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A REAPPRAISAL OF "IYL,ENCHINA (NEMATA) 1. FOR A NEW APPROACH TO THE OF TYLENCHINA

Michel LUC",Armand R. MAGGENTI**, Renaud FORTUNER***, Dewey J. RASKI** and Etienne GERAERT**** * Muséun1 national d'Histoire naturelle, Laboratoire des Vers, 61, rue de Buffon, 75005 Paris; ** Division of Nematology, University of California, Davis, CA 95616, USA; *** California Department of Food and Agriculture, Analysis and Identification (Nematology), 1220 N. Street, Sacramento, CA 95814, USA, and **** Rijksuniversiteit Gent, Instituut voor Dierkunde, Ledeganckstraat 35, 9000 Gent, Belgium.

Duringthe last three decades -parasitic Multiplication of genera also occurs in taxa have received increasing attention. This was containingnumerous species and where groups of due mainly to the discovery during the years between species can be defined, often using only one character 1943-1953 of the first efficient nematicides, DD, EDE and notof primary importance.Three examples maybe and DBCP. This discovery gave a strong impetus to cited ;in thegenus , some species may have established nematology laboratories and led tothe six nuclei (instead of the normal number of three) in the establishment of laboratories in previously " virgin ", or glandular part of the esophagus. Al1 other characters are nearly so, territoLes. As a result, there was an increase identical inthe two groups ofspecies, taking into in the numberof nematologists and taxonomicactivity. account specific variation. Nevertheless, the genus Bai- This is particularly truein those areas new to rolaimus hasbeen proposed for species having six nematology, because thesoi1 fauna is virtually unknown esophageal nuclei, Hoplolaimus being restricted to those and taxonomy is one of the few activities fitting with species having only three esophageal nuclei. Another limited material means, that too often is the situation of example in the genusHoplolaimus pertains to H. califor- young laboratories. nicus, in which the two enlargedphasmids are both As a proof of this impetusto taxonomy, we may refer posterior to thevulva instead of being situated with one to Figure 1 where the proposals for new generic taxa anterior to the vulva and the otherposterior; here too a of Tylenchina are summed up from 1913 to 1983. One new genus, Hoplolaimoides, has been proposed, based may see that theslope of the curve changesabruptly, in on this unique character for a single species. In thevery the years 1953-1957. homogeneous genus Radopholus, in two species out of Some of the recently proposed taxa we may cal1 about 30 the males are described as having a terminal " valid " taxa because theyrepresent well individualized instead of a subterminal bursa as is common to al1 the forms, notat al1 fittinginto heretofore described other species. This character alone has been used to corresponding taxa.At theopposite end of the propose the genus Neoradopholus to contain these two spectrum, too many taxa,mainly genera, have been species. proposed as new when anothersolution could have been These actions may stem from a preconceived idea to enlarge the definition of a preexisting corresponding about the optimal size of a genus. Some taxonomists taxon. In some cases one reads statements suchas : " the believe that a genus with more than 50 or 60 species genus C is proposed as new because it is intermediate becomes unmanageable and must be Split. We assume between genera Aand B "; in such cases the first action to the contrary that the number of species in a given . should have beento examine the possibility of fitting the genus may vary from one toany number. We agree that species of genera A and B together with the species of in large genera specific identification is difficult; how- genus C, in a single genus or, at least to enlarge the ever to facilitate the identification it is often possible definition of either genus A or B to include the species to define within the genus, << groups B having no taxo- of c. nomic value and no nomenclatural status, as did for

* Nenzatologist of ORSTOM. *** Associate in Division of Nentatology, University of California, Davis, CA 95616, USA.

Revue Nématol. 10 (2) :127-134 (1987) 127 M. Luc, A. R. Maggenti, R. Fortuner, D. J. Raski & E. Geraert

