Phylogenetic Relationships Among Genera of the Tetrabothriidae (Eucestoda)

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8-1989

Phylogenetic Relationships among Genera of the Tetrabothriidae (Eucestoda)

Eric P. Hoberg United States Department of Agriculture, [email protected]

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Hoberg, Eric P., "Phylogenetic Relationships among Genera of the Tetrabothriidae (Eucestoda)" (1989). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 312. https://digitalcommons.unl.edu/parasitologyfacpubs/312

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasitol., 75(4), 1989, p. 617-626 ? American Society of Parasitologists 1989

PHYLOGENETICRELATIONSHIPS AMONG GENERA OF THETETRABOTHRIIDAE (EUCESTODA)*

Eric P. Hoberg Departmentof Pathologyand Microbiology,Atlantic Veterinary College, University of PrinceEdward Island, 550 UniversityAvenue, Charlottetown, Prince Edward Island, Canada C1A 4P3

ABSTRACT:Cladistic analysis of the generic-levelrelationships within the familyTetrabothriidae was conducted. A single cladogramresulted from evaluation of 28 homologous transformationseries representing41 character states. The genus Tetrabothriuswas recognizedas plesiomorphicfollowed by Chaetophallusand Trigonocotyle. The latter was considered as the sister group for the remaining tetrabothriidgenera of marine mammals. Anophryocephalus,Strobilocephalus, and Priapocephalusare among the most highly derived genera and are postulatedas having close evolutionaryaffinities. Comparisons to previousexplicit hypothesesfor relationships among the generaindicated the presentanalysis was the most efficientphylogenetic statement (consistency index = 85.4%)for the 28 attributesevaluated. The recognitionof Tetrabothriusas primitive and a naturalgrouping of Anophryocephalus,Strobilocephalus, and Priapocephalusin part confirmedresults of previous studies of the Tetrabothriidae.

