of the Mm - Science Direct

Internarx~nal Journalfoor % 1997 Australian Soaety

Perganlon

PII: SOO20-7519(97)00140-9

Parasitology. Vol. 27. No. 12, pp, 1495 -1.51 I, li)ST for Parasmlogy. Published by Etsewr Sdence Lid Printed m Great Rxitm 002fk75f9’97 517.M) + 0 iK1

of the Mm WALTER

A. BOEGER*f

and DELANE

C. KRITSKYflj

*Depurtamento de Zoologia, Universidade Federal do Paranri, Curitiba, PR 81531490, Brazil tConseiho Nackwal de Desenvolvimento Cient@co e Tecnolbgico, Curitiba, Brazil $College of Health Professions,CampusBox 8090, Idaho State University, Pocatello. ID 83209, U.S.A. (Received

Elsevies Kql

$To whom

seiwce

w0rd.f:

1997; accepted

5 August

1997)

Ltd.

Monogenoidea:

correspondence

1 I February

should

Platyhehninthes;

be addressed.

monogenean;

E-mail:

phylogeny;

[email protected]. 1495

cladistics;

coevolution

W. A. Boeger & D. C. Kritsky

1496

grounded primarily on ontogeneticdevelopmentof the attachment organsand the feedingapparatusin various groupsof monogenoideans. Llewellyn (1982) concluded that all of the major groups of Monogenoideadevelopedon a “commonhost-stock”during the Ordovician. Recentinvestigationson coevolution within the Monogenoideausing methodsof phylogeneticsystematics,have focusedon lower taxonomic categoriesof the class.Someof thesewere attempts to interpret historical host-parasite associations at the specificand genericlevels (Klassen& BeverleyBurton, 1985, 1988;Boeger & Kritsky, 1989) while

INTRODUCTION

Boeger & Kritsky (1993) presenteda phylogenetic hypothesisfor 50familiesof Monogenoideabasedon a cladistic study of 47 character seriesrepresenting both anatomical and ultrastructural features. Their analysissuggestedtwo primary clades:the Subclass Polyonchoinearepresenting18families;and a second cladecomprisingtwo subclasses, the Polystomatoinea (with two families)and the Oligonchoinea(with 30 families). Kritsky et al. (1993) and Kritsky & Lim (1995) determinedthe phylogenetic position of the Lagarocotylidae(Order Lagarocotylidea)andSundanonchidae(Order Dactylogyridea, Suborder Tetraonchinea)within the Polyonchoinea,respectively. New information on anatomical and ultrastructural features of somemonogenoideanfamilieshas become available (Boegeret al., 1994;Kearn, 1993;Ogawa, 1994;andseeFournier &Justine, 1994)which requires re-evaluationof the current hypothesis. While phylogenetic relationships in the Monogenoideahave been object of recent investigations (also seeChisholmet al., 1995;Justine, 1991, 1993; Lambert, 1980;Malmberg, 1990),a paucity of studies on coevolution within the classexists. Bychowsky (1957)concludedthat while host switching(dispersal) was relatively common, coevolution was important historically in major groups of the class.Llewellyn (1982)provided a conceptionof coevolution basedon his (Llewellyn, 1970) phylogenetic hypothesis

others were used to reconstruct

phylogeny

of host

groups(Van Every & Kritsky, 1992). In the presentpaper, a revised hypothesis on evolutionary relationships of the Polyonchoinea is presented,basedin part on new ultrastructural and anatomicaldata. The resulting hypothesisis usedto determinecoevolutionary eventsassociatedwith the familiesof Monogenoideaand the higher taxonomic categoriesof their hosts.

MATERIALS Characters.

AND

METHODS

Homologous seriesincludedthoselistedby

Justine (1993, tables II-IV therein) for sperm structure and spermiogenesis and those derived from Boeger L K&sky (1993) andKritsky et al. (1993)by K&sky & Lim (1995) for the Polyonchoinea. Characters for sperm structure and spermiogenesis of the Lagarocotylidae were obtained from

Table l&-Character matrix used in reconstruction of evolutionary relationships of the Polyonchoinea Taxon Ancestor Monocotylidae Loimoidae Dionchidae Capsalidae Montchadskyellidae Lagarocotylidae Bothitrematidae Tetraonchoididae Anoplodiscidae Gyrodactylidae Acanthocotylidae Calceostomatidae Neodactvlodiscidae Amphibdellatidae Sundanonchidae Tetraonchidae Neotetraonchidae Dactylogyridae Diplectanidae Pseudomurraytrematidae

1

234561

00 0 00 0 ?? ? 00 0 00010110 ?? ? ?? ? ?? 1 ?? 1 00 0 ?l ? ?l ? 00 0 ?? ? ?l ? 10 0 10 0 ?? ? 00 0 00 0 00 0

0 0 0 0 0000 1 0 1000 1000 1 1 1 1 1 1 1 0 1000 1 0 1000 1000 1 1 1 1 1 1 1 0 1 0 1 0

8 0 0

0 0

1

1

? ? ? 0

0 0 0 0

0

0

? ? ? 0 0 0

0 0 0 0 0 0

0 0 0 0 10 10 1 1 1 1 11 ? 10 10 1 1 1 1 1 1

0 0 0 1 10 0 0 0 0 0 0 0 0 0 0 0

Homologous series” 9 10 11 12 0 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

00 00 00 10 10 00 00 00 00 00 01 02 00 00 00 00 00 00 00 00 00

0 1 0 0 0 1 0 ? ? ? 0 0 0 1 1 1 ? ? 0 1 1

000 000 000 100 000 100 000 ??? 000 000 ??l ??I 000 010 000 000 000 000 000 000 000

13

14

0 1 0 0 1 0 0 1 1 1 0 0 1 ? 1 0 0 ? 0 0 0

0 000 00000 0 ??l 00010 0 ??l 00010 0 ??l 00010 0 000 00000 ? ??? 00010 0 ???ooooo0 0 ??? 01000 0 m 01000 0 010 ????l 0 ??? 01000 0 000 00000 0 100 00100 1 ??? 10000 1 000 10000 1 000 10000 1 000 10000 1 ??? 10000 1 100 20000 1 100 20000 1 ??? 20000

