<span class="elsevierStyleHsp" style=""></span>&#176;C in a solution containing 10<span class="elsevierStyleHsp" style=""></span>mM Tris&#8211;HCl &#40;pH 7&#46;6&#41;&#44; 20<span class="elsevierStyleHsp" style=""></span>mM NaCl&#44; 100<span class="elsevierStyleHsp" style=""></span>mM Na<span class="elsevierStyleInf">2</span> EDTA &#40;pH 8&#46;0&#41;&#44; 1&#37; Sakozyl&#44; and 0&#46;1<span class="elsevierStyleHsp" style=""></span>mg&#47;ml proteinase K&#46; Following digestion&#44; DNA was extracted from the supernatant using DNAzol reagent &#40;Molecular Research Center&#44; Cincinnati&#44; Ohio&#41; according to the manufacturer&#39;s instructions&#46; Some tissues were extracted using the DNeasy Tissue Kit &#40;Qiagen&#44; Valencia&#44; California&#41;&#46; A fragment of the 28S ribosomal gene was amplified using the polymerase chain reaction &#40;PCR&#41;&#46; The primers Ancy55F &#40;5&#8242;-GAGATTAGCCCATCACCG AAG-3&#8242;&#41; &#40;<a class="elsevierStyleCrossRef" href="#bib0095">Plaisance&#44; Littlewood&#44; Olson&#44; &#38; Morand&#44; 2005</a>&#41; and LSU1200R &#40;5&#8242;-GCATAGTTCACCATCTTTCGG-3&#8242;&#41; &#40;<a class="elsevierStyleCrossRef" href="#bib0075">Littlewood&#44; Curini-Galletti&#44; &#38; Herniou&#44; 2000</a>&#41; were used to amplify &#40;PCR&#41; a LSU fragment&#59; also&#44; the internal primers Halio-F &#40;5&#8242;-ACCCGCTGAATTTAAGCAT-3&#8242;&#41; and Halio-R &#40;5&#8242;-TGGTCCGTGTTTCAAGAC-3&#8242;&#41; &#40;<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jim&#233;nez et al&#46;&#44; 2012</a>&#41;&#46; The PCR &#40;25<span class="elsevierStyleHsp" style=""></span>&#956;l&#41; consisted of 2&#46;5<span class="elsevierStyleHsp" style=""></span>&#956;l of 1<span class="elsevierStyleHsp" style=""></span>&#956;l of 10<span class="elsevierStyleHsp" style=""></span>&#956;M of each primer&#44; 2&#46;5<span class="elsevierStyleHsp" style=""></span>&#956;l of 10&#215; buffer&#44; 1&#46;5<span class="elsevierStyleHsp" style=""></span>&#956;l of MgCl<span class="elsevierStyleInf">2</span> 15<span class="elsevierStyleHsp" style=""></span>mM&#44; 0&#46;5<span class="elsevierStyleHsp" style=""></span>&#956;l dNTP&#39;s 10<span class="elsevierStyleHsp" style=""></span>mM&#44; 1<span class="elsevierStyleHsp" style=""></span>U of Taq DNA polymerase &#40;Platinum Taq&#44; Invitrogen Corporation&#44; S&#227;o Paulo&#44; Brazil&#41;&#44; 2<span class="elsevierStyleHsp" style=""></span>&#956;l of DNA template&#44; and 13&#46;675<span class="elsevierStyleHsp" style=""></span>&#956;l of water&#46; The PCR cycling protocol included denaturation at 94<span class="elsevierStyleHsp" style=""></span>&#176;C for 2<span class="elsevierStyleHsp" style=""></span>min&#44; followed by 35 cycles of 94<span class="elsevierStyleHsp" style=""></span>&#176;C for 1<span class="elsevierStyleHsp" style=""></span>min&#44; annealing at 50&#8211;58<span class="elsevierStyleHsp" style=""></span>&#176;C depending on dactylogyrid species &#40;<span class="elsevierStyleItalic">E</span>&#46; <span class="elsevierStyleItalic">perezponcei</span> 50<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; <span class="elsevierStyleItalic">E</span>&#46; <span class="elsevierStyleItalic">mehen</span> 55<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span> and <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span> 58<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; and <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">plectridium</span> 55<span class="elsevierStyleHsp" style=""></span>&#176;C&#41; for 1<span class="elsevierStyleHsp" style=""></span>min and final extension at 72<span class="elsevierStyleHsp" style=""></span>&#176;C for 1<span class="elsevierStyleHsp" style=""></span>min&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The reaction was performed in a MJ Research thermal cycler using a heated lid to reduce refluxing&#46; Sequencing reactions were performed using an ABI Big Dye &#40;Applied Biosystems&#44; Boston&#44; MA&#41; terminator sequencing chemistry&#44; and reaction products were separated and detected using an ABI 310 capillary DNA sequencer&#46; Contigs were assembled and base calling differences resolved using Codoncode Aligner version 3&#46;0&#46;1 &#40;Codoncode Corporation&#44; Dedham&#44; MA&#41;&#46; All sequences were deposited in GenBank database&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Alignments and phylogenentic analyses</span><p id="par0035" class="elsevierStylePara elsevierViewall">Sequences obtained in the current study from 28S &#40;D1&#8211;D3&#41; were aligned along with other species of Dactylogyridae available in GenBank using Clustal W implemented in Mega 5 &#40;<a class="elsevierStyleCrossRef" href="#bib0135">Tamura&#44; Peterson&#44; Peterson&#44; Stecher&#44; &#38; Kumar&#44; 2011</a>&#41; and adjusted manually with the Mesquite 2&#46;75 program &#40;<a class="elsevierStyleCrossRef" href="#bib0080">Maddison &#38; Maddison&#44; 2011</a>&#41;&#46; Maximum likelihood &#40;ML&#41; and Bayesian Inference &#40;BI&#41; analyses were performed &#40;<a class="elsevierStyleCrossRef" href="#bib0040">Huelsenbeck &#38; Ronquist&#44; 2001</a>&#41;&#46; The jModelTest software version 0&#46;1&#46;1 &#40;<a class="elsevierStyleCrossRef" href="#bib0100">Posada&#44; 2008</a>&#41; was used to select the best model of evolution for our dataset&#46; The model &#40;GTR<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>I<span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span>G&#41; was selected based on the Akaike information criteria&#46; The ML tree was inferred using RAxML 7&#46;0&#46;4&#44; for each dataset &#40;<a class="elsevierStyleCrossRef" href="#bib0130">Stamatakis&#44; 2006</a>&#41;&#46; Maximum likelihood clade support was assessed by bootstrap resampling with 10&#44;000 replicates&#46; Additionally&#44; Bayesian analyses were performed with the program MrBAYES version 3&#46;1&#46;2 &#40;<a class="elsevierStyleCrossRef" href="#bib0040">Huelsenbeck &#38; Ronquist&#44; 2001</a>&#41;&#46; The settings were 2 simultaneous