Abstract
Purpose
The molecular profile of specimens of Mediorhynchus gallinarum (Bhalero, 1937) collected from chickens, Gallus gallus L. in Indonesia was analysed. The aim of this study was to assess the phylogenetic position of species of Mediorhynchus within the order Giganthorhynchida.
Methods
We used one mitochondrial gene (cytochrome oxidase 1) and one nuclear gene (18S ribosomal RNA) to infer phylogenetic relationships of class Archiacanthocephala.
Results
The COI and 18S rDNA genes sequences showed that M. gallinarum had low genetic variation and that this species is sister to Mediorhynchus africanus Amin, Evans, Heckmann, El-Naggar, 2013. The phylogenetic relationships of the Class Archiacanthocephala showed that it is not resolved but, however, were mostly congruent using both genes. A review of host-parasite life cycles and geographic distributions of Archiacanthocephala indicates that mainly small mammals and birds are definitive hosts, while termites, cockroaches, and millipedes are intermediate hosts.
Conclusions
While the intermediate hosts have wide geographic distributions, the narrow distribution of the definitive hosts limit the access of archiacanthocephalans to a wider range of prospective hosts. Additional analyses, to increase taxonomic and character sampling will improve the development of a robust phylogeny and provide more stable classification. The results presented here contribute to better understanding of the ecological and evolutionary relationships that allow the host-parasite co-existence within the class Archiacanthocephala.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Definitive hosts of Archiacanthocephala have been described as strictly terrestrial [1] and include hedgehogs, marsupials, rodents, carnivores and several orders of birds [1,2,3,4,5,6,7,8]. Archiacanthocephalans use invertebrates such as millipedes, termites and cockroaches [9,10,11,12,13] as intermediate hosts. Even when there are several species descriptions and ecological aspects of their natural history, the understanding of archiacanthocephalan evolution has not benefited from extensive usage of molecular data in phylogenetic analyses as is the case of the classes Palaeacanthocephala Meyer, 1931 and Eoacanthocephala Van Cleave, 1936 [14,15,16,17,18]. As such, relationships among members of Archiacanthocephala remain mostly unclear [1, 19,20,21].
The class Archiacanthocephala is composed of four orders and four families [22] including the family Gigantorhynchidae Hamman, 1982. The genus Mediorhynchus is one of the most diverse genera within that family. It encompasses 57 species [22] that have been mainly found in Africa and Asia. Species of Mediorhynchus use cockroaches as intermediate hosts and birds belonging to distinct orders, such as Accipitriformes, Bucerotiformes, Charadriiformes, Falconiformes, Galliformes and Passeriformes, as definitive hosts [19, 23,24,25,26]. Phylogenetic analyses indicate that Mediorhynchus is monophyletic [19], but studies centered on Gigantorhynchida or Archiacanthocephala are still scarce [19, 20, 27].
Specimens of Mediorhynchus gallinarum (Bhalerao, 1937) are parasites of the chicken Gallus gallus L. in diverse Asian areas, including Borneo (Indonesia), Palawan (Philippines) and India [27]. Specimens of M. gallinarum typically attach to the intestinal lining causing histological and metabolic changes [27]. Morphologically, M. gallinarum is characterized by a cylindrical, non-segmented trunk with few sensory pits. The proboscis has no apical pores and the posterior end of the female is pointed with a terminal gonopore. The proboscis armature is composed of 18–22 longitudinal rows of 5–6 hooks each on its anterior part and 30–34 longitudinal rows of 2–6 spine-like hooks each on its posterior area [19, 27]. Eggs measure 47–57 × 24–32 μm. Previous studies indicated that M. gallinarum is sister to M. africanus Amin, Evan, Heckmann and El-Naggar, 2013 and that both allopatric species present low divergence. However, this relationship was inferred based on only one individual of M. gallinarum [19].
The aim of this study is to further assess the phylogenetic position of Mediorhynchus gallinarum within the clade of Giganthorhynchida; our taxonomic sampling also allowed us to test relationships within Archiacanthocephala. To put our findings into perspective, we also discuss ecological relationships and global distribution of intermediate and definitive hosts of the class Archiacanthocephala.
Materials and Methods
Sampling
Specimens of Mediorhynchus gallinarum were collected from 46 Isa brown chickens (Gallus gallus) from 2 different poultry farms located in the Kaliurang Sleman district, Daerah Istimewa Yogyakarta, Indonesia (107º 15′ 03′′ E–7º 34′ 51′′ S; 107º 29′ 30′′ E–7º 47′ 30′′ S). These poultry farms are situated in an open rural environment, where the chickens were maintained in extensive well-managed settings (More details, to read [27]. In 1 farm 26 chickens were examined, while in the other farm 20 were surveyed. Collected specimens were refrigerated for 2 days and then fixed in 70% ethanol.
