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Faculty Publications from the Harold W. Manter Laboratory of Parasitology, Harold W. Manter Laboratory of

12-1985

Phylogenetics and the Future of Helminth

Daniel R. Brooks University of Toronto, [email protected]

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Brooks, Daniel R., " and the Future of Helminth Systematics" (1985). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 208. https://digitalcommons.unl.edu/parasitologyfacpubs/208

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. Parasit., 71(6), 1985, pp. 719-727 ? American Society of Parasitologists 1985

INVITEDREVIEW PHYLOGENETICSAND THE FUTUREOF HELMINTHSYSTEMATICS

Daniel R. Brooks Department of , Universityof BritishColumbia, Vancouver, BritishColumbia, Canada V6T 2A9

ABSTRACT: Phylogeneticsystematics is a relativelynew formaltechnique that increasesthe precisionwith which one can make direct estimates of the history of phylogeneticdescent. These estimates are made in the form of phylogenetictrees, or .Cladograms may be converted directly into classificationsor they may be used to test various hypothesesabout the evolutionaryprocess. More than 20 phylogeneticanalyses of helminth groupshave been publishedalready, and these have been used to investigateevolutionary questions in devel- opmentalbiology, ,, , and evolutionaryecology.

WHAT IS PHYLOGENETICS? terion for classifying and (2) genealogical rela- tionships, like classifications, are inherently In 1965 and 1966, English-speaking hierarchical. were introduced to something called phyloge- The second major point which Hennig (1950) netic systematics (Hennig, 1965, 1966). The argued had to do with developing a formal gen- author of this approach, the late German ento- eral method for discovering phylogenetic rela- mologist Willi Hennig, was interested in for- tionships. Hennig objected to phylogenetic mulating what he called a "general reference sys- schemes which were based on hypothetical ideal- tem" for comparative . In an earlier work ized "archetype" ancestors. He asserted that all in German, Hennig (1950) had argued two major are composites of ancestral and derived points. First, he had distinguished between spe- traits; therefore, there are no such things as ar- cial reference systems and general reference sys- chetypes that, by definition, are all-primitive. This tems in biological classifications. Special refer- assertion led directly to Hennig's proposed meth- ence systems were those constructed to emphasize odology. If the traits exhibited by any species are a particular kind of relationship among different a combination of primitive and derived features, species. For example, a classification that placed then the traits shared by two or more species will all the parasitic helminths inhabiting be indicators of phylogenetic relationship. Shared in one category, those inhabiting in another, primitive traits indicate general phylogenetic re- and so forth, would be a special reference system lationships while shared derived traits indicate useful for categorizing helminth faunas in var- more particular phylogenetic relationships. Two ious host groups. It is doubtful that such a clas- species that share a derived trait unique to them sification would be good for much else, since it are each other's closest relatives. would place various platyhelminths, nematodes For example, adult strigeid digeneans have and acanthocephalans together in the same - parenchyma-filled bodies; this is a general trait egories. A general reference system, on the other of platyhelminths and indicates in a general sense hand, would be one that would provide the most that strigeids are related to other platyhelminths. efficient summary of the maximum amount of Strigeids also have miracidia, initial larval stages information about the species being classified. found in all digenean species. This indicates that Hennig reasoned that the logical choice for a gen- strigeids are related in general to all digeneans. eral reference system in biology would be one Finally, all strigeids have a structure on the ven- based on the genealogical, or phylogenetic, re- tral body surface called the tribocytic . This lationships of the species involved. The choice organ is found only in cyathocotylid, diplosto- of genealogy was based on two observations: (1) matid and strigeid digeneans. This trait tells us the one attribute of any or species that that strigeids are related in particular to cya- would always be constant was its history, so phy- thocotylids and diplostomatids; that is, those logenetic history should be the most stable cri- three groups are each other's closest relatives. Note also that, relative to platyhelminths as a Received 11 December 1984; revised 2 May 1985; group, the fact that strigeids have miracidia is a accepted6 May 1985. special trait, but relative to just digeneans, it is

