Russian Journal of Nematology, 1993, 1 (2). 74 - 95
Phylogeny of the order Tylenchida (Nematoda)
Alexander Yu. Ryss
Zoological Institute of Russian Academy of Sciences, Universitetskaya embankment, I, Sankt-Petersburg, 199034, Russia.
Accepted for publication 30 November 1992
Summary. The structures of the most value for the macrotaxorlomy of the class Nematoda - amphid, phasmid. deirid, lateral field and head sensory organs are situated on the lateral radii of the nematode body or near them. It is proposed to consider all these organs as a complex structural unit: athe lateral complex*. Caudal alaeof males (bursa) also belong to the lateral complex. There are I) thenon-phasmidial caudal alae (phasmids are absent from the tail). 2) the pre-phasmidial caudal alae (caudal alae are situated anterior to the phasmids, 3) the phasmidial caudal alae (phasmids are situated on the caudal alae as phasmidial ribs, alae envelop the tail). Phylogeny of the order Tylenchida is analysed by comparison of the lateral complexes of the taxa. Atctylcrtchus is the most primitive taxon. Some amendments are made to the classificatioli by Siddiqi (1 986), which is considered closest to the riatural order. The order Tylenchida consists of 4 suborders, three of them (Tylenchina, Crico~iematina,Hexatylina) possess complexes of synapomorphic characters and therefore are considered to be monophyletic. The suborder Hoplolaimina is regarded as being paraphyletic, thuscontaining the remainder of the taxonomic divisions of the order. Hoplolaimina contains 2 superfamilies: I) Dolichodoroidea: Psilenchidae, Meiodoridae n. rank: Meiodorus, Uracllydor~ts, Ncodolichodorus, Hirsclimanniclla and 2) Hoplolaimoidea: Merli~iiidaen.rank, including Pratyletrcl~oid~s,Beloliolairnidae, (correspo~idiiigto Belonolaiminae sc'nsu Siddiqi, 1986). Tylenchorhynchidae and other families of higher plant parasites. Hoplolaimoidea differs from Dolichodoroidea by the structure of the phasrnidial caudal alae of males which envelops the tail, and by a lateral field in females and juveniles reaching the hyaline portion of the tail (in Dolichodoroidea the lateral field does not reach the hyalirie portion of the tail). Psilenchidae represent a paraphyletic group which is not defined by synapomorphic characters. The most primitive taxa of Tylenchida. including Atctylcr~cl~us,belong to this group. Keys for the identificatioli of the superfamilies and the families of the suborder Hoplolaimina are given. Key-words: phylogeny, morphology, evolutioti, new taxa, Merlinnidae 11. rank, Meiodoridae 11. rank.
The order Tylenchida includes free-living plant was theauthor of the first phylogenetic concept for the feeding and mycophagous nematodes, specialized class Nematoda as a whole. He argued the Rhabditid- plant parasites and arthropod parasites with Diplogasterid ancestry of the Tylenchida in the complicated life cycles with an alternation of modern context (Filipjev, 1934). This point of view was parthenogenetic and gamogenetic generations. The developed by Paramonov ( 1962, 1970) who proposed aim of this paper is an analysis of phylogenetic the hypothesis of the origin of the higher relations in the order, using a new approach. The phytoparasitic tylenchids and of the whole order from author proposes some changes in the order primitive fungus feeders. The most important among classification on the basis of this analysis. the more recent phylogenetic papers are: the Many nematologists investigated the phylogeny fundamental monograph by Siddiqi (1986), the joint as well as the classification of the order (Chitwood & set of articles by Fortuner, Maggenti, Luc, Geraertand Chitwood, 1950; Maggenti, 1971, 198 1; Andrassy, Raski <(A reappraisal of Tylenchina,> which was later 1976; Skarbilovich, 1978, 1980; Sumenkova, 1984; published as a separate volume (Fortuner et al., 1987- Drozdovsky, 1989). A prominent contribution to the 1988) as well as the series of articles by Chizhov and phylogenetic study was made by Filipjev (1934), who co-authors (Chizhov & Berezina, 1988; Chizhov & Kruchina, 1988, 1992). In general these recent of an analysis of the diversity of the lateral complex it phylogenetic papers consider Tylenchida separately is possible to define: I) the most primitive taxon of the from the general evolution of Nematoda. For this Tylenchida by comparison with the lateral complexes reason the choice of the main characters and of closely related orders; 2) the transformations of the evolutionary directions in the transformation series of initial lateral complex within the order; 3) how the these characters depend mainly on the point of view of lateral complex transformations are in concordance each author and not on detailed comparison of the with alternations in other characters and present a taxon with all possible uout-liersa. Such a comparison general view of the evolution in the order on the basis should define the choice of the most significant char- of these data. The classification by Siddiqi (1986) is acters. Usually on the basis of the chosen characters used as the basic one for this analysis as it appears to the sums of the plesiomorphies and synapomorphies be closest to the natural order and uses the greatest are calculated. Thereafter the phylogenetic diagram number of taxonomic characters. The family with dichotomous branching is constructed, using Myenchidae (parasites of the leech coelom) and the these calculations. family Myoryctesidae (parasites of amphibian muscles) were excluded from the examination as little The proposed approach. In this article the information is available on their morphology, Tylenchida is examined from general nematological especially on the structure of the lateral complex. taxonomic principles, as Filipjev did, but with much new knowledge of this group. The most important Review of lateral complex characters for Nematoda macrosystematics are structures situated on 2 lateral radii of a threadlike body. They are: an amphid (a paired cephalic chemoreceptor), a Peristomal complex of sensilla and the phasmid, peristomal cephalic