Molecular Analysis
Genetic comparisons and phylogenetic analyses were based on DNA sequences of the mitochondrial cytochrome oxidase I (COI) gene and the nuclear 18S rDNA gene. Six Indonesian specimens of Mediorhynchus gallinarum were analyzed. Four samples were digested overnight at 55 °C and genomic DNA was isolated using a commercial extraction kit (Wizard® Genomic DNA Purification Kit, Promega, Madison, Wisconsin). A fragment of 620 bp of the COI gene was amplified using the primers detailed by Folmer et al. [28] following the protocol of Amin et al. [27]. Amplicons were sequenced using an external sequencing service (Macrogen Inc., Seoul, South Korea). Two other samples were used to acquire 18S rDNA sequences. Genomic DNA from individual worms was extracted using Qiagen DNeasy tissue kit (Qiagen Inc., Valencia, California, USA) according to manufacturer’s instructions. PCR reactions were performed in 30 μL volumes containing 2 × red PCR premix (Ampliqon, Odense, Denmark), 20 pmol of each primer and 3 μL of extracted DNA. A 809 bp fragment of the partial 18S rRNA gene was amplified using the primers MGF (5′-GATCGGGGAGGTAGTGACG-3′) and MGR (5′-ACCCACCGAATCAAGAAAGAG-3′). PCR conditions for 18S rDNA gene amplification included of an initial denaturing step of 95 °C for 5 min and 35 cycles followed by denaturing step at 94 °C for 30 s, annealing step of 59 °C for 30 s, and 30 s of extension at 72 °C, and 72 °C for 5 min as a final extension. PCR products were analysed on 1.5% agarose gel and visualized with UV transluminator. Next, the PCR products were sequenced in both directions using the same PCR primers with ABI 3130 sequencer. All DNA sequences were edited using Codon-Code (Codon Code Aligner, Dedham, Massachusetts) and deposited in GenBank (OK094072–OK094075; MW282174–MW282175).
The four new COI sequences were integrated to a matrix with all sequences of members of Archiacanthocephala available in GenBank. Downloaded sequences include one of Mediorhynchus gallinarum, M. africanus and Mediorhynchus sp. together with one sequence of Oligacanthorhynchus tortuosa (Leidy, 1850), one of Nephridiacanthus major (Bremser, 1811 in Westrumb, 1821), two of Prosthenorchis Travassos, 1915 (P. elegans (Diesing, 1851) and Prosthenorchis sp.), three of Oncicola Travassos, 1916 (Oncicola luehei (Travassos, 1917) and Oncicola sp.), and five of Macracanthorhynchus Travassos, 1917 (M. ingens (von Linstow, 1879) and M. hirudinaceus (Pallas, 1781)) (Oligacanthorhynchidae). In addition, four sequences of Moniliformis Travassos, 1915 (M. kalahariensis Meyer, 1931; M. moniliformis (Bremser, 1811), Moniliformis sp.) (Moniliformidae) and one sequence of Mayarhynchus karlae Pinacho-Pinacho, Hernández-Orts, Sereno-Uribe, Pérez-Ponce de León, García-Varela, 2017 class Eoacanthocephala and one of Heterosentis holospinus Amin, Heckmann and Ha, 2011 and Profilicollis altmani (Perry, 1942) (Palaeacanthocephala), were also downloaded and used as outgroup (Table 1). As such, the analyzed matrix has a total of 26 sequences.
Sample size for the 18S rDNA gene was slightly smaller than for COI, including the 2 new sequences of M. gallinarum and 15 sequences of members of Archiacanthocephala available in GenBank including one sequence of M. gallinarum, M. africanus, M. grandis and Mediorhynchus sp. together with one sequence of Intraproboscis sanghae Amin, Heckmann, Sist and Basso, 2021. One of O. tortuosa, N. major, M. ingens, M. hirudinaceus and Oncicola sp, and five sequences of Moniliformis (two of M. moniliformis, and one of M. kalahariensis, M. cryptosaudi and M. saudi). Finally, one sequence of Neoechinorhynchus agilis (Rudolphi, 1819) (Eoacanthocephala) and one of Echinorhynchus truttae Schrank, 1788 (Palaeacanthocephala) were used as outgroup (Table 1). As such, the analyzed matrix has a total of 19 sequences.
Sequences were aligned in Clustal as implemented in MEGA 7 [29] using default parameter values. Observed genetic p-distances (p) between haplotype and sample pairs were calculated in MEGA 7. IQ-TREE [30] was used to select the model of nucleotide substitution for each matrix (TPM3 + G4). Two methods of phylogenetic inference were implemented, Maximum Likelihood (ML) and Bayesian inference (BI) for each matrix. The ML analysis was conducted with IQ-TREE using the online implementation W-IQ-TREE (http:/iqtree.cibiv.univie.ac.at; [31]), with perturbation strength set to 0.5 and stopping rule set to 100. Clade support was calculated with 1000 ultrafast bootstrap pseudo-replications (BS). The BI analysis was conducted with MrBayes 3.1 [32]. Two independent runs with 4 heated and 1 cold Markov chains each were run for 20 million generations, with trees sampled every 1000 generations. Model parameters were estimated in MrBayes. Convergence to stable log-likelihood values was checked by plotting log-likelihood values against generation time. The first 25% of the trees sampled were discarded as burn-in; remaining trees were used to compute a 50% majority rule consensus tree and to obtain posterior probability (PP) values for each clade.