719 720 THEJOURNAL OF PARASITOLOGY, VOL. 71, NO.6, DECEMBER1985

B C D E , often called a (see Fig. 1). The two most critical parts of the method are the determination of plesiomorphic and apo- morphic traits and the resolution of conflicting data. tribocytiic org an Hennig (1966) listed a number of different ways one could determine whether a trait was plesio- miracidi a morphic or apomorphic for a given group oftaxa. There have been many recent discussions of these ;parenchyma - il led body ideas, and phylogeneticists seem to have found only two approaches to be consistently sound (see FIGURE 1. Cladogram of five diffferent platyhel minth taxa, including a "turbellariain" group (A), a Stevens, 1980 for a review). These are the "out- generalizeddigenean group (B), and t:hree strigeiform group criterion" and the "ontogenetic criterion." groups(CDE). Labels next to slash mairks on branches The criterion states that any trait found name shared traits indicating phyloggenetic relation- in at least one member of the group being studied ships. that also occurs in taxa outside the study group is plesiomorphic. Thus, a parenchyma-filled body is plesiomorphic for digeneans because there are a general trait. Explanation of a ttrait as general non-digeneans which also have parenchyma-filled (primitive) or particular (derived) thus depends bodies. Since outgroups evolve themselves, it is on the perspective of the particular study. Hennig often necessary to use more than one outgroup considered such relative assessme nts to be more to establish enough apomorphic traits to fully consistent with evolutionary consi iderations than classify a group. The ontogenetic criterion states absolute assessments. Although nniracidia are a that, given two with different adult general trait of all digenean specie:s today, in the traits, if one organism exhibits the other's adult distant past they were a unique tirait of a single trait during development, in addition to its own, ancestral species. The evolutionar y process itself its adult trait is apomorphic and the other's adult is responsible for the relative na ture of assess- trait is plesiomorphic. This approach is more ments of primitive and derived tiraits. In an at- limited than the outgroup criterion, since it works tempt to avoid what he felt were aimbiguous and only for cases in which has proceeded absolutist connotations of those terms, Hennig by adding characteristics to the ancestral devel- coined two new terms, plesiomo rphy (plesio- opmental program (this includes but is not re- near the source) and apomorphy (aipo- away from stricted to recapitulation). Substitutions in de- the source) to refer to relatively primitive and velopmental programs cannot be resolved by the relatively derived traits, respectivel[y. Shared traits ontogenetic criterion because they are ambigu- thus became symplesiomorphies and synapo- ous, and secondary deletion of steps from de- morphies. The diagnostic features of each group- velopmental programs will be misinterpreted as ing in the genealogical hierarchy vxould be those primitive absence of steps (Brooks and Wiley, traits viewed as apomorphic at thie level of that 1985). particular grouping. A parenchyima-filled body After determining which traits are apomorphic would be diagnostic of platyhelnninths relative and which are plesiomorphic, one is sometimes to other metazoans but would no t be diagnostic faced with apomorphic traits which suggest con- of digeneans, even though all dLigeneans have flicting groupings. We know the reason for such parenchyma-filled bodies. This is because other conflicts; it is the phenomenon of parallel or con- platyhelminths have parenchym a-filled bodies vergent evolution, given the general name ho- as well. In evolutionary terms, thie apomorphic moplasy, in contrast with . Homolo- traits characterizing each grouping are those traits gous traits of any taxa all co-vary with the that first evolved in the common ancestor of the phylogenetic relationships of the taxa; homopla- group. sious traits do not. So long as homoplasious traits In its simplest form, Hennig's n iethod consists do not co-vary in larger numbers than the ho- of determining plesiomorphic anid apomorphic mologous traits, phylogenetic systematic tech- traits for the various taxa one inte nds to classify. niques will pinpoint the proper phylogenetic re- The taxa are then grouped togeth4er according to lationships. The