example Geraert (1965) for Purutylenchus or Mulvey (1972) for Heterodera. Excessive splitting of genera results in the accommo- 2 oc dation in one genus of only those species very close to each other; this leads to a oligomorphic D genera (we will define and discuss this concept below). Then,after division of a genus intoseveral genera, the original genus is often raised to the rankof subfamily to reestablish the relationships between these new genera. In turn subfa- milies are raised to family rank, families to superfamily 15C rank, etc. This affects even suborders and orders as four new suborders (Sphaerulariina, Hexatylina, Myenchina, Criconematina) recently have been proposed within the orderTylenchida [Heteroderina (= Heteroderata) Skarbilovich, 1959 apparently has never been accepted by other taxonomists] and the suborder Aphelenchina has been raised to the rank of order, Aphelenchida. 1 oc We cal1 this phenomenon “ taxonomic inflation ” as taxa are devaluated at each step. As a consequence of this inflation the numberof suprageneric taxa becomes excessive in proportion to the number of genera. For example, in theclassification of proposed by Fotedar and Handoo(1978), 158 genera in the suborder Tylenchina are distributed into9 superfamilies, 32 families and 55 subfamilies; this represents ratios of 50 17.6 generaper superfamily, 4.9 per family,2.9 per subfamily. theIn most recent comprehensive classification (Siddiqi, 1986), the Tylenchida encompass 25 five suborders, eleven superfadies, 29families, 64 subfamilies (of which 24 are monogeneric) and 200 nominal genera. It is difficult to believe,when we compareNemata to other phyla, thatthe tylenchids igr?~ 1;) 2; 2;) 34 3; 4; 4; 54 5; 64 6; 7; 7Q 8; contain such a diversity of structures and forms thatso many generic and suprageneric taxa are needed to Fig. 1. Cumulativeannual number of genera described in accomodate them. Tylenchids are very much alike in Tylenchina from 1913 to 1983. their anatomy. Maggenti(1981) rejectedthis inflationary approach, based principally onminute morphologic differences, andaccepted only seven families within biology and failure to apply principles of evolution Tylenchida based on their morphology and biology. accounts for the inflation of the suprageneric taxa and An undesirable consequence of this situation is that is most apparent at the generic level where genera are the definition of the suprageneric taxadiffers according proposed for thesake of identification and nothingelse. to each taxonomist. It is evident that the concept, and Forone hundred years after the publication of the content, of the family Tylenchidaeare very different Darwin’s “ Origin ” only one school of classification was for Fotedar andHandoo (1978) and for Maggenti(1981) recognizable, and seemingly the school had not well or Siddiqi (1986). It isnow impossible to cite a thought outmethodology (Mayr, 1981). The underlying suprageneric taxon, and insome cases a genus, without theme of classifications proposed during this periodwas adding “ sensu X ” or “ following Z ”. to base classification on phylogeny and thereby reflect degree of relationship. Inthe 1950’s and ~O’S, Therefore, thepresent status of the taxonomyof taxonomistsbegan to scrutinize andquestion the tylenchids is unstable and if new taxa continue to be seeming arbitrariness and lack of methodology of the proposed atthe rate that has prevailed for the last so-called Darwin system. As a result, two new schools 20 years,then the situation canonly become worse in the of taxonomy emerged. Numerical phenetics fmt articu- future. lated by Sokal and Sneath (1963) and cladistics, whose We believe that this presentunsatisfactory status has conceptual spokesmanwas Hennig (1950). Mayr (1981), resulted from the almost total lack of interest for the during this same period, brought a more explicit ar- evolutionary approach that seeks relationships on the ticulation to Darwin’smethodology, and this system basisof morphology and biology. The disregard of became known as evolutionary taxonomy.

