crocodilians and their helminth parasites: macroevolutionary considerations

AMER. ZOOL., 29:873-883 (1989)

Crocodilians and Their Helminth Parasites:Macroevolutionary Considerations'

DANIEL R. BROOKSDepartment of Zoology, University of Toronto, Toronto, Ontario M5S 1A1, Canada

RICHARD T. O'GRADY

Division of Worms, U.S. National Museum of Natural History,Smithsonian Institution, Washington, D.C. 20560

SYNOPSIS. Crocodilian relationships supported by the phylogenetic relationships of dige-nean and nematode parasites are compared with current estimates of crocodilian phylog-eny. The parasite data support (1) the placement of Gavialis as the sister-group of thealligatorids and the crocodylids, (2) the monophyly of alligators and caimans, (3) theplacement of Caiman (as a monophyletic group) as the sister-group of Melanosuchus plusPaleosuchus, and (4) ancient origins of Crocodylus consistent with patterns of continentaldrift. The parasite data do not support the monophyly of Crocodylus, but the "misplaced"species (C. palustris and Osteolaemus) have had few parasites reported from them. Thereis evidence of widespread host-switching, but most of the ambiguity appears to result fromuneven representation of parasite groups in host species. This is probably due both touneven sampling by parasitologists and to parasite extinctions associated with crocodilianextinctions.

INTRODUCTION

The Crocodilia represents an excellenthost system for evaluating the develop-ment of methods for assessing macroevo-lutionary patterns of coevolution. Nearlya decade ago, the digenean trematodefauna of crocodilians was analyzed phylo-genetically, and the results compared qual-itatively with crocodilian biogeography andphylogeny (Brooks, 1979). In this study, weupdate that study based on (1) new infor-mation about the digenean fauna of croc-odilians and (2) information about theascaridoid nematode fauna of crocodilians,using (3) new analytical methods for assess-ing phylogenetic congruence and incon-gruence of host and parasite phylogenies.

Crocodilians are a good study groupbecause they represent a monophyleticassemblage of great age and broad geo-graphic distribution. This increases thepossibility of finding evidence for phylo-genetic constraints in host-parasite rela-tionships. The Crocodilia is also a groupof limited extant diversity (a numerical relict

1 From the Symposium on Biology of the Crocodiliapresented at the Annual Meeting of the AmericanSociety of Zoologists, 27-30 December 1987, at NewOrleans, Louisiana.

sensu Simpson, 1944), and this makes it pos-sible to examine putative coevolutionarypatterns for most of the members of thehost group. Conversely, this relictual natureof living crocodilians presents some specialproblems. The first of these is the probablerelictual nature of the parasite fauna. Hasparasite extinction, associated with hostextinction, been so extensive that nocoevolutionary patterns remain? The sec-ond problem is one of the frequency of hosttransfers by parasites. We will show thattracing the origins of the host-parasite rela-tionships we see today is made difficult forboth reasons listed above. There is evi-dence both that the helminth parasite faunaof crocodilians is depauperate and thatthere has been host-switching betweenbirds and mammals. Hence, birds, the sis-ter-group of crocodilians, host many groupsof helminths lacking in crocodilians. Thereis also evidence that major components ofthe crocodilian helminth fauna have beenacquired from helminth groups originallyinhabiting piscivorous fish. This latterfinding raises the question of whether ornot the host transfers occurred long enoughago that subsequent diversification of theparasite groups could coincide with thephylogenetic relationships of extant croc-odilians.

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874 D. R. BROOKS AND R. T. O'GRADY

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FIG. 1. Phylogenetic tree for major groups of acanthostome digeneans, with host types superimposed. Te= teleost fishes; T = turtles; C = crocodilians; O = ophidians. Arrows indicate instances of host transfersfrom teleosts.

