Phylogeny and biogeography of Rhabdochona Railliet, 1916 (Nematoda: Rhabdochonidae) species from the...

Abstract A phylogenetic analysis of 40 species

of Rhabdochona Railliet, 1916, including all 21

valid species in the Americas, resulted in 1733

equally most parsimonious trees and indicates

that Rhabdochona is arguably monophyletic.

Species from the Americas do not form a mono-

phyletic group, since each of the six clades of

Rhabdochona includes species from the Americas

and species from other continents. The synapo-

morphies defining each clade stem from the

morphology of the left spicule. Teeth number was

consistent in one clade only, suggesting that

this character, while useful for taxonomic pur-

poses, is not indicative of phylogeny. Species of

Rhabdochona associated with certain host groups,

such as salmonids, catostomids and goodeids, do

not always form monophyletic assemblages, nor

do species associated with smaller discrete areas,

such as the Mesa Central of Mexico. This indi-

cates widespread host-switching rather than

co-speciation as the main phenomenon in the

evolution of this group, at least in the species

from the Americas. Phylogenetic patterns reveal

an ancient origin for the group that probably pre-

dates current continental configurations.

Introduction

Rhabdochona Railliet, 1916 comprises 104 species

that are distributed worldwide in freshwater

fishes, except in Australia (Moravec, 1975): 41

species in the Oriental, 30 in the Palaearctic, 17 in

the Nearctic, 10 in the African and six in the

Neotropical bigeographical regions. This genus

belongs to the rhabdochonid subfamily Rhab-

dochoninae Travassos, Artigas & Pereira, 1928

(see Moravec, 1975), within the superfamily

Thelazioidea Skrjabin, 1915 (see Anderson, 2000).

The subfamily is defined (Moravec, 1975) by

rudimentary pseudolabia or lack thereof, a roun-

ded or hexagonal mouth, the common (but not

universal) presence of ‘teeth’ in the anterior end

of the vestibule, the general lack of caudal alae,

and sessile caudal papillae. Of the 23 nominal

species in the Americas, 21 belong solely to North

America. Only two, or most probably one, actu-

ally belong to the South American helminth fau-

na (Cremonte, Navone, Gosztonyi, & Kuba, 2002;

Moravec, 1972a). The 21 North American

species are primarily parasites of the Cyprinidae

(minnows), Catostomidae (suckers) and

H. H. Mejıa-Madrid (&) Æ G. P.-P. de LeonLaboratorio de Helmintologıa, Instituto de Biologıa,Universidad Nacional Autonoma de Mexico, Apdo,70–153, C.P. 04510 Mexico City, Mexicoe-mail: hhmejia@ibiologia.unam.mx

A. ChoudhuryDivision of Natural Sciences, St Norbert College, 100Grant Street, DePere, Wisconsin 54115, USA

Syst Parasitol (2007) 67:1–18

DOI 10.1007/s11230-006-9065-3

ORIGINAL PAPER

Phylogeny and biogeography of Rhabdochona Railliet, 1916(Nematoda: Rhabdochonidae) species from the Americas

H. H. Mejıa-Madrid Æ A. Choudhury ÆG. Perez-Ponce de Leon

Received: 12 October 2004 / Accepted: 11 April 2006 / Published online: 8 December 2006� Springer Science+Business Media B.V. 2006

Salmonidae (trouts) and, to a lesser extent,

Characidae (characins), Cottidae (sculpins),

Cyprinodontidae (killifishes), Goodeidae (split-

fins), Ictaluridae (Nearctic catfishes) and Percidae

(perches). Of these, at least five inhabit the most

northern tropical plateau, the Mesa Central of

Mexico, and its neighbouring freshwater basins.

Species of Rhabdochona apparently exhibit

high levels of host-specificity (Moravec, 1975).

Several species of Rhabdochona also parasitise

hosts belonging to monophyletic lineages (e.g. 43

species in cyprinids, five in salmonids, three in

catosotomids, two in goodeids, etc.). Such lineage

restriction raises the possibility of co-evolution,

but the wide distribution and diverse host-asso-

ciations of Rhabdochona spp. may also suggest an

evolutionary history of extensive ecological host

extensions and host-switching. The considerable

diversification of Rhabdochona in the Americas

provides us with the raw material to examine

these ideas in a phylogenetic context, which in

turn will provide insights into historical biogeog-

raphy of this speciose group of nematodes.

The specific aims of the present study are: to

propose a phylogenetic hypothesis for the

species of Rhabdochona in the Americas, to

determine if the group conforms a monophyletic

group in that continent by including in

this analysis some widely distributed and well-

described species from Eurasia and Africa, to

infer to what extent the species of the genus has

co-evolved with its fish hosts or host-switched

between hosts of different families, and finally to

discover the highlights of its historical biogeog-

raphy in this region.

Materials and methods

Information on the morphology of Rhabdochona

spp. and outgroups were obtained from three

sources: specimens from field collections, museum

depositions, and literature on those species not

readily available for study.

Field collections

Canada – Cystidicola farionis Fischer, 1798 and

R. milleri Choquette, 1951 collected from salmo-

nids and catostomids, respectively, in Manitoba,

Canada, during 1992.

Mexico – R. ahuehuellensis Mejıa-Madrid &

Perez-Ponce de Leon, 2003 – Rıo Balsas, Ayu-

quila, and Panuco Basins, hosts: Ilyodon whitei,

Allodontichthys hubbsi, A. tamazulae, Ataeniobius

toweri, I. furcidens and Xenotaenia resolanae, 2000,

2001 and 2003; R. guerreroensis Caspeta-Manduj-

ano, Aguilar-Aguilar & Salgado-Maldonado, 2002

– Rıo Tamazula, El Tule, host: Sicydium multi-

punctatum, 2005; R. kidderi Pearse, 1936 – Rıo

Santiago Basin, host: Haplochromis niloticus;

2001; R. lichtenfelsi Sanchez-Alvarez, Garcıa-Pri-

eto & Perez-Ponce de Leon, 1998 – Rıo Lerma and

Panuco Basins, various goodeid hosts, 2002–2003;

R. mexicana Caspeta-Mandujano, Moravec &

Salgado-Maldonado, 2000 – Rıo Mezquital Basin,

host: Characodon audax, 2003; R. xiphophori

Caspeta-Mandujano, Moravec & Salgado-Maldo-

nado, 2001 – Armerıa, Balsas and Santiago Ba-

sins, hosts: Xiphophorus helleri, Allotoca catarinae

and Xenotoca eiseni, 2001 and 2003.

