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74Russian Journal of Nematology, 2017, 25 (1), 61 - 69
Davenema obtusum gen. sp. nov. the new
thelastomatid (Nematoda, Thelastomatoidea)
from littoral cockroaches of Camiguin Island,
Philippines
1 2 Alma B. Mohagan and Sergei E. Spiridonov
'Centre for Biodiversity Research and Extension in Mindanao and Biology Department, Central Mindanao University, University Town, Musuan, 8710, Maramag, Bukidnon, Philippines 2Centre of Parasitology, A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii Prospect,
33, 119071, Moscow, Russia e-mail: s_e_spiridonov@rambler.ru
Accepted for publication 18 July 2017
Summary. The description of the new genus and species of the thelastomatid nematodes, Davenema obtusum gen. sp. nov. (Thelastomatidae, Oxyurida), is presented. These nematodes were found in the hind gut of cockroaches collected on the beach on Camiguin Island, Philippines. The most peculiar feature of the new thelastomatid is the male posterior end with two protruding lateral copulatory papillae in precloacal position. Males are aspiculate, with a flattened cephalic capsule, but without lateral projections at an anterior end. The eggshells of D. obtusum gen. sp. nov. lack an operculum. The significant differences in the nucleotide sequence of D2-D3 segment of LSU rDNA are demonstrated between Davenema obtusum gen. sp. nov. and the representatives of the genera Hammerschmidtiella and Blattophila. Key words: cockroach parasites, LSU rDNA, morphology, SEM, Thelastomatidae.
The nematodes of the superfamily Thelastomatoidea (thelastomatids) are common inhabitants of the hindgut of arthropod hosts (Adamson, 1989). Although these nematodes can be found in different arthropods, including millipedes, grubs, adult Passalidae beetles and tipulid (Diptera) larvae, the cockroaches (insects of the order Blattoidea) are probably the most common and characteristic group of insect hosts for thelastomatids (Chitwood, 1932; Zervos, 1988). The composition and taxonomic structure of the superfamily Thelastomatoidea are still poorly known and the phylogenetic links of this taxon are still obscure (Spiridonov & Guzeeva, 2009). The nematodes of this supefamily are morphologically diverse outwardly suggesting the strong basis for classification. Such features as the structure of an alimentary tract (pharynx shape, organisation of the intestine), the reproductive system (male copulatory structures, the distribution and structure of gonadal tubes, the shape of spermatozoa and eggshells) and sensory structures (the number and distribution of copulatory papillae in males) indeed provide the significant amount of diagnostic features. However, the straightforward use of such characters is prevented by obvious
parallelisms. Application of molecular data for the study of the thelastomatid phylogeny and classification increases information on taxonomic aspects, which are presumably independent or, at least, not directly correlated with morphological ones. An analysis of contradictions between morphological and molecular data is an important pre-requisite for the application of the combined data. Herein, we present the description of the new thelastomatid parasitising cockroaches from the Philippines based on the molecular and morphological data.
MATERIAL AND METHODS
Nematodes were recovered from the hindgut of four large black cockroaches collected on October 12, 2016 by David P. Mohagan between the stones on the beach of Camiguin Island, the Camiguin Province (Northern Mindanao), Philippines under WGP. No.R102016-17. The cockroaches were identified as members of the family Blattidae and then sent for more precise identification, but were lost during the postage. Nematodes were fixed in hot (60-70°C) 4% formaldehyde and processed to glycerol according to Seinhorst (1959) or frozen
Table 1. Measurements of Davenema obtusum gen. sp. nov.