possible occurrence of great the apomorphic traits they share. The result is a amounts of convergent or re- BROOKS-PHYLOGENETICSAND HELMINTHSYSTEMATICS 721 quires only that many traits be used in the anal- Classification ysis. An assumption is made that the pattern of Phylogeneticists are faced with two problems relationships indicated by a plurality of the traits in presenting their results as classifications. First, examined is the best estimate of phylogenetic they wish to make certain that classifications ac- relationships. For example, if one looks at only curately reflect our current state of knowledge a few traits of the cestodarian platyhelminths about phylogenetic descent. Second, they wish (gyrocotylideans, amphilinideans and euces- to disrupt existing classifications as little as pos- todes) one might consider the lack of an intestinal sible. Rather than recount the lively history of tract to indicate relationships with other gutless debates about the perceived dangers of phylo- groups, such as acoels, rather than with genetic classification, much of which took place trematodes and rhabdocoels. When 39 different in the pages of Systematic Zoology, I will discuss characters are considered together (Brooks et al., the reconciliation promoted most articulately by 1985a), however, the lack of a gut in these para- Wiley (198 la). Consider the phylogenetic tree in sitic groups is unambiguously delimited as a con- Figure 2. Phylogeneticists would allow any clas- vergent trait. Since this requires that large num- sification from which the tree could be directly bers of traits be analyzed together, an increasing reconstructed. The most explicit classification number of phylogeneticists have found it helpful would be: to use computer-assisted algorithms to search for the plurality pattern. The most effective algo- ABCDE rithms are the so-called "parsimony methods" TAXON A (e.g., Farris, 1970; Farris et al., 1970a, 1970b) TAXON BCDE which search for the plurality pattern by mini- TAXON B mizing the postulated number of . TAXON CDE For additional technical information, see Brooks TAXON C et al. (1984), Wiley (198 la), Nelson ana Platnick TAXON DE (1981), Eldredge and Cracraft (1980), and var- TAXON D ious articles in Systematic Zoology. TAXON E There is a mistaken impression among some However, if A-E are genera, taxon DE and taxon systematists that phylogenetics is done in the re- C might be subfamilies, taxon CDE and taxon B verse manner to what I have described. That is, families, taxon BCDE and taxon A superfami- one decides what the groups are, then decides lies, and taxon ABCDE a sub-. This could what their phylogenetic relationships are, and proliferate higher taxonomic categories to such finally interprets various characteristics, post hoc, an extent that the classification would be too in such a way as to support the phylogeny. It is unwieldy to use. Wiley (198 la) proposed a "se- the contention ofphylogeneticists, among others, quencing" convention that states that any taxon that no empirical criteria exist for "knowing" a in a classification is the sister-group (closest rel- phylogeny in this manner, and inevitably all such ative) of the taxa of equivalent rank following it. discussions rest on appeals to authority rather For example, if A-E have traditionally been than to evidence. When such recourse to au- placed in one subfamily, the sequenced classifi- thority involves one's mentor(s), it is sometimes cation could be: jokingly termed the "academic outgroup crite- subfamily ABCDE rion." Phylogenetic systematics is not used to A justify arbitrary decisions about evolutionary re- genus B lationships but as a means of evaluating char- genus C acters and arriving at decisions about groups and genus D their relationships based on the weight of evi- E dence. genus In order to reconstruct the phylogenetic tree, those WHATCAN WE DO WITHPHYLOGENETICS? five genera would have to be listed in the order Beckner (1959) stated that systematics has two shown. Genus A is the sister-group of BCDE; B functions, classification (information storage and is the sister-group of CDE; and C is the sister- retrieval) and implementation of biological the- group of DE. ory. Phylogenetics has made significant contri- Phylogenetic systematic classifications have butions in both areas. been provided for the following groups of para- 722 THEJOURNAL OF PARASITOLOGY,VOL. 71, NO. 6, DECEMBER1985