Museum collections

Coleccion Nacional de Helmintos (CNHE):

Beaninema nayaritense Caspeta-Mandujano,

Moravec, & Salgado-Maldonado, 2001 – 3937

(paratypes), R. ahuehuellensis – 4417 (holotype),

4418 (allotype), 4419 (paratypes), 5166–5173

(vouchers); R. californiensis Maggenti, Abdel-

Rahman & Cid del Prado, 1992 - 3074 (vouchers),

R. kidderi – 2698, 2699, 3286 (voucher), R. lich-

tenfelsi – 3212 (holotype), 5174–5205 (vouchers),

3213 (allotype), 3012, 3013, 3214, 3215 (paratypes),

R. mexicana – 4031 (holotype), 4032 (allotype),

4033 (paratypes), R. paxmani Maggenti, Abdel-

Rahman & Cid del Prado, 1992 – 3075 (voucher),

R. salgadoi Caspeta-Mandujano & Moravec, 2001

– 3886 (holotype), 3887 (allotype), 3888 (para-

types), R. salmonis Maggenti, Abdel-Rahman &

Cid del Prado, 1992 – 3076, R. xiphophori – 3940

(holotype), 3941 (allotype), 3942 (paratypes),

5206–5207 (vouchers). United States National

Parasite Collection (USNPC): R. canadensis Mor-

avec & Arai, 1971 – 71792, 78919, 79044 (para-

types), R. canadensis bifilamentosa Moravec &

Huffman, 1988 - 80005 (paratypes), R. catostomi

Kayton, Kritsky & Tobias, 1979 – 74896, 74899,

74900 (slides 1268–23, 1268–24) (paratypes),

R. congolensis Campana-Rouget, 1961 – 749290

(1225–10, 1225–11, voucher), R. cotti Wigdor, 1949

2 Syst Parasitol (2007) 67:1–18

– 36991, 78739, 83640 (voucher), R. decaturensis

Gustafson, 1949 - 36992, 84546 (voucher),

R. kidderi texensis Moravec & Huffman, 1988 –

80006 (paratypes), R. longleyi Moravec & Huff-

man, 1988 – 80004 (paratypes), R. ovifilamenta

Weller, 1938 – 77981 (paratype), R. penangensis

Thapar, 1950 (syn. of R. hospeti) – 60306 (voucher),

R. rotundicaudatum Byrne, 1992 – 81937 (para-

types). Harold W. Manter Laboratory of Parasitol-

ogy at the University of Nebraska, Lincoln

(HWML): R. cascadilla Wigdor, 1918 – 37587

(voucher).

Species considered

Rhabdochona spp. from the Americas (21 spe-

cies): R. acuminata (Molin, 1860), R. ahuehuell-

ensis, R. californiensis, R. canadensis, R. cascadilla,

R. catostomi, R. cotti, R. cubensis Moravec &

Coy-Otero, 1987, R. decaturensis, R. guerreroensis,

R. kidderi, R. kisutchi Margolis, Moravec &

McDonald, 1975, R. lichtenfelsi, R. longleyi,

R. mexicana, R. milleri, R. ovifilamenta, R. pax-

mani, R. salgadoi, R. salmonis and R. xiphophori.

Species not considered were R. rotundicaudatum

because of its doubtful taxonomic status (personal

observations) and R. uruyeni Dıaz-Ungrıa, 1968

(Cremonte et al., 2002). The subspecies, R. kidderi

kidderi Pearse, 1936, R. kidderi texensis and

R. canadensis bifilamentosa Moravec & Huffman,

1988, were also not considered.

Rhabdochona spp. from Africa: Three African

species were included with the foregoing:

R. congolensis, R. gambiana Gendre, 1922 and

R. paski Baylis, 1928. R. congolensis and R. paski

may be conspecific, but only adult characters were

considered (Puylaert, 1973).

Rhabdochona spp. from Eurasia: The 16 Eur-

asian species considered in the analysis were:

R. anguillae Spaul, 1927, R. coronacauda Belouss,

1965, R. denudata (Dujardin, 1945), R. ergensi

Moravec, 1968, R. fortunatowi Dinnik, 1933,

R. gnedini Skrjabin, 1946, R. hellichi (Sramek,

1901), R. hospeti Thapar, 1950, R. humili Royt-

man & Trofimenko, 1964, R. japonica Moravec,

1975, R. jiangxiensis Wang, Zhao, Wang, &

Zhang, 1979, R. oncorhynchi (Fujita, 1921),

R. phoxini Moravec, 1968, R. squalobarbi

Moravec & Sey, 1988, R. vietnamensis Moravec &

Sey, 1988 and R. zacconis Yamaguti, 1935.

Outgroups: Cystidicola farionis (Cystidicoli-

dae) was used as an outgroup as it is a represen-

tative, in some measure, of the spiruridans outside

the superfamily Thelazioidea. Beaninema nayari-

tense, Pancreatonema torriense McVicar & Gib-

son, 1975 and Vasorhabdochona cablei Martin &

Zam, 1967 (Rhabdochonidae sensu Moravec,

Salgado-Maldonado, & Cabanas-Carranza, 2001)

were also included as outgroups.

Cladistic analysis

Fifty-one characters were considered for analysis.

These included one external somatic character, 11

cephalic and oral characters, two cervical charac-

ters, 33 caudal characters, and four reproductive

characters. Characters of the 40 taxa used in the

analysis were coded in a matrix using MacClade 4

(Maddison & Maddison, 2000) as binary (28

characters) or multistate (23 characters) totalling

78 apomorphic states (Appendix 1). Characters

and character states were coded according to their

designation in the literature (Moravec, 1972a,

1975; Rasheed, 1965 and references therein). For

further information, refer to the character argu-

mentation (below). Unknown characters were

coded as ‘?’. Analyses were performed with

PAUP*V4.0b10 (Swofford, 2000). Characters

were equally weighted and unordered. The opti-

misation criterion used was ACCTRAN. Since

more than 25 species were analysed (Kitching,

Forey, Humphries, & Williams, 1998), a heuristic

search was undertaken, TBR algorithm, random

addition of taxa with 100 replicates. Due to com-

putational time limitations, a boostrap analysis

with a ‘‘fast’’ step-wise addition was performed

with 100,000 replicates in order to assess branch

support.

Character argumentation (Figs. 1, 2)

External somatic character:

1. Body lateral alae. Two states: absent – 0,

present – 1. This character has only been

found in R. coronacauda and R. squalobarbi

(see Moravec, 1975; Moravec & Sey, 1988).

Syst Parasitol (2007) 67:1–18 3

Cephalic and oral characters:

2. Anterior region. Two states: wide – 0, tapered

– 1. This character refers to the narrowed

condition of the cephalic and cervical regions

exhibited by Pancreatonema torriense as

stated by McVicar & Gibson (1975). Beani-

nema nayaritense and Rhabdochona spp.

possess the wide condition.

3. Pseudolabia. Two states: Present – 0, absent –

1. We follow Chabaud (1975) in that Rhab-

dochona spp. lack this character. Moravec

Fig. 1 Cephalic ends of males of the Rhabdochonidae: A. Beaninema nayaritense; B. Rhabdochona lichtenfelsi;C. R. decaturensis; D. R. cotti. All drawn to the same scale

(1972a, 1975) stated that this character is

present, but it was not mentioned by Rasheed

(1965). SEM observations from various species

of Rhabdochona, as compared to Cystidicola

farionis, support Chabaud’s observations.

