Introduction
The genus Heligmostrongylus Travassos, 1917 (Heligmonellidae, Pudicinae) comprises nematodes characterized by a caudal bursa with a pattern of type 2-2-1 and a synlophe with a well-developed careen made up of two continuous ridges, plus 11–12 discontinuous ridges arranged in linear series (Durette-Desset et al., Reference Durette-Desset, Digiani, Kilani and Geffard-Kuriyama2017). This genus contains nine species described from rodents of the families Cuniculidae, Dasyproctidae, Echimyidae, and Erethizontidae from the Neotropics (Durette-Desset et al., Reference Durette-Desset, Digiani, Kilani and Geffard-Kuriyama2017): Heligmostrongylus almeidai (Durette-Desset & Tchéprakoff Reference Durette-Desset and Tchéprakoff1969), Heligmostrongylus differens Lent & Freitas, Reference Lent and Freitas1938, Heligmostrongylus crucifer (Travassos, Reference Travassos1943), Heligmostrongylus elegans (Travassos, Reference Travassos1921), Heligmostrongylus sedecimradiatus (Linstow, 1899), and Heligmostrongylus squamastrongylus (Travassos, Reference Travassos1937) in Brazil, Heligmostrongylus chiarae Durette-Desset, Deharo, Santiváñez-Galarza & Chabaud, Reference Durette-Desset, Deharo, Santivañez-Galarza and Chabaud2001 in Bolivia, Heligmostrongylus echimyos Diaw, Reference Diaw1976 in French Guiana, and Heligmostrongylus proechimysi Durette-Desset, 1970 in Colombia.
In a previous helminthological survey conducted to explore the helminth diversity of wild small rodents (Cricetidae and Heteromyidae) from the Yucatan Peninsula (Mexico), we identified nematodes that showed characteristics of Heligmostrongylus from Ototylomys phyllotis Merriam, 1901 and Peromyscus yucatanicus Allen & Chapman, 1897 (Rodentia: Cricetidae), a finding that extended the host range of this genus of nematodes in the Neotropics (Panti-May et al., Reference Panti-May, Moguel-Chin, Hérnandez-Mena, Cárdenas-Vargas, Torres-Castro, García-Prieto, Digiani, Hernández-Betancourt and Vidal-Martínez2023). Their morphological characteristics revealed a priori that they belonged to an undescribed species of Heligmostrongylus; however, we did not describe it due to the few specimens found and their poor condition. In the present study, we describe this new species based on new material collected in the Yucatan Peninsula.
Materials and methods
Nematode collection and morphological characterization
Nineteen specimens of O. phyllotis and nine of Heteromys gaumeri Allen & Chapman, 1897 were trapped in a cattle ranch in the state of Yucatan, Mexico, from July 2022 to May 2023, as a part of a larger study described elsewhere (Chan-Casanova, Reference Chan-Casanova2024). Nematodes were collected from the small intestine, washed in 0.85% sodium chloride solution, and then fixed in 10% buffered formalin or preserved in 70% ethanol for morphological study. For the molecular study, some specimens were preserved in 100% ethanol and stored at –4 °C.
Nematodes were cleared and temporarily mounted in lactophenol for morphological examination. Specimens were studied/drawn using a Leica DM750 light microscope equipped with a drawing tube. Some nematodes preserved in 10% formalin were dehydrated using a graded ethanol series, critical point–dried with carbon dioxide, sputter-coated with a gold-palladium mixture, and examined at an accelerating voltage of 10 kV with a Hitachi SU1510 scanning electron microscope (SEM) at the Laboratorio de Microscopía y Fotografía de la Biodiversidad, Instituto de Biología, Universidad Nacional Autónoma de México (IBUNAM), Mexico City. The synlophe was studied following the method of Durette-Desset (Reference Durette-Desset1985). The description of the caudal bursa follows Durette-Desset & Digiani (Reference Durette-Desset and Digiani2012) and was based on fully extended bursae and observation of individual lobes. All measurements are given in micrometres unless otherwise stated. For the description of the new species, the measurements of the holotype and allotype are presented first, followed by the mean, standard deviation, and the range in parentheses of the paratypes. Classification used above the family Heligmonellidae follows (Beveridge et al., Reference Beveridge, Spratt, Durette-Desset and Schmidt-Rhaesa2014). The nomenclature and synonymy of the hosts’ species follows the American Society of Mammalogists Biodiversity Committee (2023). Prevalence (expressed as a percentage) and mean intensity with their 95% confidence intervals (CI) were estimated following Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997). Specimens were deposited in the Colección Nacional de Helmintos (CNHE), IBUNAM, Mexico City, Mexico. Vouchers of hosts were deposited in the Colección Mastozoológica, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán (FMVZ-UADY).