runs with 4 Markov chains and 5 million MCMC generations&#44; sampling every 200 generations&#44; a heating parameter value of 0&#46;2 and a &#8216;burnin&#8217; of 10&#37;&#46; Numbers at the interior branches of the consensus tree represent posterior probabilities &#40;PP&#41;&#46; Trees were drawn using FigTree program version 1&#46;3&#46;1 &#40;<a class="elsevierStyleCrossRef" href="#bib0105">Rambaut&#44; 2006</a>&#41;&#46; The genetic divergence among species &#40;<span class="elsevierStyleItalic">E</span>&#46; <span class="elsevierStyleItalic">perezponcei</span>&#44; <span class="elsevierStyleItalic">E</span>&#46; <span class="elsevierStyleItalic">mehen</span>&#44; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">plectridium</span>&#44; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span> and <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span>&#41; was estimated using uncorrected &#8220;p-distances&#8221; method with the program MEGA v&#46; 5 &#40;<a class="elsevierStyleCrossRef" href="#bib0135">Tamura et al&#46;&#44; 2011</a>&#41;&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Results</span><p id="par0040" class="elsevierStylePara elsevierViewall">Three species of <span class="elsevierStyleItalic">Haliotrematoides</span> were found parasitizing the gills of <span class="elsevierStyleItalic">L&#46; guttatus</span> in Mazatl&#225;n&#44; Sinaloa and Chamela Bay&#44; Jalisco &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; The specimens collected in the present study were compared morphologically with type and voucher specimens&#44; mainly in terms of haptoral hooks and male copulatory organ &#40;MCO&#41;&#46; The following species were found&#58;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0045" class="elsevierStylePara elsevierViewall">Dactylogyridae Bychowsky&#44; 1933</p><p id="par0050" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Haliotrematoides</span><a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46;&#44; 2009</a></p><p id="par0055" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic"><span class="elsevierStyleBold">Haliotrematoides guttati</span></span> &#40;<a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas et al&#46;&#44; 2008</a>&#41;</p><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Taxonomic summary</span><p id="par0060" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Site</span>&#58; gills&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Type host and locality&#58; Lutjanus guttatus</span> &#40;Steindachner&#41;&#44; Pacific Coast off Mazatl&#225;n&#44; Sinaloa&#44; Mexico &#40;23&#176;29&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 106&#176;36&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Host and localities&#58;</span> Chamela Bay&#44; Jalisco&#44; Mexico &#40;19&#176;31&#8242;49&#8243;<span class="elsevierStyleHsp" style=""></span>N&#44; 105&#176;04&#8242;55&#8243;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46; Mazatl&#225;n&#44; Sinaloa &#40;23&#176;13&#8242;10&#8243;<span class="elsevierStyleHsp" style=""></span>N&#44; 106&#176;26&#8242;05&#8243;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Previous records&#58;</span> Cruz de Huanacaxtle&#44; Nayarit&#44; Mexico &#40;20&#176;44&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 105&#176;22&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#59; Taboga Island&#44; Panama &#40;8&#176;49&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 79&#176;34&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#59; Perlas Archipielago&#44; Panama &#40;8&#176;22&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 79&#176;01&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Specimens deposited</span>&#58; CPPNP 7293&#44; 5 vouchers &#40;from the type locality&#41;&#44; 4 vouchers CNHE 8354 and 1 voucher USNPC 106930 &#40;from Chamela&#41;&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">DNA reference sequence&#58;</span> the 856<span class="elsevierStyleHsp" style=""></span>bp ribosomal DNA sequence of the LSU &#40;D1-D3&#41; is deposited in GenBank under accession numbers <a href="ncbi-n:HQ615993">HQ615993</a> &#40;from Mazatl&#225;n&#41; and <a href="ncbi-n:KC663673">KC663673</a>&#8211;KC663674 &#40;from Chamela Bay&#41;&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Remarks</span><p id="par0090" class="elsevierStylePara elsevierViewall">Five specimens of this species were found in Chamela bay&#44; Jalisco and 10 were found in Mazatl&#225;n&#44; Sinaloa&#44; Mexico&#44; corresponding with the genus description provided by Kritsky and Mendoza-Franco &#40;<a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46;&#44; 2009</a>&#41;&#46; This species was originally described as <span class="elsevierStyleItalic">H&#46; guttati</span> as a parasite of <span class="elsevierStyleItalic">L&#46; guttatus</span> from Mazatl&#225;n by <a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas et al&#46; &#40;2008&#41;</a>&#46; In 2009&#44; Kritsky et al&#46; found 2 specimens from the gills of snappers in Panama&#44; and based on the comparison of their specimens with the original description&#44; and their examination of the paratype and 2 voucher specimens &#40;Harold W&#46; Manter Laboratory&#44; University of Nebraska-Lincoln&#44; HWML&#44; 48570&#44; 48571&#41; transferred the species to the genus <span class="elsevierStyleItalic">Haliotrematoides</span>&#46; Following <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46; &#40;2009&#41;</a> recommendation for the need of a re-description of this species&#44; we studied in further detail our specimens and those deposited in museum collections &#40;neotype&#44; CNHE&#44; and vouchers from the USNPC from Panama&#41;&#44; and herein we provide the following details of some morphological traits&#58; dorsal anchor with a well-developed membrane 12 &#40;11&#8211;15&#41; long&#44; showing some striations on the surface of the curvature to the point&#59; in the mid portion of perforation on the anchors base&#44; a small heel is observed &#40;not observed in