1. bookVolume 59 (2022): Edition 3 (September 2022)
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A phylogenetic assessment of nematodes (Oxyuroidea: Pharyngodonidae) infecting Moroccan lizards

O. Er-Rguibi,
O. Er-Rguibi,
D. J. Harris,
D. J. Harris,
A. Aglagane,
A. Aglagane,
E. M. Laghzaoui,
E. M. Laghzaoui,
L. Kimdil,
L. Kimdil,
A. Abbad et
A. Abbad et
E.H. El Mouden
E.H. El Mouden
Publié en ligne: 17 Dec 2022
Volume & Edition: Volume 59 (2022) - Edition 3 (September 2022)
Pages: 275 - 283
Reçu: 28 Mar 2022
Accepté: 19 Jul 2022
Helminthologia's Cover Image
Helminthologia
Détails du magazine
License
Format
Magazine
eISSN
1336-9083
Première parution
22 Apr 2006
Périodicité
4 fois par an
Langues
Anglais
Introduction

Defining, cataloguing, mapping and preserving biodiversity is generally accepted to be one of the key challenges for the 21st Century. The Kingdom of Morocco possesses the richest and most varied herpetofauna of the Maghreb and the western Mediterranean, is characterized by high richness of reptiles, endemism and European relict species (del Mármol et al., 2019). Phylogenetic analyses performed over recent decades have identified notable evolutionary lineages in the Moroccan herpetofauna, several of which represent new (cryptic) species or species complexes (e.g. Barata et al., 2012; Salvi et al., 2018), demonstrating the value of incorporating molecular tools into diversity assessments. Still, despite the well-known biodiversity of reptiles, parasite diversity associated with these hosts remains poorly known. Part of the problem in estimating parasite diversity has historically been that, especially for endoparasites, identification based on morphological characters and life-cycle traits is often difficult. Parasites often present a simplified morphology (Jorge et al., 2011), and while DNA sequencing approaches should help overcome these problems, molecular studies have lagged behind those of free-ranging organisms (Criscione et al., 2005). However, application of molecular tools is starting to show that some parasites currently considered as a single species actually consist of genetically different lineages or cryptic species (e.g. Jorge et al., 2012, 2013a).

Reptiles are parasitized by various helminth species, typically occurring in depauperate communities (Aho, 1990), possibly due to characteristics of the hosts such as the simplicity of the alimentary canal, their low vagility, a nonspecialized diet, and characteristics of the parasites such as direct life cycles (Roca & Hornero, 1994). Various studies have suggested that the typical helminth infection pattern in reptiles is that few species occur frequently, while many species are rare (Birlik et al., 2015). In studies of reptiles from the Iberian Peninsula and the North of Africa, helminth fauna of assessed lizards was poor, and mainly composed by members of the family Pharyngodonidae that are often detected in insectivorous reptiles (Chabaud & Golvan, 1957; Ibrahim et al., 2005; Carretero et al., 2011; Roca et al., 2020). These are usually identified on the basis of male morphology, since females are generally similar among species (Jorge et al., 2014). Although this family includes 21 genera, only a few of these are typically found in insectivorous lizards, with Spauligodon the most commonly reported (Roca et al., 2020).

Recent nematode surveys of reptiles in the Mediterranean region resulted in several new host records and descriptions of new species (Jorge et al., 2011, 2013a, 2014). Despite the high diversity of reptiles in Morocco, parasites from these hosts remain poorly studied, with a few incidental assessments as part of surveys at the Canary Islands (e.g. Jorge et al., 2011, 2018). In this sense, no survey including molecular data has been performed for nematodes of reptiles from Morocco. Indeed, with one or two exceptions (e.g. Carretero et al., 2011), there have been few molecular studies in nematodes from reptiles across the whole of the Maghreb. The aim of this study was to fill this gap, by assessing diversity of Pharyngodonidae nematodes from six lizard species from Morocco. By sequencing exemplars for two molecular markers (fragments of the 18S rRNA and Cytochrome Oxidase 1 gene), we aim to place these in a phylogenetic framework, to potentially identify cryptic forms, and to examine patterns of host-specificity.
Materials and Methods
Parasitological procedures