4. Base of vestibule. Two states: annulated – 0;

smooth – 1. This character has not been

described in all those groups classified in the

Rhabdochonidae considered here, yet it is

illustrated in the descriptions of all other

species of rhabdochonids distinct from

Rhabdochona spp.

5. Prostom dimensions. Three states: narrow – 0,

wide – 1, expanded – 2. Our coding follows the

description of Moravec (1975). In her revision

of Rhabdochona, Rasheed (1965, p. 408) indi-

cated that the expanded condition is appar-

ently congruent with the absence (0) or

presence (1) of basal teeth (character 10). The

narrow condition is only present in Cystidicola

farionis, where no basal teeth are found; in all

other cases the prevailing condition in Rhab-

dochona is the expanded state, where the

prostom is separated from the mesostom by

basal teeth in some but not all of the species.

6. Prostom funnel-shaped. Two states: absent – 0,

present – 1.

7. Vestibule. Two states: long – 0, short – 1. The

coding was done after a meristic (not

reported here) discontinuity was found

between long and short vestibules that

apparently discriminates non-Rhabdochona

species from Rhabdochona spp., respectively.

8. Teeth. Two states: absent – 0, present – 1. This

is undeniably a character that is synapomor-

phic for the whole of Rhabdochona as a

genus. We assumed homology of the so-called

longitudinal thickenings with other species

outside this family, e.g. Cystidicola farionis,

the outgroup chosen for the analysis. We

coded this character separately from its states

due to its taxonomical importance.

9. Number of teeth in anterior prostom. Seven

states: Absent – 0, 6 – 1, 8 – 2, 10 – 3, 14 – 4, 16

– 5, 12 – 6. It has been reported that some

species may exhibit some combinations of

teeth numbers, i.e. 14 and 16 teeth

(R. ovifilamenta, Moravec & Arai, 1971); 6

and 8 (R. coronacauda, see Moravec & Sey,

1988), 14 or more (R. japonica, see Moravec,

1998). Nervertheless, when one of two states

was found in one single species, no polymor-

phisms were considered and only the most

constant condition reported in the original

description was coded. It has been demon-

strated through careful developmental studies

(Moravec, 1972b), that the third-stage larvae of

several species of Rhabdochona have only two

lateral teeth (called cystidicoline stage), that

become six in the fourth-stage larva (L4). The

dorsal and ventral teeth appear in the L4 as

single teeth, that presumably increase in

number (duplicates or triplicates) accord-

ing to species. This has been observed

in R. acuminata, R. ergensi, R. kidderi, R. on-

corhynchi and R. phoxini (see Cremonte et al.,

2002; Moravec, 1972b, 1976; Moravec & Huff-

man, 2001; Shimazu, 1996) and in R. lichtenfelsi

(personal observations). Therefore, this char-

acter could follow ontogeny, according to

Moravec and Huffman (2001), and Moravec

(1972b). As a priori considerations of recapit-

ulatory phenomena in the developmental

biology of Rhabdochona were not entertained

here, this character is treated as unordered.

10. Prostom basal teeth. Two states: Absent – 0,

present – 1. Beaninema nayaritense is

described with basal teeth in the original

description (Caspeta-Mandujano et al., 2001).

11. Dorso-ventral external teeth. Two states:

absent – 0, present – 1.

12. Lateral external teeth. Two states: absent – 0,

present – 1.

Cervical characters:

13. Deirids. Three states: absent – 0, simple – 1,

bifurcate –2.

14. Deirid position. Four states: absent – 0, ante-

rior – 1, middle – 2, posterior – 3. The position

of deirids is designated in relation to the

vestibule (Moravec, 1972a), i.e. close to the

prostom, middle of the vestibule or near its

posterior end (Moravec, 1972a).

Caudal characters:

15. Area rugosa. Two states: absent – 0, present

– 1. New observations by the authors reveal

that R. xiphophori possesses an area rugosa

in adult forms. Apparently, Caspeta-Mand-

ujano et al. (2001) described immature

specimens of this nematode, because they

described eggs found in females as imma-

16. Caudal alae. Two states: absent – 0, present

– 1.

17. Cloacal deep flap. Two states: absent – 0,

present – 1.

18. Circumcloacal papillae. Two states: absent –

0; present – 1.

19. Pedunculate papillae. Two states: absent – 0,

present – 1.

20. Papillae position. Two states: ventral – 0,

subventral and lateral – 1. This character is

present in all Rhabdochona spp., but not in

other species in the analysis.

21. Postcloacal papillae number. Two states: 2–5

pairs – 0, 6–7 pairs – 1. Six to seven pairs is

exclusive of Rhabdochona, although some

species in the latter genus present five pairs

(R. gambiana).

22. Precloacal papillae number. Two states: 1–2

pairs – 0, >2 pairs – 1. Supernumerary

precloacal papillae are exclusive of Rhab-

dochona in its apomorphic state in relation

to the outgroup.

23. Single adcloacal papillae. Two states: absent

– 0, present – 1.

24. Gubernaculum. Two states: present – 0,

absent – 1.

25. Distal end of left spicule. Six states: pointed

– 0, lancleolate pronged – 1, lanceolate thin

– 2, lanceolate wide – 3, lanceolate bifurcate –

4, lanceolate blunt – 5. (Fig. 2). Probably no

other character is so remarkably complex and

species specific within Rhabdochona as the

distal end of the left spicule of males

(Rasheed, 1965). Unfortunately, the spicule

cannot be studied well if it is not extruded

(Moravec, 1972a). Detailed examination of

this structure and SEM photographs have

revealed it is a complex tubular structure

sclerotised into three branches, two dorsal

and one ventral, this latter further divided in

some species (Fig. 2). Due to the complex

nature of the distal end of left spicules their

character states were coded based on detailed

observations and descriptions from original

papers.

In the lanceolate thin type (Fig. 2A) the distal

end of the left spicule is lanceolate, with dorsal

and ventral cuticular thickenings closely set. Most

species possess a membranous structure that

extends conspicuously beyond the distal end.

Membranous structures exhibit particularities in

each group of left spicules. In the case of those

described with a lanceolate thin left spicule, there

is limited variability in the membranous struc-

tures. An additional notch, described originally as

a bifurcation (Moravec, 1994), is present and

involves the spicule shaft and the membrane. It is

present in R. anguillae, R. ergensi, R. phoxini and

R. humili from Eurasia, and R. canadensis, R. cotti

and R. ovifilamenta from the Americas. The

following three features of the lanceolate thin

spicule provide this information.

26. Membrane of lanceolate thin spicule. Three

states: absent – 0, membrane short or indis-

tinct – 1, membrane wide – 2.

27. Extended membrane of lanceolate thin spic-

ule. Three states: absent – 0, dorsal mem-

brane extended – 1, dorsal membrane not

extended – 2.

28. Lanceolate thin spicule notch. Three states:

absent – 0, notch of membrane and blade

slight – 1, notch of membrane and blade

deep – 2.