Molecular data and analysis
We produced partial sequences of three molecular genetic markers, the cytochrome c oxidase subunit 1 (COI), the Internal Transcribed Spacer region 1 (ITS1), and the 28S rRNA, from individual worms collected from O. phyllotis and H. gaumeri. Genomic DNA was extracted from individual specimens using the DNeasy Blood & Tissue Kit (Qiagen, Hilden, Germany). A fragment of the COI was amplified using primers LCO1490/ HC02198 (Folmer et al., Reference Folmer, Black, Hoeh, Lutz and Vrijenhoek1994). Partial sequences of the ITS1 region were amplified using the primers NC16 (Chilton et al., Reference Chilton, Huby-Chilton and Gasser2003)/NC13R (Chilton & Gasser, Reference Chilton and Gasser1999). A fragment of the 28S rRNA gene was amplified using the primers 391 (Nadler et al., Reference Nadler, Carreno, Adams, Kinde, Baldwin and Mundo-Ocampo2003)/536 (García-Varela & Nadler, Reference García-Varela and Nadler2005). Thermal conditions of the polymerase chain reaction (PCR) amplifications were those described by Folmer et al. (Reference Folmer, Black, Hoeh, Lutz and Vrijenhoek1994), Sukee et al. (Reference Sukee, Beveridge and Jabbar2018), and Hernández-Mena et al. (Reference Hernández-Mena, García-Varela and Pérez-Ponce de León2017) for COI, ITS1, and 28S rRNA, respectively. The PCR primers, along with additional internal primers 503 (Nadler et al., Reference Nadler, Carreno, Adams, Kinde, Baldwin and Mundo-Ocampo2003) and 504 (Hernández-Mena et al., Reference Hernández-Mena, García-Varela and Pérez-Ponce de León2017) for 28S rRNA, were used for Sanger sequencing at Macrogen (Seoul, Korea). Contiguous sequences were assembled and edited using Geneious Pro 4.8.4 (Kearse et al., Reference Kearse, Moir, Wilson, Stones-Havas, Cheung, Sturrock, Buxton, Cooper, Markowitz, Duran, Thierer, Ashton, Meintjes and Drummond2012). Consensus sequences obtained in this study and other sequences of Heligmosomoidea available in GenBank were used for phylogenetic analyses; for the 28S rRNA gene, trimmed sequences of the domains D2–D3 were used. The alignment was generated using ClustalW (http://www.genome.jp/tools/clustalw/) with the “SLOW/ACCURATE” approach and weight matrix “CLUSTALW (for DNA)” (Thompson et al., 1994). The best-fitting nucleotide substitution model was selected for each data set with jModelTest v2 (Darriba et al., Reference Darriba, Taboada, Doallo and Posada2012) under Akaike information criterion. Phylogenetic affinities for each data set were evaluated by maximum likelihood (ML) analysis using RAxML v. 7.0.4 (Stamatakis, Reference Stamatakis2006). Bootstrap support values were estimated by running 1000 bootstrap resamples. Genetic variation within the COI, ITS1, and the D2–D3 of the 28S rRNA data sets was calculated using p-distances with MEGA 11 (Tamura et al., Reference Tamura, Stecher and Kumar2021).