THE HELMINTH FAUNA OFCROCODILIANS

The relictual nature of the faunaBrooks (1989) has investigated the dis-

tribution of helminth groups, at the ordi-nal level, among tetrapod vertebrates. Ifthose data are examined with respect tomajor amniote groups, we find evidencethat both crocodilians and the Tuatarapossess depauperate helminth faunas com-pared to their closest relatives. For exam-ple, crocodilians lack any tapeworm oracanthocephalan parasites, both of whichare major components of avian helminthfaunas. The helminths that do inhabitcrocodilians represent four orders of dige-neans and two orders of nematodes. Oneof the nematode orders is represented bya single species. We will discuss the otherfive groups, their phylogenetic relation-ships, and the nature of their historicalassociations with crocodilians.

The digenean faunaThe digenean fauna of crocodilians can

be divided into two groups. First, membersof the orders Echinostomatiformes andStrigeiformes that inhabit crocodilians andtheir closest relatives exhibit a high degreeof phylogenetic congruence with amniotes.The consistency index, which measures thedegree of fit of the data to a phylogenetictree (see Brooks et al., 1986), of this fit is93%. We will call this group the "co-evolved" group. With regard to the relictual

nature of the host group, it is pertinent tonote that the echinostomatiforms, repre-sented by a single group, are relatively moreplesiomorphic than the strigeiforms, rep-resented by five family and supra-familialgroups (see Brooks et al., 1985 for the dige-nean phylogeny). This suggests the possi-bility of extinctions in the older lineagesof digeneans correlated with extinctions inolder lineages of crocodilians.

The second group of digeneans inhab-iting crocodilians includes representatives

/

Te.O.C Te.O.C

FIG. 2. Phylogenetic tree for seven genera of ascari-doid nematodes inhabiting crocodilians, with hostgroups below generic names. Te = teleost fishes; C= crocodilians; O = ophidians. Arrows indicate hosttransfers from teleosts to crocodilians (3 cases) andfrom crocodilians to teleosts (1 case).

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PARASITES AND CROCODILIAN PHYLOGENY 875

I 2 3 4 5 6 7 8 9 10 II 12 13 14 15 16 17 18 19 20 21 22

FIG. 3. Incompletely resolved phylogenetic tree for 22 species of proterodiplostomatid digeneans, numberedfor additive binary coding. 1-3 = Proterodiplostomum; 4 = Paradiplostomum; 5 = Massoproslatum; 6 = Neelydip-lostomum; 7-12 = Pseudoneodiplostomum; 13 = Archaeodiplostomum; 14 = Mesodiplostomum; 15 = Herpetodiplo-slomum; 16—17 = Pseudocrocodilicola; 18 = Prolecithodiplostomum; 19—20 = Crocodilicola; 21 = Cystodiplostomum;22 = Polycotyle.

of the orders Opisthorchiformes and Pla-giorchiformes, both of which are relativelymore apomorphic than the Strigeiformes(Brooks et al., 1985). All the opisthorchi-

forms known from crocodilians are mem-bers of the sub-family Acanthostominae,family Cryptogonimidae. Figure 1 depictsthe phylogenetic relationships for eight

(ID

58 (IV) (V) (VI)

FIG. 4. Phylogenetic trees, numbered for additive binary coding, for eight groups of digeneans inhabitingcrocodilians. (I) = Allechinostomum (including some species originally included in Stephanoprora) (jacaretinga(37), ornata (38), crocodili (39)); (II) = Dracovermis (occidentalis (41), brayi (42), rudolphi (43), nicolli (44)); (III)= Odhneriotrema (incommodum (48), microcephala (49)), Nephrocephalus (50), Tremapoleipsis (51); (IV) = Cyathocotyle(brasiliensis (54), fraterna (55), crocodili (56)); (V) = Exotidendrium (ghariali (50), sp. (60)); (VI) = undescribedblood fluke (62); (VII) = Pachypsolus (sclerops (63)); (VIII) = Deurithitrema (gingae (64)).