In the lanceolate wide type (Fig. 2B, C, D), the

distal end of the left spicule is lanceolate and wide

to different degrees and/or ventrally distended

with a wide cuticular membrane forming dorsal

and/or ventral processes (Fig. 2B,C) or sclero-

tised ventral extensions forming ventral processes

(R. ahuehuellensis, R. guerreroensis) (Fig. 2D) or

without conspicuous extensions of the membrane

but retaining a lanceolate wide distal tip as the

outstanding feature. In R. coronacauda, R. denu-

data, R. hellichi, R. oncorhynchi, R. squalobarbi

and R. zacconis from Eurasia, and R. acuminata,

R. ahuehuellensis, R. californiensis, R. catostomi,

R. cubensis, R. guerreroensis, R. kisutchi, R. long-

leyi, R. mexicana, R. paxmani and R. xiphophori

from the Americas.

Fig. 2 Left spicules of males of Rhabdochona spp.:A. R. canadensis (lanceolate thin); B. R. californiensis(lanceolate wide); C. R. catostomi (lanceolate wide);D. R. guerreroensis (lanceolate wide); E. R. lichtenfelsi

(bifurcate); F. R. decaturensis (bifurcate); G. R. milleri(blunt); H. R. salgadoi (pronged). All drawn approxi-mately to the same scale

Species with lanceolate wide left spicules form

an interesting group that is well represented in

Asia and in the Americas. This type of spicule is

present in species infecting salmonids especially,

although species with such a spicule have been

found in cyprinids, goodeids and gobids. The ba-

sic structure of this spicule stems from the fact

that it possesses dorsal and ventral branches set

wide apart from each other. The dorsal branch is

generally stout, and in some groups it is conspic-

uoulsy longer than the ventral branch, which is

slender in comparison with the dorsal. These

branches form part of a tube-like structure that, at

its widest distal region, becomes groove-like

(described as a ventral groove in R. catostomi by

Kayton et al., 1979) and generally opens to the

right. Most of these spicules possess extensive

membranous structures, some of them even

forming ventral tooth-like processes. Some other

species possess, in addition to these extended

ventral membranous structures, sclerotised bar-

bed structures, as in R. ahuehuellensis and

R. guerreroensis. A thorough revision of these

spicules in specimens from Californian salmonids

(Maggenti, Abdel-Rahman, & Cid del Prado,

1992), R. catostomi and Mexican species reveals a

striking resemblance between them. They are

very similar to R. oncorhynchi. The presence of a

keel in this left spicule type characterises most of

these species but its position and length could be

used to distinguish them even further.

29. Keel of lanceolate wide spicule. Two states:

absent – 0, lateral keel present – 1. This

structure was first named by Moravec and

Amin (1978) when describing R. denudata

dzhalilovi from cyprinids of Afghanistan.

30. Fusion of keel of lanceolate wide spicule.

Three states: absent – 0, lateral keel fused – 1,

lateral keel free – 2.

31. Depth of keel in lanceolate wide spicule.

Three states: absent – 0, lateral keel shallow

– 1, lateral keel deep – 2.

32. Length of keel in lanceolate wide spicule.

Three states: absent – 0, lateral keel long – 1,

lateral keel short – 2.

33. Relative sizes of dorsal and ventral branches

in lanceolate wide spicules. Three states:

absent – 0, dorsal branch short – 1, dorsal

branch long – 2.

34. Dorsal branch of lanceolate wide spicule.

Three states: absent – 0, dorsal branch di-

rected upwards – 1, dorsal branch hooked –

In the lanceolate bifurcate type (Fig. 2E, F) the

distal end of the left spicule is lanceolate and

deeply bifurcate. Spicule projections are either

covered or not by a cuticular membrane. In R.

fortunatowi and R. vietnamensis from Eurasia,

and R. decaturensis, R. lichtenfelsi and R. kidderi

from the Americas.

Rhabdochona spp. bearing bifurcate left spic-

ules are widely distributed throught the world.

Some species have been recorded in the Ameri-

cas, e.g. R. lichtenfelsi. Bifurcate left spicules

possess conspicuously separate dorsal and ventral

branches enclosed by a very thin tubular spicular

cover. These branches even extend beyond

membranous structures, i.e. R. lichtenfelsi. R. de-

caturensis is here coded with a bifurcate left

spicule from new observations on material

deposited in the USNPC (Fig. 2D).

35. Furcal symmetry of bifurcate spicule. Three

states: absent – 0, furcae same size – 1, fur-

cae different size – 2.

36. Furcal size of bifurcate left spicule. Three

states: absent – 0, furcae long – 1, furcae

short – 2.

37. Furcae relative extension to membrane in

bifurcate spicule. Four states: absent – 0,

furcae without membrane – 1, furcae outside

membrane – 2, furcae inside membrane – 3.

In the lanceolate blunt type (Fig. 2G), the

distal end of left spicule is lanceolate and blunt,

with or without an indistinct bifurcation and a fine

cuticular membrane. R. gnedini and R. milleri

possess this type of spicule.

Blunt spicules are uncommon among the

species of Rhabdochona of the Americas.

Detailed observations of the left distal portion of

the left spicule of R. milleri (see Choquette, 1951;

Moravec & Arai, 1971) reveal that it is similar

to others described from widely distributed

species of east Asia and Europe, i.e. R. gnedini,

R. hospeti, R. japonica and R. jiangxiensis (see

Moravec, 1994; Moravec & Sey, 1988; Moravec &

Scholz, 1991). The bifurcation of this spicule,

nevertheless, is not comparable to the bifurcation

in the species discussed above. Its left spicule has

always been drawn from the right side (Cho-

quette, 1951; Moravec & Arai, 1971), but the left

side reveals more details of its morphology. The

similarity between R. gnedini and R. japonica

(and probably to R. hospeti) was indicated by

Moravec and Nagasawa (1998).

38. Number of branches in blunt spicule. Three

states: absent – 0, simple distended distal tip

– 1, dorsal and ventral ends duplicated – 2.

39. Thin keel in blunt spicule. Three states:

absent – 0, no ventral keel – 1, ventral keel – 2.

40. Slight bifurcation in blunt spicule. Three

states: absent – 0, blade not slightly bifurcate

– 1, blade slightly bifurcate – 2.

In the lanceolate pronged type (Fig. 2H) the

distal end of left spicule is lanceolate, accompa-

nied by an undetermined number of lateral right

prongs (approximately six in R. salgadoi) which

originate from the spicular cover.

An additional conical structure is present

in some species (R. paski, R. congolensis and

R. salgadoi). This conical structure is situated

dorsally in R. paski and ventrally in R. congolensis

(see Moravec, 1972a). A similar structure was

observed by the authors in R. salgadoi.

41. Conical structure in pronged spicule. Two

states: absent – 0, present – 1. This structure

has only been described in R. paski.

42. Left spicule, proximal region. Two states:

simple – 0, broad – 1. Broad refers to the

distention or bifurcation of this internal

region.

43. Right spicule, distal-dorsal branch. Two

states: smooth – 0, barbed – 1.

44. Right spicule, proximal region. Two states:

simple – 0, bulbous – 1.