128 Revue Nématol. 10 (2) : 127-134 (1987) Reappraisal of Tylenchina 1. New approach of taxonotny

Inthe so-called numericaltaxonomy (phenetics), offers the broadest, most flexible and least restrictive numerous characters are listed without preconceived base on which to build a classification that more truly choice, thennumbered and their relationships and reflects the phylogeny of those nematodes included in groupingsmathematically analyzed. Numerical the suborderTylenchina. Both numerical pheneticsand phenetics has proved largely unsuccessful because the cladistics are deemed by us to be too restrictive and classifications produced varied according to characters limited in retrievable information to beuseful in or programs of computationchosen. Therefore, the designing a higher classification. claim that results are objective and repeatable were not Another problemthat must beaddressed is that, until always justified (Mayr, 1981).Objectivity for this now and with few exceptions, the “ key characters ” used appraisal is also disclaimed since subjective biological for thepractical identification of species and genera, and criteria were used to assign variants to operational the rc taxonomic characters ” that are supposed to reflect taxonomic units. However, this method opened the door phylogenetic relationships between taxa of the same for the use of mathematics in taxonomic studies; as an level,have beenconfused. The result is thatthe example, multivariate analyses canbe very useful at taxonomic value of characters easy to observe and to specific discrimination. describe such as the number of lines and the areolation In thecladistic approach, whichis the opposite of the of the lateral field, and other characters linked to the preceding method, a limited number of characters are cuticle (longitudinal lines, costation, etc.) more than chosen, their ancestral or derived polarities are defined, likely hasbeen overestimated. This situation will be and then they are hierarchized. This method is said to modifiedwith the increased use of theSEM as be “ objective ” andlor “ scientific ”, but the choice of underlined by Hirschmann (1983). For example, it the characters, thedefinition of their polarities (ancestral appears more and more evident that the en face view of or plesiomorphic, versus derived or apomorphic) and the thelip region as seen by SEM,in manygroups of placement of derived States in evolutionary sequences Tylenchina, is an excellent taxonomic character at the are mainly subjective for most .characters. Therefore, family or generic level. In some cases() often more than one solution possibleis in variations are useful to define groups of species. Such reconstructing “ cladograms ” i. e. dichotomous phyletic characters, visibleonly by SEM, are fundamental to trees based on these sequences of character status. One taxonomic diagnosis of genera and species,yet they aspect of the cladistic approach open tocriticism is that cannot be used for practical identification purposes. only anatomo-morphologicdata are takeninto On theother hand, the host-parasite relationship may consideration, and not biological data that also are very constitute a source of characters that have received too importantin parasitic groups.Giving a particular little attention for the definition of various taxa. As an taxonomic rank to each branching of the cladogram is example,within Heteroderidae it appearsthat some also an undesirableconsequence ofcladistics, e.g. genera (Heterodera, G1obodera)consistentlyinduce in the Coomans (1979) for Heteroderinae-Meloidogyninae.In host multinucleate coenocytic nutritive cells, whereas that case, it required the introductionof “ tribes ”, a rank other genera (Hylonema, Rhizonenza, for example) in- intermediate between genus and subfamily. If this is duce the formation of a single giant ce11 provided with combinedwith the concept of “ superspecies ” as a single giant nucleus. Similarly, Tylenchulus and Tro- defended by Sturhan (1983), there would be five photylenchulus can be separated on the basis of differ- taxonomic ranks betweenthe species and thefamily! We ences in host reaction. donot think that such a great number of steps is Our approach in reappraising of thetaxonomy of necessary, norwould it rendermore evident the tylenchids has beento try to combinemorpho- relationships between genera; on tlie contrary, it will anatomicaldata and biological data, andto take increase the riskof discrepancies between different into consideration indications given by these characters taxonomists concerningthe rank tobe attributed to any tentatively to define evolutionary lines. Doing this, Our group of nematodes. aim is to contribute to thestabilization of, and to clarify Cladistics bases taxa exclusively on genealogy and thestatus of, variousnematode taxa rather thanto classifies characters rather thanorganisms (Mayr, 1981). propose one morenew classification of Tylenchina. We Mayr points out that thebasic weakness of cladistics is will not hesitate to use question marks when necessary the lack of a sensitive method of ranking, the cladist instead of approving or creating taxa with insufficient simply givesa new rank after each branchingpoint. The foundation or justification. evolutionary taxonomist, following Darwin, ranks taxa We agree withthe biological definition of species and by the degree of divergence from thecommon ancestor, that it is the only natural taxon corresponding biologi- often assigning a different rank to sister groups. An cally to an objective entity. We are fully aware that this example may well be the family Tylenchidae and the concept is difficult to apply in the case of thelytokous suborder Sphaerulariina. species, sibling species, etc. On thecontrary, supraspeci- The philosophy followed here is that of the Mayr fic taxa are intellectual (subjective) concepts that reflect evolutionary school. It is Our opinion that this school the human tendency to “ put in order ” things and