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(I)

87 88 89 90 94 95

(III) (IV)

FIG. 5. Phylogenetic trees, numbered for additive binary coding, for five groups of acanthostome digeneansinhabiting crocodilians. (I) = Timoniella (incognita (65), scyphocephala (66), unami (67), loossi (68), absita (69));(II) = Proctocaecum (coronarium (73), vicinum (74), gonotyl (75), productum (76), elongatum (77), crocodili (78), atae(79), nicolli (80)); (III) = Caimanicola (pavida (87), caballeroi (88), marajoara (89), brauni (90)); (IV) = Acantho-stomwn (americanum (94)); (V) = Atrophecaecum (slusarskii (95)).

major lineages of acanthostomes, updatedand modified from Brooks (1980) to showthe paraphyletic nature of Acanthostomum.Acanthostomes inhabiting crocodiliansappear to have been acquired from speciesinhabiting piscivorous fishes through fiveindependent host switches (Fig. 1). Mem-bers of the Plagiorchiformes, the relativelymost apomorphic of the four digeneanorders discussed herein, that inhabit croc-odilians represent four small groups, total-ling five species, whose sister-group rela-tionships are unclear but suggestive offour independent acquisitions. We will callthe opisthorchiform plus plagiorchiformdigeneans inhabiting crocodilians the"acquired" group.

The nematode fauna

With the exception of a single species offilarid, the nematodes known to inhabitcrocodilians are ascaridoids. The followingdiscussion is based on a phylogenetic anal-ysis of this group of ascaridoids (O'Grady,

preparation; see also Sprent, 1977;in1978a, b, 1979a, b, 1980).

The ascaridoid nematodes inhabitingcrocodilians are members of seven genera

(Fig. 2). The two relatively most plesio-morphic genera, Goezia and Terranova, areprimarily parasites of teleost fishes, withsecondary transfers to sea snakes and tocrocodilians. The other five genera forma monophyletic group of species, almost allof which inhabit crocodilians (some speciesof Dujardinascaris have apparently recolo-nized teleosts). Thus, the ascaridoids ofcrocodilians appear to be the result of threeindependent colonizations (Fig. 2). Theirhistory is similar to that of the "acquired"group of digeneans.

COEVOLUTIONARY ANALYSIS

The database

Figures 3-6 depict the current estimatesof phylogeny for the helminth groups dis-cussed above. Each tree is numbered forAdditive Binary Coding according to the pro-tocol developed by Brooks (1981; see alsoBrooks, 1988, 1989). Each phylogenetictree is treated like a complex charactertransformation series {homologous series ofWiley, 1981), in which the parasites andtheir phylogenetic relationships are embodiedin a binary code. When host taxa aregrouped phylogenetically using such par-

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FIG. 6. Phylogenetic tree, numbered for additive binary coding, for ascaridoid nematodes inhabiting croc-odilians. Groups include: Geozia (28) (holmesi (1), lacerticola (2)); Terranova (37) (caballeroi (3), crocodili (4),lanceolata (5)); Multicaecum (6) (agile (6)); Ortleppascaris (38) (antipini (7), nigra (8), alata (9)); Gedoelstascaris (31)(vanderbrandeni (10), australiensis (11)); Brevimultkaecum (32) (gibsoni (12), stekhoveni (13), tenuicolle (14), ^intoi(15), baylisi (16)); Dujardinascaris (48) (chabaudi (17), gedoelsti (18), puylaerti (19), woodlandi (20), longispicula(21), taylorae (22), dujardini (23), waltoni (24), madagascariensis (25), helicini (26), mawsonae (27)).

asite data, a parasite-based /ios/ cladogramresults. This can be compared directly withestimates of host phylogeny to provide anassessment of the degree of historical asso-ciation between host and parasite groups.

of the faunaThree methods have been developed to

help estimate the ages of lineages of species.The oldest of these is correlation of fossilevidence with the results of various geo-logical and chemical dating methods. Morerecently, estimates of the ages of lineageshave been based on models of molecularevolution ("the molecular clock") and oncorrelations between biogeographic distri-butions and models of geologic history("vicariance biogeography"). In the pres-ent study, neither fossil evidence normolecular data exist for the parasitic hel-minths of crocodilians. Hence, our esti-

mates of the age of the crocodilian hel-minth fauna must be based on bio-geographic correlations.