A C D reflect that. On the other hand, there is no way to reconstruct the phylogenetic tree (Fig. 2) from such a classification. Wiley (1981 b) has shown that no classification that includes grade groups can be consistent with the phylogeny of the group. In addition, such classifications overestimate the amount of convergent and parallel evolution that has occurred. The apomorphic traits common to C and to DE in Figure 2 would have to be due to if the taxa are placed in different in the classification. One of FIGURE2. Cladogram for five hypothetical taxa A-E. categories the maxims of parasitology is that parasites are paradigms of adaptive plasticity; hence, one sitic helminths: plagiorchiform digeneans of the would expect to find high levels of convergence genus Glypthelmins (Brooks, 1977), the genera and parallelism. This notion appears to be an of proteocephalidean cestodes (Brooks, 1978; artifact of "gradistic" classifications. A recent Brooks and Rasmussen, 1985), liolopid dige- phylogenetic analysis of digenean families (Brooks neans (Brooks and Overstreet, 1978), acanthos- et al., 1985b) showed that less than 25% of the tomine digeneans (Brooks, 1981a; Brooks and 213 characters used showed any evidence of con- Caira, 1982), some nematodes of the genus Oes- vergence or parallelism. Hence, phylogeneticists ophagostomum (Glen and Brooks, 1985), the say, no matter how useful grades might be in major groups of parasitic platyhelminths (Brooks, pinpointing ecological similarities among taxa, 1982; Brooks et al., 1985a), the families of di- they provide misleading implications about pat- geneans (Brooks et al., 1985b), elaphostrongyline of phylogenetic descent. It is not enough, nematodes (Platt, 1984), nematodes of the genus therefore, to group taxa according to "similari- Nematodirella (Lichtenfels and Pilitt, 1983), plant ty." One must know whether the similarity is cyst nematodes of the Heteroderidae (Fer- due to a shared plesiomorphic trait (ABC) or a ris, 1979), and nematodes of the family Lepton- shared apomorphic trait (DE). chidae (Ferris et al., 1981). The restriction that classifications must be Documenting evolutionary patterns consistent with the phylogenetic trees from which they are derived is a controversial aspect of phy- Phylogenetic trees produced by phylogenetic logenetic systematics. Consider Figure 2 again. analysis are explicit direct estimates of historical Let us suppose that taxa D and E are helminths patterns. As such, they can be used to provide with indirect (multi-host) cycles, complex de- an additional source of evidence for investiga- velopmental programs with discrete larval stages, tions of various evolutionary phenomenon. It is and have numerous unique morphological traits. assumed that every hypothesis about evolution- Let us further suppose that taxa A, B and C have ary mechanisms (processes) implies predictions simple (one-host) life cycles, direct development, about the expected outcome (patterns) of phy- and few unique traits. One might be tempted to logenetic descent affected by those mechanisms. classify ABCDE in the following way: Thus, phylogenetic trees can be used a priori to restrict the realm of explanations about processes TAXON ABCDE involved in evolution, or can be used a posteriori TAXON ABC to test the expected outcome of hypothesized TAXON A evolutionary processes. Applications of phylo- TAXON B to evolutionaary biology have involved TAXON C studies in (1) , (2) specia- TAXON DE tion and biogeography, (3) coevolution, and (4) TAXON D community . TAXON E One could easily justify such a classification by Developmental biology asserting that ABC and DE occupy different adaptive zones, or evolutionary "grades," and There is currently much interest in the rela- that a truly evolutionary classification ought to tionship between development and evolution. A BROOKS-PHYLOGENETICSAND HELMINTHSYSTEMATICS 723 fair amount of this interest involves a renewed development (recapitulation) larval and adult appreciation for the work of Richard Gold- traits will show the same phylogenetic relation- schmidt (1940), an outstanding helminthologist ships. But, what if particular stages arose as adap- and evolutionary ; for example, Steven tive responses to selection pressures? Then, as J. Gould of Harvard University wrote an essay deBeer (1959) pointed out, larvae and adults will of appreciation for Goldschmidt in the recent show different relationships. Digenean system- (1982) re-issue