sensilla, a lateral field subdivision of the anterior body end. The stomata1 and a cervical papilla (a deirid). The basis of this line opening with a complex of surrounding sensilla are is the lateral field - a paired surface structure of two located at the junction of the lateral radii of a body. As lateral hypodermic chords (Fig. I. A). These chords in other Nematoda, the first circle of the inner labial are extremely important structures for a basic plan of sensilla includes 6 pore-like structures; the second and the nematode anatomy. They are of particular the third circles of sensilla are also located on the head importance in a functional sense: nematode movement region, the sensilla of the third circle (cephalic proceeds by snakelike undulation in the dorso-ventral sensilla) being situated more laterally than the second planeand the lateral chords act as flexible columns for circle sensilla (outer lip sensilla) (Fig. 1. G); for the tubular nematode body. They support the ventral examples in Pratylenchus sensillulus (Anderson & and dorsal pairs of muscle fields, which are Townshend, 1985); Radopholus similis (Baldwin et antagonistic. The undulation proceeds owing to the al., 1983). Two lateral sensilla of the second circle, antagonism of these paired sets of muscles. Also there which are usually present in other Nematoda, are not are ventral and dorsal hypodermic chords. However in detected in Tylenchida. Therefore, the general tylenchids the ventral and dorsal chords are formula for the arrangement of the anterior end significantly less developed then the lateral cords, sensilla in Tylenchida is 6 + (4 submedian + 4 similarly in Secernentea and Chromadoria. The new submedian), this being a full set of sensilla. A approach here is to investigate the diversity of reduction in number of sensilla, a shift of inner labial structure of the lateral complex in the order sensilla (the lateral pair only or all of them) into a Tylenchida. The lateral complex here is regarded as a prestoma, and other transformations take place in complicated structural unit and not a sum of separate different groups. characters. This approach avoids calculations of sums It is necessary to compare the terminology used of synapomorphies and plesiomorphies. On the basis for the lip region in Tylenchida with that used for the Phylogeny of Tylenchida
dei ilp am. ISZ
m dch
Fig. 1. Morphology of the nematodes of the order Tylenchida.
A: Arrangement of structures of the lateral complex on the nematode body; 8: Transverse sectio~iof the body with the lateral chords and the bands (ridges) of a lateral field indicated; C-E: Types of male caudal alae (bursa): C - Pre-phasmidial adanal, D - Phasmidial, E - Non-phasmidial adanal; F.G:- Cephalic region: F - Lateral view, G - Face view. The corresponding projectionsare indicated by the dotted line. H: Diagram of vectors of forces in the cephalic regions of nematodes of the families Dolichodoridae and Belonolaimidae when the protractor muscles contract. For explanations see text. am - amphid, bpf - basal plate of inner cephalic framework, dch - dorsal chord, dei - deirid, cb - cephalic base, cf - cephalic framework, cp - cephalic papillae, cp + olp - cephalic papillae and outer labial papillae, ep - ekcretory pore, ilp - inner labial papillae, Ich - lateral chords, If - lateral field. Ifb - bands (ridges) of the lateral field. Isz - labial sensory zorre, m - muscle layer, olp -outer labial papillae, p - papillae of cephalic part, ph - phasmid, sto - stomatal opening, vch - ventral chord, ve - vestibulum extension, vu - vulva. non-Tylenchid Nematoda. The <
"d
Criconematina
HOPLOLAININA
f
Psilenchus
Meiodoridae n. rank.
Belonolaimidae
Hoplolaimoidea (part.)
HOPLOLAIMOIDEA
Fig. 2. Primary lateral complexes of the nematodes of the order Tylenchida.
The original lateral complexes, for the corresponding taxa are illustrated. The directions of evolution are indicated by arrows. The diversity of lateral complexes of the suborder Hoplolaimina, consisting of 2 superfamilies - Hoplolaimoidea and Dolichodoroidea (inside the rectangular contours) are illustrated in detail. The heavy arrows indicate the positions of the dorsal (dors.) and ventral (ventr.) sides of the nematode body. adanal pre-phasm. ca - adanal pre-phasmidial caudal alae. adanal termin. pre-phasm. ca - adanal terminal pre-phasmidial caudal alae, am - amphid, ca - caudal alae (bursa), cb- cephalic basis, cp+ olp -cephalic pnpillaeand outer labial papillae, dei - deirid, ilp - inner labial papillae, If - lateral field. Isz - labial sensory zone, non-phasm. ca - non-phasmidial caudal alae, ph - phnsmid, phl - phasmid-like structure. phasmidial ca - phasmidial caudal alae, phr - phasmidial rib, sto - stoma1 opening. A-A
0 -18 dors. vent. t-
J
Fig. 3. Diversity of oesophageal gland structure in the nematodes of the order Tylenchida. A-D: Lateral view; E-G:Transverse section A-A in the anterior part of the glandular body; H-J: Transversal section B-B in the posterior part of the glandular body (levels of sections A-A and B-B are marked in Figures 1-3 by lines with perpendicular arrows). A, E. H: The tylenchoid oesophagus; B. C: The lobed "hoplolaimoid" oesophagus - subventral glands are posterior to the dorsal one; B, F, I: The lobed "hoplolaimoid" oesophagus with an arrangement of the oesophageal-intestinal junction between primary subventral glands (the symmetrical type); C. G, J: The lobed *hoplolairnoid* oesophagus with an arrangement of the oesophageal-intestinal junction betwecrl the primary dorsal gland and one of the subventral glands (the asymmetrical type); D: The lobed oesophagus of the family Belonolaimidae and the subfamily Telotylenchinae of the family Tylenchorhynchidae: the dorsal gland is posterior to the subventral ones. The positions of the dorsal side of the body (dors.) and the ventral one (ventr.) are marked by heavy lines. ca - cardia, d - dorsal gland, dn - dorsal gland nucleus, in - intestine, oij - oesophageal-intestinal junction, ol - oesophageal lumen, sv - subventral gland, svn - subveritral gland nucleus.