If our phylogeny reconstructions aregenerally correct, we expect the biogeo-graphic patterns exhibited by the echino-stomatiform and strigeiform digeneans(which have apparently coevolved withamniotes) to indicate ages of origin consis-tent with the pre-continental drift originsof crocodilians. In addition, if the hel-minths that have been secondarily acquiredby crocodilians (the acanthostome and pla-giorchiform digeneans and the ascaridoidnematodes) were acquired long enough agoto have coevolved subsequently with croc-odilians that are extant, their biogeo-graphic patterns should be consistent withthose exhibited by the "primarily co-evolved" parasites. Figure 7 summarizesthe historical biogeographic information

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FIG. 7. Area cladograms based on phylogenetic rela-tionships of digeneans (solid lines) and nematodes(dotted lines) inhabiting crocodilians plotted on mapof Pangaea.

for the crocodilian helminth fauna. Thearea cladograms based on digenean dataand on nematode data have been super-imposed on a map of Pangaea. The fit ofthe digenean fauna to the area cladogram,indicated by the consistency index, is 93%and for the nematode fauna it is 85%. Thisshows pictorially that the biogeographic

data support an interpretation that thecrocodilian helminth fauna, both the coe-volved and the acquired portions, was estab-lished long enough ago to have coevolvedwith crocodilians that are extant today.

Coevolutionary relationships of the fauna

Three phenomena can affect phyloge-netic analysis of the degree of coevolutionfor any host and parasite assemblage. Themost obvious of these is host-switches, colo-nization of novel (and unrelated) hosts. Anytime this occurs and leads to speciation,host relationships indicated by parasiterelationships will pertain to historical epi-sodes of host-switching and not to historicalepisodes of host and parasite co-speciation.In contrast to host-switches, which provideincorrect estimates of host phylogeny, twoother phenomena infuse ambiguity intocoevolutionary analyses because they resultin parasite groups being unevenly repre-sented among host groups. The first ofthese is parasite extinctions. We would notbe surprised to find evidence of this for the

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Fic. 8. Host cladogram for 17 species of crocodilians based on phylogenetic relationships of their digeneanparasites. Additive binary codes (from Figs. 3-5) indicating parasite support for branches of the host cladogram:1 (Crocodylus palustris) = 95; 2 (C. acutus) = 0; 3 (C. rhombifer) = 0; 4 (Melanosuchus) = 14-15, 23; 5 {Paleosuchus)= loss of 35; 6 (Caiman latirostris) = 15, 22, loss of 28; 7 (Alligator) = 13, 16-18, 21, 31, 41, 47-48, 67, 70-71, 73, 83-84, 86-87; 8 (Caiman crocodilus crocodilus) = 37, 40, 66, 71, 88; 9 (C. c.fuscus) = 4, 20, 54, 58, 62,65; 10 (Crocodylus moreletii) = 5, 25; 11 (Cavialis) = 6, 44-47, 59, 61; 12 (Crocodylus siamense) = 7-8; 13(Osteolaemus) = 51, loss of 85, loss of 86; 14 (Crocodylus cataphractus) = 42, 46-47, loss of 53, loss of 85, lossof 86; 15 (C. niloticus) = 38-40, 50, 59, 61, 74-76, 83-84; 16 (C. johnstoni) = 7, 80; 17 (C. porosus) ,= 9-10,43, 45-47, 56-58, 60-61, 63-64, 69-72, 77-79; 18 = 68, 70-72, 88-89, 91-94; 19 = 1, 27; 20 = 2-3, 15,19, 22-24, loss of 28, 49, 91-92; 21 = 32, 52-53, 72, 93; 22 = 29, 33-34; 23 = 35; 24 = 27; 25 = 55, 57-58; 26 = 81-82; 27 = 12, 53; 28 = 85-86; 29 = 26; 30 = 28, 36.