“Homologous series are presented in an order corresponding to that under Characters in the text

15

16

17 18 19 0 0 0 0 0 0 1 1 1 1 1 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 ?? 0 0 I 0 1 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 ? 0 ? 1 1 2 2 2 2 2 2 2

Coevolution of Monogenoidea Hathaway et uf. (1993). Six new homologous series were obtained from recent literature: (1) development of the Mehlis’ gland; (2) presence/absence of spike sensilla; (3) presence/absence of an egg-filament droplet(s); (4) number of seminal vesicles; (5) presence/absence of digitiform pharyngeal processes; and (6) number of pharyngeal bulbs. Series in which the derived state represented an autapomorphy for a single ingroup taxon or a synapomorphy for the Polyonchoinea (series 6 and 13 of Kritsky & Lim, 1995; and series l-4, 13-15 and 19-21 of Justine, 1993) were excluded from analyses. Characters from Kritsky & Lim (1995) relating to the number of sperm axonemes (character 9) and presence/absence of peripheral microtubules in the mature spermatozoon (character 10) were not used because they were represented in the homologous series listed by Justine (1993). Polarization of character states was based on outgroup and functionat outgroup analyses (Watrous & Wheeler, 1981; Maddison et al., 1984) as provided by Boeger & Kritsky (1993) and Justine (1993), although polarity of some series was adjusted for the Polyonchoinea as the ingroup (see character analysis). Monophyly of the Polyonchoinea was established by Boeger & Kritsky (1993). The matrix comprised 38 homologous series (Table 1). Phylogenetic analysis. An initial hypothesis on evolutionary relationships of poiyonchoinean families was constructed manually using Hennigian Argumentation (Hennig, 1966; Wiley, 1981). Topology of the resulting cladogram was tested with HENNIG86 (distributed by S. Farris) using the ie* command to confirm that it was a most-parsimonious tree. Coez*olutionary analysis. Comparison of host and parasite cladograms was performed according to techniques described by Brooks & McLennan (1991). The phylogeny of

the families of Monogenoidea was that developed herein for the Polyonchoinea (Fig. 1) combined with that of the Polystomatoinea and Oligonchoinea from Boeger & Kritsky (1993) (Fig. 2). The host cladogram (Fig. 3), based on host characters, was a modification of the phylogeny of vertebrate groups presented by Pough et al. (1993). Modifications of this phylogeny included the inclusion of major groups of the Chondrichthyes after de Carvalho (1996); and the Actinopterygii according to Grande & Bemis (1996). The parasite phylogeny was transformed into a matrix by Addiive Binary Coding. A matrix for the host groups was then constructed based on this parasite matrix and the respective distributions of the parasite groups. Host groups parasitized by more than one family of Monogenoidea were initially considered independent entities. This host phylogeny (Fig. 4) was used to detine the plesiomoxphic host group for each family of parasites by parsimony. Once the ptesiomorphic host group for each family of Monogenoidea was de@rmh& the matrix was compressed via inclusive ORing (CX%ady & Deers, 1987). A phylogeny of the hosts was then reconstructed based solely on this parasitological information (Fig. 3) and compared with the pbylogenetic hypothesis based on host characters. The coded parasite cladogram was mapped onto the host cladogram to determine congruence. Phylogenetic Analysis using Parsimony (PAUP, version 2.4.1; I>. L. Swofford) was used to reconstruct phylogenies and determrne tree measurements. Two forms of dispersal were recognized: primary dispersal refers to the switching of an ancestral parasite to a different group of hosts resulting in the monogenoidean taxon under consideration; secondary dispersal refers to host-switching events that apparently occurred after development of thr monogenoidean taxon.

Table I-continued. Taxon

20 21 22 23

24

25

26

Ancestor Monocotylidae Loimoidae Dionchidae Capsalidae Montchadskyellidae Lagarocotylidae Bothitrematidae Tetraonchoididae Anoplodiscidae Gyrodactylidae Acanthocotylidae Calceostomatidae Neodactylodiscidae Amphibdcllatidae Sundanonchidae Tetraonchidae Neotetraonchidae Dactylogyridae Diplectanidae Pseudomurraytrematidae

00 00 00 00 00 00 ?? ,1 11 ?? 11 ?‘) ilo 00 10 30 30 20 20 30 30

0 0 0 0 0 0 0 0 0 0 1

0 0 0 0 1 0 0 0 0 0 1

0 0 0 0 1 0 0 0 0 0 1

0 0 0 0 0 0 0 ? 1 1 1

0 0 0 0 0 0 0 1 0 1 1

0 0 0 0 0 0 0 1 0 1 1

1 f-J 0 0 0 0 0 0 0

01 0 0 0 0 0 0 0 0

01 0 0 0 0 0 0 0 0

01 0 0 0 0 0 0 0 0

01 0 0 0 0 0 0 0 0

01 0 0 0 0 0 0 0 0

Homologous series 27 28 29 30 31 __00 0 0 0 0 00 1 1 0 0 10 1 1 0 0 00 0 0 1 0 00 0 0 I 0 ?? ? ? ? ? 00 0 1 1 ? ?? ? ? ? ? 01 0 ? 1 I 01 0 0 I 1 00 0 0 1 0 00 0 0 1 0 01 1 0 1 1 ?? ? ‘? ? ‘? 01 0 0 I 1 ?? ? ? ? ‘? 01 ? ‘! ” ? *?? ? ? ? ? 01 0 0 0 1 01 1 0 1 1 ?? ? ‘! ? ?

32

33

34

35

36 37 3X

0 0 0 0 0 ? 0 ” ‘j 0 0 0 0 ‘? 1 1 ? ‘! 1 1 ?

0 0 0 0 0 ? 0 7 0 0 0 0 1 ‘? 1 ‘? ? 1 0 0 ?

0 0 0 0 0 ? 0 ? ? 0 0 0 I ‘? 0 y 7 ‘! 1 0 ?

0 0 0 1 1 ” 0 ? 0 0 0 0 0 ‘j 0 ? 1 ? 0 0 ?

0 0 0 0 0 ? 1 ? ‘? I I 1 1 ? 1 ‘? ‘,7 ‘I

i 1 ?