Tetrabothriidae Linton, 1891, constitutes a independently by Hoberg (1987a) and Galkin prominent group of cestodes among marine (1987) (see Spasskii, 1958; Temirova and Skrja- mammals and seabirds predominantly in pelagic bin, 1978). Studies of the structure and ontogeny ecosystems (Baer, 1954; Temirova and Skrjabin, of larval Tetrabothrius spp. supported a sister 1978). Six genera are currently recognized: Tetra- group relationship between the Tetrabothriidae bothrius Rudolphi, 1819 (approximately 50 and some derived tetraphyllideans (Hoberg, species among Procellariiformes, Sphenisci- 1987a). Development of the metacestodes of formes, Pelecaniformes, Charadriiformes, and Tetrabothrius and Anophryocephalus appears to Gaviiformes; and 8 species among Cetacea), share a homologous pattern with Acanthoboth- Chaetophallus Nybelin, 1916 (2 species among rium Beneden, 1849. Additionally, the holdfasts Procellariiformes), Strobilocephalus Baer, 1932 of many Tetrabothrius spp. (see Baer, 1954) ap- (monotypic among Cetacea), Priapocephalus Ny- pear most similar to those characteristics of Cer- belin, 1922 (3 species in Cetacea), Trigonocotyle atobothrium Monticelli, 1892 (Oncobothriidae), Baer, 1932 (3 species in Cetacea), and Anophry- or Monorygma Diesing, 1863, and Dinoboth- ocephalus Baylis, 1922 (3 species in Pinnipedia) rium Beneden, 1889 (Phyllobothriidae) (Baylis, (Temirova and Skrjabin, 1978; Schmidt, 1986). 1926; Williams, 1968; Hoberg, 1987a). These The tetrabothriids have been classified among observations formed the basis for recognizing the Pseudophyllidea (Nybelin, 1922), Cyclo- some of these tetraphyllideans as the putative phyllidea (Fuhrmann, 1932; Wardle and Mc- sister group of the tetrabothriiids. Leod, 1952; Schmidt, 1986; and others), as a Attempts to identify the original homeo- suborder of the Tetraphyllidea (Spasskii, 1958; thermic hosts of the tetrabothriids (e.g., seabirds Temirova and Skrjabin, 1978) or in the separate or marine mammals) have been equivocal. Baer order Tetrabothridea (Baer, 1954). (1932) suggested that pinnipeds were the primary A tetraphyllidean relationship for the tetra- hosts with subsequent colonization occurring in- bothriids had been considered previously by dependently among cetaceans and marine birds. Baylis (1926) and later by Baer (1954). However, Baer (1954) later recognized seabirds as primi- Baer's hypothesis suggested that tetrabothriids tive hosts, using host specificity as an indicator were a lineage of the Proteocephalidea that di- of relationship among genera and species, and verged as the sister group for all Tetraphyllidea. considered that host-switching had occurred sec- Alternative hypotheses for the origin of the tetra- ondarily among marine mammals. Galkin (1987) bothriids from tetraphyllideans were presented attempted to refute the latter hypothesis for origin and diversification of the tetrabothriids, sug- gesting that marine mammals, particularly ce- Received 24 March 19 1989. 1989; accepted April were the initial hosts. * Paperfrom StunkardCentenary Session of the 1989 taceans, Hoberg (1987a) annual meeting of the American Society of Parasi- indicated that data were currently insufficient to tologists. corroborate any definite pattern of evolutionary 617 618 THEJOURNAL OF PARASITOLOGY, VOL. 75, NO.4, AUGUST1989 relationships for hosts and parasites within the from the collections of R. L. Rausch (RLR), and ad- family, but he considered the probability that ditional specimensare maintainedin the author'scol- lections (EPH). Specimens included: Tetrabothrius avian hosts were plesiomorphic. shinni Hoberg, 1987 (USNM 79657), T. jagerskioldi Although the family has received attention in Nybelin, 1916, T. cylindraceusRudolphi, 1819, T. lac- 2 monographs (Baer, 1954; Temirova and Skrja- cocephalusSpitlich, 1909, and T. erostrisLoennberg, bin, 1978) the taxonomy and relationships among 1896 (all EPH); Trigonocotyleprudhoei Markowski, 1955 material the and particularly for species referred (BMNH 1956.5.16.65-71, excluding genera from australis[Peale] and Steno bre- The Lagenorhynchus to Tetrabothrius have remained confused. danensis[Lesson]), T. globicephalaeBaer, 1954 (BMNH validity of the 4 subgenera (Tetrabothrius, Or- 1956.5.16.63-64), T. monticelli(Linton, 1923) (USNM iana, Neotetrabothrius, and Culmenamniculus) 8418 = T. globicephalae)and Trigonocotylesp. (USNM suggested on morphological by Baer 77368, 77679); Strobilocephalustriangularis (Diesing, grounds cf. eschrichtii named Murav'eva 1850) (USNM 74662); Priapocephalus (1954) and subsequently by Murav'eva and Treshchev, 1970 (RLR 31882); and (1975) has not been well established (see Oden- Anophryocephalusanophrys Baylis, 1922 (BMNH ing, 1982). Inadequate descriptions of the genital 1922.5.3.1-6); A. ochotensis Deliamure and Krotov, atrium and other characteristics in many species 1955 (USNM 76200; RLR 7659), and A. skrjabini and Deliamure, (USNM 75942, 75960, not allow their reliable placement at the (Krotov 1955) may 76188, and 76178, all previouslyreferred to A. ocho- subgeneric level. Recent studies of Tetrabothrius tensis). spp. (Hoberg, 1987b) have indicated the neces- sity to reevaluate the status of many species be- Character analysis cause of incomplete documentation of intraspe- Homologous charactersused in the analysis were cific variation of major diagnostic characters derived primarily from the study of material repre- (structure of genital atrium, length of male canal, senting tetrabothriids.Reference to detailed descrip- from marine number of testes) and because of the apparent tions and redescriptionsof tetrabothriids mammals 1956; and Murav'eva,1972, at- (Rees, Skrjabin lack of consistency in other morphological 1978) and seabirds (Spatlich, 1909; Nybelin, 1916; tributes. Among other genera, there has been Rawson, 1964; Burt, 1976, 1978; Andersen and considerable disagreement (Baer, 1932, 1954; Lysfjord,1982), along with monographson the Tetra- Temirova and Skrjabin, 1978; Galkin, 1987) over bothriidae(Baer, 1932, 1954; Temirova and Skrjabin, and treatmentsof other cestodes 1922; the affinities of 1978) (Linton, evolutionary Anophryocephalus, Fuhrmann, 1932; Wardle and McLeod, 1952; Wil- Strobilocephalus, and Priapocephalus. liams, 1968; Schmidt, 1986) augmentedthe study. Po- As the basis for broader studies among the larizationof characterstates was accomplishedby out- Tetrabothriidae, preliminary phylogenetic hy- group comparison (Lundberg, 1972; Wiley, 1981). were of the potheses, presented herein, were developed for Primaryoutgroups tetraphyllideans genera PhyllobothriumBeneden, 1849, Dinobothrium,Mon- the generic-level relationships within family. orygma,and Ceratobothrium.These taxa were selected Completion of analyses among the genera (and based on recognitionof some derived Tetraphyllidea later species) will promote the development of a as the putativesister group for the Tetrabothriidae(see natural classification for the group and provide Spasskii, 1958; Hoberg, 1987a; Galkin, 1987). Polarityof 3 characters(genital atrium [2]; male ca- a means of assessing earlier evaluations of evo- nal [3]; position of ovary [7, 8]) was reevaluatedwith lutionary relationships (e.g., Baer, 1932, 1954). reference to the functional outgroup (Tetrabothrius) following preliminary analyses (see Watrous and MATERIALSAND METHODS Wheeler, 1981). Four characterswere split into inde- Relationships of 6 genera of Tetrabothriidaewere pendent transformationseries to account for deri- analyzed using cladistics or phylogeneticsystematics vation of some characterstates (position of ovary [7, (Hennig, 1966; Wiley, 1981). The PAUP computer 8]; position of testes [10, 11]; shape of scolex [21, 22]; systematics program (Version 2.4), based on parsi- and structureof auricularappendages [27, 28]) (see mony criteria,was used to constructphylogenetic hy- Glen and Brooks, 1985; Hoberg, 1986). A summary potheses(Swofford, 1985). The small numberof genera of the 28 homologous series, representing41 character in the study group allowed analyses to be conducted states, is presentedbelow and in a numerical matrix with the ALLTREESoption; trees were rooted with a (Table I). Plesiomorphic states are coded as 0, apo- designatedancestor and Farris optimization was em- morphic as 1, 2, or 3. In genera containing species ployed (Swofford,1985). exhibiting both primitive and derived states, specific characterswere coded as plesiomorphic. Specimens examined An integralpart of the analysisincluded calculation Specimensof several Tetrabothriusspp. from avian of the consistency index (CI), a measure of the fit of hosts and representativesof all generaof tetrabothriids specificcharacters to the hypotheticalphylogeny (Far- (except Chaetophallus)were examined. Material was ris, 1970). Values for CI were calculatedfor individual borrowedfrom the U.S. National Museum (USNM), charactersand for overallrelationships within the fam- the British Museum of Natural History (BMNH) and ily. Additionally,the CI was used as a basis of com- HOBERG-PHYLOGENYOFTETRABOTHRIIDAE 619 parison of the present with previous explicit analysis 00 000000- phylogenies(Baer, 1932, 1954) via the TOPOLOGY N function of PAUP (Swofford,1985). r- eq 0 0 0- N rM 0