Results
Both phylogenetic trees gathered via ML and BI for COI were mostly congruent. Archiacanthocephala was found to be monophyletic and with high support (PP = 1; BS = 93; Fig. 1A). Within the archiacanthocephalan clade, two of three orders were found monophyletic. One of these is Gigantorhynchida, whose members form a moderately supported clade (PP = 0.71; BS = 72); the other is Moniliformida that appears well supported (PP = 0.99; BS = 85). Meanwhile, the family Oligacanthorhynchidae was not proven monophyletic. Oligacanthorhynchid genera fall into two main lineages. One corresponds to a clade (PP = 0.85; BS = 80) formed by all oligacanthorhynchid genera except Oligacanthorhynchus (Fig. 1A); the other lineage is formed solely by Oligacanthorhynchus. Both oligacanthorhynchid main lineages form together with Moniliformidae a trichotomy at the base of a large clade (PP = 0.89; BS = 66), which is sister to Gigantorhynchidae. As such, one of the three possible resolutions of the mentioned trichotomy implies recovering a monophyletic Oligacanthorhynchidae. All species for which more than one sequence was analysed appear monophyletic and with good support. Similarly, all recovered genera are monophyletic. The exception being Macracanthorhynchus that is paraphyletic relative to Nephridiacanthus. Macracanthorhynchus ingens is sister (PP = 1; BS = 99) to Nephridiacanthus major and not to M. hirudinaceus.
Within Gigantorhynchidae sequences of M. gallinarum showed two distinct haplotypes (haplotype I: OK094073 - OK094075 - OK094072; haplotype II: OK094074) with extremely low genetic difference (0.2%) and that form a strongly supported monophyletic group (PP = 1; BS = 100), which is sister to M. africanus in a moderately supported clade (PP = 0.78; BS = 80). Haplotypes of both species differ by 25%. The clade formed by M. gallinarum and M. africanus is sister to Mediorhynchus sp. in a moderately supported clade (PP = 0.71; BS = 72); sequences of Mediorhynchus sp. differ on the average by 28% (Fig. 1). On the average, sequences of Gigantorhynchidae differ by 30% and 29% relative to the families Moniliformidae and Oligacanthorhynchidae, respectively. Other observed values of genetic differences are shown in Table 2.
The resulting ML and BI trees for 18S rDNA are less resolved than the COI trees (Fig. 1B). Archiacanthocephala was demonstrated to be monophyletic (PP = 0.83; BS = 89) and with a large polytomy at its base that involves seven lineages. One of these is the weakly supported clade of Oligacanthorhynchidae (PP = 0.6; BS = 51), which is the single family found monophyletic. Within this family Oligacanthorhynchus tortuosa is sister to a clade (PP = 0.95; BS = 79) formed by Nephridiacanthus major, Macracanthorhynchus hirudinaceus, M. ingens and Oncicola sp. Then, the family Gigantorhynchidae was not found monophyletic but forming two lineages involved in the basal polytomy. One corresponds to a clade formed by all species of Mediorhynchus (PP = 0.97; BS = 47) and the other is formed solely by Intraproboscis sanghae (Fig. 1B) formed by Mediorhynchus sp. and M. grandis that are sister to each other (PP = 1; BS = 92), while M. africanus is sister (PP = 0.56; BS = 44) to M. gallinarum (Fig. 1B). Finally, the family Moniliformidae was not found monophyletic; four moniliformid lineages fall to the polytomy at the base of the Archiacanthocephala clade; one of these is Moniliformis saudi, another is M. moniliformis, the third is M. kalahariensis, and the last lineage is M. cryptosaudi (Fig. 1B).
Discussion
Our molecular analysis showed that Mediorhynchus gallinarum, a parasite of G. gallus from Indonesia, exhibits extremely low-level of genetic variation. Analysed haplotypes differ on average by 0.1%. We note however, that our analysed sample is small and that all specimens were collected at a single locality (a farm in this case), therefore the low level of genetic variance is not unexpected. Additional analyses should further assess the level and pattern of the genetic variation of M. gallinarum. The low divergence value found for M. gallinarun is in line with those reported for other acanthocephalans. For example, low genetic diversity has been found within species of the genera Andracantha Schmidt, 1975; Corynosoma Lühe, 1904; Profillicollis Meyer, 1931 and Heterosentis Van Cleave, 1931 [17, 18, 33,34,35]. The drivers behind those low levels of divergence are so far unclear. Further studies would clarify the effect of this pattern, if any, of the particularities of their natural history, including strict parasite-environmental links and specific host-parasite relationships [17, 34, 35].
Mediorhynchus gallinarum is highly divergent from the analysed congenerics M. africanus (25%) and Mediorhynchus sp. (28%). This result strongly supports the distinction at the species level of M. africanus from gallinarum, which was questioned by various authors since 1932 [19]. Later, molecular studies on Mediorhynchus by Amin et al. [19, 27] showed that specimens from chicken from Indonesia (M. gallinarum) are distinct from those recovered from African birds (M. africanus). In this study, we corroborate those results showing that both species are genetically highly divergent.