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FIG. 9. Host cladograms differing in placement of Osteolaemus based on biogeographic relationships ofdigeneans inhabiting crocodilians. Terminal taxa are labeled as in Figure 8. Numbered branches indicateportions of the host cladograms requiring explanations of host-switching or extinction in addition to thosenoted for Figure 8. Additive binary codes (from Figs. 3-5) indicating those additional parasite homoplasies:1 = 27; 2 = 29, 32-34, 53, 72, 93; 3 = 32, 52-53, 72-73; 4 = 1 5 , 22, loss of 28, 29, 33-34; 5 = 27; 6 = lossof 28, loss of 36; 7 = 27; 8 = loss of 26, loss of 28, loss of 36; 9 = loss of 81, loss of 82, loss of 85, loss of 86;10 = 7; 11 = 12, 53; 12 = 12, 53.

crocodilian parasites, because the hoststhemselves have experienced substantialextinction. The second phenomenon is onethat must always remain an open questionin coevolutionary studies. The host speciesthat are best studied are those that areaccessible in large numbers to parasitolo-gists.

The Digenea

Figure 8 is the host cladogram supportedby the digenean data. The consistencyindex for this cladogram is 71 %, indicatingthat less than one-third of the database is

ambiguous with respect to host relation-ships. Most of the homoplasy is due to par-allelisms (host-switches) rather thanreversals (extinctions). In addition to this,the host relationships indicated by thedigeneans do not preserve the integrity ofall the generic groupings of the crocodil-ians, or of their supra-generic relation-ships. The consistency index for the echi-nostomatiform and strigeiform digeneans(the primarily coevolved groups—charac-ters 1-64) is 74%, whereas for the acan-thostomes the CI is 64%. If we constructa host cladogram using only the primarily

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FIG. 10. Host cladogram for 14 species of crocodil-ians based on phylogenetic relationships of theirascaridoid nematodes. Additive binary codes (fromFig. 6) indicating parasite support for the host clado-gram: 1 (Gavialis) = 0; 2 (Crocodylus palustris) = 0; 3(Alligator) = 2, 7, 14, 24, 28, 30, 35; 4 (Caiman lati-rostris) = 1 5 , loss of 16, loss of 38; 5 (C. crocodiluscrocodilus) = 15, 17, 22; 6 (Melanosuchus) = 5, 12, 29,37; 7 (Crocodylus intermedius) = 9, loss of 40, loss of42, loss of 44, loss of 46, loss of 47, loss of 48; 8 (C.acutus) = loss of 45; 9 (C. rhombifer) = 7, 30; 10 (C.cataphractus) = 0; 11 (C. niloticus) = 18-19, 23, 34-35; 12 (C. novaeguineae) = loss of 31, loss of 43, lossof 45; 13 (C. johnstoni) = 6, loss of 22; 14 (C. porosus)= 1, 28; 15 = 6; 16 = 9, 13, 32; 17 = loss of 40, lossof 42, loss of 44, loss of 46, loss of 47, loss of 48; 18= 16,33, 39,41; 19 = 26, 36; 20 = loss of 43; 21 =6, 8, 10, 25, 30; 22 = 4, 11, 29, 37; 23 = 22, 27, 36,loss of 38; 24 = 31; 25 = 38, 40, 42-49; 26 = 50-52.

coevolved parasites, Crocodylus siamensis ismoved to being the sister-species of C. john-stoni and the CI is improved one step to75%. This indicates that the extensive host-switching exhibited by the acanthostomesis not responsible for the discrepancybetween the parasite-based host cladogramand current estimates of crocodilian phy-logeny.

Taking a cue from the biogeographicdata, we have fit the digenean data to ahost "phylogeny" that preserves both thebiogeography and the generic integrity ofthe crocodilian taxa (Fig. 9). The consis-tency index for these trees is 64% or 63%,depending on the placement of Osteolae-mus. The fact that the consistency indexdrops so little when the parasite data arefit to the host phylogeny, in addition to theobservations discussed in the previousparagraph, leads us to conclude that the

FIG. 11. Host cladogram based on biogeographicrelationships of nematodes inhabiting crocodilians.Terminal taxa as in Figure 10. Numbered branchesindicate portions of the host cladogram requiringexplanations of host-switching or extinction in addi-tion to those noted in Figure 10. Additive binary codes(from Fig. 6) indicating those additional parasite ho-moplasies: 1 = 9, 13, 32; 2 = 9, 13, 32; 3 = 15; 4 =loss of 38, loss of 40, loss of 42, loss of 44, loss of 46,loss of 47, loss of 48, loss of 49.

primary reason for the discrepancy betweencrocodilian phylogeny and the digenean-based crocodilian cladogram is the paucityof parasite data for the host species thatare misplaced. At present, we do not knowif this is due to uneven sampling of hostspecies or to the uneven distribution ofdigeneans among surviving crocodilians.