specimens from Panama&#41;&#44; a long inner root&#44; no developed outer root &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Ventral anchor with both roots well developed&#44; inner root 14 &#40;12&#8211;16&#46;5&#41; long and ending pointed&#44; longer than the outer root which is 6&#46;5 &#40;6&#8211;8&#41; long and rounded &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 2</a>&#41;&#46; Dorsal bar delicate&#44; round in the middle&#44; with a small knob&#44; square ends where anchor attaches &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 3</a>&#41;&#46; V-shaped ventral bar 41 &#40;38&#46;5&#8211;44&#41; wide&#44; but in description made by <a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas et al&#46; &#40;2008&#41;</a> is described as &#8220;W-shaped&#8221;&#44; this was not observed in the type specimens that were studied &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 4</a>&#41;&#46; Hooks with terminal depressed thumb directed to point&#44; point opened and beyond thumb &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 5</a>&#41;&#46; MCO tubular-shaped forming a spiral&#44; conical base with the anterior part narrower than the base&#44; and bearing a long whip heading to the anterior part of the body &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 6</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0095" class="elsevierStylePara elsevierViewall">Chamela Bay represents a new geographical record for this species&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic"><span class="elsevierStyleBold">Haliotrematoides plectridium</span></span> Kritsky &#38; Mendoza-Franco&#44; 2009</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Taxonomic summary</span><p id="par0105" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Site</span>&#58; gills&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Type host and locality&#58; Lutjanus guttatus</span> &#40;Steindachner&#41;&#44; off Taboga Island&#44; Panama &#40;8&#176;49&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 79&#176;34&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Host and localities&#58; Lutjanus guttatus</span> &#40;Steinadachner&#41;&#44; Chamela Bay&#44; Jalisco&#44; Mexico &#40;19&#176;31&#8242;49&#8243;<span class="elsevierStyleHsp" style=""></span>N&#44; 105&#176;04&#8242;55&#8243;<span class="elsevierStyleHsp" style=""></span>W&#41;&#44; and Mazatl&#225;n&#44; Sinaloa&#44; Mexico &#40;23&#176;13&#8242;10&#8243;<span class="elsevierStyleHsp" style=""></span>N&#44; 106&#176;26&#8242;05&#8243;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Previous records&#58;</span> Perlas Archipielago&#44; Panama &#40;8&#176;22&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 79&#176;01&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Specimens deposited&#58;</span> CNHE 7292&#44; 2 vouchers &#40;from Mazatl&#225;n&#41;&#59; CNHE 8353&#44; 4 vouchers &#40;from Chamela Bay&#41;&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">DNA reference sequence&#58;</span> the 856<span class="elsevierStyleHsp" style=""></span>bp ribosomal DNA sequence of the LSU &#40;D1&#8211;D3&#41; is deposited in GenBank under accession number <a href="ncbi-n:HQ615994">HQ615994</a>&#44; <a href="ncbi-n:KC713622">KC713622</a> &#40;from Mazatl&#225;n&#41;&#46; No sequences were obtained from Chamela Bay&#44; Mexico &#40;10 specimens were prepared for molecular analysis but fail to amplify&#41;&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Remarks</span><p id="par0135" class="elsevierStylePara elsevierViewall">A total of 10 specimens were found in Mazatl&#225;n&#44; Sinaloa and 19 in Chamela Bay&#44; Jalisco&#46; Our specimens are in agreement with the original description of Kritsky and Mendoza-Franco &#40;2009&#41; in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46; &#40;2009&#41;</a> from Taboga Island&#44; and from Perlas Archipelago&#44; both in Panama&#46; Records from Mazatl&#225;n and Chamela represent new geographical records for this species&#46; We observed in our specimens the following taxonomic traits&#44; some of them slightly different from specimens from Panama&#58; a membrane-like structure in the inner root of dorsal anchor&#44; 8 &#40;6&#8211;12&#46;5&#41; long&#44; no outer root developed &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 7</a>&#41;&#46; Ventral anchor with a depressed inner root&#44; with the inner root longer than the outer root&#44; 11 &#40;8&#8211;17&#41; long &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 8</a>&#41;&#46; Dorsal bar 41 &#40;36&#46;5&#8211;46&#41; wide&#44; thin and concave while in the Panama specimens the bar is smaller&#44; 35 &#40;31&#8211;37&#41; wide &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 9</a>&#41;&#46; Ventral bar concave&#44; 43 &#40;40&#8211;47&#41; wide&#44; with 2 subterminal pockets in the anterior margin &#40;convex in specimens from Panama&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 10</a>&#41;&#46; The MCO possess a filament at the end&#44; finishing bulged in our specimens &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 11</a>&#41;&#44; while this structure was not observed in Panama specimens&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0140" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic"><span class="elsevierStyleBold">Haliotrematoides spinatus</span></span> Kritsky &#38; Mendoza-Franco&#44; 2009</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Taxonomic summary</span><p id="par0145" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Site</span>&#58; gills&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Type host and locality&#58; Lutjanus guttatus</span> &#40;Steindachner&#41;&#44; off Taboga Island&#44; Panama &#40;8&#176;49&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 79&#176;34&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;</p><p id="par0155" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Host and localities&#58;</span> Chamela Bay&#44; Jalisco&#44; Mexico &#40;19&#176;31&#8242;49&#8221;<span