Revue Nématol. 10 (2) :127-134 (1987) 129 M. Luc, A. R. Maggenti, R. Forttrner, D. 'j?Raski & E. Geraert creatures. However, authors of such taxa seldom take Pratylenchus,). Suchgenera are easily into consideration the evolutionary lines that can bq. defined, but their species aremore difficult to traced from al1 the available data. The genus is the first differentiate from each other. step of this arrangement or classification and as such, Both kinds of genera can Co-exist in the same family the closest to the natural entities. From the genera are or subfamily, as is the case with Pratylenchoides and derived al1 the superior taxa. Pratylenchus. Thus Our first step was to reconsider generic validity In reviewing genera within Tylenchina we enlarged and placement. In order to accomplish this we followed their definition and accepteda greater intrageneric two precepts. The first is that Our perceptions of what variability. In several instances, we synonymized genera constitutes a generic or suprageneric taxon, hasnot to be that had been created by splitting formergenera on the eternal; they correspondto a momentin systematics and basis of few and/orsecondary rank characters. This additional data may changeOur concepts. For example, resulted in some cases, in theenlargement of the concept when the genus Brachydorus de Guiran & Germani, of the family. Subfamilies donot constitute an 1968, was described from a single species, it was clear obligatory taxonornic step; they should be usedonly that this genus wasclose to , differing when groups of genera can be properly defined and mainly by two characters : a long, regularly effilated tail when the subfamilycategory helps to clarify the and a relatively short stylet,whereas the hitherto relationship between these genera withinthe farnily. We described Dolichodorus species had avery long stylet and do not accept the creation of subfamilies as a kind of a short, rounded tail, sometimes with a short spicate routine taxonomicprocedure that results in some terminus. Later Brachydonls swampi Koshy, Raski & families, forexample, Heteroderidae, in several Sosamma, 1971 was described in which the stylet was monogeneric and often monospecific subfamilies. longer and thetail shorter than thoseof the type species; then Dolichodoruslongicaudatus Doucet,1981 was described with styleta shorter than in otherDolichodonu Evolution and systematics in Tylenchina species and a long conicaltail, intermediate between Brachydonls and those Dolichodorus species with a Clearly, it is not possible to write on systematics spicate tail. Therefore, the original species of withoutusing words, such as degenerated, evolved, Brachydorus could represent only the extreme of ancestral, regressed, transformed etc... concerning variability in tail shape andstylet length within the genus certain characters; and, such words as closer, deriving Dolichodorus. from, related to,etc... when writing on taxa. As a Onthe otherhand, two genera that have been consequence evolution is always implied when dealing synonymized, later can berestored when new important with the classification of living forms. Even the most differences are discovered. This is the case, for example, classical phenetist taxonomists (alpha taxonomy) use of Tylenchulus and Trophotylenchulzls that were these terms, thus weakening thearguments between synonymized by Maggenti (1962) onthe basisof pheneticevolutionaryand (gamma taxonomy) significant morpho-anatomical resemblances.However, classifications. a recent study of Cohnand Kaplan (1983)shows When applied to plant-parasitic nematodes, in this significant differences in the host relationship of these reappraisal limited to the Tylenchina, these terms are two genera, and consequently it now appears that each more often clichés than facts. The problem is should be considered as a valid taxon. complicated by the fact that thereare only a few fossil The second preceptwe followed in Our reassessment nematodes and of these the mostancient, in amber, are of genera is that the species are not always grouped in dated about 40 million years, and are quite like those the same way in different genera. In one case there is a living today (Poinar, 1984). On the other hand, due to large or eurymorphic genus, a conceptwell-known and the generally wide range of host for the same used in other branches of zoology and other natural genus or eventhe samespecies, and also to the apparent sciences; it means that one or more characters can Vary uncertainty of phylogenetic lines in plants, it appears progressively from one species theotherto nearly impossible to trace a Co-evolution of host and (morphocline) within the same genus. In such genera, parasite as it has been proposedfor some animalparasite species are easily identified and separated from each groups such:as Trichostrongyloidea(Durette-Desset, other, but the limits of the genusitself are more difficult 1985). Generallyspeaking, plant parasitic nematodes to assess. A good example of a eurymorphic genus is appear to ignore botanics, and as a consequence render Pratylenchoides in which theglandular part of the studies of Co-evolutionof parasite andhost often esophaguscan Vary from abutting bulb-like glands meaningless. However, interesting researches have been (P. rnagnicaztda) to a longoverlap over the intestine carried out (Krall' & IO.all', 1970; Stone, 1979) (P. ritteri). concerning Heterodera and related genera. Among In contrast there are oligomorphic generain which al1 Tylenchina, this group apparently is derived (cysts), and the species closely resemble each other (for example, peculiar because of their generally narrow rangeof host