0 0 0 I I ‘! ’ ,; ‘f ? ? : ‘! ‘T I) ‘1 ‘.’ ‘? ” ‘? ?

0 0 0 1 1 ‘.’ I ‘! ” Cl 0 I 0 ‘) 0 ! ” ‘,’ 0 0 ‘1 -

1498


Fig. 1. New hypothesis of sister-group relationships of the families of Polyonchoinea (Monogenoidea). Numbers preceding the slash refer to postulated evolutionary changes as indicated in the character analysis; those occurring after the slash refer to the number of homoplasious events in respective branches.

RESULTS

AND

DISCUSSION

Character analysis Numbers in parentheses preceding the definition of a character state refer to coding in the matrix: (0) represents the plesiomorphic state and (?) denotes missing or inapplicable data. Numbers in brackets

pertain to respective evolutionary changes depicted in the cladogram (Fig. 1). New characters and characters of spermatozoa and spermiogenesis obtained from Justine (1993) are designated by single or double asterisks, respectively. 1. Eyes of oncomiracidium. (00) 2 pairs. (10) 2 pairs, posterior pair fused [81]. (?I) Eyes absent [53,76].

Coevolution of Monogenoidea


1500

4 I I I

GNATHOSTOMATA --------------------------------------------------------------------------------~ I I

OSTEICHTHYES r----------------------------------------------------------~ I I

I I I I

I;

CHONDRlCHTHYES i-‘-----‘----‘--y

I I I I

I 8 : I

ElASMOBRANCHll ,“-----~I .

I; ’ 1 fm , !r’-------------; ) ACTlNOPTERYGll

I I I

SARCOF’TERYGII -------------------------------------; “CHOANATA” i-------------------------------: I I TETRWODA : ,-------------------------J I I I I : AMPHIBIA I i----------I , ! I

I I

I I 1 I I I I

,-AMNIOTA - - - - - - - - -; i I I

Fig. 3. Cladogram showing phylogenetic relationships of host groups. Higher taxonomic categories are indicated by horizontal labels. Modified from Pough et al. (1993), Grande & Bemis (1996), and de Carvalho (1996).

2. Eyes of adult. (0) 2 pairs. (1) 2 pairs, posterior pair fused [43]. 3. Circumoral sucker. (0) Present. (I) Absent [8]. 4. Intestine. (0) Double (bifurcated). (1) Single [38, 791.

5. &ecu. (0) Nonconfluent. (1) Confluent [12]. (?) Gut single. 6. Testis. (0) Single. (1) Double [ll]. 7. Vus deferens. (0) Intercaecal or ventral to gut. (1) Looping left caecum or left margin of single gut


Fig. 4. Cladogram of host groups of Monogenoidea constructed from parasitohgical data alone and using all hosts groups. Dashed lines indicate postulated primary dispersal of parasite groups; dotted lines indicate instances of secondztry dispersal (dispersal after development of the family group). Each host group is labeled with its taxonomic epithet followed by the group of Monogenoidea with species parasitizing its members.

[23]. K&sky & Lim (1995)assigned(?)to families with speciespossessing a single gut (series4). However, the vasdeferensloopingthe left margin of the singlegut is hereinconsideredhomologous to its looping the left caecumin specieswith a bifurcated gut; the Bothitrematidae, Tetraonchoididae, Anoplodiscidae, Neotetraonchidae and Tetraonchidae were assigned(1). Most descriptiveaccountsof acanthocotylidsindicate an intercaecal vas deferens(e.g., Malmberg & Fernholm, 1989) but Kearn (1993)showsthe vas deferenslooping the left caecumin Enoplocotyle kidukoi (Acanthocotylidae). The Acanthocotylidae was also assigned(I) since the latter

condition apparently represents the plesiomorphicstatefor the family. 8. Mule copulatory organ. (0) Sclerotized. (1) Muscular [IO, 551.Although accessoryscleritesare present in Enoplocotvle kidakoi (Acanthocotylidae), the malecopulatory organ in this species is a muscular bulb &earn, 1993). RecentIy oviparous gyrodactylids, with the male eopulatory organ a sclerotizedtube articulated to a sclerotizedaccessorypiece(s),werecollectedfrom southernBrazil (Cartes & Boeger,unpubhsbd). This information

is incorporated

into the parasite

matrix. 9. .4ccessorypiece. (0) Absent. (1) Present [ZJ].

1502

W. A. Boeger& D. C. Kritsky

Kearn (1993) described four accessory sclerites associated with the male copulatory organ in Enoplocotyle kidakoi (Acanthocotylidae). We assumethesestructuresto be homologouswith the accessorypiece of other polyonchoineans basedon Hennig’sAuxillary Principle. 10. Genital aperture(s). (00) Male and femalesystems open to external surfaceby a common ventral pore. (10)Male and femalesystemsopento external surfaceby a common lateral pore [13]. (01) Male andfemaleaperturesseparate:maleventral; femaledextrolateral, ventral [52]. (02) Male and femaleaperturesseparate,sublateral[57]. In egglaying gyrodactylids, the uterine pore opensseparately from the male pore on the right ventral surfaceof the anterior trunk (Boegeret al., 1994; Kritsky & Boeger, 1991). In viviparous gyrodactylids,the uterine pore isalsoseparatedfrom the malepore but opensmidventrally slightly posterior to the male aperture(D. C. Kritsky, 1971. Studieson the fine structure of the monogenetic trematode Gyrodactylus eucaliae Ikezaki and Hoffman, 1957.Doctoral thesis,University of Illinois, Urbana, IL); the Gyrodactylidae wascoded (01)becausethis stateisconsideredplesiomorphic for the family. The poresare separateand occur on the left ventral surfaceof the body in Enoplocotyle kidakoi (Acanthocotylidae) (Kearn, 1993); this is the plesiomorphic state for the Acanthocotylidae and wascoded(02). 11. Pathway of germariumloviduct. (0) Intercaecal [84]. [l] Looping right caecumor margin of gut [5, 27, 701. 12. Vagina. (000) 1 ventrolateral vagina. (100) 1 midventral vagina [17, 261.(010) 2 bilateral vaginae [71]. (??l) Vagina absent [51]. Kritsky & Lim (1995)consideredthe Acanthocotylidae to have the plesiomorphicstate(oneventrolateral vagina) basedon older literature. However, Keam (1993) has shown that the “vagina” of the Acanthocotylidae representsthe uterine pore (female genitalpore) and that a true vaginal poreisabsent in Enoplocotyle kidakoi. Thus, the Acanthocotylidae is coded (??l), reflecting apparent lossof the vagina. 13. Egg. (0) Oval. (1) Tetrahedral [6, 20, 39, 62, 751. 14. Shape of kaptor. (0) Disc-shaped.(1) Globose[69]. 15. Number and distribution of hooks in oncomiracidium. (000) 14marginal, 2 central. (100) 12 marginal,2 central [63,82]. (010) 16marginal[37]. (??l) 14marginal [2, 181. 16. Number and distribution of hooks in adult. (00000) 14 marginal, 2 central. (10000) 10 marginal, 2 central, 4 dorsal [68]. (20000) 8 marginal, 2 central, 4 dorsal[83]. (01000)16marginal[40,54].