Character Holotype, male Paratype, males (n = 5) Allotype, female Paratype, females (n = 8)
Body length 912 892±34 (839-928) 2368 2212±421 (1392-2752)
Maximum width 110 92±11 (84-110) 224 199±58 (109-304)
Buccal cavity (length) 7 6±0.7 (5-7) 10 10.3±0.7 (9-11)
Oral annulus length 6 5.6±0.5 (5-6) 7 7.5±0.5 (7-8)
Body width at oral annulus 14 14±0.8 (13-15) 22 25±1.5 (22-26)
Second annulus length - - 17 15±2.0 (12-18)
Body width at second annulus - - 35 33±1.7 (31-36)
Nerve ring from anterior end 140 140±3.2 (136-144) 111 103±5.9 (97-114)
Excretory pore from anterior end 215 221±6 (215-227) 357 355±13 (341-374)
Pharynx length 202 207±6 (201-216) 321 321±17 (281-336)
Corpus length 135 133±2.9 (130-135) 203 203±16 (178-224)
Corpus maximal width 15 16±0.6 (15-16) 58 62±4.8 (56-67)
Isthmus length 39 41±2.1 (39-43) 54 48±6.1 (40-55)
Basal bulb length 32 31±1.0 (30-32) 64 62±12 (40-82)
Basal bulb width 29 29±2.0 (27-31) 83 78±9.8 (67-96)
Vulva from anterior end - - 541 552±19 (523-573)
Tail length 136 162±12 (142-173) 720 795±210 (528-1104)
Egg shell - - 76 x 32 74-77 x 32-35
a 8.3 9.8±1.0 (8.3-11.0) 10.5 11.5±1.9 (8.2-14.2)
b 4.5 4.3±0.3 (3.9-4.5) 7.4 6.9±1.4 (112-146)
c 6.4 5.5±0.6 (5.1-6.4) 3.3 2.9±0.7 (2.1-3.8)
V% - - 23 23±0.8 (21-26)
alive for a molecular analysis. The drawing tube for Eclipse E200 (Nikon, Tokyo, Japan) was used to make measurements and drawings. The images of a female anterior end were obtained with a JSM-6380LA (JEOL, Tokyo, Japan) electron microscope after standard dehydration in ethanol and acetone, drying at critical point and coating with gold/palladium.
For the molecular study, single nematodes per tube were kept at -18°C and then processed according to Holterman et al. (2006). The worm-
lysis solution was prepared immediately before DNA extraction containing 950 ^l of mixture of 2 ml of 1M NaCl, 2 ml of 1M Tris-HCl (pH 8) plus 5.5 ml of deionized water plus 10 ^l of mercaptoethanol and 40 ^l of proteinase K (20 mg ml1). Nematodes were transferred to 25 ^l of sterile water and after addition of 25 ^l of worm-lysis solution; each tube was incubated at 65°C for 90 min. The tubes with homogenate were then incubated at 99°C for 5 min to deactivate proteinase
K and 0.8-1.2 ^l of homogenate was used as PCR template. PCR reactions were performed using Encyclo Plus PCR kit (Evrogen®, Moscow, Russia) according to the manufacturer's manual. Primer pairs D2A (5'-ACA AGT ACC GTG AGG GAA AGT TG-3') and D3B (5'-TCG GAA GGA ACC AGC TAC TA-3') were used to amplify D2-D3 expansion segment of LSU rDNA fragment (Nunn, 1992). PCR cycling parameters included primary denaturation at 94°C for 3 min followed by 34 cycles 94°C for 30 s, 57°C for 30 s and 72°C for 1 min, followed by post-amplification extension at 72°C for 7 min. PCR reaction products were visualised in agarose gel and bands were excised for DNA extraction with Wizard SV Gel and PCR Clean-Up System (Promega, Madison, USA). Samples were directly sequenced using the same primers as used for primary PCR reactions.
The obtained D2-D3 LSU rDNA sequence was deposited in NCBI GenBank as MF503149. Sequence alignments were generated using Clustal X (Thompson et al., 1997) under default values for gap opening and gap extension penalties. MEGA 7.0.14 (Kumar et al., 2016) was used to infer phylogeny and estimate the nucleotide differences with three methods of analysis (Maximum Parsimony - MP; Neighbour Joining - NJ; and Maximum Likelihood - ML).
DESCRIPTION
Davenema obtusum gen. sp. nov.
(Fig. 1-2)
Measurements (Table 1).
Holotype (male): L = 912 ^m, max. diam. = 108 ^m, pharynx = 202, tail length = 136 ^m. (no. 1290 in the Museum of Helminthological collections of the Centre of Parasitology, A.N. Severtsov Institute of Ecology and Evolution, Moscow).