RESULTS %0 - C14 0 00 N N 0~ Characters tn - - C-4 0 0 0 N 1) Genital pore (position). Two states: 0 = v lateral; 1 = ventrolateral. C14 0 0 0- N ,M 0 2) Genital atrium (structure). Among tetra- en r4 0 0 - - N0-~ phyllideans the genital atrium is unmodified, N whereas, among all tetrabothriids, except Priapo- eq 0 0N-NN 0 cephalus, it is complex. Coding of this character cli 000000- was accomplished by functional outgroup (Tet- 0 rabothrius) following preliminary analysis. Three N 00 0 0-- 0 states: 0 = with extensive muscular modification; oll 00 00 -- 0 1 = dorsal component of atrium reduced, ventral 00 aspect with deep muscular concavity; 2 = atrium 0 0 0- 0- 0 cli 0, weakly developed, with vestigial ventral concav- 00 0a0 00-- 0 ity. f- 3) Male canal. A character unique to the Tet- 00 00 0- 0 rabothriidae (Baer, 1954), except Priapocepha- -0 ?n 0 00 N N N - lus, also coded by functional outgroup. Two states: .0U 0 = 1 = absent. co present; G 4) Cirrus sac (shape). Two states: 0 = cylin- (s m 00 00 - -0 drical; 1 = ovoid. = 5) Uterine pore. Two states: 0 multiple; 1 00 00 - -0 = single. 6) Uterus (extent). When completely gravid, 0 00 0 0- 0 t:3 the sacculate uterus extend the os- may beyond 0 00 -0 00 0 moregulatory canals. Two states: 0 = beyond canals; 1 = within canals. 00 x 7, 8) Ovary (position). Split into 2 transfor- Q 00 I mation series (see Glen and Brooks, 1985; Ho- -0 I berg, 1986) and coded with reference to the func- r- 000-00- 0m tional outgroup, the ovary may be in the anterior .0 00 0- 00 0 I> (0, 0), (0, 1), or posterior (1, 0) region 0 6C equatorial .0 of the proglottid. Character 7. Two states: 0 = 00 1 = Character 8. Two states: r., 00 anterior; posterior. 0 0 - 00-00 = = i00 0 anterior; 1 equatorial. 0) 9) Testes (number). Two states: 0 = testes > 0) 100; 1 = few testes. 0) 10, 11) Testes (position). Split into separate .0 0) transformation series, the testes may surround 0 0 0 0 - - - 0 the ovary (0, 0), be postovarian (1, 0) or lateral C)- 0.c to the ovary (0, 1). Character 10. Two states: 0 CO = 1 = Character 11. Two 0) surround; postovarian. *? = states: 0 surround; 1 = lateral. "0). 12) Testes (position). Two states: 0 = con- .0 00 tained within osmoregulatory canals; 1 = ex- C- . CZ) 0n tending beyond canals. = 0 13) Testes (position). Two states: 0 dorsal; 0) 1 = dorsal and ventral fields. CO _i t5 3 3 t H 0 14) Vitelline gland (form). Two states: 0 = follicular; 1 = compact. ^e , 65 620 THEJOURNAL OF PARASITOLOGY, VOL. 75, NO.4, AUGUST1989