(00100) 12 marginal, 2 central [64]. (00010) 14 marginal [l, 19, 281.(????l)Hooks absent [46]. The character state “14 marginal” was recoded from (99919)in Kritsky & Lim (1995)to (00010) becausethe stateis apparently derived from loss of the central pair of hooks in the “14 marginal, 2 central” statein the Polyonchoinea. 17. Shape of hooks. (0) Unhinged. (1) Hinged [34]. 18. Anchor. (0) Presentin at leastone developmental stage.(1) Absent in all developmentalstages[47, 561. 19. Number of anchors (when present in at least one developmental stage). (0) 1 pair, ventral. (1) 2 pairs, ventral [59]. (2) 2 pairs, 1 ventral, 1 dorsal 1731. 20. Bars (when anchors present in at least one developmental stage). (00) Absent [72]. (10) 1 ventral

[31]. (11) 2 ventral [33]. (20) 1 ventral, 1 dorsal [78]. (30) 1 ventral, 2 dorsal[80, 871. 21. *Meklis’ gland. (0) Small, inconspicuous.(1) Massive, well developed [48]. Oviparous gyrodactylids possessa large glandular mass surrounding the oiitype (Harris, 1983; Kritsky & Boeger, 1991;Boegeret al., 1994),which apparently representsthe plesiomorphicstate for the family. In viviparous gyrodactylids,which do not produce eggs,the Mehlis’ gland is incipient or reduced, apparently representinga secondarily derived state within the family. Similarly, Kearn (1993) reports an enlarged Mehlis’ gland in Enoplocotyle kidakoi (Acanthocotylidae). Membersof all other polyonchoineanfamiliesapparently possess smallMehlis’ glands. 22. *Spike sensilla (compound sensilla comprised of modified cilia). (0) Absent. (1) Present[22, 491.

Lyons (1969) reported compound sensillawith modifiedcilia in the cephalicregionsof adult Gyrodactylus sp. (Gyrodactylidae) and the oncomiracidia of Entobdella soleae (Capsalidae)and near the pharynx of adult Acanthocotyle elegans (Acanthocotylidae). Compoundsensillawerealso reported in the cephalic lobes of adult Enoplocotyle kidakoi (Acanthocotylidae) by Kearn (1993).Each of thesefamiliesreceiveda (1) in the matrix. 23. *Egg droplet. (0) Absent. (1) Present[21, 501.An amorphous substanceassociatedwith the filamentsof the eggsof oviparousgyrodactylids was reported by Harris (1983)and Kritsky & Boeger (1991). Egg-filament droplets have also been reported in the acanthocotylids Acantkocotyle lobiancki and Enoplocotyle kidakoi by Keam (1967,1993,respectively)and two species of Capsalidae, Entobdella soleae and E. australis, by Keam (1963, 1978,respectively).In E. soleae, the


30!