Both analyses show that phylogenetic relationships into the Class Archiacanthocephala are not fully resolved. For example, the resulting COI tree showed that the family Oligacanthorhynchidae is not monophyletic (Fig. 1A). Genera of this family fall in two main lineages; one formed by the genera Macracanthorhynchus, Nephridiacanthus, Oncicola, and Prosthenorchis, and the other by Oligacanthorhynchus, the type genus. In contrast, the resulting 18S rDNA tree showed that the family Oligocanthorhynchidae is monophyletic (Fig. 1B). This result needs to be further explored as the lack of monophyly may be due to the short sequence fragment analysed not having enough information to resolve some relationships. We also note that our sampling of oligocanthorhynchid is incomplete as samples of six genera were not included; as such, the monophyly of the family should be further tested with broader taxonomic sampling. Having said that, we note that the systematics of Acanthocephala is still unstable; most groups have been proposed on the basis of morphological trenchant characters and have not been tested with an explicit phylogenetic approach [15, 33, 36]. Even for the classification of the class Palaeacanthocephala, which has been the focus of diverse studies based on morphological and molecular data, several authors suggested that it still needs adjustments due to the lack of monophyly in some families [14, 16,17,18]. These conclusions agree with our findings regarding Oligacanthorhynchidae. Due to the lack of molecular data available for several members of Archiacanthocephala, our finding should be regarded as preliminary. Future studies, including a wider taxonomic and character sampling should generate a robust phylogeny that would be the basis for a more stable classification of the Archiacanthocephala.
Host-Parasite Relationships and Distribution (Fig. 2)
A high degree of host specificity has been reported for Mediorhynchus [25, 37]. Adult specimens of M. gallinarum are commonly found in chickens of the family Phasianidae from diverse Asian locations [27]. In contrast, adults of M. africanus are mostly found in birds of the families Numididae and Phasianidae from Africa [19]. However, most of the other species of Mediorhynchus use as definitive hosts passeriform birds from diverse continents [23,24,25]. Species of termites and cockroaches have been reported as intermediate hosts [23]. Aspects such as the vagility and capacity of migration of definitive hosts have been indicated as having a direct effect on the genetic variation of acanthocephalans [34, 35, 38]. In addition, narrow host-parasite relationships could be related to low presence of intermediate or paratenic hosts, that accumulate the infective stage and also, probably, limits the accessibility to a wide range of predators [25, 37].
For parasites belonging to the family Moniliformidae, host-parasite relationships seem to be even stricter. Mammals have been identified as definitive hosts including the family Erinaceidae from Africa and Asia, the giant anteater, primates, and rodents mainly from South America, and occasionally birds [1, 2, 4, 39]. Intermediate hosts are mostly cockroaches [1, 4]. Morphologically cryptic species of Moniliformis, which are basically differentiated genetically [18], differ in their hosts; Moniliformis saudi Amin, Heckman, Mohammed and Evans, 2016 parasites the desert hedgehog Paraechinus aethiopicus (Ehrenberg, 1832) from Saudi Arabia [4], while, M. cryptosaudi Amin, Heckmann, Sharifdini, Albayati, 2019 parasitizes the long-eared hedgehog Hemiechinus auritus (Gmelin, 1770) in Iraq [18]. Cases of cryptic speciation have been commonly suggested for acanthocephalans in distinct classes [35, 38,39,40]. These authors concluded that their genetic variation, in part, could be explained likely by environmental influences together with host specificity [35, 38, 40].
The family Oligacanthorhynchidae is the most diverse of Archiacanthocephala [22]. Hosts reported for members of this family such as Oligacanthorhynchus tortuosa, include the Virginia opossum Didelphis virginiana Allen, 1900 and the millipede Narceus amaricanus (Palisot de Beauvois, 1817) as intermediate host [11]. Raccoons, Procyon lotor Linnaeus, 1758 from USA and Bassariscus astutus (Lichtenstein, 1830) from Nicaragua are the definitive hosts of Macracanthrohynchus ingens, while its intermediate host is the millipede Chicobolus spinigerus (Wood), 1864 from USA [7, 11]. Macracanthrohynchus hirudinaceus has been reported parasitizing the wild boar Sus scrofa from Iran, Japan and USA and beetles of the family Scarabaeidae family are the intermediate hosts [41,42,43]. For Nephridiacanthus major, the erineaceid long-eared hedgehog Hemiechinus auritus was reported as definitive host in Iran [20], while the intermediate hosts are beetles of the family Tenebrionidae and cockroaches [20].