The NematodaFigure 10 is the host cladogram sup-

ported by the nematode data. The consis-tency index for this cladogram is 64%,somewhat lower than that for the digeneandata (Fig. 8). The majority of the ambiguity(homoplasies in parasite distributionsamong hosts) stems from reversals ratherthan parallelisms, supporting an interpre-tation of widespread extinctions in the par-asite fauna (assuming adequate sampling).Again using the biogeographic data, wehave fit the nematode data to the host"phylogeny" shown in Figure 11. The con-sistency index for this host cladogram is54%. Eight of the 15 extra steps requiredto fit the nematode data to this configu-ration are reversals, or putative extinc-tions, for Crocodylus palustris. Aside fromthis single placement, there is little differ-

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FIG. 12. Host cladogram for 19 species of crocodilians based on the biogeographic relationships of theirhelminth parasites (digeneans and ascaridoid nematodes). Names of terminal taxa and parasite support foreach branch of the host cladogram as for Figures 8-11.

ence between the fits obtained for thenematode data in Figures 10 and 11. Hence,the discrepancy between the crocodilianphylogeny and the nematode-based hostcladogram stems from a paucity of parasitedata for the host taxa. As with the dige-neans, this may result from uneven sam-pling of crocodilians by parasitologists orto parasite extinctions, and is probably theresult of both.

The total database

We will compare the digenean andnematode fauna of crocodilians in threeways. First, the fit of the total helminthfauna to the host "phylogeny" based onbiogeographic relationships (Fig. 12) is59%. Approximately half of the ambiguityresults from putative extinctions (reversals).Second, we have constructed a consensustree (Fig. 13) depicting portions of the dige-nean-based host cladogram and the nema-tode-based host cladogram that agree witheach other. Twelve of the 19 species ofcrocodilians that have had parasitesreported from them have had both dige-neans and nematodes reported. Finally, wehave produced a host cladogram based onthe combined digenean-nematode data-base (Fig. 14). This cladogram has a con-

sistency index of 68%, and most of the rea-son for the better fit of the data to Figure14 than to Figure 12 is due to the place-ment of Crocodyluspalustris. Otherwise, thedigenean data, the nematode data, the bio-geographic relationships, and the com-bined data set all give consistent results.

CONCLUSIONS

Uneven sampling of crocodilians for hel-minth parasites, coupled with probableparasite extinctions associated with croc-odilian extinctions, leads to ambiguity in

FIG. 13. Consensus tree depicting relationshipsamong 12 species of crocodilians based on host rela-tionships supported by both digenean and ascaridoidnematode phylogenies. Terminal taxa as in Figures8-12.