45. Right spicule shape. Two states: straight

(parallel sides) – 0, pyramidal form or ‘boat-

shaped’ – 1.

46. Spicule ratio. Four states: 0–1:2.0 – 0, 1:2.1–

1:4.0 – 1, 1:4.1–1:6.0 – 2, 1:6.1–1:14.0 – 3.

47. Tail. Five states: conical pointed – 0,

rounded or blunt – 1, with sharp cuticular

spike – 2, with small cuticular processes – 3,

terminus conoid with pointed mucron – 4.

This is another character that shows

remarkable variability. We have coded the

different types of tails according to the lit-

erature and specimens available. Tails with

terminal small cuticular processes present in

some African, American and Asian species

deserve closer attention. While the number

of processes is variable (not considered

here), this character is sexually polymorphic,

except in R. salgadoi from Mexico, where

both males and females present this char-

acter (personal observations). Such poly-

morphism was not included in the present

analysis and the state was coded as it is

described or was observed in females.

Reproductive characters:

48. Egg protuberances. Four states: smooth – 0,

floats – 1, filaments at or near poles – 2,

flock-like structures – 3. These different

covers are not exclusive to the eggs of

Rhabdochona, as other groups taxonomi-

cally related to this genus possess them, i.e.

Cystidicola farionis.

49. Vagina direction. Two states: posteriorly – 0,

anteriorly – 1.

50. Vulval position. Two states: anterior – 0,

middle – 1. This character was coded

according to the original descriptions where

generic differentiation within the Rhab-

dochonidae is by a distinct position of the

vulva (Moravec, 1975).

51. Vulval lips. Three states: symmetrical – 0,

asymmetrical upper lip (larger of the two) – 1,

asymmetrical lower lip (larger of the two) – 2.

Results

Cladistic analysis produced 1,733 equally

parsimonious trees (not shown) 176 steps long,

with a consistency index (CI) of 0.49 and reten-

tion index (RI) of 0.69. A strict consensus tree

was then obtained (Fig. 3). This tree shows six

different clades, albeit with no resolution of five

of them due to a polytomy situated next to the

nodes that nest R. gambiana, R. cotti and R. an-

guillae. All clades contained at least one species

from the Americas. Bootstrap values are indi-

cated in the same figure. The following descrip-

tion of results is based on Fig. 3. Character states

were taken from one of the 1733 trees and

simultaneously compared with their position in

another 100 trees drawn at random.

The overall results show that Rhabdochona

species represent a monophyletic group and this is

based upon three synapomorphic characters: 4–1

(base of vestibule smooth), 20–1 (papillae posi-

tion subventral and lateral) and 25–5 (left spicule

distal blunt). All 1733 trees are in agreement with

the sister group relationships between the out-

groups used in this study and Rhabdochona spp.

Interestingly, Cystidicola farionis appears as the

sister taxon of Rhabdochona. The African species

R. gambiana appears as the sister species of

the ancestor of two groups, one containing two

sister species, R. anguillae and R. cotti, and the

other including the remaining species, with an

unresolved basal polytomy. Within this clade,

supported by 43–1 (right spicule distal-dorsal

branch barbed), five subclades appear to be

monophyletic, each supported by characters

derived from the form of the left spicule.

The only characters that showed a high CI

(c.1.00) are those that are related to left spicule

structure (characters 25 to 41). Only in one case

was teeth number a synapomorphic character (9–

1, 6 teeth) that groups seven species that include

five American and two Asian species (Fig. 3). The

high level of homoplasy observed in these dif-

ferent subclades of Rhabdochona spp. stems from

the lack of resolution of most of the characters

analysed; there are 48 ambiguous synapomor-

phies that are really homoplastic characters and

25 unambiguous synapomorphies distributed in

the strict consensus tree as stated above (Fig. 3).

Bootstrap analysis (Fig. 3) shows that the

clades obtained seemingly have very low support

values. The monophyly of the species of Rhab-

dochona is moderately supported (79% bootstrap

estimate) as well as other three subclades, e.g.

(ahuehuellensis, guerreroensis), (coronacauda,

squalobarbi) and (salgadoi, (congolensis, paski)).

A low value was obtained from the (congolensis,

paski) clade. Despite these results, most of the

clades with low to negligible bootstrap values

are nevertheless supported by unambiguous syn-

apomorphies. Bootstrap analysis shows that

B. nayaritense is closely related to C. farionis and

Rhabdochona spp. What was unexpected is a clo-

ser relationship of C. farionis to Rhabdochona spp.

than to other species of rhabdochonids. Never-

theless this result should be taken with caution, as

our analysis precludes any discussion of rhabdo-

chonid relationships outside Rhabdochona spp.

The mapping of hosts of the Rhabdochona spp.

onto the strict consensus tree (Fig. 4) indicates

that Cyprinidae is the main host group but does

not host any major clade of Rhabdochona. Map-

ping of geographical areas onto the strict con-

sensus tree (Fig. 5) indicates no consistent pattern

of geographical relationships.

Discussion

Phylogenetic considerations

The hypothesis herein presented sums up our

present knowledge of the phylogenetic and bio-

geographical relationships within Rhabdochona.

While phylogenetic hypotheses of nematodes

based on morphology have been problematic and

show that such characters exhibit a high degree of

homoplasy (Blaxter, 2001) in this particular

group, morphological hypotheses still represent

important starting points in understanding the

historical patterns and processes of diversification

in these organisms.

The position of Cystidicola farionis is surprising

and reveals that this species is probably more

closely related to Rhabdochona than to other

rhabdochonids. However, sister group relation-

ships between outgroups is beyond the scope of this

paper and deserves further and detailed analyses.

Only three synapomorphies support the mono-

phyly of Rhabdochona: smooth base of vestibule,

i.e. with no annulation (4–1); papillae position,

which seems to have evolved from a ventral to a

Vasorhabdochona cablei

Beaninema nayaritense

Pancreatonema torriense

Cystidicola farionis

kisutchi*

mexicana*

californiensis*

cascadilla*

cotti*

milleri*

acuminata*

cubensis*

xiphophori*

salgadoi*

longleyi*

catostomi*

denudata

oncorhynchi

zacconis**

hellichi

hospeti

gnedini

anguillae

coronacauda

japonica

jiangxiensis

squalobarbi

congolensis

gambiana

ahuehuellensis*

guerreroensis*472

vietnamensis

kidderi*

decaturensis*463

fortunatowi

lichtenfelsi*430

canadensis*

ovifilamenta*

phoxini

ergensi

humili

paxmani*481

salmonis*481

Fig. 3 Strict consensus of 1733 cladograms of Rhabdoch-ona spp. One asterisk indicates American species. Twoasterisks indicate species present in both Asia and

America. The number above the branches is the characternumber and below its corresponding state. The number inbold entered above the branches is the bootstrap value