Male. Body reaching maximum width approximately on border of second and third body parts. From that level, it tapers towards anterior and posterior ends. Posterior end narrowing abruptly just behind cloaca level followed by a thin tail filament. Flattened cephalic capsule present on anterior body end. Body thinly (< 1 m) annulated posterior to cephalic capsule. At the beginning of expanded part, coarse folds of cuticle present. Lateral alae absent. Cephalic capsule without lateral projections. Buccal cavity cylindrical, gymnostom walls cuticularised. Pharynx with well-defined corpus, isthmus and bulb. Corpus club-like, only slightly expanding posteriorly. Nerve ring surrounding isthmus. Basal bulb with valves. Excretory pore located posterior to pharynx base, leading into vesicle-like structure
with single channel directed posteriad. Intestine thin-walled. Lateral chords of hypoderm with granulated cytoplasm. Testis reflexing at beginning of expanded portion of body. Different stages of spermatogenesis discernible in testis: from rounded cells near flexure to elongated 5-6 ^m long club-like bodies at mid-testis. Vas deferens transparent, situated in posterior part of expanded body portion. Pericloacal area elevated. Adcloacal projection flaplike, ending at posterior with short, digitate process. Four pairs of caudal copulatory papillae. A pair of prominent lateral papillae 16-17 ^m high located precloacally. Two pairs of medium-sized, subventral papillae situated: one near cloacal opening and another on tail filament. A pair of small papillae situated on margins of adcloacal projection (Fig. 1D). Spicule and gubernaculum absent.
Allotype (female): L = 2368 ^m, max. diam. = 224 ^m, pharynx = 321, tail length = 720 ^m. (no. 1291 in the Museum of Helminthological collections of the Centre of Parasitology, A.N. Severtsov Institute of Ecology and Evolution, Moscow).
Female. Body spindle-shaped with long tail filament. Maximal body diameter near mid-body. Annuli 22-25 ^m wide at anterior body half and 1215 ^m at posterior. Anteriormost 8-9 annuli conspicuous Fig.2,A), bulging, cuticle thickened. Lateral alae starting at level of intestine proventriculus, expanding from 10-12 ^m at mid-body to 20 ^m at level of posterior part of intestine. Alae terminating at base of tail filament, just anterior to phasmid openings. Buccal cavity cylindrical, without strong culticularisation of walls. Cheilostom with thin lining. Beneath the stoma bottom, strongly cuticularised plates near lumen of stegostom discernible (Fig. 1G). Anterior part of pharynx surrounding stegostom barrel-shaped, transparent (without muscular fibres). Corpus with tight bundles of muscular fibers, expanding posteriorly into metacorpal bulb. Nerve ring surrounding isthmus in front of metacorpal bulb. Isthmus thin, cylindrical. Basal bulb with valves and additional cuticular plates between valves and cardia. Cardia 20 ^m long, protruding into anterior part of intestine (proventriculus). Excretory pore located posterior to pharynx base, leading into 80-90 ^m long excretory vesicle with X-shaped system of four excretory channels. Intestine filled with granulated material (bacterial cells). Vulval lips flat. Muscular vagina 160-180 ^m long. Two uteri filled with eggs. Eggshells elongated, with characteristic for many thelastomatids shape (Fig. 1I) with longitudinal axis curved, without operculum.
Host. Cockroaches of the family Blattidae.
Fig.1. Davenema obtusum gen. sp. nov. A - entire male, lateral view; B - entire male, ventral view; C - male anterior end, lateral view; D - male posterior end, ventral view; E - male posterior end, lateral view; F - entire female, subventral view; G - female anterior end, lateral view; H - female pharynx, lateral view; I - egg-shell. Scales in micrometres.
Fig.2. SEM images of the anterior end of a female of Davenema obtusum gen. sp. nov. A - first cuticular annuli; B - cephalic capsule. Scales in micrometres.
Type locality. Rocky beach at Mambajao on Camiguin Island. Collection date: 12 October 2016.
Etymology. The new genus is named in honour of David P. Mohagan (University of Central Mindanao, Bukidnon), the collector of the nematode hosts. Specific name reflects the absence of lateral protruding structures of the anterior end of males.