Results
Thirteen specimens of O. phyllotis and six specimens of H. gaumeri were infected with nematodes of the genus Heligmostrongylus. Ototylomys phyllotis was usually coinfected with Heligmosomoidea gen. sp. cf. Vexillata, Strongyloides sp., Syphacia spp., and Raillietina sp., while H. gaumeri had coinfections with Vexillata vexillata (Hall, 1916), Strongyloides sp., and Trichuris silviae Panti-May & Robles, 2016. Next we provide a taxonomic description of the new species of Heligmostrongylus based on specimens from the type host (O. phyllotis). Measurements of the new species isolated from O. phyllotis and H. gaumeri, as well as measurements of other species of Heligmostrongylus are presented in Table 1 for comparative purposes.
Table 1. Host and main morphological features and measurements of Heligmostrongylus species
Measurements given in micrometres unless otherwise specified. General measurements are presented as a single range.
Abbreviations: dae, distance from anterior end; dpe, distance from posterior end.
Heligmostrongylus yucatanensis n. sp. (Figures 1–2 and Table 1)
Figure 1. Line drawings of Heligmostrongylus yucatanensis n. sp. (a) Anterior part of female, ventral view. (b–d) Transverse sections of the body of female, at level of the oesophagus (b), mid-body (c), and the uterus (d). (e–g) Transverse sections of the body of male, at level of the oesophagus (e), mid-body (f), and spicules (g). (h) Posterior part of female showing cuticular ridges, tail, ovejector, and distal uterus, dorsal view. (i) Posterior part of male, right lateral view. (j) Male caudal bursa, ventral view. (k) Male caudal bursa, ventral view. (l) Tip of spicule, lateral view. Scale bars: (a–g, j–k) 100 μm; (h–i) 200 μm; (l) 30 μm.
Figure 2. SEM micrographs of Heligmostrongylus yucatanensis n. sp. (a) Head of female, apical view. (b) Section of female at mid-body, dorso-lateral view. (c) Middle part of female body, dorsal view (left side towards the bottom of the page). (d) Posterior part of male, ventral view, showing closed caudal bursa and ventral cuticular inflation. (e) Posterior part of female, dorsal view, showing torsion of the posterior extremity. Scale bars: (a) 10 μm, (b) 300 μm, (c) 50 μm, (d–e) 100 μm.
Description
General: Medium-sized nematodes. Cephalic vesicle present (Figure 1a). In apical view, triangular oral opening surrounded by thin rim; two amphids and six external labial papillae visible (Figure 2a). Deirids small, situated usually posterior to nerve ring (Figure 1a). Excretory pore located slightly anterior to distal end of oesophagus (Figure 1a). Ventral cuticle at anterior region of copulatory bursa with inflation (Figures 1j–k, 2d). Posterior extremity of female twisted approximately 180° to left (Figure 2e).
Synlophe (studied in three males and three females): Cuticle with longitudinally interrupted ridges (except those forming careen), arranged in linear series (Figure 2b–c). Careen present, supported by two hypertrophied ridges similar in size. Ridges appearing posterior to cephalic vesicle and disappearing just anterior to pre-bursal papillae in male (Figure 2d) and at level of vestibule in female. In both sexes, 11–12 (careen, 4–5 dorsal, 5 ventral) ridges at level of distal oesophagus (Figure 1b, e) and 13 ridges (careen, 5 dorsal, 6 ventral) at mid-body (Figure 1c, f). Within distal third of body length, size of ridges forming the careen decreasing progressively; 13 ridges (careen, five dorsal, six ventral) at level of distal uterus in female (Figure 1d) and same at level of the middle portion of the spicules in male (Figure 1g). Right side (opposite to careen) free of ridges (Figure 1b-g, Figure 2b-c). Axis of orientation of ridges sub-frontal, directed from right to left (Figure 1b–g).