The definitive hosts of the genus Oncicola are small mammals. For example, adult O. luehei parasiteze the opossum D. virginiana and the coatis Nasua narica (Linnaeus, 1766) distributed in North, Central and South America [44]. For other species of Oncicola, other mammals like the feral cat Felis catus Linnaeus, 1758, the Indian mangoose Herpestes auropunctatus Hodgson, 1836, the foxes Vulpes vulpes Linnaeus, 1758 from Lebanon and the ocelot Leopardus pardalis Linnaeus, 1758 were reported as definitive hosts, and the Caribbean termite Nasutitermes acajutlae (Holmgren) as the intermediate host [8,9,10, 12, 48]. Additionally, lizards, African green monkeys and birds serve as paratenic hosts for species of Oncicola [8, 9].
Acanthocephalans of the genus Prosthenorchis have been reported parasitizing neotropical primates, mainly individuals of the family Callitrichidae, distributed in the Brazilian Atlantic forest and Colombia [5, 6, 45]. Also, adult specimens have been collected from lemurs in Madagascar and vertebrates belonging to the family Felidae in Africa [49, 50]. Likewise, individuals of this genus have been reported in primates of the neotropical origin housed at a zoo collection in Moscow, and the larvae were found in cockroaches Blattela germanica, captured around primate cages [46]. In general, species of Blattodea and Coleoptera contains the larval stages of Prosthenorchis [5, 46, 47]. Other members of this family such as adults of Tchadorhynchus sp. have been reported in Hyaena hyaena (Linnaeus, 1758) from Africa [49]. Individuals of Cucullanorhynchus constrictruncatus Amin, Van Ha and Heckmann, 2008, collected from the leopard Panthera pardus (Linnaeus), adults of Paraprosthenorchis ornatus Amin, Van Ha and Heckmann, 2008 from Chinese pangolin Manis pentadactyla Linnaeus, and adult species of Sphaerechinorhynchus macropisthospinus Amin, Wongsawad, Marayong, Saehoong, Suwattanacoupt, and Sey, 1998, collected in tiger, Panthera tigris (Linnaeus). These last three species were collected in hosts from Hanoi Zoological Park, Hanoi, Vietnam [51].
Individuals of the genus Multisentis sp. have been reported from termites as the intermediate host, and as the definitive hosts in the numbat Myrmecobius fasciatus from Australia [52]. Additionally, acanthocephalan adults of Neoncicola sp. were obtained from bats around Paraguay, South America [53].
Conclusion
This study suggests that the link between definitive hosts and the acanthocephalan parasites is mediated by the selection of their intermediate hosts as food items. Also, even if some intermediate hosts have distribution across distinct continents, i.e., cockroaches, being able to extend the parasite transmission in distant geographic localities, the definitive hosts, that disperse infective stages, have a more limited distribution, resulting in more or less geographically restricted dispersal for members of Archiacanthocephala. In summary, the results presented here contribute to further understanding of the ecological and evolutionary relationships that allow the host-parasite co-existence within the class Archiacanthocephala, which needs adjustments due to inapparent monophyly of some families. Also, due to the lack of molecular data available for several members of Archiacanthocephala, our finding should be regarded as preliminary. Future research needs increased collection efforts, integrating morphological and molecular data, as well as increased field-based observations of parasitic life cycle, to further our understanding of ecological and phylogenetic relationships of members of the class Archiacanthocephala.
Availability of Data and Material
Sequences are available in GenBank.
Code Availability
Not applicable.
References
Guerreiro-Martins NB, Robles MR, Navone GT (2017) A new species of Moniliformis from a Sigmodontinae rodent in Patagonia (Argentina). Parasitol Res 116:2091–2099. https://doi.org/10.1007/s00436-017-5508-9
Amin OM, Pitts RM (1996) Moniliformis clarki (Acanthocephala: Moniliformidae) from the Pocket Gopher, Geomys bursarius missouriensis, in Missouri. J Helminthol Soc Wash 63:144–145
Neiswenter SA, Penceand DB, Dowler RC (2006) Helminths of sympatric striped, hog-nosed, and spotted skunks in west-central Texas. J Wildl Dis 42:511–517. https://doi.org/10.7589/0090-3558-42.3.511
Amin OM, Heckmann RA, Mohammed O, Evans RP (2016) Morphological and molecular descriptions of Moniliformis saudi sp. n. (Acanthocephala: Moniliformidae) from the desert hedgehog, Paraechinus aethiopicus (Ehrenberg) in Saudi Arabia, with a key to species and notes on histopathology. Folia Parasitol. https://doi.org/10.14411/fp.2016.014