class="elsevierStyleHsp" style=""></span>N&#44; 105&#176;04&#8242;55&#8221;<span class="elsevierStyleHsp" style=""></span>W&#41;&#44; and Mazatl&#225;n&#44; Sinaloa&#44; M&#233;xico &#40;23&#176;29&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 106&#176;36&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Previous records&#58;</span> Perlas Archipielago&#44; Panama &#40;8&#176;22&#8242;<span class="elsevierStyleHsp" style=""></span>N&#44; 79&#176;01&#8242;<span class="elsevierStyleHsp" style=""></span>W&#41;&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Specimens deposited&#58;</span> CNHE 7291 and CNHE 7546&#44; 4 vouchers &#40;from Mazatl&#225;n&#41; and CNHE 8355&#44; 4 vouchers&#44; 2 vouchers USNPC 106934&#8211;106935 &#40;from Chamela Bay&#41;&#46;</p><p id="par0170" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">DNA reference sequence&#58;</span> the 856<span class="elsevierStyleHsp" style=""></span>bp ribosomal DNA sequence of the LSU &#40;D1&#8211;D3&#41; is deposited in GenBank under accession numbers <a href="ncbi-n:HQ615995">HQ615995</a>&#44; KC713623&#8211;KC713627 &#40;from Mazatl&#225;n&#41; and KC663675&#8211;KC663678 &#40;from Chamela Bay&#41;&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Remarks</span><p id="par0175" class="elsevierStylePara elsevierViewall">A total of 10 worms of this species were found in Mazatl&#225;n&#44; Sinaloa and 11 from Chamela Bay&#44; Jalisco&#46; The specimens collected in the present study&#44; conform to the description provided by Kritsky and Mendoza-Franco &#40;2009&#41; in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46; &#40;2009&#41;</a>&#46; The finding of this species in <span class="elsevierStyleItalic">L&#46; guttatus</span> from Mazatl&#225;n and Chamela represent new geographical records&#46; Our specimens show a delicate and short membrane in the outer root of the dorsal anchor&#44; possessing a straight and relatively long point 24 &#40;23&#8211;26&#41; long&#44; and a straight shaft &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 12</a>&#41;&#44; meanwhile in the specimens from Panama the point is 21 long&#44; and shaft is slightly curved&#44; but differences might be due to intraspecific morphological variation&#46; Ventral anchor with inner root small in our specimens&#44; while in those from Panama the inner root is larger &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 13</a>&#41;&#46; Dorsal bar slightly curved with short spine-like projections&#44; anteriorly directed on each end&#44; while specimens from Panama have 2 angled base dorsal bar &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 14</a>&#41;&#46; The specimens of the present study possess a straight ventral bar&#44; with 2 submedial pockets along the anterior margin and subterminal anterior notches &#40;dorsal view&#41;&#44; with a triangular ridge at the mid-portion of the anterior margin &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 15</a>&#41;&#44; however in specimens from Panama this was not apparent&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Systematic position and genetic divergence of <span class="elsevierStyleItalic">Haliotrematoides</span> spp&#46;</span><p id="par0180" class="elsevierStylePara elsevierViewall">A total of 16 sequences were generated for the 3 species of <span class="elsevierStyleItalic">Haliotrematoides</span> recorded in this study&#58; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span> &#40;3 specimens&#41;&#44; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">plectridium</span> &#40;2 specimens&#41; and <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span> &#40;11 specimens&#41;&#59; additionally&#44; 13 specimens of other 2 species of dactylogyrids were also sequenced&#58; <span class="elsevierStyleItalic">E&#46; mehen</span> &#40;5&#41;&#44; and <span class="elsevierStyleItalic">E</span>&#46; <span class="elsevierStyleItalic">perezponcei</span> &#40;8&#41;&#46; The phylogenetic tree inferred from maximum likelihood analysis is shown in <a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 16</a>&#46; The maximum likelihood tree &#40;&#8722;ln likelihood<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>32&#44;275&#46;20&#41; is presented&#44; as the topology obtained from ML analysis was similar to the consensus tree of the Bayesian analysis&#46; Likewise&#44; the values of posterior probabilities are presented in the ML tree for comparison&#46; The intra and interspecific genetic divergence &#40;uncorrected <span class="elsevierStyleItalic">P</span>-distances&#41; of species collected from snappers in Chamela Bay and Mazatl&#225;n is shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46; <span class="elsevierStyleItalic">Euryhaliotrema</span> and <span class="elsevierStyleItalic">Haliotrematoides</span> are not sister groups&#44; and genetic divergence between genera varied from 20&#46;5 to 24&#46;2&#46; The 3 species of <span class="elsevierStyleItalic">Haliotrematoides</span> differ in a range that varied from 4&#46;8&#37; between <span class="elsevierStyleItalic">H&#46; guttati</span> and <span class="elsevierStyleItalic">H&#46; spinatus</span>&#44; and 17&#46;3&#37; between <span class="elsevierStyleItalic">H&#46; plectridium</span> and <span class="elsevierStyleItalic">H&#46; spinatus</span>&#46; Intraspecific variation is very low&#44; with the exception of that found among isolates of <span class="elsevierStyleItalic">H&#46; guttati</span> &#40;6&#37;&#41; and <span class="elsevierStyleItalic">H&#46; spinatus</span> &#40;8&#37;&#41;&#46; This intraspecific variation and the tree topology may indicate that these 2 species could represent a species complex&#46; In the first case&#44; the 3 isolates of <span class="elsevierStyleItalic">H&#46; guttati</span> are not monophyletic&#44; although this relationship is supported by low bootstrap and posterior probability values&#46; Instead&#44; the isolates of <span class="elsevierStyleItalic">H&#46; spinatus</span> conform a monophyletic clade&#44; although 2 subclades are