of The Material Basis of Evolu- atics has lived with such a dilemma for over 50 tion. One major topic concerns the phenomenon years. Should the classification of digeneans be of , or differential rates of devel- based on larval (especially cercarial) or adult opment. Fink (1982) devised a rigorous formal- characters? There have been two schools of ism using phylogenetics for detecting various thought opposed to each other. Each one thought forms of heterochrony in the of any that either larvae or adults were the adaptive group of species. Helminthology appears to be a stage and thus inappropriate for classification. A treasure-trove of potential studies in this area. phylogenetic analysis of digeneans (Brooks et al., For example, we know of no digenean life cycles 1985b) suggested that the larval stages were not which include both rediae and daughter sporo- recapitulations; thus, they should be the adap- cysts. Phylogenetic analysis suggests that rediae tive stage. And yet, data for larvae and data for are plesiomorphic. Are daughter sporocysts adults supported the same classification when unique larval stages favored by analyzed phylogenetically. Apparently, there are over rediae to such an extent that we never find some inherent developmental constraints on them together, or are rediae and daughter spo- "adaptive response." rocysts linked developmentally? Brooks et al. Finally, phylogenetic analysis can help us rec- (1985b) suggested that if the development of the ognize cases in which the same name has been pharynx and gut were retarded (paedomorphosis) applied to life cycle patterns which evolved in in species having rediae, the resulting rediae different ways. For example, phylogenetic anal- would be sacs of germinal cells with a birth pore ysis of the higher groups of parasitic platyhel- and no other structure-the definition of a minths (Brooks et al., 1985a; O'Grady, 1985) daughter sporocyst! Whether this is due to re- indicated that digenean life cycles evolved by the tarded rate of development (neoteny) or retarded addition of (1) a host and of (2) new initiation of development (pre-displacement) in larval features characterizing development in the each particular case is not known. But this find- primitive molluscan host. Cestode life cycles, on ing from a phylogenetic analysis leads us to look the other hand, evolved by the addition of (1) for an explanation in developmental biology an invertebrate host and of (2) new adult features rather than in ecology or population biology. A characterizing development in the primitive ver- third form of paedomorphosis occurs when the tebrate host. Thus, the "complex life cycles" of duration of development is retarded (progene- digeneans and of cestodes evolved in almost ex- sis). For example, during the of most actly opposite manners. The one thing common plagiorchiform digeneans, the coils of the uterus to both cases is that the most conservative part become more extensive and expand from being of the developmental program is found in the only intercecal to having extracecal portions as acquired host type and the innovative part of the well. The presence of extracecal loops in the adult developmental program is found in the primitive is a plesiomorphic trait. And yet, members of host type. Those of us who were trained to think two sub-genera of Glypthelmins are character- in terms of host colonizations leading to mor- ized by having only intercecal loops as adults. phological change in parasite evolution find such Clearly, the uterine development does not pro- discoveries interesting. ceed as far in those species. The mechanistic ex- Although we helminthologists often lament the planation for such occurrence is more likely to paucity of life cycle studies done in our groups, be found in developmental biology than in any I suspect that more is known about the ontoge- discussions of the selective value of the relative netic pathways of helminths than of many other fecundity of species with "big" and "little" uteri. groups of organisms. That is the reason we can A second area of investigation involves the so easily find interesting questions when using expected relationship between larval and adult the results of phylogenetic analysis to make pre- traits in evolution. It is clear that whenever evo- dictions about undiscovered aspects of evolution lution proceeds by adding traits at the end of and development. 724 THEJOURNAL OF PARASITOLOGY,VOL. 71, NO 6, DECEMBER1985