TABLE II. Consistency indices of charactersused in 25) Bothridia (muscularization). Four states: the analysis of the Tetrabothriidae. 0 = slight; 1 = moderate; 2 = great; 3 = absent. 26) Apical development (excluding auricular Character number Character CI appendages). Three states: 0 = slight; 1 = moderate; 2 = great. 1 Genital pore-position 1.0 2 Genital atrium-structure 1.0 27, 28) Auricular structures. A complex char- 3 Male canal 1.0 acter split into independent transformation se- 4 Cirrus sac-shape 0.50 ries. In the Tetrabothrius and Chaetophal- 5 Uterine pore 0.50 genera 6 Uterus-extent 1.0 lus, as in Dinobothrium, there is a single auricle 7 Ovary-position 0.50 fused to an anteromedial extension on each both- 8 Ovary-position 1.0 9 Testes-number 0.50 ridium (0, 0) (see Spiitlich, 1909; Linton, 1922; 10 Testes - position 1.0 Baylis, 1926; Rees, 1956; Andersen and Lysfjord, 11 Testes-position 1.0 1982). In all species of Anophryocephalus, there 12 Testes-position 1.0 13 Testes-position 1.0 are a pair of auricular structures, generally not 14 Vitelline gland-form 0.50 fused, directed laterally and medially on the an- 1.0 15 Neck-length terior margin of each bothridium (1, 0) (Baer, 16 Genital ducts-position 1.0 17 Genital ducts-position 1.0 1954; Murav'eva and Popov, 1976). In Strobilo- 18 Osmoregulatory canals-dorsal 0.50 cephalus, there is a single auricle directed later- 19 Scolex-osmoregulatory canals 1.0 20 Scolex-embedded 1.0 ally from each bothridium (2, 0) (Baer, 1954). 21 Scolex-shape 1.0 Trigonocotyle is characterized by 3 independent 22 Scolex-shape 0.667 auricular appendages on the margins of the both- 23 Bothridia- shape 1.0 24 Bothridia-depth 1.0 ridia (0, 1) (Baer, 1932, 1954; Temirova and 25 Bothridia-muscularization 1.0 Skrjabin, 1978), whereas auricles are absent in 26 Apical development 1.0 Character 27. Four states: 27 Auricles-structure 1.0 Priapocephalus (3, 0). 28 Auricles-structure 1.0 as in Tetrabothrius (0); as in Anophryocephalus (1); as in Strobilocephalus (2); as in Pri- apocephalus (3). Character 28. Two states: sim- 15) Neck (length). Two states: 0 = short; 1 = ilar to Tetrabothrius (0); as in Trigonocotyle (1). long. of the Tetrabothriidae 16) Genital ducts (position). Two states: 0 = Phylogeny between osmoregulatory canals; 1 = ventral to A single cladogram for the 6 genera of Tetra- canals. bothriidae resulted from an analysis of 28 ho- 17) Genital ducts (position). Two states: 0 = mologous series representing 41 character states median; 1 = ventral. (Fig. 1). This phylogenetic hypothesis was strongly 18) Osmoregulatory system (dorsal canals). supported with a CI of 85.4% (minimum length Two states: 0 = fully developed; 1 = atrophied. = 41; required changes = 48), indicating a good 19) Scolex (osmoregulatory canals). Two fit of these data to the cladogram. Consistency states: 0 = simple, tubular; 1 = subtegumental values for individual characters are presented in and reticulate. Table II. Homoplasy was postulated for parallel 20) Scolex (position in host). Two states: 0 = development in 1 character (ovoid cirrus sac in superficial contact with intestinal mucosa; 1 = Tetrabothrius and Strobilocephalus) and evolu- embedded in mucosa. tionary reversals of 6 additional attributes (uter- 21, 22) Scolex (shape). Split into separate ine pore, position of ovary, number of testes, transformation series, the scolex may be rect- form of vitelline gland, dorsal osmoregulatory angular and flat (0, 0), rectangular and cuboidal canals, and shape of scolex). These latter in- (1, 0), round and flat (0, 1) or globular (0, 2). stances of homoplasy were largely associated with Character 21. Two states: 0 = rectangular and Anophryocephalus, Strobilocephalus, and Pri- flat; 1 = rectangular and cuboidal. Character 22. apocephalus. Three states: 0 = rectangular and flat; 1 = round Monophyly for the Tetrabothriidae is strongly and flat; 2 = globular. supported by a synapomorphy for the antero- 23) Bothridia (shape). Four states: 0 = rect- ventral position of the vitelline gland (a consis- angular; 1 = round; 2 = triangular; 3 = absent. tent character excluded from the present analy- 24) Bothridia (depth). Four states: 0 = shal- sis). Additional characters including the dorsal low; 1 = intermediate; 2 = deep; 3 = absent. uterine pore (5) and compact form of the vitelline HOBERG-PHYLOGENYOFTETRABOTHRIIDAE 621