formed&#44; each with high support values &#40;99&#47;1&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 16</a>&#41;&#46; Even though this could represent a case for the existence of cryptic species&#44; since morphological characters distinguishing those groups are not observed&#44; the inclusion of other molecular markers and a larger sample size is necessary to test the hypothesis of a species complex&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0185" class="elsevierStylePara elsevierViewall">Species of the genus <span class="elsevierStyleItalic">Haliotrematoides</span> herein studied are nested within the Ancyrocephalinae sensu lato &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 16</a>&#41;&#46; Sequences of 2 species of <span class="elsevierStyleItalic">Haliotrema</span> described as parasites of <span class="elsevierStyleItalic">Sciaenops ocellatus</span> L&#46; &#40;Sciaenidae&#41; in China &#40;one of them <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">schenzhenensis</span>&#44; Wang&#44; Lui&#44; &#38; Zhou&#44; 2003&#41;&#44; are nested as the sister group of <span class="elsevierStyleItalic">H&#46; plectridium</span>&#44; a relationship highly supported by bootstrap and posterior probability values&#46; We were unable to confirm the taxonomic determination of that species since we had no access to museum specimens&#46; This is what the DNA sequence data suggest&#44; however this need to be taken with caution&#44; because it is possible that the species from China may actually belong to the genus <span class="elsevierStyleItalic">Haliotrematoides</span>&#44; but this needs to be determined when type-specimens are studied&#46;</p></span></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Discussion</span><p id="par0190" class="elsevierStylePara elsevierViewall">In this study new geographical records of 3 species of <span class="elsevierStyleItalic">Haliotrematoides</span> are presented&#44; and a few details of the morphology of these species are given to complete their taxonomic description&#46; In addition&#44; the specimens collected were sequenced and new data was generated for the 28S rRNA gene&#44; establishing sister-group relationships of the genus within the Ancyrocephalinae sensu lato&#46; Genetic divergence values indicate that the species <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span> and <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span> potentially represent a species complex&#46; Unfortunately&#44; we found no characters that allowed us to distinguish the specimens on morphological grounds&#46; However&#44; since we used in this study only 1 molecular marker&#44; we took a conservative position and we decided to only recognize the potential existence of 2 cryptic species&#46; These results need to be further corroborated by using at least another molecular marker such as <span class="elsevierStyleItalic">cox</span>1&#44; which is more variable and may be more precise in identifying genetic lineages corresponding with separate species&#44; and also it has been proven to be useful in achieving comprehensive species descriptions that facilitate reliable species diagnostics and rapid assessment of biodiversity&#44; as in the case of species in the genus <span class="elsevierStyleItalic">Gyrodactylus</span> von Nordmann&#44; 1832 &#40;<a class="elsevierStyleCrossRef" href="#bib0035">Hansen&#44; Bakke&#44; &#38; Bachmann&#44; 2007</a>&#41;&#46;</p><p id="par0195" class="elsevierStylePara elsevierViewall">A single molecular marker has been used in previous studies on monogenoids when characterizing new species or describing genetic divergence&#59; some studies used either a ribosomal marker &#40;such as internal transcribed spacers&#41; &#40;<a class="elsevierStyleCrossRef" href="#bib0045">Huyse &#38; Volckaert&#44; 2002</a>&#41;&#44; or a mitochondrial gene such as <span class="elsevierStyleItalic">cox</span>1 &#40;<a class="elsevierStyleCrossRef" href="#bib0030">Hansen&#44; Bachmann&#44; &#38; Bakke&#44; 2003</a>&#41;&#46; However&#44; when the potential presence of cryptic species is recognized &#40;<a class="elsevierStyleCrossRefs" href="#bib0085">Nadler &#38; P&#233;rez-Ponce de Le&#243;n&#44; 2011&#59; P&#233;rez-Ponce de Le&#243;n &#38; Nadler&#44; 2010</a>&#41;&#44; the use of several molecular markers in the context of a phylogenetic analysis&#44; and the proper characterization of genetic divergence is highly recommended&#46; This approach has been followed in some species of monogenoids by authors such as <a class="elsevierStyleCrossRef" href="#bib0150">Zi&#281;tara and Lumme &#40;2003&#41;</a> and <a class="elsevierStyleCrossRef" href="#bib0070">Kuusela&#44; Zi&#281;tara&#44; and Lumme &#40;2008&#41;</a>&#46;</p><p id="par0200" class="elsevierStylePara elsevierViewall">The partial fragment of the 28S rRNA &#40;D1-D3&#41; gene has been widely used to investigate the phylogenetic relationships among some dactylogyrids &#40;<a class="elsevierStyleCrossRefs" href="#bib0005">Blasco-Costa&#44; Miguez-Lozano&#44; Sarabeev&#44; &#38; Balbuena&#44; 2012&#59; Dang&#44; Levsen&#44; Shander&#44; &#38; Bristow&#44; 2010&#59; Plaisance et al&#46;&#44; 2005&#59; &#352;imkov&#225;&#44; Mat¿jusov&#225;&#44; &#38; Cunningham&#44; 2006&#59; Singh &#38; Chaudhary&#44; 2010&#44; 2011</a>&#41;&#46; Our results support the classification scheme proposed by <a class="elsevierStyleCrossRef" href="#bib0055">Kritsky and Boeger &#40;1989&#41;</a>&#44; who described the polyphyletic and paraphyletic nature of this group of monogenoids&#46; In our study&#44; Ancyrocephalinae was also not recovered as a monophyletic group&#46;</p><p id="par0205" class="elsevierStylePara elsevierViewall">As an additional result of our research&#44; sequences of specimens of other ancyrocephalid monogeneans infecting the spotted rose snapper were obtained&#44; particularly specimens of <span class="elsevierStyleItalic">E&#46; perezponcei</span> that were collected from the gills of <span class="elsevierStyleItalic">L</span>&#46; <span class="elsevierStyleItalic">guttatus</span>&#44; a