130 Revue Nématol. 10 (2) : 127-134 (1987) Reappraisal of Tylenchina 1. New approach of taxononzy plants. For the mostpart, hosts are limited to one or only or juveniles(galls, cysts andlor gelatinous matrix) a few close botanical families. associated or not with egg diapause. Consequently, any attempt to relate the evolution of plant within Tylenchina, when al1 available TREND2. DEGENERATION OF MALE ESOPHAGEAL SYSTEM. information and^ the principles of paleontology are not adhered to is an intellectual game. We must be aware Maleshave atendency to have lessdeveloped, thatthe forms we are looking at now represent atrophied, non-functional digestive tracts exemplified contemporary extremities of numerous lines that have by degeneration of esophagus, esophageal glands, and, evolvedvertically through time, whereas systematic in the ultimate phase, stylet. The first step (male stylet groupings are horizontal. The Tylenchidaappear to shorter than female stylet, and median esophagealbulb less developed in the male) exists in nearly al1 groups of have their " roots " in . The search for a Tylenchina,oftenaccompanied withmodified cornmon ancestor" to different groups is a legitimate speculative undertaking. The " horizontal " groupings (narrower) lip area and weaker sclerotization of the labial of classifications often combine forms more framework. convergent than linked phylogenetically. For example The last step(degeneration of esophagus and of the superfamilyHeteroderoidea was proposed by stylet) exists in several groups : al1 Criconematoidea Golden (1971) to group within Tylenchina saccate or (stylet present onlyin some malesof Tylenchulinae) and globose females fixed on or in the roots of plants. This some Pratylenchidae (Radopholus) and groupinghas received little acceptance,because its (Acontylus). artificial character is immediately evident. Another If it is obvious that males without stylet and/or with example of artifical grouping is familythe degenerated esophagus cannotfeed, this does not mean Neotylenchidae. Other artificial groupings may be pre- that al1 males with N normal )> stylet and esophagus feed sent in theclassification that are notso easily identified. (allegedly Meloidogyne and perhaps Pratylenchoides). These foregoing statements are cautionary and not meant to reject references to evolution in classification. TREND3. REGRESSIONAND DISAPPEARANCE OFFEMALE By definition a classification should reflect phylogeny. POSTERIOR GENITAL BRANCH. STRUCTUREOF THE CRUS- ' Phylogenetic trendsare apparent within Tylenchida and TAFORMERIA some will be described below. This trend is not observed in Criconematoidea where Inorder to acceptphylogenetic trends among there is no trace of posterior branch, even as a Tylenchina, one must understand that : post-uterine sac. In othergroups, the occurrence of this - different Statesof a character (e.g. one or two regressionis sporadicand nearly always a PUS of ovaries) canbe present even in narrowtaxonomic variable length and structure remains present. divisions (subfamilies or even genera) aswell as in superfamilies or suborders; WithinTylenchina, outside Criconematoidea, we each character, or group of characters, even if they estimate thatthe regression or the absence of the - posterior female genital branch does not characterize are anatomically closelyrelated, have to be assessed separately; any of the families or subfamilies. This is contrary to - these trendsamong characters often are Andrassy's(1976) concept of families within independent and evolved separately; as a consequence, Tylenchina.Fully developed female genital branches a mixing of ancestral and derived characters in thesame may coexistwith a reducedposterior branch in the same taon must be considered as normal. family(Tylenchidae), subfamily () or even, but rarely, in the same genus as for example in (= Rotylenchoides). At the subfamily Phylogenetic trends level, couplets of genera exist that closely resemble each other, where one hastwo complete branches (didelphy) TREND1. GENERAL TENDENCY AMONG FEMALES, FROM andthe other only one,i.e., Pratylenchoides and Aprutylenchoides in Pratylenchidae. Onecomplete THE ANCESTRAL VERMIFORM STATE, TO BECOME IN- FLATED, GLOBOSE OR SACCATE (anterior) female genital (monodelphy)branch is the derived character state. Some genera withthis character This trend (i) exists in different groups (, have female J4 bearing a genital primordium with two Pratylenchidae, Hoplolaimidae,Heteroderidae, Crico- branches. Studies on ce11 lineage (Sternberg & Horvitz, nematoidea); ii) is mostoften correlated with an 1981; Horvitz & Sternberg,1982) revealed ashort endo-, semiendo-, or sedentary parasitic existence of the evolutionary distance betweenmono- and didelphy, females and oftenis accompanied by a host response in since the death loss of a single ce11 could transform a the vicinity of the stylet (nutritive cells) (seetrend 7); (iii) didelphic into a monodelphic species. Horvitzand is correlated with an increased production of eggs and Sternberg(1982) concluded that " derivation of sometimes a coincident system of protection for eggs monodelphy from didelphyhas probably appeared