U) :D U) :D_J U) U) I D LLJ :D I -J 0 LU EL LU I JCLI 0 _1J I 0 0 >- o I 0J 0 I Q- 0 0 I 0 z i m IL

21 28

1524 25

:22 23

9 14

FIGURE 1. Cladogramfor generic level relationshipsof the Tetrabothriidae.Apomorphic charactershave been mapped on and designated by slashes; postulated evolutionary reversals and parallel development are indicated by stars and crosses, respectively.This hypothesis has a CI = 85.4%representing a minimum of 41 steps and 48 postulatedchanges. gland (14) are constant within the group but have leted. Three cladograms of equal length (CI = postulated evolutionary reversals associated with 77.8%) were found. All differed slightly with re- Priapocephalus. spect to the topology of Tetrabothrius, Chaeto- The genera Tetrabothrius and Chaetophallus phallus, and Trigonocotyle but not in the group- are postulated as relatively plesiomorphic with ing or placement of the Anophryocephalus- respect to Anophryocephalus, Strobilocephalus, Priapocephalus clade. This corroborates the and Priapocephalus (Fig. 1). The inclusive group- character transformation series for the scolex and ing of these latter genera results from the ven- supports the sister group association of Strobilo- trolateral position of the genital pore (1), rela- cephalus and Priapocephalus. neck and an dorsal tively long (15), atrophied DISCUSSION osmoregulatory system (18). A sister group re- Character evolution lationship for Strobilocephalus and Priapo- cephalus is based on 7 synapomorphies, partic- Analyses presented herein provide a founda- ularly the extent of the testes beyond the tion for postulating several trends in character osmoregulatory canals (12), ventral aspect of the evolution among the Tetrabothriidae. A suite of genital ducts (17), and the reticulate structure of characters associated with the scolex has been the osmoregulatory canals in the scolex (19). influenced by hypertrophy of the apical region Additional foundation for the derived rela- with concomitant reduction in the complexity tionship of Priapocephalus resulted from a sub- and eventual loss of the auricles (as exemplified sidiary analysis in which all characters of the by Priapocephalus). A parallel situation is ap- scolex and genital atrium (19-28; 2, 3) were de- parent in the simplification of the structurally 622 THEJOURNAL OF PARASITOLOGY, VOL. 75, NO.4, AUGUST1989 intricate genital atrium, which is most strongly Following detailed study of scoleces from im- developed among species of Tetrabothrius.Al- mature specimens of Priapocephalus,Temirova though these charactersare of considerable di- and Skrjabin(1978) concluded that the globular agnostic importance, their exclusion from the holdfast actually representeda "pseudoscolex" analysisdoes not substantiallyalter the topology that was derived secondarily from the anterior of the cladogram(Fig. 1). Thus, robust support proglottidsduring early development in the de- for this phylogenetichypothesis is indicated and finitive host (see Baer, 1954). Their contention an Anophryocephalus-Priapocephalusclade ap- was based on the structureof the parenchyma, pears to have a firm empirical basis. presence of longitudinal musculature, and os- Attributes of the scolex have figured promi- moregulatorycanals. Thus, it was consideredthat nently in attempts at explicit phylogenetic re- the "truescolex" was lost duringthe initial stages construction for the tetrabothriids(Baer, 1932, of development and that the pseudoscolex was 1954) or in discussionsof genericevolution with- not structurallyor ontogeneticallyhomologous in the family (Baylis, 1926; Temirova and Skrja- to holdfastscharacteristic of othertetrabothriids. bin, 1978; Galkin, 1987; Hoberg, 1987a). Struc- There was also a suggestionof paedomorphosis tural similarities of the scolex in Tetrabothrius (postdisplacement;see Fink, 1982) in the ontog- spp. (4 auriculate bothridia) and some tetra- eny of the pseudoscolex as development was phyllideans had been recognized previously thought to be precededby penetrationof the in- (Baylis, 1926; Baer, 1954; Temirova and Skrja- testinal mucosa of the definitive host by meta- bin, 1978); however, the extent to which these cestodes. attributesrepresented homologies was disputed Observationsof Priapocephalusand Strobilo- (see Andersen and Lysfjord, 1982). Hoberg cephalusduring the present study appear to re- (1987a) provided independent ontogenetic data fute contentions by Baer (1954) and Temirova for Tetrabothriusthat for the first time firmly and Skrjabin(1978) concerningstructure of the corroborated hypotheses for scolex homology scolex. In both genera,there is a globularholdfast among tetrabothriidsand tetraphyllideans.The with extensivedevelopment of longitudinalmus- presence of homologous auriculate appendages culature. Additionally, the osmoregulatoryca- in Tetrabothrius,Trigonocotyle, and all species nals comprise a highly reticulate anastomosing of Anophryocephalus,as reported herein and system of tubules that are subtegumentalin lo- confirmed for Strobilocephalustriangularis (see cation. These attributes,in addition to other rec- Baer, 1954), establishes a basis for monophyly ognized synapomorphieslinking Strobilocepha- of these tetrabothriids. lus and Priapocephalus (Fig. 1), support the In contrast to "typical tetrabothriids,"Pri- placement of the latter genus and structuralho- apocephaluswas characterizedby an absence of mology of the holdfast. However, the potential auricularstructures or vestigial bothridia (Baer, for paedomorphicdevelopment of the scolex in 1954; Temirova and Skrjabin,1978). The amor- Priapocephalusis of considerableinterest. Such phous, globular scolex characteristicof this ge- a pattern would parallel that known (Hoberg, nus, in conjunction with a number of plesio- 1987a) for Tetrabothriusand Anophryocephalus, morphic attributes (multiple uterine pores, suggestinga degreeof uniformityin morphogen- follicularvitelline gland, elongate cirrus sac and esis of the adult holdfastwithin the family Tetra- apparentlack of a complex genital atrium) has bothriidae. This heterochronicsequence in on- contributedto the controversyabout generic af- togenyof the scolexis thoughtto be uniqueamong finities of these cetacean parasites (Baer, 1932, the Eucestoda(Hoberg, 1987a). 1954; Temirova and Skrjabin, 1978; Galkin, of 1987). Baer(1932) consideredPriapocephalus to Comparison phylogenies be highly derived and close to Strobilocephalus, Baer (1932, 1954) presentedthe only explicit but he later(1954) suggestedindependent origins phylogenies for genera of the Tetrabothriidae, for both generafrom advancedTetrabothrius spp. whereas Rees (1956), Temirova and Skrjabin among cetaceans.Temirova and Skrjabin(1978) (1978), Galkin (1987), and Hoberg (1987a) dis- considered Priapocephalusand Tetrabothriusas cussed some potential relationships among the sister groupssharing a common ancestor(proto- genera.The evolutionarytrees developed by Baer tetrabothriidwith tetraphyllideanaffinities) while were redrawn(Figs. 2, 3) to allow direct com- also suggestingthat among representativesof the parison with the present phylogeny via the TO- former, the scolex was highly modified. POLOGY function of PAUP (Swofford, 1985). HOBERG-PHYLOGENYOFTETRABOTHRIIDAE 623 oOQ- 4 0D T- I- 0 o :Z _r HL 0 < CL F-H