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FIG. 14. Host cladograms for 19 species of crocodilians based on phylogenetic relationships of their digeneanand ascaridoid nematode parasites. Additive binary codes (from Figs. 3-6) indicating parasite support for thebranches of the host cladogram (digenean codes first, then nematode codes, separated by a slash): 1 (Gavialis)= 27-28, 36/0; 2 (Crocodylus palustris) = 0/0; 3 (Alligator) = 13, 16-18, 21, 31, 41, 47-48, 67, 70, 73, 83-84, 86-87/2, 7, 14, 28, 30, 35; 4 (Melanosuchus) = 14-15, 23/5, 9, 12-13, 22, 29, 37; 5 (Paleosuchus) = lossof 35; 6 {Caiman latirostris) = 15, 22/loss of 16, loss of 38; 7 (C. crocodilus crocodilus) = 4, 20, 54, 58, 62,65/9, 13, 17, 22, 32; 8 (C. c.fuscus) = 37, 40, 66, 71, 88; 9 (Crocodylus moreletii) = 5, 25, 27/0; 10 (C. acutus)= 0/loss of 45; 11 (C. rhombifer) = 0/7, 30; 12 (C. intermedius) = 0/9, loss of 40, loss of 42, loss of 44, loss of46, loss of 47, loss of 48; 13 (C. siamensis) = 7, 8/0; 14 (Osteolaemus) = 12, 51, 53/0; 15 (Osteolaemus) = 51,loss of 85, loss of 86/0; 16 (Crocodylus cataphractus) = 42, 46-47, loss of 53, loss of 85, loss of 86; 17 (C.niloticus) = 38-40, 50, 59, 61, 74-76, 83-84/0; 18 (C. novaeguineae) = 0/loss of 31, loss of 43, loss of 45; 19(C. johnstoni) = 7, 80/6, loss of 22; 20 (C. porosus) = 9-10, 43, 45-47, 56-58, 60-61, 63-64, 69-72,77-79/1, 28; 21 = 0/6; 22 = 1, 27, loss of 29, loss of 33, loss of 34/0; 23 = 2-3, 15, 19, 22-24, 32, 49,52-53, 72, 90-92/0; 24 = loss of 28/15; 25 = 0/loss of 40, loss of 42, loss of 44, loss of 46, loss of 47, lossof 48; 26 = 28-29, 33-35/16, 33, 38-39, 41; 27 = 68, 70-72, 88-89, 91-94, loss of 28, loss of 36/26, 36;28 = 0/loss of 43; 29 = 55, 57-58/6, 8, 10, 25, 30; 30 = 12, 53/0; 31 = 81-82/4, 11, 29, 37; 32 = 0/22,27, 36, 38; 33 = 85-86/0; 34 = 0/31; 35 = 28, 36/38, 40, 42-49; 36 = 0/50-52.

assessing the degree of phylogenetic asso-ciation between crocodilians and their hel-minths. The weight of evidence for thehelminth data (Fig. 14) does support anumber of conclusions consistent with cur-rent estimates of crocodilian phytogeny.First, Gavialis is placed as the sister-groupof the alligatorids and crocodylids. Second,the alligatorids are supported as a mono-phyletic group, and within that group, Alli-gator is the sister-group of the caimans, Cai-man is the sister-group of Melanosuchus andPaleosuchus, and Caiman latirostris is the sis-ter-species of the two sub-species of C. croc-odilus. However, the monophyly of the cai-man clade is supported only by a suite ofputative extinctions in the nematode fauna.

Third, an ancient origin of crocodilians issupported by the biogeographic relation-ships of their helminths; in particular, Croc-odylus species indicate relationships consis-tent with patterns of continental drift. Inthe past, it seems that there has been anopinion that if crocodilians were ecologi-cally similar enough to share parasites, theymust be relatively young or not related atall. This study suggests that crocodiliansare both old and ecologically conservative.In addition to being numerical relicts (sensuSimpson, 1944), they are also phylogeneticrelicts (sensu Simpson, 1944; see Brooks andBandoni, 1988).

The monophyly of Crocodylus is not com-pletely supported by the parasite data.

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Crocodylus palustris is placed as the sister-group of Gavialis, and Osteolaemus is placedeither as the sister-group of the AfricanCrocodylus or as the sister-group of the Afri-can plus Australian/Oceanian Crocodylus(Fig. 14). Relationships among Crocodylusspecies are ambiguous in proportion to thenumber of helminths reported from them.The relationships indicated by the consen-sus tree are consistent with most estimatesof crocodilian phylogeny.

The most extensive attempt to elucidatecrocodilian phylogeny has been the workof Densmore (Densmore, 1983; Densmoreand Dessauer, 1984). Our study supportsmany of Densmore's findings, but not all.In particular, our study suggests an ancientorigin for Crocodylus that finds biogeo-graphic and coevolutionary data in conflictwith the molecular clock hypothesis. It isdifficult to compare our study with Dens-more's work. We understand the problemswith the parasite database, and haveattempted to point out sources of ambi-guity. Densmore's work differs from oursin two major analytical approaches. First,we use character variables for tree con-struction, while he uses genetic distances.Second, we use a parsimony algorithm,while he uses phenetic algorithms for con-structing trees from the data. Hence, thereis little common ground beyond the finalproduct for comparisons and discussion.We are pleased that our findings agree withhis for so many points, but we are unsurewhat to make of the discrepancies betweenour sets of findings. Clearly, more work inall areas is called for.