Helminths were collected from pellets, which were obtained through spontaneous defecation or by gentle abdominal massage of six lizard species: Chalcides mionecton, Chalcides montanus, Chalcides polylepis, Quedenfeldtia moerens, Quedenfeldtia trachyblepharus, and Tarentola mauritanica from Morocco (Table 1 and Fig. 1), between January 2019 to September 2021. These pellets were stored in 96 % ethanol. Faecal pellets were inspected for nematodes using a stereomicroscope. Specimens were mounted on temporary slides with a glycerol : water (1 : 1) solution, after which they were identified under a microscope, based on previous descriptions (Lucker, 1952; Skrjabin et al., 1967; Ashour et al., 1992; Amer & Bursey, 2008; Mašová et al., 2009; Pereira et al., 2017). All extracted specimens were photographed as a record. Further details regarding helminth collection and identification are given in Er-Rguibi et al. (2022).

Fig. 1

Map of Northern Morocco with the geographic locations of sampled nematodes. Their respective hosts species are in Table 1.

Fecal samples from which parasitic nematodes were recovered and included in the genetic analysis.

CodeNematode speciesHost speciesLocality18SCoI
26Spauligodon auziensisTarentola mauritanicaOunagha, Essaouira  
32Spauligodon auziensisTarentola mauritanicaDar Bouzza, CasaOP548559OP558784
111Spauligodon sp.Quedenfeldtia trachyblepharusOukaïmeden, MarrakechOP548558 
112Spauligodon sp.Quedenfeldtia trachyblepharusOukaïmeden, MarrakechOP548557 
131Spauligodon sp.Chalcides montanusOukaïmeden, MarrakechOP548556 
164Spauligodon sp.Quedenfeldtia trachyblepharusOukaïmeden, MarrakechOP548555 
205Spauligodon sp.Quedenfeldtia moerensFom Jrana, ChichaouaOP548554 
219Spauligodon sp.Quedenfeldtia trachyblepharusAit El Qaq, MarrakechOP548553 
234Spauligodon auziensisTarentola mauritanicaAït Aammour ou Ali, AzrouOP548552OP558785
283Spauligodon sp.Quedenfeldtia trachyblepharusAit El Qaq, MarrakechOP548551 
377Spauligodon sp.Quedenfeldtia trachyblepharusImlil, MarrakechOP548550 
1149Spauligodon auziensisTarentola mauritanicaAdmin Forest, AgadirOP548549 
1213Parapharyngodon micipsaeChalcides mionectonEl Ghazoua, EssaouiraOP548548 
1447Spauligodon sp.Quedenfeldtia moerensBigoudine, ArganaOP548547OP558786
1476Spauligodon sp.Chalcides polylepisOued Tensift, MarrakechOP548546OP558787
1480Thelandros alatusChalcides mionectonOued Tensift, MarrakechOP548545 
1550Thelandros alatusChalcides polylepisOued Tensift, MarrakechOP548544 
Genetic analysis

Extractions of genomic DNA were performed using individual nematodes, according to the saline method (Maia et al., 2014). Two partial genes were amplified: the nuclear 18S rRNA (18S) gene and the mitochondrial Cytochrome c Oxidase subunit I (COI). The COI fragment was amplified using the primers LCO and HCO from Folmer et al. (1994), while the 18S was amplified using Nem 18SF and Nem 18SR from Floyd et al. (2005). Polymerase chain reactions were performed in a total volume of 15 μl, consisting of PCR buffer at 1 × concentration; MgCl2 at 1.5 mM; dNTPs at a concentration of 0.2 mM for each nucleotide; primers at 0.5 μM each; BSA at 0.4 μg/μl (bovine serum albumin) (Roche Applied Science); and Taq DNA polymerase (Invitrogen Corporation) 0.025 units/μl and 1 μl of DNA template. PCR conditions were 35 cycles of: 30 sec at 94°C, 30 sec at 50 – 54°C and 1 min at 72°C, with an additional denaturation step of 3 min at 94°C and ending with a final extension at 72°C for 10 min. Successful amplified products, confirmed through electrophoresis, were cleaned and sequenced by a commercial facility (Gene Wiz, Germany).
Phylogenetic analysis