secernentes is considered to be a slit-like, ventrally the other genera the amphid is positioned in the labial curved, postlabial amphid. This amphidial shape is sensory zone. Therefore Alelylenchus and Psibnchus primitive also for the subclass Chromadoria, and is may be considered as representing the most primitive considered to be the most primitive form for the whole form in the order Tylenchida. The amphid is wide class of Nematoda (Lorenzen, 1981). Therefore it is funnel-shaped in Psilenchus and slit-like, stretched logical also to consider that this amphidial shape is the longitudinally, ventrally curved in Alelylenchus most primitive in the Tylenchida. Of the above- (Geraert & Raski, 1987). Geraert and Raski (1987) mentioned taxa only Aletylenchusand Psilenchus have characterized this general anterior-end shape as being an amphid situated posteriorly in the cephalic base. In Filenchus-like, i.e. the amphid being postlabial, slit- Phylogeny of Tylenchida like, ventrally curved (the structure of the lateral slit-like amphid of Atetylenchus becomes transversal complex of Tylenchidae, to which Fibnchus belongs, (Psilenchus) and is repositioned in the labial sensory is examined below). Therefore the amphid of zone (Antarctenchus;Fig. 2). The stylet in Psilenchus Atetylenchus is an example of the most primitive is devoid of knobs, as in Atetylenchus. Stylet knobs are amphidial form and position. The transverse slit-like present in all other genera in the order Tylenchida. amphid of Psilenchus appears to be a development Also in Antarclenchus only four submedian papillae from the ventrally curved amphid of Atetylenchus. In remain from the peristomal sensilla of the second and SEM micrographs of Psilenchus sp. from New Zealand third circle (4 + 4) (Fig. 2). (Sher & Bell, 1975) the ventrally curved slit-like Doichodorus. In Dolichodorus the amphid amphids, located in the postlabial zone, were readily remains longitudinally stretched, postlabial (Fig. 2), apparent. Atetylenchus may therefore be considered as but the cephalic region in this genus is transformed the most primitive form in the order Tylenchida by its into a 4-lobed structure with a strongly developed lateral complex structure. This genus also possesses a labial disc. These developments of the lip region are weakstylet, lacking knobsand the primitive tylenchoid correlated with the enlargement of the stylet in oesophagus. Within the Tylenchida only Atetylenchus Dolichodorus. Nematodes of this genus are and Psilenchus possess a stylet without knobs. In other ectoparasites of roots. Similar changes of the lip region, tylenchids this protmsible stoma has 3 knobs, to which - an enlarged stylet, an enlarged labial disc and the the protractor muscles are attached. The stylet of presence of a 4-lobed lip region have developed in Atetylenchus resembles the tubular stoma of the parallel with the Belonolaimidae, which also are primitive Secernentea (orders Rhabditida, ectoparasites of roots. The parallel development of the Diplogasterida). A stylet without knobs also occurs in lip region shape in Dolichodorus and belonolaimids is the related order Aphelenchida, i.e. corresponds the believed to be the result of similar adaptation to the out-state for the character. In the tylenchoid protraction of the large stylet. oesophagus the glandular part forms a non-lobed The lip region is the bearing for the stylet compact body followed by the cardia, i.e. oesophageal prdtractor muscles. As every bearing, the lip region sphincter (Fig. 3. A). In the more developed should be steady to deformation displacements, specialized genera of Tylenchida the posterior part of caused by outer forces. The deformation can be elastic the oesophagus is transformed secondarily into the (reversible) or residual. With elastic deformation the gland lobe and the cardia is displaced anteriorly body shape is restored to the initial shape after the (Filipjev, 1936; Paramonov, 1970; Seinhorst, 197 1 ; cessation of loading, but residual deformation is non- Siddiqi, 1971; Ryss, 1987; - Fig. 3. D). Therefore reversible. The cephalic framework prevents non-re- Atetylenchus may be considered the most primitive versible deformation of the lip region arising from genus in the Tylenchida by the structure of the lateral contraction of the stylet protractor muscles. complex and other characters. The vector forces in the lip region are presented in / Fig. 1. H. The protractor muscles attach. to the body Evolution of the lateral complex in wall near the junction of the cephalic framework basal those genera of the suborder Hoplolaimina which are rela red to plate with the body wall. This point is marked on the A tetylenchus diagram by the letter A. Also the muscles may be attached to the basal plate of the framework or to the Psilenchus and Antarctenchus. Development of vestibulum extension (Fig. 1. F). The protractor the lateral complex in the line Atelylenchus - muscles contract during protraction of the stylet. The Psilenchus - Antarctenchus are evident. The force of the strain FI acts along the lines AB and AlBl development of the lateral complex concludes in a (Fig. 1. H). Here the outer surface of the lip region (the change of form and position of the amphid. The initial curved contour ACD) is influenced by an expansion force, and the base of the lip region (the straight the protractor muscles of the stylet. The high arched segment AE in the flatness of the cephalic framework lobed form of a lip region therefore should be basal plate) is influenced by a pressure force. considered as an adaptation to the increased pressure Naturally, the longer and more robust the stylet, the loading in the long-stylet tylenchids. greater are the expansion and pressure forces. It is Thus, the lobed, high arched, shape of a lip region caused by the enlarged mass of the stylet as well as by should be optimum for the maximum strains of the enlarged mass of the stylet protractor muscles. expansion and pressure arising from the stylet During expansion the tensile strength of the lip movement outside the body. Probably therefore the region surface is important. The curved contour ACD 4-lobed shape of the lip region arose independently in has a reserve of length for the expansion. This reserve Dolichodorus and Belonolaimidae, the two taxa of is characterized by the difference between the length ectoparasites with long stylets. of the curved segment ACD and the length of the According to the lateral complex, particularly in straight segment AD. The more curved the segment amphid shape, the genus Dolichodoruscould be traced ACD, the more stable the lip region is to the expansion from Atetylenchus only (Fig. 2). The set of secondary force. Therefore, the lip region in the long-stylet transformations in Dolichodorus are: deirid is tylenchs is highly curved. It can be considered as an reduced, lateral field transforms from the 3-band adaptation to cope with the increased loads. structure (4 incisures) in Atetylenchus into a Zband During loading the curve ACD tends to become one (3incisures) in Dolichodorus, tail is shortened and straighter. It means that the lip region undergoes the in connecting with it the initial adanal bursa of ring-shaped expansion strains during contraction of Atetylenchus has been transformed in Dolichodorus the protractor muscles. These strains increase, as the into the pre-phasmidial adanal-termina1,'i.e. into