ACKNOWLEDGMENTS

Funds for this study were made availablethrough operating grant A7696 from theNatural Sciences and Engineering Councilof Canada to D.R.B., and a Smithsonianpost-doctoral fellowship to R.O.G. Weexpress special thanks to Dr. David Blairfor permission to use unpublished recordsof helminths in Australian crocodiles. Ms.Cheryl Macdonald prepared the illustra-tions.

REFERENCES

Brooks, D. R. 1979. Testing hypotheses of evolu-tionary relationships among parasites: The dige-neans of crocodilians. Amer. Zool. 19:1225-1238.

Brooks, D. R. 1980. Revision of the Acanthostomi-nae Poche, 1926 (Digenea: Cryptogonimidae).Zool. J. Linn. Soc. 70:313-382.

Brooks, D. R. 1981. Hennig's parasitological method:A proposed solution. Syst. Zool. 30:229-249.

Brooks, D. R. 1988. Macroevolutionary comparisonsof host and parasite phylogenies. Ann. Rev. Ecol.Syst. 19:235-259.

Brooks, D. R. 1989. Coevolution of vertebrates andtheir helminth parasites. /nR.C. Ko (ed.), Currentproblems in parasitology. Univ. Hong Kong Press,Hong Kong. (In press)

Brooks, D. R. and S. M. Bandoni. 1988. Coevolutionand relicts. Syst. Zool. 37:19-33.

Brooks, D. R., R. T. O'Grady, and D. R. Glen. 1985.Phylogenetic analysis of the Digenea (Platyhel-minthes: Cercomeria), with comments on theiradaptive radiation. Can. J. Zool. 63:411-443.

Brooks, D. R., R. T. O'Grady, and E. O. Wiley. 1986.A measure of the information content of phy-logenetic trees and its use as an optimality cri-terion. Syst. Zool. 35:571-581.

Densmore, L. D. 1983. Biochemical and immuno-logical systematics of the Order Crocodilia. In M.K. Hecht, B. Wallace, and G. H. Prance (eds.),Evolutionary biology Vol. 16, pp. 397-465. PlenumPress, New York.

Densmore, L. D. and H. C. Dessauer. 1984. Lowlevels of protein divergence detected betweenGavialis and Tomistoma: Evidence for crocodilianmonophyly? Comp. Biochem. Physiol. 77B:715-720.

Simpson, G. G. 1944. Tempo and mode in evolution.Columbia Univ. Press, New York.

Sprent, J. F. A. 1977. Ascaridoid nematodes ofamphibians and reptiles: Dujardinascaris. J. Hel-minthol. 51:251-285.

Sprent, J. F. A. 1978a. Ascaridoid nematodes ofamphibians and reptiles: Goezia. J. Helminthol.52:91-98.

Sprent, J. F. A. 1978i. Ascaridoid nematodes ofamphibians and reptiles: Gedoelstascaris n.g. andOrtleppascaris n.g. J. Helminthol. 52:261-282.

Sprent, J. F. A. 1979a. Ascaridoid nematodes ofamphibians and reptiles: Multicaecum and Brevi-multicaecum. J. Helminthol. 53:91-116.

Sprent, J. F. A. 1979i. Ascaridoid nematodes ofamphibians and reptiles: Terranova. J. Helmin-thol. 53:265-282.

Sprent, J. F. A. 1980. Ascaridoid nematodes of Sire-nians—the Heterocheilinae redefined. J. Hel-minthol. 54:309-327.

Wiley, E. O. 1981. Phylogenetics, the theory and methodof phylogenetic systematics. Wiley-Intersci., NewYork.

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crocodilians and their helminth parasites: macroevolutionary considerations

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