Sequences obtained were compared with those from GenBank using BLAST to confirm the taxonomic identity of the amplified products. Related sequences of Spauligodon, Parapharyngodon, and Thelandros published in previous studies and available in GenBank were included in the analyses. Sequences were aligned using MUSCLE alignment tool implemented in MEGA 10.1.8 with default parameters. The alignment lengths consisted of 595 bp (36 taxa) and 867 bp (47 taxa) for the CO1 and 18S respectively. Maximum likelihood was performed using PhyML 3.0 (Guindon & Gascuel, 2003) executed online (http://www.atgc-montpellier.fr/phyml/), both for defining the most appropriate model of molecular evolution under the AIC criterium, and to estimate a phylogeny. Branch support was estimated using bootstrap (Felsenstein, 1985) with 1000 replicates. The model selected in both cases was GTR+I+G. Phylogenies were also performed using Bayesian inference, implementing the most appropriate parameters according to the estimated models. Bayesian analyses were performed in MRBAYES 3.2.7a (Huelsenbeck & Ronquist, 2001) and run in duplicate for 10 × 106 generations with random starting trees, sampling every 1000 generations. The first 250 trees were discarded as ‘burn-in’, after verifying that stationarity was reached by plotting log-likelihood values against generation time. A 50 % majority-rule consensus tree was used to summarize the trees sampled from the post-burn-in trees. New sequences generated in this study were submitted to GenBank (Table 1).
Ethical Approval and/or Informed Consent

The research related to animal handling complied with all the relevant national regulations and institutional policies for the care and use of animals. The authorization for sampling of wild animals was granted by Cadi Ayyad University, Marrakech, Morocco. A field-work permit was issued by “Haut-Commissariat aux Eaux et Forêts et à la Lutte Contre la Désertification (HCEFLCD)”.
Results

Three different genera were identified using microscopy. Identification of Spauligodon was based on 125 adult specimens (81 females and 44 males). These were identified as small cylindrical nematodes, sexually dimorphic, with males approximately one quarter the length of female. Lateral alae present in male, absent in female. Anterior extremity tapered, mouth surrounded by 3 small lips, each with shallow midline indentation; dorsal lip with 2 sessile papillae, ventrolateral lips with 2 sessile papillae and 1 prominent lateral amphid. Identification of Paraphyngodon was based on 6 adult specimens (4 females and 2 males). These were identified as small nematodes, whitish in colour, males smaller than females, sexual dimorphism moderate. Body fusiform, cuticle with distinct transverse striations beginning just behind the cephalic extremity and continuing to the anus. In males, lateral alae well developed, initiating anteriorly somewhere at the level of bulbus and extending posteriorly to last third of body. Oral opening subtriangular, surrounded by three lips, in female separated into six parts. Identification of Thelandros was based on 104 adult specimens (80 females and 24 males). These were identified as robust nematodes with prominent annulations beginning just behind cephalic extremity and continuing to anus. Cuticle with distinct longitudinal striations approximately 4 apart. Moderate sexual dimorphism. Triangular oral opening surrounded by 3 bilobed lips, 1 small pedunculate amphid on each ventrolateral lobe. Lateral alae absent. Males without caudal alae; caudal filament terminal, directed posteriorly. Females with vulva post equatorial. We followed Hering-Hagenbeck et al. (2002), considering Parapharyngodon distinct from Thelandros for the following reasons: Males of Thelandros have a genital cone, pendulant papillae outside the genital cone, lateral alae are absent, and the tail is terminal and directed posteriorly; males of Parapharyngodon lack a genital cone, mammiliform papillae surround a more-or-less terminal anus, lateral alae are present, and the tail is subterminal and directed dorsally.