Salmonidae*

Characidae*

Salmonidae*

Cyprinidae*

Cottidae*

Catostomidae*

Characidae*

Poeciliidae*

Goodeidae*

Cyprinodontidae*

Ictaluridae*

Catostomidae*

Cyprinidae

Salmonidae

Cyprinidae**

Cyprinidae

Scaphirhynchinae

Anguillidae

Cyprinidae

Amblycipitidae

Cyprinidae

Characidae

Cyprinidae

Goodeidae*

Gobidae*

Cranoglanidae

Cichlidae*

Catostomidae*

Cyprinidae

Goodeidae*

Cyprinidae*

Catostomidae*

Cyprinidae

Salmonidae*

Fig. 4 Host families superimposed on the strict consensus of 1733 cladograms of Rhabdochona species. An asteriskindicates hosts associated with American species of Rhabdochona

Nearctic*

Neotropical*

Nearctic*

Neotropical*

Nearctic*

Neotropical*

Nearctic*

Palaearctic

Palaearctic, Nearctic**

Palaearctic

Palaearctic, Oriental

Palaearctic

Palaearctic, Oriental

Oriental

African

Neotropical*

Oriental

Nearctic, Neotropical*

Nearctic*

Palaearctic

Nearctic*

Palaearctic

Nearctic*

Fig. 5 Area cladogram of the species analysed and theoutgroup species of Rhabdochona superimposed on thestrict consensus of 1733 cladograms. An asterisk indicates

the biogeographical regions associated with Americanspecies of Rhabdochona

subventral position (20–1); and a lanceolate blunt

left spicule (25–5), which seems to have evolved

from a pointed terminus condition. The increase

in papillae number (22–1) and the simple form of

the proximal section of the left spicule (42–0)

groups C. farinonis with Rhabdochona spp.

Most characters are homoplastic. Characters

that would appear to be consistent (sensu

Kitching et al., 1998) are actually not informative

for uncovering phylogenetic relationships, e.g.

teeth number, egg protuberances and tail form.

As our analyses show, apparently, 14 teeth

appear to be the plesiomorphic state of

Rhabdochona. Six teeth appear as a synapomor-

phy for (kisutchi, acuminata, cubensis, xiphophori,

longleyi (coronacauda, squalobarbi)) with chan-

ges to R. kisutchi which has 10 teeth, R. acuminata

14 (reversal) and R. coronacauda, which has eight

teeth (although six teeth have also been recorded

by Moravec & Sey, 1988). In another clade con-

taining (congolensis + paski), eight teeth appears

as a homoplasy because it appears again only in

R. coronacauda. Therefore, there is no strong

support from the results that the species of

Rhabdochona are grouped consistently and/or

congruently by number of teeth.

Egg filaments, which were thought three dec-

ades ago could bring together distinct species of

Rhabdochona (Moravec, 1975), do not support

any monophyletic groups. The presence of basal

teeth as a character appears only in Rhabdochona

but is shared outside the genus with Beaninema

nayaritense. According to our results, it seems

that this character might not be homologous in

B. nayaritense and Rhabdochona spp.

Cuticular processes on the tail are present in a

number of African and Asian species of Rhab-

dochona. R. salgadoi is the only known species

from the Americas that possesses this character.

Nevertheless, R. gambiana, which shares this

character with other African species, is situated at

the base of the present tree, while the others that

possess this character are mostly grouped in one

clade formed by (salgadoi (congolensis (paski))).

Analysis of character distributions in the clad-

ogram shows that homoplasy is concentrated in

the cephalic and caudal regions, where more

variable characters could be coded. Nevertheless,

the greater number of homoplasies in reproduc-

tive traits is due to the nature of the egg protu-

berances (filaments, flock-like coverings, polar

caps or smooth covers).

Several published revisions of Rhabdochona

have addressed the phylogenetic relationships

within the broader scope of the Rhabdochonidae

(see Skrjabin, Sobolev, & Ivashkin, 1971, for a

brief account). The account of Moravec (1972b)

describes some general trends in the evolution of

Rhabdochona, with the support of onto genetic

evidence. He stated that the primitive teeth

number is six based on the developmental stages

of these nematodes, where two teeth precede six

teeth in the third and fourth larval stages,

respectively. In contrast, our analysis indicates

that 14 teeth represent the plesiomorphic state.

The presence of six teeth most likely arose as a

paedomorphic character that probably originated

but once. This is not new in the extensive litera-

ture of the genus, since Puylaert (1973) had al-

ready pointed to the probable paedomorphic

origin of several characters in some of the African

species of Rhabdochona.

In describing the distal tip of left spicules, there

seems to be a clear departure from a basic lan-

ceolate type. We have observed in R. salgadoi

that, despite their possessing prongs in this part of

the spicule, there is a basic lanceolate framework

onto which the so-called ‘cone’ structure is

superimposed (Moravec, 1972c). Character states

25–1 (left spicule distal pronged) and 41–1

(presence of cone-shaped structure in left spicule)

support the relationship between R. salgadoi

and the African species R. congolensis and

R. paski.

Our premise for coding left spicule distal end

variations was that such a complex structure,

especially in some species, would likely not be

acquired more than once. So, very limited modi-

fications might derive from any of these five

categories, more especially in Rhabdochona than

in its putative sister genera, simply because the

latter exhibit a more generalised type of spicule.

Other characters might vary in these latter species,

but the left spicule form remains quite constant.

In assigning character codes for the left spicule

we have followed closely the terminology of

Moravec (1972a, b, c) and Moravec & Arai

(1971), for South American, Asian, African

and North American species, respectively, and

Rasheed (1965). We have re-defined terms from

other authors (Byrne, 1992; Maggenti et al., 1992;

Kayton et al., 1979) that are clearly equivalent to

the original terms used in Moravec’s descriptions.

For example, the rounded ventral, or ventral,

conical rounded protuberance is redescribed here

as an extended ventral process formed by a mem-

brane or a ventral tooth-like process formed by a

membrane. In some cases, i.e. R. ahuehuellensis

and R. guerreroensis, we have imported the use of

‘barb’ (a term originally used for the ‘ventral

barb’ of R. catostomi, a structure equivalent to the

‘‘wide cuticular membrane forming a ventral

process’’ of R. oncorhynchi, see Fig. 2 and Kayton

et al., 1979) for a structure that is actually scle-

rotised and not only formed by a ventral mem-

branous process or tooth-like process, as in many

Rhabdochona spp. from Asia and North America,

i.e. R. denudata, R. oncorhynchi, R. squalobarbi,

R. zacconis, R. californiensis, R. catostomi,

R. cubensis, R. kisutchi, R. paxmani, etc.

From the phylogenetic analysis of Rhabdoch-

ona spp. it seems that species could be better

grouped by spicule form than by any other char-

acter, mainly because all other characters exhibit

such low variability so as to render them of very

limited use in phylogenetic analyses. Yet, those

characters are valuable for taxonomic purposes.

As we could code at least four spicule types

within Rhabdochona, we have re-classified this

structure in order to include all species analysed

in this study, to relate some species directly

to species in the Americas, and to eliminate

ambiguities in future descriptions of species of

Rhabdochona.