species previously described by <a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas et al&#46; &#40;2008&#41;</a>&#44; as well as specimens of <span class="elsevierStyleItalic">E</span>&#46; <span class="elsevierStyleItalic">mehen</span>&#44; a species described by <a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jim&#233;nez et al&#46; &#40;2012&#41;</a>&#44; both from Mazatl&#225;n&#46; The taxonomic status of the genus <span class="elsevierStyleItalic">Euryhaliotema</span> has been also unstable&#46; The genus was proposed by <a class="elsevierStyleCrossRef" href="#bib0060">Kritsky and Boeger &#40;2002&#41;</a> and&#44; in a recent review of the genus by <a class="elsevierStyleCrossRef" href="#bib0050">Kritsky &#40;2012&#41;</a>&#44; the author discovered that some specimens collected from snappers possessed a mixture of morphological features&#44; and decided to include the species of <span class="elsevierStyleItalic">Euryhaliotrematoides</span> within the genus <span class="elsevierStyleItalic">Euryhaliotrema</span>&#46; The species described by <a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jim&#233;nez et al&#46; &#40;2012&#41;</a> as <span class="elsevierStyleItalic">Euryhaliotrematoides mehen</span> infecting <span class="elsevierStyleItalic">L&#46; guttatus</span> from Mazatl&#225;n was then transferred to <span class="elsevierStyleItalic">Euryhaliotrema</span> by <a class="elsevierStyleCrossRef" href="#bib0050">Kritsky &#40;2012&#41;</a>&#46; The molecular results we obtained herein confirm the proposal by <a class="elsevierStyleCrossRef" href="#bib0050">Kritsky &#40;2012&#41;</a> since <span class="elsevierStyleItalic">E&#46; perezponcei</span> nests as the sister species of <span class="elsevierStyleItalic">E</span>&#46; <span class="elsevierStyleItalic">mehen</span>&#46; The presence of <span class="elsevierStyleItalic">E&#46; perezponcei</span> as a parasite of <span class="elsevierStyleItalic">L&#46; guttatus</span> in Chamela represents a new geographical record&#44; and the fact that sequences of individuals of this species from Mazatl&#225;n and Chamela Bay are nearly identical may indicate that&#44; irrespective of the geographical distance between localities&#44; populations of the spotted rose snapper move along the Pacific coast of Mexico&#46;</p></span></span>"
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              "titulo" => "Taxonomic summary"
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              "titulo" => "Systematic position and genetic divergence of Haliotrematoides spp&#46;"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Specimens of wild populations of the spotted rose snapper&#44; <span class="elsevierStyleItalic">Lutjanus guttatus</span> &#40;Steindacher&#41; were studied for monogenean parasites in 2 localities along the Mexican Pacific coast &#40;Mazatl&#225;n&#44; Sinaloa and Chamela Bay&#44; Jalisco&#41;&#46; Five species of dactylogyrids were found on the gills of their hosts&#58; <span class="elsevierStyleItalic">Haliotrematoides guttati</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas&#44; Fajer-&#193;vila&#44; &#38; Lamothe-Argumedo&#44; 2008</a>&#41;&#44; <span class="elsevierStyleItalic">H&#46; plectridium</span> Kristky and Mendoza-Franco in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky&#44; Tingbao&#44; &#38; Yuan&#44; 2009</a>&#44; <span class="elsevierStyleItalic">H&#46; spinatus</span> Kristky and Mendoza-Franco in <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46; &#40;2009&#41;</a>&#44; <span class="elsevierStyleItalic">Euryhaliotrema perezponcei</span><a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas&#44; Fajer-&#193;vila &#38; Lamothe-Argumedo&#44; 2008</a> and <span class="elsevierStyleItalic">E&#46; mehen</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jim&#233;nez&#44; Garc&#237;a-Gasca&#44; &#38; Fajer-Avila&#44; 2012</a>&#41;&#46; Freshly collected specimens provided an opportunity to study and compare specimens from different localities in further detail and few morphological characters were added to the description of each species&#46; Additionally&#44; a fragment of 856<span class="elsevierStyleHsp" style=""></span>bp of the 28S ribosomal RNA &#40;D1&#8211;D3&#41; was obtained for all the sampled monogeneans&#44; and a phylogenetic analysis along with all available sequences of dactylogyrids was conducted to establish the systematic position of the species within the Ancyrocephalinae&#46; Our results suggest that species of <span class="elsevierStyleItalic">Haliotrema</span> might be included in <span class="elsevierStyleItalic">Haliotrematoides</span> genus&#46; In addition&#44; the genetic divergence data suggest that <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span> and <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span> may represent a species complex&#59; however&#44; this asseveration needs additional data&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Se estudiaron los monog&#233;neos que parasitan poblaciones silvestres de &#8220;pargos&#8221; o &#8220;huachinangos&#8221;&#44; <span class="elsevierStyleItalic">Lutjanus guttatus</span> &#40;Steindacher&#41; en 2 localidades de la costa del Pac&#237;fico mexicano &#40;Mazatl&#225;n&#44; Sinaloa y Bah&#237;a de Chamela&#44; Jalisco&#41;&#46; Se recolectaron 5 especies de dactylog&#237;ridos de las branquias de sus hospederos&#58; <span class="elsevierStyleItalic">Haliotrematoides guttati</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas et al&#46;&#44; 2008</a>&#41;&#44; <span class="elsevierStyleItalic">H&#46; plectridium</span> Kristky and Mendoza-Franco en <a class="elsevierStyleCrossRef" href="#bib0065">Kristky&#44; Tingbao&#44; and Yuan &#40;2009&#41;</a>&#44; <span class="elsevierStyleItalic">H&#46; spinatus</span> Kristky and Mendoza-Franco en <a class="elsevierStyleCrossRef" href="#bib0065">Kritsky et al&#46; &#40;2009&#41;</a>&#44; <span class="elsevierStyleItalic">Euryhaliotrema perezponcei</span><a