Male (based on holotype and 19 paratypes): 10.7, 8.7 ± 0.9 (6.6–10.2) mm long and 118, 107.1 ± 13.8 (85–138) wide (careen included) at mid-body. Cephalic vesicle 80, 70.4 ± 7 (60–88) long and 40, 32.5 ± 4.2 (25–40) wide. Nerve ring, deirids, and excretory pore situated at 245, 214.1 ± 20.8 (170–250), 362, 278 ± 32.5 (220–335), and 455, 386.3 ± 42.7 (310–485) from apex, respectively. Oesophagus 408, 346.8 ± 30.8 (295–400) long.
Caudal bursa subsymmetrical with dorsal ray well developed (Figure 1j). Pre-bursal papillae observed (Figures 1j, 2d). Pattern of type 2-2-1. Rays 2 smallest, slightly curved inwards. Rays 3, 5 and 6 approximately equal in length. Rays 4 and 5 diverging at distal third of common trunk of rays 3–6, rays 4 slightly shorter. Rays 8 long, arising symmetrically from the proximal third of dorsal ray. Dorsal ray long, divided at proximal third, proximally to arising of rays 8, into two branches, each one bifurcated at distal third into 2 sub-branches, rays 9 (external) and rays 10 (internal) (Figure 1j–k). Rays 9 and 10 long, comparable in length, rays 9 slightly shorter. Rays 9 strongly curved laterally at a right angle and crossing ventrally rays 8. Genital cone poorly developed, not sclerotized, 40, 41 ± 5.4 (30–50) long and 40, 40.4 ± 3.5 (32–45) wide, hidden by the ventral cuticular inflation. Spicules subequal, alate, with pointed tips curved in a right angle, enclosed in an expanded membrane (Figure 1l), 665, 655 ± 32.1 (580–700) long and representing 6.2, 7.6 ± 0.8 (6.7–9.5) % of body length. Gubernaculum absent. Telamon not observed.
Female (based on allotype and 19 paratypes): 16.6, 14.8 ± 1.8 (11.8–17.7) mm long and 110, 122.5 ± 15.9 (92–150) wide (careen included) at mid-body. Cephalic vesicle 66, 65.6 ± 5.2 (55–75) long and 40, 35.3 ± 4.5 (30–45) wide. Nerve ring, deirids, and excretory pore situated at 250, 212.2 ± 31.5 (175–280), 322, 245.6 ± 57.9 (105–330), and 462, 367.7 ± 45.5 (290–458) from apex, respectively. Oesophagus 430, 363 ± 33.6 (300–450) long. Monodelphic. Vulva situated at 120, 109.9 ± 16.2 (80–140) from caudal extremity. Vagina vera 68, 63.9 ± 7.6 (50–80) long, vestibule 152, 134.2 ± 13.9 (115–160) long, sphincter 50, 41.9 ± 4 (35–50) long, infundibulum 165, 151.6 ± 25.8 (110–185). Uterus 3.4, 3.3 ± 0.5 (2.5–4.1) mm long, representing 20.8, 22.7 ± 2.9 (17.6–26.8)% of body length, containing 108, 107 ± 19 (77–148) eggs. Eggs 55–62, 64 ± 4 (58–75) long and 32–40, 35 ± 4 (28–45) wide; based on five eggs measured from the allotype and 66 from the paratypes. Tail conical, 45, 38.9 ± 4.9 (30–45) long. Posterior extremity (approximately from ovejector level, coincident with reduction in size of ridges of the careen) undergoes a torsion of 180° to left, or counterclockwise; resulting in vulva and anus opening on the functionally dorsal surface of the worm (Figures 1h, 2e). This torsion is evidenced through the rotation of the cuticular ridges and the position of the vulva and anus in relation to the careen.
Type host: Ototylomys phyllotis Merriam, 1901 (Rodentia, Cricetidae, Tylomyinae), male, voucher specimen (No. 1720) deposited at FMVZ-UADY. Other specimens FMVZ-UADY–1694,1696, 1698, 1719.
Other hosts: Heteromys gaumeri Allen & Chapman, 1897 (Rodentia, Heteromyidae, Heteromyinae) (FMVZ-UADY–1686, 1695, 1697, 1718). Peromyscus yucatanicus Allen & Chapman, 1897 (Rodentia, Cricetidae, Neotominae) in Panti-May et al. (Reference Panti-May, Moguel-Chin, Hérnandez-Mena, Cárdenas-Vargas, Torres-Castro, García-Prieto, Digiani, Hernández-Betancourt and Vidal-Martínez2023).