Revue Nénzatol. 10 (2) : 127-134 (1987) 131 M. Luc, A. R. Maggenti, R. Fortuner, D. 3. Raski & E. Geraert repeatedly during evolution and hence isa poor some groups, as for example Dolichodoridae, shortand taxonomic indicator ”. We agree with their conclusion. long tails rnay coexist. A more significant difference in the female repro- men the male tail is shortened, the caudal alae ductive systemis arrangement of the cells of the colum- envelop the tail (peloderan type); when tail is long, the ned uterus (= crustaformeria, tri- or quadricolumella). alae areadanal (leptoderan). Withinderived groups Following observationsmade by Geraert (1986) : in (Heteroderidae, Tylenchulidae)the caudal alae are very Criconematoida these cells are not arranged in rows; in weakly developed or even absent. some families of ,considered as more ancestral (Tylenchidae and Dolichodoridae), the cells TREND7. EVOLUTIONOF PLANT PARASITIC HABIT FROM are arranged in four rows (quadricolumella); some ECTOPARASITIC TO ENDOPARASITIC, AND MIGRATORY TO Anguinidae also have four rowsof cells while other genera in this family show a (secondary?) arrangement SEDENTARY in multiple rows. In families considered as more derived This is correlated with Trend 1 in which the females (Belonolaimidae, Pratylenchidae and Hoplolaimidae) have a tendency to become obese. the cells are arranged in three rows (tricolumella). In This biological character can have significance at the Meloidogyne and inless derived heteroderids like Rhizo- family level, for example Tylenchidae (primarily nemu, the cells also are arranged in three rows (Geraert, ectoparasitic), Belonolaimidae and Hoplolaimidae unpubl.) while in other more derived heteroderids the (ecto-endoparasites), Pratylenchidae(migratory endo- rows can no longer be seen. parasites) and Heteroderinae-Meloidogyninae (seden- tary endoparasitic). TREND4. REINFORCEMENTOFSTYLET AND OF LABIAL SCLEROTIZATION TREND 8. EVOLUTIONFROM AMPHIMIXIS TO PARTHENO- This appears to be linked with the evolution from GENESIS mycophagous habits to active root parasites of higher This is difficult to evaluate, because for manyspecies plants. But a reverse can be observed in some evolved the dataare lacking :often no maleshave been described Tylenchoidea (Meloidogyninae, Nacobbinae)where the in a species, but the original population is composed female, sessile within the roots, has a stylet weaker than only of a fewfemales and itis not always reported if their that of the male or evenof 2nd stage juveniles. spermathecaecontain sperm or not. Nevertheless, it Criconematoidea also reiterate this line of evolution; in appears that in the moreancestral families (Tylenchidae, the more derived Tylenchulinaethe sessile females, have Dolichodoridae, Belonolaimidae) the various generacan a weak stylet and the male stylet is degenerate. be assumed to contain a very large majority of amphi- mictic species, whereas, for example in Hoplolaimidae TREND5, DIFFERENTIALELONGATION OF ESOPHAGEAL and Pratylenchidae, more derived, some genera (He& GLANDS (INTESTINAL OVERLAPPING) cotylenchus in Hoplolaimidae, Prutylenchus in Praty- In theancestral state thethree glands are in a definite lenchidae) contain a majority ofparthenogenetic species. bulb-like structure, not overlapping the intestine and In the derived family Heteroderidae,the ancestral sub- generally there is a well developed esophago-intestinal family Heteroderinaecontains a majority of amphimictic valve (= cardia). Transitional cases are present in some species, whereas the derived subfamily Meloidogyninae families, for example, Pururotylenchus (Hoplolaimidae), is primarily parthenogenetic. with “ bulb ”, where an intestinal overlapping is the rule. Even in a genus (somespecies of Prutylenchoides, within TREND9. EVOLUTION OF AMPHIDIAL APERTURES the Pratylenchidae)this lackof an overlap canbe Among Nemata theevolutionary development of the observed.Moreover, wehave included in the family amphid aperture appears to proceed in thedirection of Belonolaimidae (= Tylenchorhynchidae)genera with increased surface area, probably to enhance sensitivity. and without intestinal overlapping of the esophageal WithinTylenchina two lines are evident, one that glands. dead-ends (Tylenchidae) and one that proceeded along This enlargement of the esophageal glandsmay affect with other adaptationsto plant parasitism. The amphid primarily the subventral glands (mostfrequently) or the apertureamong ancestral Tylenchidae is pore-like, dorsal gland. whereas, the derived apertureis sinuous, longitudinally elongate and dit-like. Since this form of aperture is TREND6. SHORTENING OF TW limited to the family, it is considered an evolutionary Long tails are considered as ancestral. In this trend dead-end thatdid not contribute to the further Tylenchidae and Belonolaimidaehave to be considered development of plant parasitism. In the remainder of retaining the more ancestral state as opposed to HO- Tylenchina the pore-like aperture undergoes a steady plolaimidae, Pratylenchidae and Heteroderidae. But in enlargement becoming more and more cavernous.