class="elsevierStyleCrossRef" href="#bib0020">Garc&#237;a-Vargas&#44; Fajer-&#193;vila &#38; Lamothe-Argumedo&#44; 2008</a> and <span class="elsevierStyleItalic">E&#46; mehen</span> &#40;<a class="elsevierStyleCrossRef" href="#bib0125">Soler-Jim&#233;nez et al&#46;&#44; 2012</a>&#41;&#46; El material permiti&#243; observar la morfolog&#237;a en mayor detalle y comparar ejemplares de diferentes localidades aportando algunos caracteres morfol&#243;gicos a la descripci&#243;n de las especies&#46; Se obtuvo la secuencia de un fragmento de 856<span class="elsevierStyleHsp" style=""></span>bp del gen ribosomal 28S &#40;dominios D1 a D3&#41;&#44; de este modo se estableci&#243; la posici&#243;n sistem&#225;tica de &#233;stas&#44; en conjunto con las secuencias de otros dactylog&#237;ridos&#44; dentro de la filogenia de los Ancyrocephalinae&#46; Este an&#225;lisis revel&#243; que las especies de <span class="elsevierStyleItalic">Haliotrema</span> podr&#237;an incluirse en el g&#233;nero <span class="elsevierStyleItalic">Haliotrematoides</span>&#46; Asimismo&#44; los datos de divergencia gen&#233;tica sugieren que <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span> y <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span> podr&#237;an representar un complejo de especies&#44; aunque esto requiere ser verificado con datos adicionales&#46;</p></span>"
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Drawings of <span class="elsevierStyleItalic">Haliotrematoides guttati</span> from <span class="elsevierStyleItalic">Lutjanus guttatus</span> found in Chamela Bay&#44; Jalisco and Mazatl&#225;n&#44; Sinaloa&#44; Mexico&#46; 1&#44; dorsal anchor&#59; 2&#44; ventral anchor&#59; 3&#44; dorsal bar&#59; 4&#44; ventral bar&#59; 5&#44; hook&#44; male copulatory organ &#40;MCO&#41;&#46; All measurements are in micrometers&#46;</p>"
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          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Drawings of <span class="elsevierStyleItalic">Haliotrematoides plectridium</span> from <span class="elsevierStyleItalic">Lutjanus guttatus</span> found in Chamela Bay&#44; Jalisco and Mazatl&#225;n&#44; Sinaloa&#44; Mexico&#46; 7&#44; dorsal anchor&#59; 8&#44; ventral anchor&#59; 9&#44; dorsal bar&#59; 10&#44; ventral bar&#59; 11&#44; male copulatory organ&#46; All measurements are in micrometers&#46;</p>"
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Drawings of <span class="elsevierStyleItalic">Haliotrematoides spinatus</span> from <span class="elsevierStyleItalic">Lutjanus guttatus</span> found in Chamela Bay&#44; Jalisco and Mazatl&#225;n&#44; Sinaloa&#44; Mexico&#46; 12&#44; dorsal anchor&#59; 13&#44; ventral anchor&#59; 14&#44; dorsal bar&#59; 15&#44; ventral bar&#46; All measurements are in micrometers&#46;</p>"
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          "en" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Phylogenetic tree obtained through from maximum likelihood &#40;ML&#41; analysis based on the 28S sequences for selected dactylogyrid species&#44; with some species of diplectanids used as outgroups&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Monogenean&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Locality&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">CNHE&#47;USNPC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">GenBank&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleItalic">Haliotrematoides guttati</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Chamela Bay&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">8354&#47;106930&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleInterRef" id="intr0018" href="ncbi-n:KC663673">KC663673</span>&#8211;663674&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Mazatl&#225;n&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Chamela Bay&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">KC663675&#8211;KC663678&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">Mazatl&#225;n&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">7291&#47;&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top"><span class="elsevierStyleInterRef" id="intr0015" href="ncbi-n:HQ615995">HQ615995</span>&nbsp;\t\t\t\t\t\t\n
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          "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Dactylogyrid species reported in the present study from the gills of <span class="elsevierStyleItalic">Lutjanus guttatus</span> from Chamela Bay&#44; Jalisco and Mazatl&#225;n&#44; Sinaloa&#44; Mexico&#46; CNHE-Coleccion Nacion de Helmintos&#44; UNAM&#44; M&#233;xico&#46; USNPC &#8211; United States National Parasite Collection&#44; USA&#46;</p>"
        ]
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          "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Uncorrected pairwise distances of the partial sequences of the 28S rRNA gene among species analyzed from Chamela Bay&#44; Jalisco and Mazatl&#225;n&#44; Sinaloa&#44; Mexico&#46; Values are given as a percentage &#40;&#37;&#41;&#46;</p>"
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            0 => array:3 [
              "identificador" => "bib0005"
              "etiqueta" => "Blasco-Costa et al&#46;&#44; 2012"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Molecular phylogeny of <span class="elsevierStyleItalic">Ligophorus</span> &#40;Monogenea&#58; Dactylogyridae&#41; and their affinities within the family Dactylogyridae"
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                            3 => "J&#46;A&#46; Balbuena"
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                    0 => array:2 [
                      "doi" => "10.1016/j.parint.2012.06.004"
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                        "tituloSerie" => "Parasitology International"
                        "fecha" => "2012"
                        "volumen" => "61"
                        "paginaInicial" => "619"
                        "paginaFinal" => "627"
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              "identificador" => "bib0010"