Molecular phylogeny. The sequencing of the D2-D3 LSU rDNA sequences from two males and two females revealed their complete identity and proved conspecificity. The search for similar sequences in NCBI GenBank using BLAST (Altschul et al., 1990) revealed a set of related sequences, which were used for comparison. The phylogenetic trees obtained with three different methods demonstrated the identical interrelationships and the strong support for subclades of the thelastomatids parasitic in cockroaches (node A, Fig. 3). The basal nodes of the trees obtained with three methods were always weakly supported, and the topology of basal clades consisting of thelastomatids of different hosts (diplopods, beetles, mole-crickets) differed between the phylogenies obtained with different methods. A group of 'Hammerschmidtiella-like' genera ('Ham-merschmidtiellinae' - see Discussion) was the clade strongly supported by all methods of analysis that were used (group B, Fig. 3). This entire clade was subdivided into several subclades, also with strong support. The sequence of D. obtusum gen. sp. nov. stood out from all these subclades and linked with
the basal node for 'Hammerschmidtiellinae' (group B, Fig. 3). There is an obvious contradiction between the molecular data and existing taxonomy in the position of Blattophila sequences in the clade. Two Blattophila species with known D2-D3 LSU rDNA sequences cluster together with two different thelastomatid genera (Blattophila sp. GQ3 68461 with Malaspinanema sp. and Blattophila peregrinata KX752428 with Suifunema sp.). The pairwise comparison of the taxa in this clade demonstated that D. obtusum gen. sp. nov. was closer to Blattophila than Hammerschmidtiella. The GQ368461 sequence of Blattophila sp. was the closest to Davenema, with the nucleotide difference with Hammerschmidtiella sequences of 107-117 bp (Table 2). The intrageneric nucleotide differences within the Hammerschmidtiella genus do not exceed 69 bp, while the differences between separate genera are on the level of 92-132 bp. The only exception from that is the 62 bp difference between Blattophila sp. (GQ368461) and Malaspinanema sp. (92 bp). The monophyletic status of the genus Blattophila is not obvious from the morphology as the species with completely different shape of a pharynx, eggshells and a male posterior end are now included. Further studies are needed to elucidate the composition of this genus and its relationships with other thelastomatids.
Cosmocercoides tonkinensis AB908160 Heth impalutiensis KM226162
_ Hystrignathus sp. GQ368469
Cameronia multiovata GQ368470
- Blatticola blattae GQ368472
Desmicola sp. GQ368463 Thelastoma sp. GQ368468 The I as to ma bulhoesi KP172224 Thelastoma sp. JQ343845
h:
Cordonicola sp. GQ368464
- Davenema obtusum gen.sp.nov.
100 100 100
10 bp
94 100
95
100 100 100
Malaspinanema sp. GQ368460 Blattophila sp. GQ368461
B
group
100 100 100
HT
HSuifunema sp. KX024651 Blattophila peregrinata KX752428 Bilobostoma sp. GQ368462 Hammerschmidtiella diesingi JQ343843 Hammerschmidtiella diesingi KP172227 Hammerschmidtiella diesingi EU365628 Hammerschmidtiella diesingi KP172226 j— Hammerschmidtiella keeneyi KX752430 '— Hammerschmidtiella cristata EU365629
r Leidynema appendiculata JQ343844 L Leidynema appendiculata KC540759 Severianoia sp. EU365631 Cranifera cranifera EU365632 - Aoruroides cochinchinensis F J936558 Protrellus sp. KU674962
I Protrellus sp. KU674961
_i— Travassosinema sp. GQ368471
Travassosinema dalei HM769761
Fig.3. Phylogenetic relationships of Davenema obtusum gen. sp. nov. with other thelastomatids The bootstrap values are presented in frames near corresponding nodes (upper value - MP, middle value - NJ, lower value - ML). For MP and NJ analyses - 1000 pseudoreplicates; for ML - 500 pseudoreplicates. Tamura-Nei model for ML analysis, rates among sites Gamma distributed with Invariant sites (G+I).
Table 2. The pairwise nucleotide differences in the partial LSU rDNA sequences of Davenema obtusum gen. sp. nov. and related thelastomatids.