droplet consists of several accumulations along Fusedfrom the start of spermiogaesis.(1) Separthe elongate egg filament, which is considered a ate, then fuseduring spermiogenesis [4,30]. Based secondary, although homologous to the droplet on outgroup comparison, Justine (1993) conin E. australis, development. An egg-filament sidered flagellae initially free from the middle droplet hasnot beenreported in any other memcytoplasmicprocessto be the plesiomorphicstate bersof the Polyonchoineaor its sistergroup, the for the Monogenoidea.However, initial analyses Oligonchoinea+Polystomatoinea, and is consuggestedthat fusion of the flagellaeand cvtosideredapomorphic. plasmicmiddle processoccurredwithin the cnm24. *Number of seminal vesicles. (0) 1. (1) 2 [32]. 2 mon ancestor of the Polyonchoinea and ir is. seminalvesiclesoccur in the Gyrodactylidae and therefore, plesiomorphicfor the ingroup under Tetraonchoididae (see Boeger et al., 1994), in consideration.Thus, the polarity of this serieswas Enoplocotyle kidakoi (Acanthocotylidae) (see reversedfor the presentstudy. Kearn, 1993)and in Anoplodiscus cirrusspiralis 30. **External ornamentation of the cell membrane in (Anoplodiscidae)(seeRoubalef al., 1983; Ogawa, zone of differentiation oj- spermarid, (0) Present 1994).Double seminalvesiclesreported in some [85]. (1) Absent [9]. Dactylogyridae, e.g., Dawestrema, Schilbetrema 31. **Number of centrioles in the spermatozoon. (0) 2 and Schilbetrematoides, by Kritsky et al. (1985) centrioles.(1) 1 centriole [42,61]. and Kritsky & Ku10 (1992a,1992b)appearto be 32. **CentrioZe adjunct. (0) Absent. (1) Present1741. secondarilyderived. Within the Dactylogyridae, a centriolar adjunct 25. *Digitifbrm prqjection within the pharynx. (0) is present in Pseudodactylogyrus and absentin Absent [45]. (1) Present [35]. Digitiform proCleithrarticus (seeJustine, 1993).Basedon parjections occur within the pharynges of gyrosimony, the apomorphicstatewasassignedto the Dactylogyridae. Absenceof a centriolar adjunct dactylids and acanthocotylids(seeKritsky, 1971, in Cleithrarticus is considereda secondary10~3in Doctoral thesis,cited above; Kearn, 1993,respectively), and in some bothitrematid and anothe Dactylogyridae. plodiscid specimenswe studied. Kritsky (1971, 33. **Axoneme structure in mature spermoto:non. (0) Circular. (1) Noncircular [66, 771. Doctoral thesis,cited above) indicated that the projections contain the terminations and open- 34. ** Axonemal b microtubules during spermiogene,si.$. ingsof ductsfrom glandslocatedwithin the pos(0) Complete.(1) Incomplete[67, 861. (0) Normal. (1) Bead-like[14]. terior pharyngeal bulb. As far as we are aware, 35. **Mitochondrion. in zone of dzlferentiation c!f sperpharyngealprojections are derived featuresthat 36. **Microtubules matid. (0) Present.(1) Absent [25]. do not occur in any speciesof the outgroups or 31. **Ontogeny of microtubules in the zone qf’ dif: other Polyonchoinea. 26. *Number ofpharyngeal bulbs. (0) 1 2441. (1) 2 [36]. ferentiation. (0) Persisting.(1) Disappearing1151. microtubule during sperThe pharyngesof acanthocotylids,gyrodactylids 38. **Single peripheral miogenesis. (0) Absent. (1) Present[16, 29. 581. and anoplodiscidscomprisetwo tandem bulbs (seeKearn, 1993;Boegeret al., 1994;Roubal et ul., 1983,respectively).Each of thesefamilieswas Phylogeny of the Polyonchoinea assignedthe apomorphicstate. 27. **Number of axonemes during spermiogenesis. Our hypothesisfor the phylogeneticrelationshipsof (00) 2. (10) 1+ 1 altered[7]. (01) 1from the begin- polyonchoineanfamilieswithin the Monogenoidea--ning of development[41, 601.This series,com- one of 18 equally parsimonious trees produmd prising multiple apomorphic states,was recoded through the analysis(consistencyindex= 62%; retenby binary coding. Within the Monocotylidae, Jus- tion index = 17%; length= 88bis presentedin Fig. 1. tine (1993) . , identified a fourth state (one+one Previoushypotheses(Boeger& Kritsky, 1993;Kritsky axonemedisappearing)in Heterocotyle. However, & Lim, 1995)included the Acanthocotylidae in the Calicotyle (Monocotylidae) hastwo normalaxon- Order Capsalidea as sister group to the Capemes. As a result, the plesiomorphicstate is salidae+ Dionchidae. In the presenthypothesis,the assignedto the Monocotylidae basedon parsi- Acanthocotylidae serves as sister group to the Gyrodactylidae within the Order Gyrodactylidea. The mony. 28. **Nucleus in distaf region of mature spermatozoon. sister relationship of the Acanthocotylidae and (0) Distal region with nicleus and other cyto- Gyrodactylidae is supportedby six synapomorphies, plasmicelements.(1) Distal region with nucleus three of which exhibit 100%consistency:(1) presence of a massive, well-developed Mehlis’ gland; (2) only [3, 65, 881. 29. **Cytoplasmic middle process and Jlagella. (0) absenceof a vagina; and (3) presenceof separateven-

1504


tral male and female genital apertures. Homoplasy of the remaining three characters is represented by apparent parallel (convergent) evolution in (1) the development of an egg droplet with the Capsalidae, (2) presence of spike sensilla in larval capsalids, and (3) loss of eyes in the oncomiracidium in the Amphibdellatidae. The sister-group relationships within the Gyrodactylidea were identical in all 18 trees produced through the analysis using HENNIG86 (Fig. 1). The remaining 17 trees differed from that in Fig. 1 primarily by the relative positioning of the Lagarocotylidae, Montchadskyellidae and Calceostomatidae within the respective cladograms. This variation is apparently due in part to the presence of missing data (?) in the matrix (see Kritsky & Lim, 1995). The new composition of the Gyrodactylidea, which includes Bothitrematidae, Tetraonchoididae, Anoplodiscidae, Gyrodactylidae and Acanthocotylidae, corresponds to that of the Subclass Articulonchoinea proposed by Malmberg (1990) for species with hinged haptoral hooks. However, the relative position of the taxon containing these five families in the phylogenetic hypothesis does not justify its elevation to the level of subclass (Fig. 2). Coevolution of the Monogenoidea The host cladogram based on host characteristics (Fig. 3) has incongruences with that reconstructed from parasitological data (Fig. 4). These incongruences indicate that host occurrences of the Monogenoidea cannot be explained solely by cospeciation and that host switching and/or sympatric speciation are apparently associated with the origins of several monogenoidean taxa. Extinction events are also required to explain extant host-parasite associations. Comparison of the host and parasite cladograms produces a percentage of similarity of 56% when all host groups are used and 71% when only postulated plesiomorphic-host groups are considered. Brooks (1989) postulated that stem divergence of the trematodes, monogenoideans and cestodarians occurred in association with placoderm hosts prior to divergence of the Chondrichthyes and Osteichthyes and that at least two instances of sympatric speciation and/or dispersal would be necessary to explain extant host-parasite relationships. In his analysis, initial divergences within the trematode and cestodarian lineages apparently occurred in association with origins of the Chondrichthyes and Osteichthyes; he did not resolve plesiomorphic host groups for primary lineages in the Monogenoidea. Our analysis suggests that initial divergence within the Monogenoidea, resulting in the Polyonchoinea