Catenacci LS, Colosio AC, Oliveira LC, De Vleeschouwer KM, Munhoz AD, Deem SL, Pinto JMS (2016) Ocurrence of Prosthenorchis elegans in free-living primates from the atlantic forest of Southern Bahia, Brazil. J Wildl Dis 52:364–368. https://doi.org/10.7589/2015-06-163
de Oliveira AR, Hiura E, Guião-Leite FL, Flecher MC, Braga FR, Silva LPC, Sena T, de Souza TD (2017) Pathological and parasitological characterization of Prosthenorchis elegans in a free-ranging marmoset Callithrix geofroyi from the Brazilian Atlantic Forest. Pesqui Vet Bras 37:1514–1518
Hartnett EA, Léveillé AN, French SK, Clow KM, Shirose L, Jardine CM (2018) Prevalence, distribution and risk factors associated with Macracanthorhynchus ingens infections in raccoons from Ontario, Canada. J Parasitol 194:457–464. https://doi.org/10.1645/17-202
Becker AAMJ, Rajeev S, Freeman MA, Beierschmitt A, Savinon V, Jm W, Bolfa P (2019) Extraintestinal acanthocephalan Oncicola venezuelensis (Oligacanthorhynchidae) in small indian mongooses (Herpestes auropunctatus) and African green monkeys (Chlorocebus aethiops sabaeus). Vet Pathol 56:794–798. https://doi.org/10.1177/0300985819848502
Nickol BB, Fuller CA, Rock P (2006) Cystacanths of Oncicola venezuelensis (Acanthocephala: Oligacanthorhynchidae) in Caribbean termites and various paratenic hosts in the U.S Virgin islands. J Parasitol 92:539–542. https://doi.org/10.1645/GE-3557.1
Fuller CA, Nickol BB (2011) A description of mature Oncicola venezuelensis (Acanthocephala: Oligacanthorhynchidae) from a feral house cat in the U.S Virgin Islands. J Parasitol 97:1099–1100. https://doi.org/10.1645/GE-2849.1
Richardson DJ, Hammond CI, Richardson KE (2016) The florida Ivory millipede, Chicobolus spinigerus (Diplopoda: Spirobolidae): a natural intermediate host of Macracanthorhynchus ingens (Acanthocephala: Oligacanthorhynchidae). Southeast Nat 15:7–11. https://doi.org/10.1656/058.015.0113
Santos EGN, Chame M, Chagas-Moutinho VA, Santos CP (2017) Morphology and molecular analysis of Oncicola venezuelensis (Acanthocephala: Oligacanthorhynchidae) from the ocelot Leopardus pardalis in Brazil. J Helminthol 91:605–612. https://doi.org/10.1017/S0022149X16000651
Nascimento Gomes AP, Silva Cesário C, Olifiers N, Bianchi RC, Maldonado A Jr, do Val Vilela R (2019) New morphological and genetic data of Gigantorhynchus echinodiscus (Diesing, 1851) (Acanthocephala: Archiacanthocephala) in the giant anteater Myrmecophaga tridactyla Linnaeus, 1758 (Pilosa: Myrmecophagidae). Int J Parasitol. Parasites Wildl 10:281–288. https://doi.org/10.1016/j.ijppaw.2019.09.008
García-Varela M, Nadler SA (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. J Parasitol 91:1401–1409. https://doi.org/10.1645/GE-523R.1
García-Varela M, Nadler SA (2006) Phylogenetic relationships among syndermata inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol 40:61–72. https://doi.org/10.1016/j.ympev.2006.02.010
Verweyen L, Klimpel S, Palm HW (2011) Molecular phylogeny of the Acanthocephala (Class Palaeacanthocephala) with a paraphyletic assemblage of the orders polymorphida and echinorhynchida. PLoS ONE. https://doi.org/10.1371/journal.pone.0028285
Presswell B, García-Varela M, Smales LR (2017) Morphological and molecular characterization of two new species of Andracantha (Acanthocephala: Polymorphidae) from New Zealand shags (Phalacrocoracidae) and penguins (Spheniscidae) with a key to the species. J Helminthol 92:740–751. https://doi.org/10.1017/S0022149X17001067
Amin OM, Heckmann RA, Sharifdini M, Albayati NY (2019) Moniliformis cryptosaudi n. sp. (Acanthocephala: Moniliformidae) from the Long-eared Hedgehog Hemiechinus auritus (Gmelin) (Erinaceidae) in Iraq; a case of incipient cryptic speciation related to M. Saudi in Saudi Arabian. Acta Parasitol 64:195–204. https://doi.org/10.2478/s11686-018-00021-9
Amin OM, Evans P, Heckmann RA, El-Naggar AM (2013) The description of Mediorhynchus africanus n. sp. (Acanthocephala: Gigantorhynchidae) from galliform birds in Africa. Parasitol Res 112:2897–2906. https://doi.org/10.1007/s00436-013-3461-9
Amin OM, Sharifdini M, Heckmann RA, Zarean M (2020) New perspectives on Nephridiacanthus major (Acanthocephala: Oligacanthorhynchidae) collected from hedgehogs in Iran. J Helminthol. https://doi.org/10.1017/S0022149X2000073
Amin OM, Heckmann RA, Sist B, Basso WU (2021) A review of the parasite fauna of the Black-bellied Pangolin, Phataginus tetradactyla Lin. (Manidae), from central Africa with the description of Intraproboscis sanghae n. gen., Sp. (Acanthocephala: Gigantorhynchidae). J Parasitol 107:222–238. https://doi.org/10.1645/20-126