1 2 3 4 5 6 7 8 9 10 11
1 Hammerschmidtiella diesingi JQ343843 -
2 Hammerschmidtiella diesingi KP172227 1 -
3 Hammerschmidtiella diesingi EU365628 3 2 -
4 Hammerschmidtiella diesingi KP172226 2 1 1 -
5 Hammerschmidtiella keeneyi KX752430 62 63 63 62 -
6 Hammerschmidtiella cristata EU365629 69 68 68 67 38 -
7 Bilobostoma sp.GQ368462 108 109 108 108 99 106 -
8 Blattophila peregrinata KX752428 132 131 132 130 114 117 124 -
9 Blattophila sp. GQ368461 102 101 101 100 102 99 95 95 -
10 Suifunema sp. KX752428 132 131 132 130 114 117 124 124 95 -
11 Malaspinanema sp. GQ368460 121 120 120 119 113 113 116 101 62 101 -
12 Davenema obtusum MF503149 117 116 117 115 108 107 107 104 92 104 110
Differential diagnosis. The most peculiar feature of Davenema gen. nov. is the organisation of a male posterior end. Keeping the general resemblance with other 'Hammerschmidtiella-like' thelastomatids, a male tail of Davenema displays two protruding lateral copulatory papillae in precloacal position (Fig. 4). In two related genera (Hammerschmidtiella and Blattophila), the lateral caudal papillae are smaller and situated on the level of cloacal opening or posterior to it. The shape of the male tail of D. obtusum gen. sp. nov. resembles that of Hammerschmidtiella in the presence of a postcloacal narrow median protuberance. Such protuberance is absent in those Blattophila species for which males are described. The anterior end of D. obtusum gen. sp. nov. males ends with a flattened cephalic capsule, which is wider than the first annulus of the body cuticle. No lateral projections at a male anterior end reported for Hammerschmidtiella species were observed. Davenema obtusum gen. sp. nov. males are aspiculate. Conversely, the majority of Hammerschmidtiella and Blattophila species are characterised by having a single rudimentary spicule (Carreno, 2017). A tiny gubernaculum, which is absent in the new species, was described for H. diesingi and H. andersoni (Leibesperger, 1960; Adamson & Nasher, 1987). The eggshells of D. obtusum gen. sp. nov. lack an operculum whereas eggshells of Hammerschmitiella are operculate and those of Blattophila were reported to be with or without an operculum (Carreno, 2017). The morphological peculiarities of the nematodes described herein along with the significant differences in the nucleotide sequence of D2-D3 segment of LSU rDNA speak in favour of establishing a new genus, named here Davenema gen. nov.
© O
Y
Fig.4. Diagram of the copulatory papillae localization on male tail in three genera of thelastomatids: Blattophila (A), Davenema gen.nov. (B) and Hammerschmidtiella (C).
However, the comprehensive diagnostic scheme for the group of 'Hammerschmidtiella-like' genera of thelastomatids cannot be provided now due to the lack of morphological data on males in some genera
(Bilobostoma, Malaspinanema) (Jex et al, 2005). The provisional diagnosis of the genus is proposed:
Davenema gen. nov.
Hammerschmidtiellinae. Lateral projections of anterior end of a male absent. Vulva in anterior position (V 20-25%). Eggshells without operculum. Large lateral copulatory papillae in males situated anterior to cloacal opening. Adcloacal flap-like projection present.
DISCUSSION
The studies on thelastomatids of Philippine cockroaches started more than 80 years ago when B.G. Chitwood & M.B. Chitwood (1933) published the descriptions of several species of this family from Panesthia javanica. The place of the collection of these cockroaches in the Philippine Archipelago was not then specified. Together with the description of new species of the genera Aorurus Leidy, 1849, Leidynema Schwenk in Travassos, 1929 and Leidynemella Chitwood & Chitwood, 1933, the species Blattophila sphaerolaima Cobb, 1920 was redescribed. The general appearance and main morphological features of the nematodes found during the dissection of cockroaches from Camiguin Island strongly resembled those of Hammerschmidtiella. The species of this latter genus inhabit a hindgut of cockroaches, though some species were reported parasitising diplopods (Rao, 1958). The anterior end of females with a rounded cephalic capsule, a pharynx with the swollen posterior part of a corpus, the size and body shape of males - all these characters correspond to the morphology of the genus Hammerschmidtiella. More detailed morphological study of the nematodes found in the present study has revealed a set of differences from the known species of this genus. The main difference between the genera lays in the morphology of a male posterior end. The oversized lateral copulatory papillae of the new nematode are situated anterior to an adcloacal projection, unlike in Hammerschmidtiella and Blattophila. Other differences include the structure of eggshells without operculum vs with operculum, a specific ornamentation of the frontal circumoral cuticle and an armament of the female stegostom. In regard to the eggshell shape, there are several types of eggshells reported for the related genus Blattophila, operculated and non-operculated as well as regularly ellipsoid and with the curved longitudinal axis of the shell (Carreno, 2017). Thus, up to now the taxonomic value of characters related to the eggshell structure is still not obvious.