1116 23-25 27 i 23-25

22-27

26 27

5 9 14 15 23-25

FIGURE2. Cladogram prepared from phylogeny by Baer (1932) with character evolution evaluated by TO- POLOGY function. Characters are those in Figure 1; CI = 80% representing a minimum of 40 steps and 50 postulated changes (Chaetophallus deleted from analysis). Branch labels: OUTG, outgroup; ANOP, Anophry- ocephalus; STRO, Strobilocephalus; PRIA, Priapocephalus; TRIG, Trigonocotyle-, TETR, Tetrabothrius.

Characterswere mapped onto these alternative characters,respectively. Figure 3 was drawn to trees and optimized by Farrisoptimization (Far- recognizeBaer's (1954) contentionthat avian tet- ris, 1970) to allow a determination of the effi- rabothriidswere primitive and that 2 advanced ciency of the competing hypotheses (see Brooks lineages were apparentamong genera in mam- et al., 1985a). malianhosts. Consequently,Chaetophallus, with Baer (1932) recognized 2 lines of evolution the "classicaltype scolex," representsspecies of from Anophryocephalus.Based on the assump- Tetrabothriusthat Baer (1954) consideredto be tion that auricular appendages were absent in among the most primitive of those occurring Anophryocephalus,progressive development of among avian hosts (Procellariiformes).Exten- the apical region led to the derivation of Stro- sive radiation of Tetrabothriusspp. occurred bilocephalusand Priapocephalus(Fig. 2). In con- among seabirdsbut was apparentlyaccompanied trast, modification of the apical region with de- by minimal morphologicaldiversification of the velopment of auricularappendages occurred in scolex (Baer, 1954). In contrast,species of Tetra- Trigonocotyleand Tetrabothrius(here including bothriusamong marine mammals were thought Chaetophalluswith Tetrabothrius).Although the to be derived from those among seabirds with groupingof Anophryocephalus,Strobilocephalus subsequentevolution involving trends in the re- and Priapocephalusis supported, Baer's (1932) ductionof the bothridiaand atrophyof the apical hypothesis is less efficient (CI = 80%, length = region (Baer, 1954; Rees, 1956). Thus, Trigon- 50 steps; versus 87% for the present cladogram ocotyle was considered as originatingindepen- with Chaetophallusdeleted). Evolutionary re- dently from this latter group of Tetrabothrius versals are postulated for 8 characters(5, 9, 14, spp. with continuedalteration of the auriclesand 15, 18, 23, 24, 25) and paralleldevelopment for atrophy of the apical zone. However, hypertro- 2 attributes(4,7). phy of the apical region was postulated for The more detailed phylogeny postulated by Anophryocephalus,Strobilocephalus and Priapo- Baer (1954) was considerablyless parsimonious cephalus,with the latteralso being independently (CI = 57.7%; length = 71 steps) with parallel derived from Tetrabothriusspp. among ceta- derivation (characters4, 7, 8, 12, 13, 17, 18, 19, ceans. These hypotheses for independent deri- 20, 22, 26) and evolutionary reversals (1, 2, 3, vation, adaptation,and convergenceaccount for 5, 9, 14, 15, 22, 23, 24, 25, 26, 27) of 11 and 13 the increasedlength of the tree, and 7 of 11 cases 624 THEJOURNAL OF PARASITOLOGY, VOL. 75, NO.4, AUGUST1989