Type locality: Rancho Santa María (21°15’ 48.2"N, 88°16’ 31.4"O), municipality of Panabá, state of Yucatan, Mexico.
Other localities: Vallazoo, municipality of Valladolid, Santa Cruz cattle ranch, municipality of Tizimin, state of Yucatan, and Balam Nah eco-hotel, municipality of Felipe Carrillo Puerto, state of Quintana Roo, Mexico, in Panti-May et al. (Reference Panti-May, Moguel-Chin, Hérnandez-Mena, Cárdenas-Vargas, Torres-Castro, García-Prieto, Digiani, Hernández-Betancourt and Vidal-Martínez2023).
Site of infection: Small intestine.
Prevalence (CI) and mean intensity (CI): 68.4% (43.4–87.4%) and 44 (25.9–69.1) in O. phyllotis, and 66.7% (29.9–92.5%) and 9 (4.5–15.8) in H. gaumeri.
Material deposited: Holotype male (No. 13039), allotype female (No. 13040), and a total of 46 paratypes (O. phyllotis: No. 13041, 13042; H. gaumeri: No. 13043, 13044) were deposited at CNHE.
GenBank accession numbers: COI (PQ429005, PQ429006), ITS1 (PQ472082, PQ472083), 28S rRNA (PQ454599, PQ454600, PQ454601).
ZooBank Life Science Identifier: 735B0E1F-B5D4-4FEC-B969-294F63FB2799.
Etymology: The species epithet refers to the geographic region where the species was detected (Yucatan Peninsula, Mexico).
Diagnosis
The genus Heligmostrongylus includes nine species parasitic in Neotropical rodents. The presence of developed rays 9 in H. yucatanensis allows its discrimination from H. squamastrongylus and H. echimyos, which have rays 9 minute or merged with rays 10. The new species has rays 9 comparable in length to rays 10, which allows it to be distinguished from H. sedecimradiatus, H. differens, and H. elegans, which have rays 9 much shorter than rays 10. The new species is also distinguished from H. chiarae and H. proechimysi by having dorsal ray dividing proximally, about the same level at which rays 8 arise, while in these two species the fork of dorsal ray is distal to the arising of rays 8. Additionally, H. chiarae and H. proechimysi rays 9, although well developed, are straight and directed posteriorly. Heligmostrongylus almeidai differs from the new species by having rays 4 hypertrophied and well separated from rays 5 and by having each spicule ending into dissimilar tips.
The most similar known species to H. yucatanensis is H. crucifer by having long developed rays 9; dorsal ray dividing at proximal third about the same level at which rays 8 arise; and rays 9 arising from mid-length of dorsal ray and crossing over rays 8 ventrally. However, the pathway of rays 9 is different in both species: in H. crucifer rays 9 are first directed latero-posteriorly in an angle of ca. 45°, crossing over rays 8, and then bent towards the posterior bursal margin becoming parallel and external to rays 8; while in the new species rays 9, though first directed latero-posteriorly in an angle of ca. 45°, then bent laterally, or even antero-laterally, crossing over rays 8 in a nearly right angle. The spicule tips of H. yucatanensis are bent in a nearly right angle and enclosed in an expanded membrane while in H. crucifer the spicule tips are simply pointed. Finally, H. yucatanensis is the only species in the genus presenting a cuticle inflation in the anterior region of the bursa.
Molecular confirmation
Specimens assignable to H. yucatanensis were found not only in rodents of two different species, but also in different families during this study. Nematodes provisionally identified as Heligmostrongylus sp., isolated from P. yucatanicus in the Yucatan Peninsula (Panti-May et al., Reference Panti-May, Moguel-Chin, Hérnandez-Mena, Cárdenas-Vargas, Torres-Castro, García-Prieto, Digiani, Hernández-Betancourt and Vidal-Martínez2023), shared morphological and morphometrical characters with the specimens isolated from O. phyllotis and H. gaumeri, such as the pattern of the bursal rays, the tips of the spicules, the ventral inflation of the bursa, spicule length (570–620) and the torsion of the female posterior end. Characteristics that, in the present study, are considered diagnostic of the new species.