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FIGURE3. Phylogenetics and biogeography. 3a. Cladogramof species of cestode genus Acanthoboth- rium occurring in freshwater stingrays (redrawn from Brooks et al., 1981). 3b. Cladogram of species of ces- tode genus Rhinebothroides, all occurring in freshwater stingrays (redrawn and corrected from Brooks et al., FIGURE 4. Phylogenetics and coevolution. 4a. 1981). 3c. Map of South America showing geographic Mapping of host (solid lines and letters) and parasite distribution patterns for taxa in 3a and 3b. 3d. Clado- (dotted lines and letters) cladograms. 4b. Genera of the gram showing historical relationships among various digenean family Liolopidae (dotted lines) and their ver- South American river systems. tebrate hosts (solid lines). 4c. Species of cestode genus Proteocephalusoccurring in NorthAmerican salaman- ders (dotted lines) and their hosts (solid and of Biogeography patterns speciation lines). Numbers refer to the following species of Pro- If one places a phylogenetic tree for a group teocephalus:(1) sireni, (2) aberrans,(3) alternans,(4) of species on a map of the areas in which the amphiumae, (5) amphiumicola, (6) loennbergii,(7), cryptobranchi,and (8) filaroides. various species occur, there is often a very marked concordance between the biological history of the species and the geological history of the areas 1977, 1978, 1979, 1981a; Brooks and Overstreet, (see Fig. 3). Documenting the extent of this his- 1978; Brooks et al., 1981). Parasitic helminths torical relationship between areas and species is with complex life cycles are especially good sub- the province of a relatively new approach to bio- jects for such studies because their historical pat- geography called vicariance biogeography (see terns are at least partly a manifestation of the Croizat et al., 1974; Nelson and Platnick, 1981; histories of their various host groups. Vicariant Cracraft, 1983). Phylogenetic analyses of hel- patterns shown by parasites thus symbolize vi- minth groups form a significant proportion of cariant patterns for a variety of different organ- the documented cases of such vicariance (Brooks, isms. BROOKS-PHYLOGENETICSAND HELMINTHSYSTEMATICS 725