Following previous descriptions (Lucker, 1952; Skrjabin et al., 1967; Ashour et al., 1992; Amer & Bursey, 2008; Mašová et al., 2009; Pereira et al., 2017; Er-Rguibi et al., 2022) samples from hosts of the genus Chalcides were identified as Thelandros alatus or Parapharyngodon micipsae. All other samples were identified as belonging to the genus Spauligodon. Of these, only Spauligodon auziensis from Tarentola mauritanica hosts could be identified to the species level. Sixteen of 17 nematode specimens had their 18S rRNA successfully sequenced. Based on the estimate of phylogeny derived from 18S rRNA sequences (Fig. 2), the species of Spauligodon formed a highly distinct clade. Within this, some forms could be distinguished, including S. nicolauensis from the Cape Verde islands, S. auziensis from the hosts T. mauritanica, and a group from hosts of the genus Chalcides (C. montanus, C. ocellatus and C. polylepis). However, several specimens from the geckos Quedenfeldtia moerens and Quedenfedtia trachyblepharus were identical for this region, and also identical to sequences from GenBank of both Spauligodon saxicolae and Spauligodon carbonelli. The sample identified as P. micipsae was sister taxa to P. micipsae from Gallotia caesaris from the Canary Islands. Thelandros was not a monophyletic group, although some estimates of relationships were poorly supported. Considering the CO1 marker, only 4 samples (all Spauligodon) were successfully amplified. Based on this more variable marker (Fig. 3) two samples from Tarentola mauritania hosts were apparently S. auziensis, related to other specimens from this host species. A specimen from Quedenfeldtia was distinct from all comparative sequences, but with poorly supported relationships. The remaining sample from a Chalcides polylepis host formed a distinct lineage with another Spauligodon sp. from a Chalcides sp. host, also from Morocco. These together were sister taxa to S. nicolauensis, from the Cape Verde islands.
Discussion

In principle, the geographic distribution of parasite diversity is predicted to match that of host diversity (Jorge & Poulin, 2018). Under this expectation, Morocco with its high diversity of reptile species should also harbor extensive nematode diversity within these hosts. However, this diversity remains essentially unassessed. In this study, we made a preliminary assessment of nematodes in pellets from six reptile host species. While it is known that there is a significantly lower detectability of nematodes from pellets compared to studies of intestines (Jorge et al., 2013b), this noninvasive approach can be used to give some baseline data on the parasites occurring in reptiles in this region.

As expected, the nematodes identified all belonged to three genera, Parapharyngodon, Thelandros and Spauligodon, which are typically identified within insectivorous reptiles (e.g. Mašová et al., 2009; Carretero et al., 2011; De Sousa et al., 2018). Exact relationships between these, and even the monophyly of these genera, has been widely debated (e.g. De Sousa et al., 2018; Pereira et al., 2018).

Fig. 2

Estimate ot relationships derived from the 18S rRNA gene sequences using a Bayesian approach. Values above branches represent Bayesian posterior probabilities and those below represent ML bootstrap support values (both given as percentages). Specimen code descriptions are given in Table 1. * These samples are considered as belonging to Patapharyngodon following de Sousa et al. (2018), but are listed on GenBank as Thelandros

Fig. 3

Estimate of relationships derived from the CO1 mitochondrial gene sequences using a Bayesian approach. Values above branches represent Bayesian posterior probabilities and those below represent ML bootstrap support values (both given as percentages). Specimen code descriptions are given in Table 1.

Using universal 18S rRNA primers, we were able to amplify and sequence a region of this gene for all but one of our samples. The specimens of Spauligodon from Morocco fell into three distinct lineages, reflecting the reptile hosts they were recovered from. Seven specimens of Spauligodon from the geckos Quedenfeldtia moerens and Quedenfedtia trachyblepharus were identical for the 18S rRNA region, and also identical to sequences from Gen-Bank of Spauligodon saxicolae and Spauligodon carbonelli, that had been recovered from lacertid lizards in the Iberian Peninsula and Turkey (Jorge et al., 2011, 2014). Three samples of Spauligodon from the gecko Tarentola mauritanica were also identical, to Spauligodon auziensis previously recovered from T. mauritanica from central Morocco (Jorge et al., 2011, 2018). The two samples of Spauligodon from the skinks Chalcides polylepis and Chalcides montanus were related to Spauligodon sp., also from skinks Chalcides ocellatus, from Sardinia (Jorge et al., 2018).