With the purpose to test if the worms isolated from O. phyllotis and H. gaumeri were conspecific or represented a complex of morphologically similar species, we obtained and compared sequences of the COI, ITS1, and the D2–D3 expansion domains of the 28S rRNA. Published sequences of the 28S rRNA of provisionally identified as Heligmostrongylus sp., isolated from P. yucatanicus and O. phyllotis in the Yucatan Peninsula (Panti-May et al., Reference Panti-May, Moguel-Chin, Hérnandez-Mena, Cárdenas-Vargas, Torres-Castro, García-Prieto, Digiani, Hernández-Betancourt and Vidal-Martínez2023) were also included in the phylogenetic analysis.
Seven nucleotide sequences of H. yucatanensis were obtained in this study: three from worms collected from O. phyllotis (one for each genetic marker, COI, ITS1, and 28S rRNA) and four from worms collected from H. gaumeri (one for both COI and ITS1, and two for 28S rRNA). Details of each dataset used to construct phylogenetic trees are given in Supplementary material (Table S1).
The amplified COI fragments of the new species were aligned with other nine sequences of heligmosomoid nematodes; alignment of 460 base pairs. The sequences of H. yucatanensis isolated from O. phyllotis and from H. gaumeri were identical, and both were positioned as a sister taxon to the clade formed by the sequences of Vexillata convoluta (Caballero & Cerecero, 1943) and Nippostrongylus sp., although with low support (bootstrap = 15) (Figure 3). The new species had a genetic difference of 11% and 12% compared with those of Nippostrongylus sp. and V. convoluta, respectively. Unfortunately, there were no COI sequences available from other representatives of the Pudicinae which could have produced a resolved phylogeny.
Figure 3. Maximum likelihood (ML) phylogenetic tree of Heligmosomoidea inferred with COI sequence data. GenBank accession numbers precede species name, followed by host name. Bootstrap support values for ML are provided at the nodes. The new sequences of the present study are in bold.
The ITS1 dataset of heligmosomoid nematodes from rodents included 27 sequences, with an alignment length of 488 pb. In the phylogenetic tree, the two sequences of H. yucatanensis were placed as a sister clade to another one formed by nematodes of the genera Nippostrongylus, Stilestrongylus, Hassalstrongylus, Vexillata, Carolinensis, and Guerrerostrongylus (bootstrap = 100) (Figure 4). The genetic difference among the sequences of H. yucatanensis from O. phyllotis and from H. gaumeri was 0.2% when compared to each other. As with the results obtained for the COI sequences, analysis of the ITS1 sequences recovered a similar tree topology but with most nodes highly supported (Figure 4).
Figure 4. Maximum likelihood (ML) phylogenetic tree of Heligmosomoidea inferred with ITS1 sequence data. GenBank accession numbers precede species name, followed by host name. Bootstrap support values for ML are provided at the nodes. The new sequences of the present study are in bold.
The dataset of the D2-D3 expansion domains of the 28S rRNA of heligmosomoid nematodes from rodents included 23 sequences, with an alignment length of 714 pb. The phylogenetic tree of 28S rRNA clustered the three new sequences of H. yucatanensis from O. phyllotis and from H. gaumeri in a high supported clade (bootstrap = 100) together with the sequences previously reported for the same species (originally reported as Heligmostrongylus sp.) isolated from O. phyllotis and from P. yucatanicus (Figure 5). The genetic distance among the five sequences of H. yucatanensis ranged from 0 to 0.1%.
Figure 5. Maximum likelihood (ML) phylogenetic tree of Heligmosomoidea inferred with D2-D3 expansion domains of the 28S rRNA sequence data. GenBank accession numbers precede species name, followed by host name. Bootstrap support values for ML are provided at the nodes. The new sequences of the present study are in bold.