The biogeography of Rhabdochona

A closer examination of the results also reveals

several salient aspects of the biogeography and

host associations of Rhabdochona. The origin of

Rhabdochona is most probably related to extinct

basins flowing into the Tethys Sea, with an early

presence in eastern North America, as exempli-

fied by the position in the tree of R. cotti. Some

more recent exchanges might have given rise to

new species of Rhabdochona, as each of the five

clades from our analysis show.

Species of Rhabdochona in the Americas do

not represent a monophyletic group. This indi-

cates that they do not have a single origin, be it by

dispersion or vicariance. What is constant in all

resolved subclades where species of the Americas

are present is that in most cases every pair of

sister species appears to be represented by an

American species and another one from a dif-

ferent continental area. This was anticipated by

Moravec and Arai (1971) and Moravec (1975).

Rhabdochona spp. have been reported from all

of the biogeographical zones of the world, except

for the Australasian region. The foregoing anal-

ysis includes species from every region of the

world and from all their hosts reported to date

(Figs. 4, 5). Fig. 4 indicates few patterns of po-

tential host-parasite co-evolutionary relationships

that stem from the unresolved nature of the

analysis. In the clade of Rhabdochona spp.

parasitising Pacific salmonids (Oncorhynchus

spp.) and goodeids, the basal members are all

from the western region of the continent and

eastern Asia with what appears to be instances of

host-extensions from cyprinids into salmonids and

goodeids. What is most striking is that the Cyp-

rinidae seems to be the main host family in all of

the biogeographical zones where Rhabdochona

spp. have been found, except for South America

where there are no cyprinids.

It is evident from the foregoing discussions that

the biogeographical pattern within Rhabdochona

is a very old one. It seems likely that Rhabdoch-

ona diversified mainly within the northern basins

and drainages of the former Tethys Sea, a sce-

nario consistent with the presence today of a

great number, but not the majority, of Rhab-

dochona spp. in the Black and Caspian Sea

regions. Nevertheless, the ancestry of the species

of Rhabdochona that parasitise freshwater fishes

in the Americas shows evidence of Trans-Pacific

geographical relationships that are most probably

due to dispersal (as in the species that parasitise

Salmonidae/Goodeidae). Such evidence is sup-

ported by the close relationship between those

species that have been found in eastern Asia and

western North America, i.e. (zacconis, denudata,

hellichi, catostomi, californiensis, mexicana, on-

corhynchi, paxmani, salmonis, ahuehuellensis and

guerreroensis).

It is noteworthy that the principal host group of

Rhabdochona spp., the Cypriniformes (e.g. Cyp-

rinidae and Catostomidae), are absent from the

Neotropical region. This could explain the spar-

sity of species in that subcontinent and the

absence of phylogenetic relationships between

the African and South American species.

Acknowledgements Special thanks go to Luis Garcıa-Prieto, CNHE, who kindly lent the specimens of the Mexi-can species. Berenit Mendoza-Garfias helped with the SEMphotographs. Special recognition is given to Dr Scott L.Gardner, Curator HWML, for the space and time given to

one of us (HHMM), and to Dr Agustın Jimenez-Ruız,during a pleasant summer in Lincoln, Nebraska. We aregreatly indebted to Dr Eric Hoberg and Patricia Pillit(USNPC), who lent us most of the American and Canadianspecimens. AC wishes to thank Patrick Nelson, Departmentof Zoology, University of Mantioba, Winnipeg, Canada, forhis invaluable help in the field. Thanks are also due to DrVirginia Leon Regagnon, CNHE, for reading a preliminaryversion of this manuscript. This work was funded by thePrograma de Apoyo a Proyectos de Investigacion e Inno-vacion Tecnologica (PAPITT-UNAM) grant no. IN200605CONACYT-47233 to GPPL, and project PAEP 201302DGEP-UNAM to HHMM; AC acknowledges supportthrough a 2003 St. Norbert College Faculty DevelopmentGrant.

Table 1 Data matrix for Rhabdochona spp. Characters are numbered and coded as in the text

Characters 1111111111222222222233333333333444444444455123456789012345678901234567890123456789012345678901

Vasorhabdochona cablei 011011000000130000000000000000000000000001011000010Beaninema nayaritense 011021110100120000000001000000000000000001011010000Pancreatonema torriense 001011000000130011000010000000000000000001011010010Cystidicola farionis 010000115011000100100101000000000000000000001012010kisutchi 011121113100220000011101300000002100000000101211010paxmani 011121113100220000011101300012110000000000111211012lichtenfelsi 011121113100210000011101400000000022300000011222010mexicana 011121113100210000011101300012111000000000001213010californiensis 011121114100220000011101300012121000000000111140011salmonis 011121113100220000011101300012111000000000111211012cascadilla 011121114100220000011101220000000000000000111120011kidderi 011121114100220000011101400000000021100000101320010decaturensis 011121114100120000011101400000000022200000001320010canadensis 011111114000210000011101221000000000000000110222010cotti 011111114000120000011101210000000000000000010112010milleri 011121114100220000011101500000000000022200101122010acuminata 011121114100110000011101300000002200000000111210010cubensis 011111111000230000011101300000002100000000111220110xiphophori 011111111000111000011101300000002200000000111112110ovifilamenta 011121114100210000011101212200000000000000101112010salgadoi 011121114100220000011101100000000000000010001130010ahuehuellensis 011121113100210000011101300012201000000000111112012guerreroensis 011121116100210000011101300012201000000000111122012longleyi 011121111100120000011101300000002100000000111222010catostomi 011111114000221000011101300012121000000000101112010denudata 011111114000220000011101300011001000000000111113010oncorhynchi 011121113100221000011101300012111000000000111223010zacconis 011111114000221000011101300011001000000000111222010phoxini 011111114000220000011101222200000000000000001113010ergensi 01111111400022000001110122200000000000000011111201?hellichi 01111111400022000001110130001100100000000011111201?humili 011111114000211000011101222100000000000000111?2201?hospeti 011121114100220000011101500000000000022100111?1201?gnedini 011121114100220000011101500000000000021000111212010fortunatowi 011121114100210000011101400000000021100000111222010

Appendix

References

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Blaxter, M. L. (2001). Molecular analysis of nematodeevolution. In M. W. Kennedy, & W. Harnett (Eds.),Parasitic nematodes (pp. 1–24). Wallingford: Com-monwealth Agricultural Bureaux International.

Byrne, P. J. (1992). Rhabdochona rotundicaudatum n. sp.and a redescription of R. cascadilla Wigdor, 1918(Nematoda: Thelazioidea) from minnows in southernOntario, Canada. Canadian Journal of Zoology, 70,476–484.

Caspeta-Mandujano, J., Moravec, F., & Salgado-Maldo-nado, G. (2001). Two new species of rhabdochonids(Nematoda: Rhabdochonidae) from freshwater fishesin Mexico, with a description of a new genus. Journalof Parasitology, 87, 139–143.