Cuticular structures of a female anterior end differ between the species of the genus Hammerschmidtiella (Guzeeva & Spiridonov, 2009; Camino & Villalobos, 2012; Carreno, 2017). In general, the morphological features of the nematodes found in the cockroaches of the Camiguin Island do not indicate unequivocally their generic independence, and only molecular evidence strongly supports such a decision. Hitherto, the sequence of D2-D3 expansion segment of the large ribosomal subunit is the only basis for the molecular phylogeny of thelastomatids (Jex et al, 2006; Spiridonov & Guzeeva, 2009), as few data for other loci are published. An analysis of this locus carried in the present study did not resolve basal nodes of the thelastomatid phylogeny, but demonstrated the high level of support for some terminal groups of thelastomatid genera. One of such well-defined evolutionary groups is a clade containing the genera Hammerschmidtiella, Bilobostoma, Suifunema, Blattophila, Malaspinanema and Davenema gen. nov. In the recent classifications of the Phylum Nematoda (Adamson & Van Waerebeke, 1992a, b, c; De Ley & Blaxter, 2002), the superfamily Thelastomatoidea is divided into four families: Thelastomatidae Travassos, 1929, Travassosi-nematidae Rao, 1958; Hystrignathidae Travassos, 1919 and Protrelloididae Chitwood, 1932 (Adamson & Van Waerebeke, 1992a, b, c). All the 'Hammerschmidtiella-like' genera belong to the family Thelastomatidae. An existence of well-defined groups of genera in Thelastomatidae suggests the use of taxa with the subfamily rank. In the detailed revision of the nematodes parasitic in invertebrates, Kloss (1960) proposed several subfamilies of Thelastomatidae, and one of these, Hammer-schmidtiellinae Kloss, 1960, can be used to incorporate these phylogenetically close genera. Skrjabin et al. (1966) accepted this subfamily in their revision of Thelastomatoidea. The subfamily 'Hammerschmidtiellinae Chitwood, 1932' taxon was used in some publications (e.g., Gantait Venkat & Venkataraman, 2013). To our knowledge, Chitwood published in 1932 only one paper, which could have contained the diagnosis of this superfamily: 'A synopsis of the nematodes parasitic in insects of the family Blattidae'. An analysis of this publication did not reveal the diagnosis or any other mention of the new subfamily Hammerschmidtiellinae. Thus, it is in the revision of Kloss (1960) where this subfamily was proposed for the first time.
It can be concluded that the sequence of D2-D3 expansion segment of LSU rDNA is an informative locus for the study of the thelastomatid phylogeny
on the species-genus level but not on the subfamilies-families level. Molecular data have confirmed the monophyletic status of the group of the thelastomatid genera with the morphology resembling that of Hammerschmidtiella. The subfamily Hammerschmidtiellinae Kloss, 1960 can accommodate this set of genera. In the same time, phylogenetic analysis demonstrated that the sequences of two studied species of Blattophila clustered with representatives of different genera of thelastomatids suggesting the possibility that the genus Blattophila is not a monophyletic group but an artificial grouping of forms that are not closely related.
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Резюме. Дано описание нового рода и вида теластоматид - Davenema obtusum gen. sp. nov. (Thelastomatidae, Oxyurida). Эти нематоды были обнаружены в задней кишке тараканов, собранных на пляже острова Камигуин на Филиппинах. Наиболее примечательной особенностью описанных теластоматид является наличие двух крупных, сильно выступающих латеральных папилл на хвостовом конце самца, отсутствие у самцов спикулы и латеральных выступов на головном конце. Оболочки яиц D. obtusum gen. sp. nov. лишены крышечки. Показаны существенные различия в нуклеотидных последовательностях D2-D3 участка большой субъединицы рибосомы (LSU rDNA) между Davenema obtusum gen. sp. nov. и изученными представителями родов Hammerschmidtiella и Blattophila.