the curvatureof thecorresponding part of thecontour ACD terminal bursa 'with a distinct posterior gap between increases. The reserve of the cuticular surface in the tail and caudal alae (Fig. 2). form of longitudinal folds in the lip region is necessary Meiodorinae with its pore-like amphid located in for the tensile strength of this expansion strain. In Yhe the labial sensory zone it evidently may be traced only long-stylet tylenchs the lip region has the 4-lobed from Antarctenchus. In the Meiodorinae the stylet shape with longitudinal folds (depressions) between becomes massive and as a result of the tail shortening lobes. The lobed shape of a lip region can also be the pre-phasmidial bursa transforms from adanal into considered as an adaptation to the increased loads. adanal-terminal. The genus Hirschmanniella is The resistance of the cephalic framework base to closely related to Meiodorinae by the structure of the pressure depends not only on the solidity of the basal lateral complex. Earlier this genus was considered in plate of the framework (the vector of the resistance the family Pratylenchidae. Hirschmanniella differs force of skeleton material F2 along the axis AE is however from the Pratylenchidae and from other H) indicated on Fig. 1. but also on the projection of the higher hoplolaimoid families by the non-division into maximum radial line of the cephalic framework (Fig. sectors of the lip region into sectors (this feature is 1.8), the vector of the resistance force of skeleton peculiar to meiodorins as well) ;and by the lateral field material F3 along the axis EC) on the cephalic not reaching the hyaline portion of the tail terminus, framework base (F3' along the axis AE). Therefore, by the adanal bursa not reaching the terminus and by the greater the maximum radius of a lip region EC, the phasmids in males not forming ribs on the caudal passing through the radial septa (the blade) of the lip alae, as occurs in pratylenchids and other region skeleton, (i.e. the more high arched the outer hoplolaimoid families, but are arranged on the tail as contour of the lip region ACD) , the greater the solidity in Meiodorinae. These characters suggest that the of the skeleton base along the line AE. Also its meiodorins and Hirschmanniella be considered as a resistance is increased to possible strains, caused by family Meiodoridae n. rank consisting of 2 subfamilies: Phylogeny of Tylenchida
Meiodorinae including the genera Meiodorus and also do not reach the tail terminus. The bursa of these Brachydorus and Hirschmanniellinae including the taxa is pre-phasmidial, adanal. In Pratylenchoidesand single genus Hirschmanniella only. Merliniinae the bursa becomes terminal, caudal alae SEM photographs of the lip region in Meiodorus enclosing the tail tip, - in connection with the lateral festonatus have been published (Doucet, 19851, of field displacement to the terminus. Phasmids, that in Hirschmanniella: H. miticausa (Bridge et al., 19831, Atetylenchus, Psibnchus and Antarctenchus are H. spinicaudata (Aubert & Luc, 1983, H. mucronata positioned posterior to the caudal alae on the tail, are (Siddiqi, 1986). Six inner lip papillae and 4 submedian situated in Pratylenchoides and Merliniinae on the groups each of 2 papillae are seen distinctly in the caudal alae, forming the so-called <
Following the pattern of phylogenetic relationships developed in the analysis above (Fig. 5) the evolution of the niches for the order Tylenchida may be proposed. It is premature to analyse the evolution of the nutrition requirements and food sources of different taxa. Biotopes colonised by Aletylenchus, Psilenchus, Anturctenchus and Tylenchina may be considered primitive niches for the order. These are litter and the above-ground moss- lichen layer. The descendants of the primitive Tylenchida have progressed to parasitism in and on roots of the higher plants from these initial niches. Thus the majority of Hoplolairnina and Criconematina RHABDITIDA I have moved into the mineral soil layers. From the initial niche, more branches, including Diiylenchus- like forms, evolved as entornoparasites or parasites in SECEBNENTEA galls on aerial parts of plants i.e. Hexatylina. CHROMADORIA: LEPTOLAIMINA The origin of Tylenchida
The author of the present paper shares the view that Tylenchida and Aphelenchida originated from Rhabditoid-Diplogastcroid ancestors (Fig. 5). These Fig.5. The diagram of phylogenetic relationships of the order Tylenchida and of the ancestry of the latter. views have been described in classical papers by Filipjev (1934), Chitwood & Chitwood (1950), worm body from an obstacle to a movement. The Paramonov (1 970) and Andrassy (1976). The posterior ovary and oviduct have been considered as primitive Tylenchida - Alctylenchus - correspond to the obstacles (Paramonov, 1970; Chizhov & Kruchina, the characters of the lower Secernentea by the 1988, 1992). But when the vulva is moved to the structure of the lateral complex: ventrally curved posterior the posterior body cavity becomes filled postlabial amphid, presence of a deirid and phasmid, again by the anterior genital tract. Therefore, the and having3 bandsof the lateral field. According to the above-mentioned point of view appears unconvincing. opinions of some authors, Secernentea may have In three non-phasmidial orders - Tylenchina, originated from the Chromadoria (Andrassy, 1976; Hexatylina, Criconematina reductions in the posterior Drozdovsky, 1989). The closest to Secernentea taxa body part of females are present. The posterior branch among Chromadoria are the Plectidae which possess a of the female reproductive tract and the tail phasmids deirid and Teratocephalidae which possess phasmid- are reduced. Probably this is connected with an like papillae in the tail. These two families were related opposition of the more mobile part of the body anterior by Lorenzen (1981) to the suborder Leptolaimina in to the vulva to the less mobile part posterior to the the order Chromadorida, which represents the vulva. However in the higher Hoplolaimina (the paraphyletic group located at the base of the phyletic majority of Hoplolaimoidea) a deirid located in the tree of Chromadoria as well as the whole class anterior body part is reduced. Nernatoda. Thus it may be supposed, based upon the lateral complex structure of Ateiylenchus that the Meiodoridae and the group of higher hoplolaimoid origin of the order Tylenchida proceeded very close to families: Tylenchorhynchidae, Hoplolaimidae, the time when Secernentea split from the primitive Pratylenchidae, Rotylenchulidae, Nacobbidae, Chromadoria. Meloidogynidae, Heteroderidae). Phasmid present Keys to the suborders, superfamilies and families (except Aphasmotylenchus in Hoplolaimidae). Lateral of the order Tylenchida as well as diagnoses and field with 4, more rarely 1, 3, 6 incisures reaching taxonomic volumes of the groups, whose contents hyaline part of tail terminus (superfamily differ from that in classifications by Siddiqi (1986); Hoplolaimoidea) or not reaching it (superfamily Fortuner et al., (1987, 1988); Chizhov and Kruchina Dolichodoroidea). Bursa pre-phasmidial: adanal, (1988, 1992), are proposed. adanal-terminal or phasmidial terminal. The paraphyletic group, lying at the base of the Key to suborders of the order phylogenetic trunk of the order Tylenchida. Tylenchida Type family: Hoplolaimidae Filipjev, 1934.