and Polystomatoinea + Oligonchoinea clades (Figs 5 and 6) also occurred on a “placoderm” host. While resolution of historical/evolutionary events associated with early gnathostomes is extremely poor, initial diversification of the Monogenoidea apparently involved either sympatric speciation on the ancestral gnathostome or an additional dispersal event prior to divergence of the Chondrichthyes and Osteichthyes. Initial divergences in the two primary clades of Monogenoidea parallel those postulated by Brooks (1989) for the trematodes and cestodarians by being associated with the development of the chondrichthyans and osteichthyans (Figs 5 and 6); extinction and dispersal were prevalent in the later history of each primary monogenoidean clade. The analysis suggests that the relative importance of coevolution is different for the two lineages. Congruence of the host cladogram and the cladogram for the Polyonchoinea is 64% when all host groups are used and 89% when considering only postulated plesiomorphic-host groups. These respective values are both 83% for the Polystomatoinea + Oligonchoinea clade. C’oevolution oj the Polyonchoinea The hypothesis for the coevolution of the Polyonchoinea and their hosts is presented in Fig. 5. Extinctions of polyonchoinean lineages occurred with origins of the Holocephala, Polypteriformes, Acipenseriformes and Sarcopterygii. Cospeciation within the Polyonchoinea is associated with the Order Monocotylidea as parasites of elasmobranchs, with origins of the Loimoidae and Monocotylidae linked to divergence of the Galeomorphii and Squalea, respectively. Secondary dispersion of monocotylids to Holocephala (Fig. 4) is supported by the independent finding by Chisholm et al. (1995) that genera of monocotylid species from these hosts represent derived taxa. These ideas conflict with the hypothesis on origin of the Monocotylidae offered by Lambert (1982), who suggested that the family had its origin associated with dispersal by an ancestor from the Neopterygii into the Elasmobranchii. Lambert’s (1982) hypothesis is a less parsimonious explanation, because it requires added secondary dispersions and ignores the sister relationship of monocotylids and loimoids. The evolution of the remaining families of Polyonchoinea apparently occurred within the Neopterygii (Fig. 5). However, three cases of primary dispersion into parallel host groups are evident. Members of the monotypic Lagarocotylidae and Neodactylodiscidae parasitize a salamander (Urodela) and the coelacanth (Actinistia), respectively, and their occurrence in these hosts represent cases of primary


Fig. 5. Summary of the proposed historical relationships of Polyonchoineaand their hosts. The parasite &&gram (solid lines) is superimposed on that (broad grey lines) of their plesiomorphic hosts. Dotted lines indicatepostulated extinction of parasite clades; dashed-dotted lines indicate postulated primary dispersal of parasite clades.

dispersion. Also, amphibdellatids are parasites of Squalea The Polypteriformes, Acipenseriformes and Sarcopterygii do not serve as plesiomorphic hosts for any extant polyonchoinean family. Our analysis suggests that parasitism of Polypteriformes, Urodela and Anura by gyrodactylids resulted from secondary host switching subsequent to development of the Gyrodactyl&e on neopterygian fishes. Gyrodactylids on cephalopods (Mollusca) and arthropods, two host groups not considered in the analysis, and acanthocotylids on Myxinoidea (hagfishes) and Squalea are also outcomes of secondary dispersal. Three apparently independent cases of secondary dispersal

also occurred within the Capsalidae to the Gztleomorphii, Squalea and Acipenseriformes (Fig. 4). The Iagotrematidae (Polyonchoinea) is likely polyphyletic and currently contains species par&&ing Urodela and Testudomorpha in Eurasia and South America, respectively. While information on characters was insufficient to include the family in the phylagenetic analysis of the Monogetidea to d&ermine monophyly of the taxon (see Boeger & I&r&sky, 1993), the Iagotrematidae probably has its or&i&s) in the clade that developed within the Neop&ygii, suggesting that they dispersed to their salama&er and turtle hosts. The character supporting the possible origin of the Iagotrematidae in the Neopterygii is pres-

1506


Fig. 6. Summary of the proposed historical relationships of Oligonchoinea and Polystomatoinea and their hosts. The parasite cladogram (solid tines) is superimposed on that (broad grey lines) of their plesiomorphic hosts. Dotted lines indicam postulated extinction; dashed-dotted lines indicate postulated primary dispersal of parasites.

ence of an accessorypiece associatedwith the male copulatory organ (MaAC-Garzon t Gil, 1962).Iugotremauruguayens&wasoriginally describedwith an intercaecalvas deferens,but this character must be verified; structure of the sperm in this speciesis unknown.

and the Polystomatoineawith osteichthyans.Subsequenthost switching(dispersal)or extinction events occurredin theseparasiteclades.

Oligonchoinea The initial divergence in the Oligonchoinea coincideswith divergencewithin the Chondrichthyes, Coevolutionof the Oligonchoinea and Polystomatoinea which apparently provided the vicariant event that A summary of the hypothesisfor the coevolution resultedin the Chimaericolideacoevolving with the of the Oligonchoineaand Polystomatoineaand their Holocephala and the ancestor of the Diclybothrihostsis presentedin Fig. 6. The analysissuggests that idae+ Hexabothriidae+ Mazocraeidea associated originsof the two subclasses coincidewith divergence with the Elasmobranchii. Lambert’s (1982) hypothesis developed in association with of the Chondrichthyes and Osteichthyes,with the that the Hexabothriidae Oligonchoineaassociatedwith the chondrichthyans the Elasmobranchii is supported, although secondary


dispersalof a hexabothriid (the ancestorof Callorhynchocotyle)to the Holocephalaoccurred. Coevol-, utionary analysisof the generaof Hexabothriidaeand their chondrichthyan hosts supports this idea since hexabothriids from holocephalansoccupy derived positionswithin the phylogeny of the family (Boeger & Kritsky, 1989).The origins of the Diclybothriidae (parasitesof Acipenseriformes)and the Mazocraeidea (parasitesof marineNeopterygii) resultedfrom independent primary dispersalevents of their ancestors from the Elasmobranchiito ancestralmembersof their respectivehost groups(Fig. 6). A competing hypothesis for the origin of these groupsincludesextinction of the parasitecladewithin the Chondrichthyesand cospeciationof the Oligonchoinea-t Polystomatoineagroup with divergenceof the Actinopterygii and Sarcopterygii. Extinction would also be necessaryto explain absenceof these wormsin the Polypteriformes,but the Diclybothriidae and Mazocraeideawould have cospeciatedwith the Acipenseriformesand Neopterygii, respectively.Dispersal would account for the presenceof hexabothriids and chimaericolidson the Elasmobranchii and Holocephala.This hypothesis,however, is less parsimonioussinceit requiresan additionalextinction event and fails to offer an adequateexplanation for extant mazocraeideans asparasitesalmostexclusively of marinefishesor freshwaterfishesof comparatively recentmarineorigin. While transition from marine to freshwateris formidableand many animal groups have been unable to achieveit, the latter co-speciation(as opposedto dispersal)hypothesisfor the Mazocraeideawould predict that major taxonomic lineagesof theseparasites shouldhave coevolved with primary freshwaterhost groupsaswell astheir marinecounterparts.Only two mazocraeideanfamilies,the Octomacridaeand Diplozoidae. parasitize primary fish groups (the Catostomidae and Cyprinidae, respectively). However, parasitesof these families likely dispersedto these primary fish groups after invasion of freshwater by their anandromoushosts(seebelow).The former dispersalhypothesisfor the Mazocraeidea(Fig. 6), while not limiting the parasitesto a marine environment, would accommodatepresent-dayhost preferencesof mazocraeideans in that somehost groups (i.e. some or all primary fish families)may have divergedprior to dispersalof the common mazocraeideanancestor to the Neopterygii. In contrast, the polyonchoinean clade.in which parasitesof the Neopterygii are consideredto have coevolved with their hosts(Fig. 5), containsseveralexamplesof major lineageswith primary fish families as hosts (Dactylogyrinea, Tetraonchinea,Gyrodactylidea). Within the Mazocraeidea, only the Suborder Dis-