132 Revue Nématol. 10 (2) :127-134 (1987) Reappraisal of Tylenchina 1. New approach of taxonomy

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TREND10. EVOLUTIONOF THE '' FACE " knobs; esophagus withDG0 close to stylet base, median In the ancestral state, it is represented by a distinct bulb fusiform with smallvalve; esophageal glands short and abutting; cellular intestine a well-developed ' oraldisc surrounded by six lip sectorswell wi+ esophago-intestinal valve; deirids present; phasmids individualized and equally developed.This structurehas punctiform,and caudal; female gonads didelphic, been transformed in various ways : fusion of the lip amphidelphic, outstretched, equally developed, with a sectors together, fusion of the oral disc with lip sectors, quadricolumellar crustaformeria; malegonad mon- regression and disappearance of the lateral lip sectors, etc.. orchic; caudal alae leptoderan, small; amphimictic . re-production; mycophagous. No contemporary nematode fits entirely with such a TREND1 1. REGRESSION OF ESOPHAGO-INTESTINAL description : although Psilenchus, a representative of VALVE Tylenchidae,appears the closest formtheto A well-developed, conspicuous esophago-intestinal prototylenchid, differing from it onlyby the shortening valve appears characteristic of ancestral groups with of the tail and the structure of the face, as seen with bulb-like esophagealglands (Tylenchidae, Belonolai- SEM. midae) and maybe retained in some ancestral genera of morederived families (Pratylenchoides, Conclusion Apratylenchoides in Pratylenchidae, Antarctylus in Hoplolaimidae) wherethe esophageal glandsoverlap thc The diversityof thearrangement between the intestine. In other genera of these families, the valve is different state of the various characters led usto much reduced. In Criconematoidea, despite the consider that these characters, constituting the trends, bulb-like structure of these glands, no esophago- have evolved separately, i.e. not at the same rate, with intestinal valve has been reported. arrests and sometimes reversals. As aconsequence ancestral and derived characters may be found together TREND12. DISAPPEARANCEOF DEIRIDS in thesame .To describe a given species as more derived than another species means that the number The presence of deirids appears to be ancestral; they andlor weightof the derived characters are greater in the are recorded only in Tylenchidae,Anguinidae, some former than in the latter. This is true for taxa at every Belonolaimidae, and a single genus (Pratylenchoides) of level. Pratylenchidae. Deirids generally are said to be absent Conflicting views of the evolution of one group can in Criconematoidea although they have been observed result from giving more weight to one character than on second stage juveniles of Tylenchulus semipenetrans, another. For example, within Heterodera S. lato, Green Trophotylenchulus mangenoti and T. jloridensis (Mag- (1975) takes into consideration vulval area morphology genti,1962). and estimates thatthe H. crucqerae group is more ancestral and the Globodera group more derived, the TREND13. EVOLUTIONOF PHASMIDS cacti group (= Cactodera) being intermediate. Stone The ancestral position of the phasmid is caudal. In (1979) had a contraryopinion when taking into some Tylenchidaeaphasmid-like structure occurs consideration the structure of the 2d stage juvenile face erratically along the body. Another evolutionleads from as seenwith SEM. This constitutes a very clear the normal punctiform phasmid to thelarge scutellum illustration of differing interpretation of the evolution of present in some generaof Hoplolaimidae. Phasmidsare different characters in the same group. absent in Criconematoidea andin onegenus of In theseries of articles which will constitute the body Hoplolaimidae (Apkasnzatylenchus), and in females and of Our Reappraisal of Tylenchina (excludingby the fact males of some Heteroderidae. Sphaerulariina and Aphelenchina) wewill apply the principles of these " trends " to the individual families and the classification of Tylenchina. The a prototylenchid D We are consciousthat no taxonomy can be a definitively established one, but Our aim is to propose From the studyof evolutionary trendsin Tylenchina, anapproach permitting to reduce the taxonornic we can imagine the prototylenchid. This hypothetical inflation which actually deserves the final aim of the ancestral form combines the ancestral state of every taxonomy, i.e. to presenta clear picture of the character studied above. ordered relationships in a group of living organisms. Female and male vermiform,closely resembling each other; no sexual dimorphism; body short to medium size; tail elongated to filiform; lip area not offset, six REFERENCES discrete lip sectors, amphids pore-like, labial framework ANDR~~SSY,1. (1976). Evolution as a basis for the systelnatization weaklydeveloped; stylet thin, short, with small basal of nematodes. London, Pitman Publishing, 288 p.