While the distinction of Spauligodon was evident in our analysis of 18S rRNA, the separation of Parapharyngodon was more complex. Although molecular data does support distinction of this genus relative to Thelandros, many species have not been included in analyses. Pereira et al. (2018), using an integrative approach, proposed a clear separation between Thelandros and Parapharyngodon, but included only one representative species of Thelandros in the molecular phylogeny. De Sousa et al. (2018) also indicated that Parapharyngodon was distinct from Thelandros collected from the Canary Islands and Cape Verde islands, but that from Gallotia lizards previously considered Thelandros galloti should be reassigned to Parapharyngodon, as P. galloti. They further suggested that preliminary morphological assessments supported this reassignment, for example since this species lacks caudal alae and has long and wide lateral alae, both typical characteristics of Parapharyngodon (Astasio-Arbiza et al., 1988). On the other hand, P. galloti males had wider alae and longer oesophagus than representatives of Parapharyngodon, highlighting the difficulties of assigning these species to the appropriate genus without molecular data. Abdel-Ghaffar et al. (2020) recently described a new species as Thelandros chalcidiae from Chalcides ocellatus in Egypt. Based on 28S rRNA sequence data, they showed it was closely related to P. galloti (still considered as a member of Thelandros) and Parapharyngodon micipsae. In our analysis, we identified a Parapharyngodon sp. from Chalcides mionecton. Based on morphological aspects, it was considered to be P. micipsae, a species found in many different reptile hosts including lacertids (Martin & Roca, 2004), skinks (Ibrahim et al., 2005), geckos (Mašová et al., 2009) and agamas (Elmahy & Harras, 2019). Following the 18S rRNA analysis, this was closely related to P. micipsae from Gallotia lizards from the Canary Islands (De Sousa et al., 2018), and then P. galloti and P. echinatus. That T. chalcidiae is also closely related to P. galloti shows how difficult it is to assign species to the different genera based on morphological characters. Highlighting the diversity of nematodes found in Chalcides skinks, in another C. mionecton and Chalcides polylepis, representatives of Thelandros were identified, which we considered as T. alatus based on morphological characters, the type species of Thelandros. Based on the 18S rRNA analysis, these were distinct from Parapharynogodon, but also from Thelandros tinerfensis from Tarentola gomerensis hosts in the Canary Islands, thus making Thelandros paraphyletic. Overall, representatives of Spauligodon, Thelandros and Parapharyngodon were identified in Chalcides skinks in Morocco, but which species of Spauligodon is still unclear.

Although we only obtained 4 sequences from Spauligodon species using the CO1 primers, the estimate of phylogenetic relationships derived from this gene is still highly informative (Fig. 3). Unlike with the more conservative 18S rRNA sequences, all Spauligodon species could be distinguished with this marker, and intra-specific variation identified. Two samples from T. mauritanica again grouped with samples identified as S. auziensis. Intraspecific variation within S. auziensis was high, up to 12.6 % uncorrected sequence divergence, although all the samples were collected from the same host species. One specimen from Quedenfeldtia moerens was highly distinct from all other comparative sequences, but relationships of this from were poorly supported. Specimens of Spauligodon were recently identified in Quedenfedtia trachyblepharus (Er-Rguibi et al., 2021), and the results of this study demonstrate that they are genetically distinct from other known Spauligodon species. The fourth specimen, from C. polylepis, was found to be sister taxa to another Spauligodon sp., also from a Chalcides sp., and these in turn were related to Spauligodon nicolauensis from the Cape Verde islands.