/it)‘:

cocotylineacontainsfamilies(Diplozoidae and Octomacridae) with members restricted to freshwater fishes. However, the suborder occupies a comparatively derived position within the Oliggonchoinea (Fig. 2) and its commonancestorlikely parasitizeda marine or anandromoushost. That ancestral discocotylineanssecondarilyinvadedfreshwaterhabitats and hosts,is suggestedby dispersionmechanismsof its extant host groups. Members of the Discocotylidae, the basalfamily of the suborder,are mainly parasitesof Salmonidae,a fish family probably of marineorigin but with freshwaterand anandromous species(but seeStearley, 1992, for other views on origin of the Salmonidae).Apparently, when the ancestorof the Salmonidaeinvaded freshwater,it carried with it the common ancestor of the Discocotylinea, which later dispersedto some primary freshwaterfish groups,the Catostomidae,Cyprinidae and Characiformes,resulting in the origins of the Diplozoidae and Octomacridae. In our hypothesis(Fig. 6), dispersionof the ancestral mazocraeidean,a parasite of ancestral Elasmobranchii, into the Neopterygii is postulated. The ancestorof the Elasmobranchiiwasmarine, and dispersalof the ancestralparasitefrom it to Neopterygii likely occurredwithin this environment.The ancestor of Elasmobranchii(host of the ancestral speciesof Mazocraeidea) sharedthe oceanswith Neopterygii for a long period of time before diverging into the Galeomorphii and Squalea.Fossilsof neopterygian fishesdate from the late Permian, while fossilsof hybodontid sharks (the apparent sister group to extant sharksandrays) areknown from the late Paleozoic and were dominant during the Triassic q.t~~d Jurassic(Nelson, 1994). A similar scenario explains the present-day host distribution of the Diclybothriidae, which apparently dispersedfrom an ancestralelasmobranchhost to the Acipenseriformes,a group of freshwaterand anandromousfishesof marineorigin. Although dispersion likely took placein the marineenvironment. it is not clear from our hypothesiswhether it occurred !o :t marine or anandromousacipenseriformwith subsequentcoevolution in freshwaterhosts. Polystomatoineo

The hypothesisfor this clade suggeststhat polystomatoineanscoevolved with hosts of the Osteichthyes(Fig. 6). Extinction wasa commonevent and is postulatedto have occurred with divergenceof the Actinopterygii, Actinistia, Dipnoi and Amniota. Coevolution of polystomatoineansoccurred within the Amphibia with postulatedinstancesof secondary dispersalto the Urodela, Dipnoi and Amniota (turtles

1508


and the hippopotomus) by the Polystomatidae (Fig. 4).

In this hypothesis,primary extinction appearsto be the most significantaspectof the history of the parasiteswith their hosts.However, at leastone event of extinction and one of secondarydispersalmay not be necessaryto explain extant host distributions within this clade. Concinnocotyla australensis is a parasite of the gills of an Australian dipnoan, Neoceratodus forsteri. Pichelin et al. (1991)placed this parasitein the Concinnocotylinaeof the Polystomatidae,which basedon our analysis, suggeststhe secondarydispersalevent of its ancestor to the Dipnoi from an amphibian host. However, the Concinnocotylinae should probably be elevated to family rank based on a preliminary phylogeneticanalysissuggestingits more basalposition within the Polystomatoinea(Fig. 7). Concinnocotyla australensis possesses severalsymplesiomorphic characters shared with the Oligonchoinea (egg with filament; eyes present, albeit unpigmented),which would have to be considered reversals(homoplasies) if the subfamily is retainedin the Polystomatidae.If the Concinnocotylinaeactually hasa more basalposition within the Polystomatidae,

its origin would be associatedwith the divergence of the Dipnoi and Tetrapoda, and postulation of an extinction with secondary dispersalto the Dipnoi would not be necessary. Extinctions postulatedwith divergenceof the Actinistia andAmniota during the evolutionary history of the Polystomatoineaare not astroubling. Likelihood of extinction of the clade in the Actinistia, with one extant species,Latimeria chalumnae, is high basedon the hypothesisthat organismsestablishedin small geographicareas(or smallhost groups)face a higher probability of extinction than those with extensive distributions. Most amniotes(with exception of the Testudomorpha),on the other hand, areterrestrial or semi-terrestrial.Sincethe Monogenoideaare external parasitesrequiring aquatic hosts for survival, it is predictable that extinction within hosts invading “dry” land would occur. We postulatethat the Anura is the plesiomorphic host group of the Polystomatidaesinceconsideration of Urodela as the plesiomorphichost group would requirean unnecessary dispersalof polystomatidsinto the Anura. This decision allows support of cospeciationof the two familiesof this suborderwith

/ eyes absent in larva

egg lacking filament eyes absent in adult TO OLlGONCHOlNEA sclerotizatlon of wall of haptoral suckers

Fig. 7. Preliminaryhypothesis on evolutionaryrelationships of theConcinnocotylinae in thePolystomatoinea. Evolution of some characters indicatedby slashes (m.c.o.,malecopulatoryorgan).