Revue Nétnatol. 10 (2) : 127-134 (1987) 133 M. LUC,A. R. Maggenti, R. Fortuner, D. J. Raski & E. Geraert

COHN,E. & KAPLAN, D. T. (1983).Parasitic habits of HORVITZ,R. H. & STEINBERG,P. W. (1982).Nematode Trophotylenchztlusfloridensis (Tylenchulidae)and its posternbryonic ce11 lineage. J. Nematol, 14 : 240-248. taxonornicrelationship to Tylenchulussemipenetrans and I-L’, E. & IZRALL’,H. (1978). [The revision of the plant allied species. J. Nematol., 15 : 514-523. nernatodesofthe family Heteroderidae (Nernatoda, COOMANS, A. (1979). General principles of systernatics with Tylenchida) by using a comparative ecological method of particularreference to speciation. In : Lamberti, F. & studyingtheir phylogeny]. In : Printsipy i izucheniya Taylor,C. E. (Eds) Rootknotnematodes (Meloidogyne vzaimootnosheniimezdhu paraziticheskimi nematodani i species). Systematics, biology and control.London, Academic rasterniyumi, USSR, Tartu, Akad. Nauk Estonoskoi SSR : Press : 1-19. 39-56. DURETTE-DESSET,M.-C. (1985. Trichostrongyloid nerna- MAGGENTI, A. R. (1962). The production of the gelatinous todes and their vertebrate host: reconstruction of the phy- rnatrixand itstaxonomic significance in Tylenchulus logeny of a parasite group. Adv. Parasitol. 24 : 239-306. (Nernatoda :Tylenchulidae). Proc. helminth. Soc. Wash.,29 : FOTEDAR,D. N. & HANDOO,Z. A. (1978). A revised scheme 139-144. of classificationof to orderTylenchida Thorne, 1949 MAGGENTI, A.R. (1981). GeneralNematology. NewYork, (Nematoda). J. Sci. Univ. Kashmir, 3 (1975) : 55-82. Springer-Verlag, VIII + 372 p. GERAERT,E. (1965). The genus . Nematologica, MA=, E. (1981). Biological classification:Towards a synthesis 11 : 301-334. of opposing methodologies. Science, 216 : 510-516. GERAERT,E. (1986). The useof thefemale reproductive MULVEY, R.H. (1972). Identification of Heterodera cysts by system in the classificationof the Tylenchida (Nernatoda). terminal and cone structures.Can. J. Zool., 50 : 1277-1292. Revue Nématol., 9 : 296 [abstr.]. POINAR,G. O. (1984). Fossil evidence of nematode parasitism. GOLDEN, A. M. (1971). Classificationthe of genera and higher Revue Nématol., 7 : 201-203. categoriesof the order Tylenchida (Nematoda). In : SIDDIQI,M. R. (1974). Tylenchztlussenzipenetrans. CIH Zuckerman, B. M., Mai, W. F. & Rohde, R.A. (Eds).Plant Descript. Pl.-par. Nernatodes, Set. 3, No 34 : 3 p. ParasiticNematodes. Vol. I. London,Academic Press : 191-232. SIDDIQI,M. R.(1986). TylenchidaParasites of Plantand . Farnham Royal, UIC, Commonw. agric. Bureaux, GREEN,C. D. (1975). The vulvalcone and associated x + 645 p. structures ofsome cyst nernatodes (genus Heterodera). SOKAL,R. R. & SNEATH,P. H. A.(1973). Pn’nciples of Nematologica, 21 : 139-199. Numerical Taxonomy 2d ed. rev. San Francisco, Freernan, de GUIRAN,G. & GERMANI,G. (1968).Brachydorus tenuisn.g., 573 p. n.sp.(Nematoda : Dolichodorinae),associé à Ravenala STERNBERG,P. W. & HORVITZ,R. H. (1982). Gonadal ce11 madagascariensis sur la côte est-malgache. Nenzatologica, lineageof thenernatode Panagrellusredivivus and 14 : 447-452. implications for the evolution by modification of the ce11 HENNIG,W. (1950). Grundziigeeiner Theon’e des lineage. Developm. Biol., 88 : 147-168. phylogenetischenSysternatik. Berlin,Deutsche Zentral- STONE,A. R. (1979). Co-evolution of nematodes and plants. verlag, 370 p. Symbol. Bot. Upsal, 22 : 46-61. HIRSCHMANN,H. (1983). Scanning electron microscopy as a STURHAN,D. (1983). The useof the subspecies and the tool in nernatode taxonorny. In : Stone, A. R., Platt, H. M. superspecies categories in nernatode taxonomy. In : Stone, & Khalil, L. F. (Eds). Concepts in Nematode Systematics, A.R., Platt, H. M. & Khalil, L. F. (Eds). Concepts in London, Acadernic Press : 95-111. Nematode Systematics. London, Academic Press : 41-53.

Accepté pour publicationle 13 juin 1986.

134 Revue Nématol. 10 (2) : 127-134 (1987)