Chabaud, A. (1975). Keys to genera of the Order Spiru-rida. Part 1. Camallanoidea, Dracunculoidea, Gna-thostomatoidea, Physalopteroidea, Rictularioidea andThelazioidea. In R. C. Anderson, A. G. Chabaud, &S. Willmott (Eds.), CIH keys to the nematode parasitesof vertebrates, No. 3. Wallingford: CommonwealthAgricultural Bureaux International, 27 pp.

Choquette, L. P. E. (1951). On the nematode genusRhabdochona Railliet, 1916 (Nematoda: Spiruroidea).Canadian Journal of Zoology, 29, 1–16.

Cremonte, F., Navone, G. T., Gosztonyi, A. E., & Kuba, L.(2002). Redescription of Rhabdochona (Rhabdoch-ona) acuminata (Nematoda: Rhabdochonidae) fromfreshwater fishes from Patagonia (Argentina), thegeographical implications. Journal of Parasitology, 88,934–941.

Kayton, R. J., Kritsky, D. C., & Tobias, R. C. (1979).Rhabdochona catostomi sp. n. (Nematoda: Rhab-dochonidae) from the intestine of Catostomus spp.(Catostomidae). Proceedings of the HelminthologicalSociety of Washington, Vol. 46, pp. 224–227.

Kitching, I. J., Forey, P. L., Humphries, C. J., &. Williams,D. M. (1998). Cladistics. The theory and practice ofparsimony analysis, No. 11. The Systematics Associ-ation Publication. Oxford: Oxford University Press,228 pp.

Maddison, D. & Maddison, W. (2000). MacClade 4.Analysis of phylogeny and character evolution. Sun-derland, MA: Sinauer Associates Inc. (CD-ROM).

Maggenti, A. R., Abdel-Rahman, F., & Cid del Prado, I.(1992). New species of Rhabdochona Railliet, 1916(Nemata: Rhabdochonidae) from rainbow trout inCalifornia streams. Journal of Nematology, 24,224–227.

McVicar, A. H. & Gibson, D. I. (1975). Pancreatonematorriensis gen. nov., sp. nov. (Nematoda: Rhabdoch-onidae) from the pancreatic duct of Raja naevus.International Journal for Parasitology, 5, 529–535.

Moravec, F. (1968). Species of the genus RhabdochonaRailliet, 1916 (Nematoda: Rhabdochonidae) fromfishes of Czechoslovakia. Folia Parasitologica, 15,29–40.

Moravec, F. (1972a). General characterization of thenematode genus Rhabdochona with a revision of theSouth American species. Vestnık CeskoslovenskeSpolecnosti Zoologicke, 36, 29–46.

Moravec, F. (1972b). Studies on the development of thenematode Rhabdochona (Filochona) ergensi Mora-vec, 1968. Folia Parasitologica, 19, 321–333.

Moravec, F. (1972c). A revision of African species of thenematode genus Rhabdochona Railliet, 1916. VestnıkCeskoslovenske Spolecnosti Zoologicke, 36, 196–208.

Moravec, F. (1975). Reconstruction of the genus Rhab-dochona Railliet, 1916, with a review of the speciesparasitic in fishes of Europe and Asia. Studie CSVAV,No. 8 (104 pp.). Prague: Academia.

Moravec, F. (1976). Observations on the development ofRhabdochona phoxini Moravec, 1968 (Nematoda:Rhabdochonidae). Folia Parasitologica, 23, 309–320.

Moravec, F. (1994). Parasitic nematodes of freshwaterfishes of Europe. Prague, Dordrecht: Academia, Klu-wer Academic Publishers, 473 pp.

Table 1 continued

Characters 1111111111222222222233333333333444444444455123456789012345678901234567890123456789012345678901

anguillae 011111114000110000011101210000000000000000011210010coronacauda 111121112100120000011101300000002100000000101230010japonica 011111114000220000011101500000000000022100111212010jiangxiensis 011111114000220000011101500000000000010000011120010vietnamensis 011121114100220000011101400000000011100000101220110squalobarbi 111121111100120000011101300000002100000000100220010congolensis 011121112100120000011101100000000000000010001130010paski 011121112100120000011101100000000000000010001110010gambiana 011111116000130000010101500000000000010000001231010

Moravec, F. (1998). Nematodes of freshwater fishes of theNeotropical region. Prague: Academia, 464 pp.

Moravec, F., & Amin, A. (1978). Some helminth parasites,excluding monogenea, from fishes of Afghanistan.Acta Scientiarum Naturalium Academiae ScientiarumBohemoslovacae–Brno, 12, 1–45.

Moravec, F., & Arai, H. P. (1971). The North and CentralAmerican species of Rhabdochona Railliet, 1916(Nematoda: Rhabdochonidae) of fishes, includingRhabdochona canadensis sp. nov. Journal of theFisheries Research Board of Canada, 28, 1645–1662.

Moravec, F., & Huffman, D. G. (2001). Observations onthe biology of Rhabdochona kidderi texensis, a para-site of North American cichlids. Journal of Helmin-thology, 75, 197–203.

Moravec, F., & Nagasawa, K. (1998). Helminth parasitesof the rare endemic catfish, Liobagrus reini, in Japan.Folia Parasitologica, 45, 283–294.

Moravec, F., Salgado-Maldonado, G., & Cabanas-Carranza, G. (2001). New observations on Vasorhab-dochona cablei (Nematoda: Rhabdochonidae) withremarks to the family Rhabdochonidae. Helmintho-logia, 38, 231–235.

Moravec, F., & Scholz, T. (1991). Observations on somenematodes parasitic in freshwater fishes in Laos. FoliaParasitologica, 38, 163–178.

Moravec, F., & Sey, O. (1988). Nematodes of freshwaterfishes from North Vietnam. Part 2. Thelazioidea,Physalopteroidea and Gnathostomatoidea. VestnıkCeskoslovenske Spolecnosti Zoologicke, 52, 176–191.

Puylaert, F. A. (1973). Rhabdochonidae parasites dePoissons africains d’eau douce et discussion sur laposition systetmatique de ce groupe (Vermes-Nema-toda). Revue de Zoologie et de Botanique Africaine,87, 647–665.

Rasheed, S. (1965). A preliminary review of the genusRhabdochona Railliet, 1916 with description of a newand related genus. Acta Parasitologica Polonica, 13,407–424.

Shimazu, T. (1996). Mayfly larvae, Ephemera japonica, asnatural intermediate hosts of salmonid nematodes,Sterliadochona ephemeridarum and Rhabdochonaoncorhynchi, in Japan. Japanese Journal of Parasitol-ogy, 45, 167–172.

Skrjabin, K. I., Sobolev, A. A., & Ivashkin, V. M. (1971).Spirurata of animals and man and the diseases causedby them. Part. 4. Thelazioidea Jerusalem: Israel Pro-gram for Scientific Translations, 610 pp.

Swofford, D. L. (2000). PAUP*: Phylogenetic analysisusing parsimony (and other methods) 4.0 Beta(CD-ROM). Sunderland, MA: Sinauer AssociatesInc.

Phylogeny and biogeography of Rhabdochona Railliet, 1916 (Nematoda: Rhabdochonidae) species from the...

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