1. Phasmids present on tail (except Ayhasmotyl- enchus), female reproductive system usually paired ... Key to superfamilies of ...... Hoplolaimina Hoplolaimina - Phasmids absent, phasmid-like structures may 1. Male caudal alae enclosing tail tip, phasmidial: present in postmedian body part lying dorsally from phasmids form phasmidial ribs on alae, lateral field of lateral field, female reproductive system unpaired ...... larvaeand females reach hyaline part of tail terminus ...... 2 ... Hoplolaimoidea 2. Phasmid-like structures present dorsally ...... - Male caudal alae adanal or adanal-terminal, from lateral field in postmedian body part (usually pre-phasmidial: phasmids posterior to caudal alae on at level of vulva) ...... Tylenchina the tail, lateral fields of larvae and females do not - Phasmid-like structures in postmedian body reach hyaline part of terminus at significant distance part absent ...... 3 (in Neodolichodor~rs only in juveniles of the youn- 3. Oesophagus criconematoid: metacorpus fused gest free stages) Dolichodoroidea with procorpus, stylet usually occupies whole pro- ...... corpus (in redrawn up state), amphids lateral, slit- Superfamily Hoplolaimoidea like, dorso-ventral, oral aperture I-shaped; parasites Filipjev, 1934 (Paramonov, 1967) of plant roots ...... Criconematina - Oesophagus non-criconematoid, metacorpus Diagnosis. Hoplolaimina. Male caudal alae not fused with procorpus, amphid dorso-sublateral, phasmidial, enveloping tail. Phasmids form slit-like or pore-like, oral aperture rounded pore- phasmidial ribs on tail. Lateral fields of females and form. Mycophages and entomoparasites, parasites of larvae reach hyaline part of tail terminus. aerial organs of higher plan6 ...... Hexatylina Type family: Hoplolaimidae Filipjev, 1934.
Suborder Hoplolaimina Chizhov & Key to families of Hoplolaimoidea Berezina, 1988 (syn. Heteroderata Skarbilovich, 1959) 1. Deirid present ...... Diagnosis. Tylenchida. Amphid postlabial: ...... Merliniidae Siddiqi, 197 1 (n.rank). longitudinal, ventrally curved, V-shaped or dorso- - Deirid absent ...... 2 ventral; or labial: dorso-vental, sometimes pore-like. 2. Lip region 4-lobed. Amphidial apertures on the Deirid present (Psilenchidae, Merliniidae including end of longitudinal non-annulated lateral tubes, Pratylenchoides) or absent (Dolichodoridae, situated in theanterior part of annulated lip region ...... Phyloge~~yof Tylenchida ...... Belonolaimidae Whitehead, 1960. Family Merliniidae Siddiqi, 1971 - Lip region truncated, conical or rounded, am- (n.rank). phids are small slits directed dorso-ventrally or pore- Diagnosis. Hoplolaimoidea. Deirid present. like, located on the lip sensilla zone ...... 3 Amphids labial, small dorso-ventral slits or pore-like. 3. Female body lemon-shaped or saccate ...... 4 Lateral field with 4 or 6 incisures. Terminal tail cuticle - Female elongate, cylindrical ...... 8 abnormally thickened. Vulva usually with epiptygma. 4. Oesophageal glands in the form of lobe, lying Spicules usually tubular. on the anterior part of intestine dorsally ...... 5 Type-genus: Merlinius Siddiqi, 1970. - Oesophageal glands in the form of lobe, lying Other genera: Prutylenchoidcs Winslow, 1958 on the anterior part of intestine ventrally ...... 6 (included in the family for the first time), 5. Female reproductive system paired, lip region Amplimerlinius Siddiqi, 1976, Geoccnurnus Thorne & of males hemispherical, oesophagus and stylet in ma- Malek, 1968, Hexudorus lvanova & Shagalina, 1983, les degenerated, gubernaculum protrusible ...... Nagelus Thorne & Malek, 1968, Scutylenchus ...... Achlysiella Hunt, Bridge & Machon, 1989 Jairajpuri, 1971. (Pratylenchidae Thorne, 1949). - Female reproductive system unpaired, lip region Family Tylenchorhynchidae of males truncated, conical, stylet and oesophagus of Eliava, 1964 males well-developed, gubernaculum non-protrusible...... Nacobbidae Chitwood in Chitwood & Diagnosis. Hoplolaimoidea. Deirid absent. Chitwood, 1950 (Nucobbus Thorne & Allen, 1944). Amphids labial, small dorso-ventral slits or pore-like. 6. Orifice of dorsal gland at the distance equal to Lateral field'with 4, rarely 3 incisures. Oesophageal the stylet length from stylet base or more ...... glands in a bulb, abutting intestine, cardia lying ...... Rotylenchulidae Husain & Khan, 1967. posterior to glands; or glands form a lobe, a dorsal - Orifice of dorsal gland at the distance shorter gland (with a large nucleus) lying at the end of a lobe. than stylet length from stylet base ...... 