Amin OM (2013) Classification of Acanthocephala. Folia Parasitol 60:273–305. https://doi.org/10.14411/fp.2013.031
Nickol BB (1977) Life history and host specificity of Mediorhynchus centurorum Nickol 1969 (Acanthocephala: Gigantorhynchidae). J Parasitol 63:104–111
Amin OM, Dailey MD (1998) Description of Mediorhynchus papillosus (Acanthocephala: Gigantorhynchidae) from a Colorado, U.S.A, population, with a discussion of morphology and geographical variability. J Helminthol Soc Wash 65(2):189–200. https://doi.org/10.1006/jipa.1998.4766
Smales LR (2002) Species of Mediorhynchus (Acanthocephala: Gigantorhynchidae) in Australian birds with the description of Mediorhynchus colluricinclae n. sp. J Parasitol 88:375–281. https://doi.org/10.2307/3285592
Minott-Picado P, Caballero Castillo M (2007) Determinación de Salmonella spp. y endoparásitos en zanates (Quiscalus mexicanus) del parque de Cañas, Guanacaste, Costa Rica. RCSP 16(31):27–35
Amin OM, Heckmann RA, Sahara A, Yudhanto S (2013) The finding of Mediorhynchus gallinarum (Acanthocephala: Gigantorhynchidae) in chickens from Indonesia, with expanded description using SEM. Comp Parasitol 80:39–46. https://doi.org/10.1654/4562.1
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Trifinoupoulus J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res 44:232–235. https://doi.org/10.1093/nar/gkw256
Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
García-Varela M, Aznar FJ, Pérez-Ponce de León G, Piñero D, Laclette JP (2005) Molecular phylogeny of Corynosoma Lühe, 1904 (Acanthocephala), based on 5.8S and internal transcribed spacer sequences. J Parasitol 91:345–352. https://doi.org/10.1645/GE-3272
Rodríguez SM, D’Elía G, Valdivia N (2017) The phylogeny and life cycle of two species of Profilicollis (Acanthocephala: Polymorphidae) in marine hosts off the Pacific coast of Chile. J Helminthol 91:589–596. https://doi.org/10.1017/S0022149X16000638
Rodríguez SM, Diaz JI, D’Elía G (2017) Morphological and molecular evidence on the existence of a single estuarine and rocky intertidal acanthocephalan species of Profilicollis Meyer, 1931 (Acanthocephala: Polymorphidae) along the Atlantic and Pacific coasts of southern South America. Syst Parasitol 94:527–533. https://doi.org/10.1007/s11230-017-9716-6
Monks S (2001) Phylogeny of the Acanthocephala based on morphological characters. Syst Parasitol 48:81–116. https://doi.org/10.1023/a:1006400207434
Nickol BB (1969) Acanthocephala of Louisiana with description of a new species of Mediorhynchus. J Parasitol 55:324–328
Goulding TC, Cohen CS (2014) Phylogeography of a marine acanthocephalan: lack of cryptic diversity in a cosmopolitan parasite of mole crabs. J Biogeogr 41:965–976. https://doi.org/10.1111/jbi.12260
Amin OM, Rodríguez SM, Heckmann RA (2019) Morphological updates and molecular description of Heterosentis holospinus Amin, Heckmann, Ha, 2011 (Acanthocephala: Arhythmacanthidae) in the Pacific Ocean off Vietnam. Parasite 26:73. https://doi.org/10.1051/parasite/2019072
Steinauer ML, Nickol BB, Orti G (2007) Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite. Mol Ecol 16:2097–4109. https://doi.org/10.1111/j.1365-294X.2007.03462.x
Richardson DJ (2005) Identification of cystacanths and adults of Oligacanthorhynchus tortuosa, Macracanthorhynchus ingens, and Macracanthorhynchus hirudinaceus based on proboscis and hook morphometrics. JAAS 59(30):205–209
Mowlavi GR, Massoud J, Mobedi I, Solaymani-Mohammadi S, Gharagozlou MJ, Mas-Coma S (2006) Very highly prevalent Macracanthorhynchus hirudinaceus infection of wild boar Sus scrofa in Khuzestan province, south-western Iran. Helminthol 43:86–91. https://doi.org/10.2478/s11687-006-0017-x
Kamimura K, Yonemitsu K, Maeda K, Sakaguchi S, Setsuda A, Varcasia A, Sato H (2018) An unexpected case a Japanese wild boar (Sus scrofa leucomystax) infected with the giant thorny-headed worm (Macracanthorhynchus hirudinaceus) on the mainland of Japan (Honshu). Parasitol Res 117:2315–2322. https://doi.org/10.1007/s00436-018-5922-7
Gazi M, Sultana T, Min GS, Park YC, García-Varela M, Nadler SA, Park JK (2012) The complete mitochondrial genome sequence of Oncicola luehei (Acanthocephala: Archicanthocephala) and its phylogenetic position within Syndermata. Parasitol Int 61:307–316. https://doi.org/10.1016/j.parint.2011.12.001
Falla AC, Brieva C, Bloor P (2015) Mitochondrial DNA diversity in the acanthocephalan Prosthenorchis elegans in Colombia based on cytochrome c oxidase I (COI) gene sequences. Int J Parasitol Parasites Wildl 4:401–407. https://doi.org/10.1016/j.ijppaw.2015.08.002