              "etiqueta" => "Dang et al&#46;&#44; 2010"
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                    0 => array:2 [
                      "titulo" => "Some <span class="elsevierStyleItalic">Haliotrema</span> &#40;Monogenea&#58; Dactylogyridae&#41; from cultured grouper &#40;<span class="elsevierStyleItalic">Epinephelus</span> spp&#46;&#41; with emphasis on the phylogenetic position of <span class="elsevierStyleItalic">Haliotrema cromileptis</span>"
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                          "autores" => array:4 [
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                            3 => "G&#46;A&#46; Bristow"
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            2 => array:3 [
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              "etiqueta" => "Froese and Pauly&#44; 2014"
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                        "titulo" => "FishBase&#46; World Wide Web electronic publication"
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            3 => array:3 [
              "identificador" => "bib0020"
              "etiqueta" => "Garc&#237;a-Vargas et al&#46;&#44; 2008"
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                      "titulo" => "Two new species of Dactylogyridae &#40;Mongenoidea&#41; on rose spotted snapper&#44; <span class="elsevierStyleItalic">Lutjanus guttatus</span> &#40;Osteichthies&#58; Lutjanidae&#41;&#44; from the coasts of Nayarit&#44; Sinaloa&#44; Mexico"
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                      "titulo" => "Description of three new species of <span class="elsevierStyleItalic">Gyrodactylus</span> vonn Nordmann&#44; 1832 &#40;Monogenea&#41; parasitising <span class="elsevierStyleItalic">Oreochromis niloticus niloticus</span> &#40;L&#46;&#41; and <span class="elsevierStyleItalic">O&#46; mossambicus</span> &#40;Peters&#41; &#40;Cichlidae&#41;"
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            6 => array:3 [
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              "etiqueta" => "Hansen et al&#46;&#44; 2007"
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                        "tituloSerie" => "Trends in Parasitology"
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              "etiqueta" => "Huelsenbeck and Ronquist&#44; 2001"
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                      "titulo" => "The crossroads of molecular&#44; typological and biological species concepts&#58; Two new species of <span class="elsevierStyleItalic">Gyrodactylus</span> Nordmann&#44; 1832 &#40;Monogenea&#58; Gyrodactylidae&#41;"
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        "texto" => "<p id="par0210" class="elsevierStylePara elsevierViewall">We would like to thank the following people for the loan of specimens of <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">guttati</span>&#44; <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">plectridium</span> and <span class="elsevierStyleItalic">H</span>&#46; <span class="elsevierStyleItalic">spinatus</span>&#44; Eric Hoberg and Patricia Pilitt from United States National Parasite Collection&#44; Luis Garc&#237;a Prieto from the CNHE and Rosy Medina from the CPPNP&#59; to fishermen in Chamela Bay&#44; Jalisco&#44; Mazatl&#225;n and Sinaloa&#44; for their help to obtain the fish&#46; To Berenit Mendoza Garfias&#44; Rosario Briosio Aguilar&#44; Neptal&#237; Morales Serna&#44; Aline Rojas S&#225;nchez and Rosy Medina for their help during field work&#46; To Mart&#237;n Garc&#237;a Varela for his assistance with molecular analysis&#46; This work was partly supported by PAPIIT IN204514 to GPPL&#46; AGV thanks DGAPA-UNAM for a Postdoctoral scholarship&#46;</p>"
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Article information

ISSN: 18703453
Original language: English

DOI:10.1016/j.rmb.2015.04.027

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Year/Month	Html	Pdf	Total

2024 November	3	0	3
2024 October	11	3	14
2024 September	15	9	24
2024 August	31	3	34
2024 July	11	8	19
2024 June	11	2	13
2024 May	12	9	21
2024 April	6	1	7
2024 March	17	5	22
2024 February	16	8	24
2024 January	11	4	15
2023 December	8	11	19
2023 November	12	4	16
2023 October	37	3	40
2023 September	18	2	20
2023 August	4	2	6
2023 July	9	7	16
2023 June	8	9	17
2023 May	5	1	6
2023 April	6	5	11
2023 March	5	2	7
2023 February	14	5	19
2023 January	9	0	9
2022 December	21	4	25
2022 November	9	12	21
2022 October	12	7	19
2022 September	13	15	28
2022 August	19	8	27
2022 July	11	6	17
2022 June	7	5	12
2022 May	9	6	15
2022 April	13	8	21
2022 March	12	7	19
2022 February	10	4	14
2022 January	12	10	22
2021 December	6	6	12
2021 November	17	8	25
2021 October	11	15	26
2021 September	8	6	14
2021 August	14	3	17
2021 July	10	9	19
2021 June	6	2	8
2021 May	15	9	24
2021 April	37	9	46
2021 March	18	5	23
2021 February	7	6	13
2021 January	6	6	12
2020 December	8	5	13
2020 November	12	7	19
2020 October	6	6	12
2020 September	8	3	11
2020 August	18	3	21
2020 July	8	3	11
2020 June	10	1	11
2020 May	20	2	22
2020 April	13	6	19
2020 March	9	6	15
2020 February	10	2	12
2020 January	15	15	30
2019 December	10	3	13
2019 November	7	2	9
2019 October	13	2	15
2019 September	20	4	24
2019 August	8	2	10
2019 July	7	3	10
2019 June	30	10	40
2019 May	93	2	95
2019 April	38	13	51
2019 March	6	1	7
2019 February	4	2	6
2019 January	4	1	5
2018 December	1	2	3
2018 November	2	2	4
2018 October	3	12	15
2018 September	12	3	15
2018 August	11	3	14
2018 July	2	0	2
2018 June	8	1	9
2018 May	7	6	13
2018 April	15	1	16
2018 March	2	0	2
2018 February	3	2	5
2018 January	3	0	3
2017 December	5	0	5
2017 November	4	1	5
2017 October	6	4	10
2017 September	7	3	10
2017 August	8	3	11
2017 July	7	0	7
2017 June	14	34	48
2017 May	15	1	16
2017 April	2	8	10
2017 March	5	77	82
2017 February	11	10	21
2017 January	7	1	8
2016 December	20	6	26
2016 November	24	3	27
2016 October	32	7	39
2016 September	21	4	25
2016 August	11	1	12
2016 July	8	2	10

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