7 Type-genus: Tylcnchorhynchus Cobb, 19 13. 7. Excretory pore anterior to median bulb ...... Meloidogynidae Skarbilovich, 1959. The family includes only subfamilies - Excretory pore posterior to median bulb ...... Tylenchorhynchinae Eliava, 1964, Trophurinae ...... Heteroderidae Filipjev & Schuurmans Paramonov, 1967, Macrotrophurinae Fotedar & Stekhoven, 1941. Handoo, 1978 (3 subfamilies with a non-lobed 8. Oesophageal glands in a bulb abutting inte- glandular part of an oesophagus) and Telotylenchinae stine with cardia lying posterior to glands; if glands Siddiqi, 1960 (with a lobe of oesophageal glands, in form a lobe extending over intestine then the dorsal which the dorsal gland is the longest). Contents of all gland (with large nucleus) is the longest ...... these subfamilies are considered in the senseof Siddiqi ...... Tylenchorhynchidae Eliava, 1964. (1986). - Oesophageal glands forming a lobe extending over intestine, subventral glands (with small nu- Superfamily Dolichodoroidea Chitwood in Chitwood & Chitwood, cleus) are the longest ...... 9 1950 (Siddiqi, 1986) 9. Lip region low, broad, the ratio of stylet length to lip region width not more than 2.5 ...... Diagnosis. Hoplolaimina. Male caudal alae pre- ...... Pratylenchidae Thorne, 1949. phasmidial (phasmids outside the caudal alae, on the - Lip region high, narrow, the ratio of stylet tail), adanal or adanal-terminal. Lateral field of length to lip region width 3 or more ...... females and juveniles (in Neodolichodorus - in ...... Hoplolaimidae Filipjev, 1934. juveniles of early stages) does not reach the hyaline part of terminus; if it reaches, so in the form of a single Subfamily Meiodorinae Siddiqi, incisure. 1976 Type-family: Dolichodoridae Chitwood in Diagnosis: Meiodoridae. Glands in posterior bulb Chitwood & Chitwood, 1950. Other families: Psilenchidae Paramonov, 1967, abutting intestine. Male caudal alae adanal-terminal. Meiodoridae Siddiqi, 1976 (n. rank). Type-genus: Meiodorus Siddiqi, 1976. Other genera: Rruchydorus de Guiran & Germani, Key to families of Dolichodoroidea 1968, Neodolichodnr~tsAndrassy, 1976.
1. Deirid present ...... Psilenchidae Subfamily Hirschmanniellinae - Deirid absent ...... 2 Fotedar & Handoo, 1978 2. Amphid longitudinal slit-like, coming outside Diagnosis: Meiodoridae. Glands in the form of the labial zone into cephalic basis, lip region 4-lobed lobe extending over intestine. Male caudal alae adanal with prominent labial disc ...... to subterminal...... Dolichodoridae (Dolichodorus Cobb, 19 14) Type-genus: Hirschmunniella Luc el Goodey, - Amphid pore-like, on the anterior margin of 1964. labial zone, indistinct, lip region truncated, conical to No other genera. rounded, with unsignificant labial disc or without disc ...... Meiodoridae Siddiqi, 1976 (n. rank) REFERENCES
Family Dolichodoridae Chitwood in Anderson. R. V. & Townshend, J. L. 1985. A new species of root Chitwood & Chitwood, 1950 lesion nematode (Pratylenchidae: Nematoda) in Canada, with a scanr~ingelectron microscope study of its head morphology. Diagnosis: Dolichodoroidea. Amphids Carradiarr Jofrrtrol of Zoology 63: 2378-2382. longitudinal slit-like, coming outside the labial zone Andrassy, 1. 1976. Evolutiotr as a busis for tltc systettrufizaliotz of into cephalic basis, lip region 4-lobed with prominent trc~trrcltodrs.Lol~dol~, UK, Pitma11Publishir~g. 288 pp. labial disc. Male caudal alae pre-phasmidial, adanal- Aubert, V. & Luc M. 1985. Observatio~~au microscope electronique terminal, - i.e, there is a gapat the posteriorsideof ala, a balayage de Hirschrtrurrrriell spirticuudala (Sch. Stekh., 1944) (Nemnta: Pratylenchidae). Revue dc Nenratologic 8: separating terminus from bursa1 ala. 179-181. Type-genus: Dolichodorus Cobb, 19 14. Baldwin, J. G., Luc, M. & Bell, A. H. 1983. Cor~tributionto thestudy No other genera. of the ge~~usProtyl~rrclroidc~s Wit~slow (Nematoda: The monotypic group, differing from other Tylenchid;~). K~vrrc.dc N~~trrcitologic~6: 1 1 1 - 125. families