Sokolov SG, Alshinetsky MV, Berezin MV, Efeykin BD, Spiridonov SE (2016) Acanthocephalans Prosthenorchis cf. elegans (Archiacanthocephala: Oligacanthorhynchidae), parasites of primates in the Moskow zoo. Parazitologiia 50:185–196
Stunkard HW (1965) New intermediate hosts in the life cycle of Prosthenorchis elegans (Diesing, 1851), an acanthocephalan parasite of primates. J Parasitol 51:645–649
Schmidt GD (1972) Oncicola schacheri sp. n., and other Acanthocephala of Lebanese mammals. J Parasitol 58:279–281
Schmidt GD (1972) Revision of class Archiacanthocephala Meyer, 1931 (Phylum Acanthocephala), with emphasis on Oligacanthorhynchidae Southwell et Macfie, 1925. J Parasitol 58:290–297
Amin OM (1985) Classification. In: Crompton DWT, Nickol BB (eds) Biology of the Acanthocephala. Cambridge University Press, Cambridge, pp 27–72
Amin OM, Van Ha N, Heckmann RA (2008) New and already known acanthocephalans mostly from mammals in Vietnam, with descriptions of two new genera and species in Archiacanthocephala. J Parasitol 94:194–201
Smales L (1997) Multisentis myermecobius, gen. et. Sp. nov. (Acanthocephala: Oligacanthorhynchidae), from the numbat, Myrmecobius fasciatus, and a key to genera of the Oligacanthorhynchidae. Invertebr Taxon 11:301–307
Smales L (2007) Oligacanthorhynchidae (Acanthocephala) from mammals from Paraguay with the description of a new species of Neoncicola. Comp Parasitol 74:237–243
García-Varela M, Pérez-Ponce de León G, de la Torre P, Cummings MP, Sarma SSS, Laclette JP (2000) Phylogenetic relationships of Acanthocephala based on analysis of 18S ribosomal RNA gene sequences. J Mol Evol 50:532–540. https://doi.org/10.1007/s002390010056
Near TJ, Garey JR, Nadler SA (1998) Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences. Mol Phylogenet Evol 10:287–298. https://doi.org/10.1006/mpev.1998.0569
Weber M, Wey-Fabrizius AR, Podsiadlowski L, Witek A, Schill RO, Sugár L, Herlyn H, Hankeln T (2013) Phylogenetic analyses of endoparasitic Acanthocephala based on mitochondrial genomes suggest secondary loss of sensory organs. Mol Phylogenet Evol 66:182–189. https://doi.org/10.1016/j.ympev.2012.09.017
Telford MJ, Holland PW (1993) The phylogenetic affinities of the chaetognaths: a molecular analysis. Mol Biol Evol 10:660–676. https://doi.org/10.1093/oxfordjournals.molbev.a040030
Pinacho-Pinacho CD, Hernández-Orts JS, Sereno-Uribe AL, Pérez-Ponce de León G, García-Varela M (2017) Mayarhynchus karlae n. g., n. sp. (Acanthocephala: Neoechinorhynchidae), a parasite of cichlids (Perciformes: Cichlidae) in southeastern Mexico, with comments on the paraphyly of Neoechinorhynchus Stiles & Hassall, 1905. Syst Parasitol 94:351–365. https://doi.org/10.1007/s11230-017-9704-x
Sarabeev V, Tkach Ie, Sueiro RA, Leiro J (2020) Molecular data confirm the species status of Neoechinonirhynchus personatus and N yamagutii (Acanthocephala, Neoechinorhynchidae) from the Atlantic and Pacific Grey Mullets (Teleostei, Mugilidae). Zoodiversity 54:1–10
Acknowledgements
We thank Alex González for his assistance with the laboratory work in Sistematica Lab from Universidad Austral of Chile.
Funding
SMR was supported by postdoctoral FONDECYT 3190348. OMA was supported by an institutional grant from the Parasitology Center, Scottsdale, Arizona, USA, RAH was supported by Biology Department funds, Brigham Young University, Provo, Utah, USA, and GD was supported by FONDECYT 1180366.
Author information
Authors and Affiliations
Contributions
OMA and RAH collected samples and provided original descriptions and research of the species reported and reviewed the manuscript. SMR and GD analysed and interpreted data. SMR wrote the first draft of the manuscript. All authors reviewed and approved the text.
Corresponding author
Ethics declarations
Conflict of interest
There is no competing interest among the authors and compliance with all relevant ethical standards.
Ethical approval
The authors declare that this study was conducted in compliance with all guidelines on the care and use of animals.
Consent to participate
All authors approve the participation.
Consent for publication
All authors approve the publication.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rodríguez, S.M., Amin, O.M., Heckmann, R.A. et al. Phylogeny and Life Cycles of the Archiacanthocephala with a Note on the Validity of Mediorhynchus gallinarum. Acta Parasit. 67, 369–379 (2022). https://doi.org/10.1007/s11686-021-00472-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11686-021-00472-7