I 509

Lagarocotyle salamandrae initial divergencein the Amphibia. Parasitismby the (Polyollchoinea: Lagarocotylidea). Second International Symposii~m of MnnoPolystomatidaein the Testudimorphaisconsideredto genea, Montpellier, France, 5-7 July 1993. UniversitC be the result of secondarydispersalsincepolystomes Montpellier II, Sciences et Tbhniques du Languedoc. are only found in freshwater speciesof turtles. If a Montpeilier, France, p. 125. Systematics. IJniversity irl longer associationwith the Testudimorpha existed, Hennig W. 1966. Phylogenetic Illinois Press, Urbana, IL. marineturtles would beexpectedto be parasitizedby Justine J.-L. 1991. Cladistic study in the Monopnea l,Plathesewormsaswell. tyhelminthes), based upon a parsimony analysis of sper-

miogenetic and spermatozoa1 ultrastructural International

.4cknowledgements-The authors wish to thank Dr Sherman Hendrix and Dr K. Ogawa for allowing accessto specimens of Bothitrema bothi and Anoplodiscus tai and A. spari, respectively. Dr Dan Brooks provided a prepublication review of the manuscript. This study was supported by the Conselho National de Desenvolvimento Cientifico e Tecnohjgico, Brasil (CNPq).

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APPENDIX

Identification of postulated evolutionary changes follow in bold numbers (respective homoplasies are listed in parentheses; reversals to symplesiomorphic states are identified by an asterisk): 1 (19, 28), 14 marginal hooks (adult); 2 (18), 14marginal hooks (oncomiracidium); 3 (65,88), distal region of mature spermatozoon with nucleus only; 4 (30), cytoplasmic middle process and flagella separate, then fuse during spermiogenesis; 5 (27, 70), germarium/oviduct looping right caecum or margin of gut; 6 (20,39,62,75), egg tetrahedral; 7, one + one altered axoneme during spermiogenesis; 8, circumoral sucker absent; 9, external ornamentation of the cell membrane in zone of differentiation of spermatid absent; 10 (55) male copulatory organ muscular; 11, testes double; 12, caeca confluent; 13, genital pore common, lateral; 14, mitochondrion of sperm bead-like; 15, microtubules in zone of differentiation (during spermiogenesis) disappearing; 16 (29,58), single peripheral microtubule during spermiogenesis present; 17 (26). 1 midventral vagina; 18 (2). 14 marainal hooks (oncdmiracidium); 19 (1,28),’ 14 marginal hioks (adult); 20 (6,39,62,75), egg tetrahedral; 21(50), egg droplet present; 22 (49), spike sensilla present; 23, vas deferens looping left caecum or left margin of single gut; 24, accessory piece present; 25, microtubules in zone of differentiation of spermatid absent; 26 (17), 1 midventral vagina; 27 (5, 70), germarium/oviduct looping right caecum or margin of gut; 28 (1, 19), 14 marginal hooks (adult); 29 (16, 58), single peripheral microtubule during spermiogenesis present; 30 (4) cytoplasmic middle process and flagella separate, then fuse during spermiogenesis; 31, 1 ventral bar; 32, 2 seminal vesicles; 33, 2 ventral bars; 34, hinged hooks; 35, digitiform projections present in pharynx; 36, 2 pharyngeal bulbs; 37, 16 marginal hooks (oncomiracidium); 38 (79), intestine single; 39 (6, 20, 62, 75), egg tetrahedral; 40 (54), 16 marginal hooks (adult); 41 (60), 1 axoneme in spermatozoon from beginning of spermiogenesis; 42 (61), 1 centriole in spermatozoon; 43, 2 pairs of eyes, posterior pair fused (adult); 44*, 1 pharyngeal bulb; 45’, digitiform pharyngeal processes absent; 46, hooks absent (adult); 47 (56), anchor absent in all developmental stages; 48, Mehlis’ gland massive; 49 (22), spike sensilla present; 50 (21), egg droplet present; 51, vagina absent; 52, separate male and female genital pores, male pore ventral, female dextrolateral, 53 (76), eyes absent (oncomiracidium); 54 (40), 16 marginal hooks (adult); 55 (lo), male copulatory organ muscular; 56 (47), anchor absent in all developmental stages; 57, male and female genital pores separate, sublateral; 58 (16, 29), single peripheral microtubule during spermiogenesis present; 59,2 pairs of ventral anchors; 60 (41), 1 axoneme in spermatozoon from beginning of spermiogenesis; 61 (42), 1 centriole in spermatozoon; 62 (6,20,39,75), egg tetrahedral; 63 (82), 12 marginal, 2 central hooks (oncomiracidium); 64, 12 marginal, 2 central hooks (adult); 65 (3, 88), distal region of mature spermatozoon with nucleus only; 66 (77). axoneme non-circular in mature

Coevolution of Monogenoidea spermatozoon; 67 (86), axonemal b microtubules incomplete during spermiogenesis; 68, 10 marginal, 2 ventral, 4 dorsal hooks (adult); 69, haptor giobose; 70 (5, 27), germarium/oviduct looping right caecum or margin of gut; 71, 2 bilateral vaginae; 72’, bars absent; 73, 2 pairs of anchors, 1 dorsal, 1 ventral; 74, centriole adjunct present; 75 (6, 20, 39. 62), egg tetrahedral; 76 (53), eyes absent (oncomiracidium); 77 (66), axoneme non-circular in mature spermatozoon: 78, 1 ventral, 1 dorsal bar; 79 (38), intestine single;

Ifii

80 (87), 1 ventral, 2 dorsal bars; 81, 2 pairs of eyes.posterior pair fused (oncomiracidium); 82 (63). 12 marginal, 2 central hooks (oncomiracidium); 83, 8 marginal, 2 ventral, 4 dorsal hooks (adult); 84’, germarium/oviduct intercaecal; 8S’, external ornamentation of the cell membrane in zone of differentiation of spermatid present; 86 (67). axonemal h microtubules incomplete during spermiogenesis; 87 (80). 1 ventral, 2 dorsal bars; 88 (3, 65). distal region of mature spermatozoon with nucleus only.