The absence of intraspecific sequence variations in COI, and genetic distances (0–2%) in the D2-D3 expansion segments of 28S rRNA and ITS1 provide strong support that the specimens isolated from O. phyllotis, H. gaumeri and P. yucatanicus are conspecific.
Discussion
Although morphologically and molecularly identical, male and female specimens isolated from H. gaumeri were smaller than those from O. phyllotis (Table 1). These differences may be related to the smaller size of H. gaumeri compared to O. phyllotis (39–67 g vs. 65–99 g) but also to the fact that H. gaumeri is frequently parasitized by another dominant nematode, Vexillata vexillata (Hall, 1916). Intensity of infection, size, age and diet of the host, recent or previous infections and coinfections with other worms, are factors that may also cause variations in the body size of helminths (Saldanha et al., Reference Saldanha, Leung and Poulin2009; González et al., Reference González, Gómez and Hamann2019).
The presence of a ventral cuticular inflation anterior to the bursa had not been previously recorded in species of Heligmostrongylus or any other nematodes of Pudicinae. There are reports of similar structures in species of Heligmosomoides (Heligmosomidae) parasitizing North American rodents, such as Heligmosomoides bullosus Durette-Desset, 1967, Heligmosomoides montanus Durette-Desset, 1967, and Heligmosomoides bibullosus Alnaqeb, Greiman, Vandegrift, Campbell, Meagher & Jiménez, Reference Alnaqeb, Greiman, Vandegrift, Campbell, Meagher and Jiménez2022 (Durette-Desset et al., Reference Durette-Desset, Kinsella and Forrester1972; Alnaqeb et al., Reference Alnaqeb, Greiman, Vandegrift, Campbell, Meagher and Jiménez2022). Although this structure might initially seem to interfere with mating, it is notable that in at least two of the aforementioned species (H. bullosus and H. montanus), as well as in H. yucatanensis, the presence of this anteroventral inflation of the bursa is also accompanied by varying degrees of torsion in the posterior end of the females (Durette-Desset et al., Reference Durette-Desset, Kinsella and Forrester1972). It is possible that in all these species, the torsion of the posterior end of the female parallels the presence of the ventral prebursal inflation in the male, so that both modifications may interact to ensure better attachment during copulation (Digiani & Kinsella, Reference Digiani and Kinsella2014).
Heligmostrongylus yucatanensis occurs in cricetid and heteromyid rodents from the Yucatan Peninsula. It is important to highlight that before the present record, all the species of this genus were only known from caviomorph rodents. Of the nine known species of Heligmostrongylus, six have been reported in Echimyidae, two in Erethizontidae, and one in Erethizontidae, Cuniculidae, and Dasyproctidae (Table 1). The occurrence of H. yucatanensis in three phylogenetically distant rodent species suggests that this nematode species could have the ability to expand its host range by colonizing new hosts. In disturbed environments (e.g., crop fields, ranches) where food resources and vegetation cover are limited, rodents can share burrows (Durán-Antonio & González-Romero, Reference Durán-Antonio and González-Romero2018). As a result, infective stages of parasites may be acquired by rodents that share burrows which could favour the transmission of parasites among hosts.
Supplementary material
The supplementary material for this article can be found at http://doi.org/10.1017/S0022149X24000750.
Acknowledgements
The authors thank Marco Torres-Castro for his help in collecting rodents, Wilson Isaias Moguel-Chin for his support in DNA extraction and molecular analysis, Berenit Mendoza-Garfías for the SEM micrographs, and Guadalupe Isabel Pech Simá for the drawings.
Data availability statement
Not applicable.
Financial support
This research received no specific grant from any funding agency, commercial or not-for-profit sectors.
Competing interest
The authors declare none.
Ethical approval
Protocols used in this study were approved by the Bioethics Committee of the Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán (protocol number CB-CCBA-L-2022-001). Rodent trapping was conducted under license from the Mexican Ministry of Environment (license number SGPA/DGVS/02974/22).