0 I

9 14 22-24

FIGURE3. Cladogramprepared from phylogeny by Baer (1954), with characterevolution evaluated by TOPOLOGY function. Characters are those in Figure 1; CI = 57.7% representing a minimum of 41 steps and 71 postulated changes. Branch labels as in Figure 2 except OUTG is replaced by TPHY, Tetraphyllidea.

of parallel evolution are postulated for Strobilo- scolex and genital atrium have been the primary cephalus and Priapocephalus. attributes considered in earlier evaluations (Baer, Temirova and Skrjabin (1978) suggested that 1932, 1954; Rees, 1956; Temirova and Skrjabin, Tetrabothrius and Priapocephalus shared a com- 1978). Although such were important in the cur- mon ancestor directly related to tetraphyllideans. rent study, a suite of other homologous charac- Relationships of other genera were unresolved ters, not previously considered in evolutionary although they suggested that Anophryocephalus studies of the family, strongly supported the and Trigonocotyle were phylogenetically younger cladogram. In concordance with some previous and derived from Tetrabothrius. Strobilocepha- studies, Tetrabothrius was postulated as rela- lus was thought to be without definite associa- tively plesiomorphic (Baer, 1954; Rees, 1956; tion, an opinion refuted in the present study by Temirova and Skrjabin, 1978; Galkin, 1987; synapomorphies associated with the genital Hoberg, 1987a) and the natural grouping of atrium in the former genus and Anophryoceph- Anophryocephalus, Strobilocephalus, and Pri- alus. apocephalus was reinforced (Baer, 1932; Hoberg, Galkin (1987) and Hoberg (1987a) considered 1987a). Completion of phylogenetic analyses of Tetrabothrius as relatively primitive while sug- genera and species of the Tetrabothriidae will gesting a derived status for such genera as Anoph- provide for development of a natural classifica- ryocephalus and Priapocephalus. Galkin (1987) tion for the group, an objective means of assess- in accordance with Baer (1932, 1954) and Rees ing previous phylogenetic hypotheses for rela- (1956) suggested that Anophryocephalus repre- tionships among species (e.g., Baer, 1954), and sented the base of a lineage in which ensued pro- a basis of comparison to determine the degree gressive development of the apical region. of congruence between the phylogenetic histories of parasites and hosts as an indicator of parasite- host coevolution or colonization (see Brooks and Conclusions Wiley, 1986; Brooks, 1988). The latter also may The present analysis constitutes a more effi- promote an evaluation of the role of parasite cient phylogenetic hypothesis for generic-level adaptive radiation in the evolution of this marine relationships within Tetrabothriidae than those parasite fauna (see Brooks et al., 1985b; Hoberg, provided in previous studies. Characters of the 1986, 1987a). HOBERG-PHYLOGENYOFTETRABOTHRIIDAE 625

ACKNOWLEDGMENTS FINK,W. L. 1982. The conceptual relationshipbe- tween ontogeny and phylogeny. Paleobiology 8: Specimens of some tetrabothriids were kindly 254-264. loaned by Dr. R. H. Bray and Dr. D. I. Gibson FUHRMANN,O. 1932. Les teniasdes oiseaux.Memoi- of the British Museum (Natural History), Dr. J. res de L'Universitede Neuchatel 8: 1-383. R. Lichtenfels of U.S. National Museum, Dr. R. GALKIN,A. K. 1987. 0 stanovlenii netsiklofillidnykh tsestod parazitov chaek. Trudy Zoologicheskogo L. Rausch and Dr. A. Adams of the University InstitutaAN SSSR (Leningrad)161: 3-23. of Washington, and Dr. M. D. Dailey of Cali- GLEN,D. R., ANDD. R. BROOKS. 1985. Phylogenetic fornia State University, Long Beach. The study relationshipsof some strongylatenematodes of benefitted from discussions with Dr. D. R. primates.Proceedings of the HelminthologicalSo- of 52: 227-236. Brooks, Dr. R. L. Rausch, and Dr. R. T. O'Gra- ciety Washington HENNIG,W. 1966. Phylogenetic systematics. Uni- dy. 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