by shape of lip region and amphidial aperture Bridge, J., Mortimer, J. J. & Jackson, G. V. H. 1983. form. Hirschrrrurrrrit~llur~riticorrsu r~.sp. (Nematod;~: Pratylenchidae) and its pathoge~~ecityon taro (Colocasi:~escule~~ta). Revutp de Family Meiodoridae Siddiqi, 1976 Nct~rutologie6: 285-290. (n.rank) Chitwood, B. G. & Chilwood, M. B. 1950. At1 lrrtroductiorr to Ncrtrutology. Baltimore, Mor~umcr~talPrint Co. 21 3 pp. Diagnosis: Dolichodoroidea. Amphid pore-like, Chizhov, V. N. & Berezina, N. V. 1988.IStructure and evolution of on the anterior margin of labial zone, lip region the female ger~italsystcm of nematodes of the order Tylenchida (Nematoda). 2. Primary didelphic species). Zoologichtsky truncated, conical to rounded, with insignificant labial Zlrurrru167: 485-494. disc or without disc. Male caudal alae pre-phasmidial: Chizhov, V. N. & Kruchina, S. N. 1988. IPhyloget~yof thenematode adanal, adanal-terminal, subterminal. order Tylenchida (Nematoda) I. Zoologich~~skyZhurtrul 67: Type-subfamily: Meiodorinae Siddiqi, 1976 1282-1 293. Other subfamily: Hirschmanniellinae Fotedar & Chizhov, V. N. & Kruchina, S. N. 1992. [The systematics of thc Handoo, 1978 nematode order Tylet~chida (Nematoda) 1. Zoofogicl~esky Phylogeny of Tylenchida
Zhurna17 1: 5- 1 6. Ryss, A. Y. 1981. [Morphoge~lzsisof the female genital system in the Doucel, M. E. 1985. A new species of Meiodorus Siddiqi, 1976 superfamily Tylerlchoidea (Nematoda) 1. Parozito/ogiya 15: (Nematoda: Tylenchida) from Cordoba, Argerltilia. Revue de 533-542. Norrofologie 8: 53-57. Ryss, A. Y. 1987. [Types of the parasitism of the plant nematodesand Drozdovsky, E. M. 1989. [On theclassificatioli of theclassNematoda the problem of all evolution of the superfamilies Tylenchoidea to thesubclasses level and on the phyloger~eticrelations between and Hoplolaimoidea (Tylenchida)] . Parazifologiclreskij some Nematoda taxa belonging to the Chromadoria line of sbornik, Zoologicallrrstitute of the USSR Acuderny of Sciertces evolution]. Proceeditrgs of tlreZoological Itrstituteof the USSR 34: 169-191. Acaderny of Sciences 194: 39-59. Ryss, A. Y. 1988. [Root Parasitic Notratodcs of the Fartlily Filipjev, I.N. 1934. The classificutiotr of tlrefi-ee-livirrg rretr~atodes Pratylerrclrid~~i~(Tyletrchido)of the World Fautra] . Leningrad. and their relatiorr to the parasitic ttcrtrotodes. Smithsoniati Nauka. 368 pp. Ilistitution, 8 pl, 63 pp. Ryss, A. & Krall, E. 1981. Classification of the superfamilies -Filipjev. I. N. 1936. Ueber freilebetide und pfla~~ze~iparasitische Tyle~~choideaand Hoplolaimoidea with notes on the phylogeny Gatturigen der Tylenchinen. Travoux de fItrstitrct Zoologiquc, of the suborder Tylenchilia (Nematoda). Procerditrgs of the rle PAcodemie des Sciertces dc, f URSS 3: 537-550. Acodetrty of Scic,rrcts of tire Estoniort Republik. Diologia 30: Fortuncr, R., Geraert. E.. Luc, M., Maggenti, A.R. & Raski, D. J. 288-298. 1987-1988 (Contributors). A reappraisal of Tylet~china Seinhorst, J. M. 1971. The structure of the glandular part of the (Nemata). Extraits de: Revue de Nernatologie 1987, 10: 127- oesophagus of Tyletlchida. Nettrutologica 17: 43 1-443. 232 (parts 1-8), 10: 409-444 (part 10); 1988, 1 1 : 159-1 88 Sher, S. A. & Bell, A. H. 1975. Scarl~li~~gelectrotl micrographsof the (parts 9, 1 I). anterior region of some species of Tylerlchoidea (Tylenchida: Gcraert. E. & Raski, D. J. 1987. A reappraisal of Tylenchina Nematoda) . Jourtrul o/Nerrra!ology 7: 69-83. (Nemata;. 3. The family Tylenchidae Orley, 1880. Revlcc. de Siddiqi, M. R. 1971. Structure of the oesophagus in the classification Nenratologie 10: 1 43- 1 6 1. of the stlperfamily Tyle~~choidea(Nematoda). in dint^ Journal Lorenzen, S. 1981. Entwurf eines pbyloger~etischen Systems der of Nettrutology 1 : 25-43. freileber~denNematoden. Veroffentlichurrgerr des Irutituts /lrr Siddiqi, M. R. 1978. The unusual positiorl of the phasmids in Mc~eresforsckung in Brerrrerl~uvetr, Suppleme111 17. Coslettchus costutus (De Mali. 1921) get]. n., comb. n. and Komissio~isverlagFraliz Leuwer. Bremen, 472 S. other Tylerlchidae (Nematoda: Tyle~ich~da).Nentutologica 24: Luc, M. & Fortuner, R. 1987. A reappraisal of Tylenchinn 449-455. (Nemata) .5. The family Dolichodoridae Chitwood et Chitwood, Siddiqi, M. R. 1980. The origin and phylogerly of the nematode 1950. Revue de Nerrratologie 10: 177- 18 I. orders Tylerichida Thorne, 1949 and Aphelenchida n. ord. Maggenti, A.R. 1971. Nemic relationships and the origirls of plant Hebrrirrtlrological Abstract, Ser. B. 49: 143- 170. parasitic nematodes. In: Plartt Parasitic Ncrtrcltodes. (M. Siddiqi. M. R. 1986. Tyli~rrclridu:Parusites of Plattts ntrd Insects. Zucherman, W.F. Mai & R. A. Rohde. Eds.) pp. 65-81. New Serit Albans, Commoliwealth Agricultural Oureaux. 