To conclude, our new data clarifies several aspects regarding the presence of nematodes in reptiles from Morocco. Each lineage of parasite is quite specific to a related group of hosts, with S. auziensis in Tarentola mauritanica, another lineage in both species of Quedenfeldtia, another only in species of Chalcides, and another previously identified lineage from Podarcis vaucheri. While the universal 18S primers employed successfully amplified almost all samples, variation was too low to distinguish between some accepted species, while the CO1 region showed much greater variation. While classification of species to Spauligodon is relatively straightforward, some species considered as Thelandros may be better reassigned to Parapharyngodon, highlighting the difficulty of distinguishing between these genera using morphological characters. Other markers, such as 28S rRNA, and improved primers for amplifying CO1 across additional species, may help resolve some of these taxonomic issues. Several lineages of Spauligodon, particularly those from Chalcides and possibly also from Quedenfeldtia hosts form divergent lineages and probably warrant consideration as full species, pending detailed morphological assessments. This highlights the undescribed diversity within Morocco and the Maghreb region, and the need for additional surveys of this poorly known parasite fauna.

Fig. 1

Map of Northern Morocco with the geographic locations of sampled nematodes. Their respective hosts species are in Table 1.
Map of Northern Morocco with the geographic locations of sampled nematodes. Their respective hosts species are in Table 1.

Fig. 2

Estimate ot relationships derived from the 18S rRNA gene sequences using a Bayesian approach. Values above branches represent Bayesian posterior probabilities and those below represent ML bootstrap support values (both given as percentages). Specimen code descriptions are given in Table 1. * These samples are considered as belonging to Patapharyngodon following de Sousa et al. (2018), but are listed on GenBank as Thelandros
Estimate ot relationships derived from the 18S rRNA gene sequences using a Bayesian approach. Values above branches represent Bayesian posterior probabilities and those below represent ML bootstrap support values (both given as percentages). Specimen code descriptions are given in Table 1. * These samples are considered as belonging to Patapharyngodon following de Sousa et al. (2018), but are listed on GenBank as Thelandros

Fig. 3

Estimate of relationships derived from the CO1 mitochondrial gene sequences using a Bayesian approach. Values above branches represent Bayesian posterior probabilities and those below represent ML bootstrap support values (both given as percentages). Specimen code descriptions are given in Table 1.
Estimate of relationships derived from the CO1 mitochondrial gene sequences using a Bayesian approach. Values above branches represent Bayesian posterior probabilities and those below represent ML bootstrap support values (both given as percentages). Specimen code descriptions are given in Table 1.

Fecal samples from which parasitic nematodes were recovered and included in the genetic analysis.

Code Nematode species Host species Locality 18S CoI
26 Spauligodon auziensis Tarentola mauritanica Ounagha, Essaouira    
32 Spauligodon auziensis Tarentola mauritanica Dar Bouzza, Casa OP548559 OP558784
111 Spauligodon sp. Quedenfeldtia trachyblepharus Oukaïmeden, Marrakech OP548558  
112 Spauligodon sp. Quedenfeldtia trachyblepharus Oukaïmeden, Marrakech OP548557  
131 Spauligodon sp. Chalcides montanus Oukaïmeden, Marrakech OP548556  
164 Spauligodon sp. Quedenfeldtia trachyblepharus Oukaïmeden, Marrakech OP548555  
205 Spauligodon sp. Quedenfeldtia moerens Fom Jrana, Chichaoua OP548554  
219 Spauligodon sp. Quedenfeldtia trachyblepharus Ait El Qaq, Marrakech OP548553  
234 Spauligodon auziensis Tarentola mauritanica Aït Aammour ou Ali, Azrou OP548552 OP558785
283 Spauligodon sp. Quedenfeldtia trachyblepharus Ait El Qaq, Marrakech OP548551  
377 Spauligodon sp. Quedenfeldtia trachyblepharus Imlil, Marrakech OP548550  
1149 Spauligodon auziensis Tarentola mauritanica Admin Forest, Agadir OP548549  
1213 Parapharyngodon micipsae Chalcides mionecton El Ghazoua, Essaouira OP548548  
1447 Spauligodon sp. Quedenfeldtia moerens Bigoudine, Argana OP548547 OP558786
1476 Spauligodon sp. Chalcides polylepis Oued Tensift, Marrakech OP548546 OP558787
1480 Thelandros alatus Chalcides mionecton Oued Tensift, Marrakech OP548545  
1550 Thelandros alatus Chalcides polylepis Oued Tensift, Marrakech OP548544  

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