645 pp. York, London, Academic Press. Skarbilovich, T. S. 1978. [A short classification of high taxa of the Maggenti, A. R. 1981. General Nettralology. New York, Heidelberg, nematodes from the order Tyle~ichida Thorne, 19491. Berlin, Springer Verlag. 372 pp. Byulletetr' Vsesoyuzt~o~oltrstituto Gcfrtrintologii 23: 31 -35. Paramonov, A. A. 1962. [Principlts of the Pltytolrelrtritrtl~ology]. Skarbilovich. T. S. 1980. [A short taxo~lomicsystem of families, Vol.l., Moscow, Nauka. 480 pp. subfamilies and genera with type speciesof the nematodes in the Paramonov. A. A. 1970. [Prittciples of tl~ePlrytohrlrtrirrtlrology]. order Tyle~ichidaThor~ie, 19491. Byullet~~t~'Vsesoyuznogo Vol. 3. Moscow, Nauka. 256 pp. Irrstitutu Geftrritrtologii 26: 66-79. Raski. D. J. & Maggenti, A. R. 1983. Tylenchidae: Morphological Sumenkova, N. 1. 1984. [Colilemporary views or1 the origiri arld diversity in a natural evolutionary group. In: Corrcepts itr evolutiori of the nematodes of the order Tylenchida]. Itogi Nernatode Systenratics. (A. R. Stone, H. M. Platt & L. F. Nauki i Telrtliki. Moscow, VINITI 4: 5-27. Khalil. Eds.) pp. 13 1-1 42. London, Academic Press. Yuen, P. H. 1966. Further observaliolis on NelicotyCtrchus vr~lgc~ris Roman, J. & Hirschmann. H. 1969. Embryogenesis and Yuen. Nrrrrafologicu 1 1 : 623-637. postembryogenesis in species of Pratylencl~us (Nematoda: Zuckerman, B. M. & Slrich-Harari, D. 1963. The life stages of Tylenchidae). Proceedirrgs of tlrc Helttrir~thologicalSociety of HelicotyLtichus trrrtlticitrctus (Cobb) ill banana roots. Washittgtott 36: 164- 174. Nettuitologicu 9: 347-353 A. Ryss
P~ICCA.m. @nnore~unHeMaTon o-rpnna Tylenchida (Nernatoda). Pesloue. CTPYKT~~LI,~a~6onee BaxHble mu MaKpoTaKcotioMnn Knncca Nernatoda: a~@b~n,@an~un, nefipnn, 6oaosoe none, OKO~O~OTOBO~~KOMflneKC CeHCMnJl - PaCnOnOXeHbl Ha ~OKOB~IXJlyKlaX Tens MnM s6nn3u 0T HWX. npemarae~cupaccMarpneaTb wx KaK enuHylo cnoxHylo c~py~rypyu npMcnobtTb eil ~asoa~neuna~epanbtlb18 KOMnneKC*. K naTepanbHoMy KOMIlneKCy Tylenchida OTHOCUTCSI M 6ypca CaMUOB, KOTOpau MOXeT 6blTb ~~c@~DMM- n~anbH0fi(Ha XBOCTe OTCYTCTBYIOT (bil3MM~bl).npen@a3MMnManbt!ofi (6ypcanbHble Kpblnbfl ptlCflOnoXeHbl Ilepen @as~nna~n)u @a3~nnuanb~ofi (@an~nnb~ pacnonoxetibl Ha 6ypcanb~blxKpblnbnx u Rune 6yp~anbHbl~pe6ep. 6ypca oxeaTbrsaeT XBOCT).@unore~na oTpana Tylenchida npoatianu~upoaa~anyTeM cpaeHeHnn naTepanbHblx KOMflneKCOB. He~aTonblPOna Atetylencl~usCnenyeT PaCCMaTpclBaTb KaK ~an6oneenpnMtITnRHble. Han6onee 6nu3~a K ~CT~CTB~HHO~~CMCTeMil HeMaTOn, flpeWOXeHHan Siddiqi (1986). B paMKaX OTpuna Tyler~chidapa:CMZlTpMBaIOTCfl 4 nonoTpnna, u3 KOTOP~IX TPM: Tylenchina, Criconematina, Hexatylina 06nanalo.r KoMnneKcaMn cn~ano~op@uil (MOHO@W~~TM'IH~I),a Hoplolairnina npencTaanner co6ofi napa@une~u~~ec~ufiocTa-roK TaKcoHoMuvecKoro rpynnuposaHnn o-rpwna. Hoplolaimina BKnlotlaeTnea Han~eMefi~TUa:Dolichodoroidea (Psilenchidae, Meiodoridae n. rank.: Meiodorus, Rraclrydorus, Neodolicl~odorus, Hirscl~rrrut~niella,Dolichodoridae: Dolichodorus) n Hoplolaimoidea (Merliniidae n. rank.. BKnmllamuee Prutyletzcl~oides, Belonolaimidae, cooTseTcroyloqee Belonolaiminae sensu Siddiqi, 1986, Tyle~~chorhynchidae,Hoplolaimidae u npyrne ce~efic~naB~ICLIJMX @TO- napa3u~os).floplolairnoidea ornnxlae-rca OT Dolichodoroidea oxoa~b~oa~ouefixeoc~ @an~wnc1anb~oil6ypcofi caMqos M nOCTWratOqWM ~M~~MHOBO~(30HbI XBOCTa ~OKOB~IMnOneM nMWlHOK M CaMOK (y Dolichodoroidea 6ypca npen@a3~nnnanb~an,6o~osoe none He nocTnraeT IWI~MHOBO~~~OH~IXBOCTB). Psilenchidne npencraenneT coboil llapa@~neT~4e~~ylOrpynny, He 06'be~M~~e~yloCMHB~~OMOP@MWMM, KYAa OTHOCHTC%l ~au6oneeIlPMMHTHBHble Tylenchida. uKnloqaa Atetylcrlchus. npenc~aone~K~IO~I mu onpeneneclnu nonoTpanou, a TaKxe ~ance~efic~on nonce~eAc~snonoTpnna Hoplolaimina.