Wiley (1981a) presented a formal methodol- (Brooks, 198 lb: crocodilians and digeneans; Glen ogy designed to use a combination of phyloge- and Brooks, in press: Great Apes and helminths), netics and biogeography to test speciation models. the parasite data produced a host-group phylo- Thus far, no helminthologist has used this pro- genetic tree consistent with those produced using tocol in analyzing speciation patterns. characteristics of the hosts themselves. In the third case (Brooks, 1981 b: freshwater stingrays Coevolution and helminths), the only existing phylogenetic Ehrlich and Raven (1964) defined coevolution tree for the hosts is the one based on parasite as an ecological phenomenon, a matter of "step- data. A fourth study, using parasitic copepods wise reciprocal response" between any two species and their scombrid (mackerel) hosts (Cressey with "close and evident" ecological relation- et al., 1983) also found good agreement between ships. Parasitologists since von Ihering (1891) parasite data and the host phylogeny. have recognized another sense of coevolution; Communityecology that is, the historical relationship between hosts and parasites, which is often pronounced. And Parasite faunas represent excellent model sys- yet, this historical component is missing from tems for studying community ecology. When almost all assessments of putatively coevolved phylogenetic trees, biogeography and host rela- systems (Brooks, 1979; Mitter and Brooks, 1983; tionships are known for a variety of parasites Brooks and Mitter, 1984). Phylogenetics offers a inhabiting the same host group, an assessment method for documenting the degree to which of the historical aspects of community structure contemporaneous host-parasite relationships re- can be made. Of primary concern is the origin flect long-standing associations between the host of the various ecological life history traits which group and the parasite group. The method is characterize the interactions among the various analogous to that used in vicariance biogeogra- members of the community. If ecological traits phy (see Fig. 4). Studies in which this method- are treated like any other kind of trait, and are ology has been applied using groups of parasitic analyzed phylogenetically, one can determine helminths include frogs and their intestinal di- which ecological traits are present in a commu- geneans (Brooks, 1977), crocodilians and their nity because of contemporaneous interactions and digenean parasites (Brooks, 1979a), freshwater which are present because of ancestral condi- stingrays and their helminth parasites (Brooks et tions. For example, if two species of intestinal al., 1981), and Great Apes and their helminths helminth inhabit different parts of the gut, is the (Glen and Brooks, in press). Other phylogenetic separation due to competitive exclusion on the analyses of helminths which have examined co- part of the contemporaneous species, or is it due evolution at some level include Brooks (1978, to differences in site preference on the part of 1981a), Brooks and Caira (1982), Brooks and their ancestors? This approach to explaining the Glen (1982), Brooks and Overstreet (1978), evolution of ecological life history traits has been Brooks and Rasmussen (1985), Deardorff et al. explored by Brooks (1980) and, combined with (1981), Lichtenfels and Pilitt (1983), and Platt biogeography and coevolution, expanded into a (1984). Platt (1984) was the first to look closely research program called historical ecology at the possible coevolution of members of a hel- (Brooks, 1985). minth group and their intermediate hosts. The degree of historical relationship in many of these PHYLOGENETICSAND THE FUTURE OF HELMINTHSYSTEMATICS studies has been found to be quite high. Any parasites that have an historical relation- In most branches of biology, systematics de- ship with their hosts act like homologous traits veloped wholly from a tradition of natural his- of their hosts; that is, they co-vary with their tory and comparative . Parasitolog- host phylogeny. From this notion, Brooks (1981 b) ical systematics has developed with a very developed a formal method for using parasite pronounced influence from medical and veteri- data to assess host phylogeny independently of nary diagnostics, which stresses unique traits and any assumptions about degree of coevolution and separation of taxa rather than relationships among without needing a host phylogeny. This has al- taxa. Given parasite diversity, this approach has lowed helminth parasite data to be used as an been quite effective and highly productive. Now independent source of evidence about host phy- that our knowledge of parasite diversity is ex- logeny in three studies. In two of those studies tensive, though far from exhaustive, we are in a 726 THEJOURNAL OF PARASITOLOGY,VOL. 71, NO. 6, DECEMBER1985 position to study many questions about rela- vided me with a small yearly operating grant to tionships. Phylogenetics offers an analytical tech- partially defray some research costs. nique that will aid such studies greatly. LITERATURECITED One of the most active areas of biological re- BECKNER, M. 1959. The of thought. search is A more biological way today . Columbia University Press, New York. unified view of evolution is emerging, one that BROOKS,D. R. 1977. Evolutionary history of some encompasses previous achievements in popula- plagiorchioid trematodes of anurans. Systematic tion genetics and population ecology and com- Zoology 26: 277-289. 1978. status of bines them with developmental biology and phy- Systematic proteocephalid cestodes from and in North logenetic systematics. This broader explanatory America with descriptions of three new species. framework will provide a common ground for Proceedings of the Helminthological Society of molecular biologists, organismic biologists and Washington 45: 1-28. ecologists (see Brooks, 1984, for a brief review; 1978. Evolutionary history of the cestode order Proteocephalidea. Systematic Zoology 27: see Campbell, 1982, for a readable summary; see 312-323. Brooks and Wiley, 1986, for a proposed unified 1979a. Testing hypotheses of evolutionary theory of evolution). Systematic helminthology relationships among parasitic helminths: The di- (indeed systematic parasitology), by virtue of its geneans of crocodilians. American Zoologist 19: 1225-1238. tradition of broad training incorporating tax- . 1979b. Testing the context and extent of host- onomy, ecology and life cycle studies, finds itself parasite coevolution. Systematic Zoology 28: 299- in an unparalleled position in the sociology of 307. biology. Our very training programs are tailor- . 1980. and non-inter- made to produce biologists with a broad enough active parasite community structure. Systematic 29: 192-203. roles in the new Zoology background to assume leadership . 1981 a. Revision of the Acanthostominae evolutionary biology. Many systematic botanists (Digenea: Cryptogonimidae). Zoological Journal and systematic entomologists are also broadly of the Linnaean Society 70: 313-382. trained. It is therefore distressing to realize that 198 lb. Hennig's parasitological method: A solution. 30: 229- the number of such traditional pro- proposed Systematic Zoology graduate 249. grams in parasitology has declined precipitously 1982. Higher level classification of parasitic in the past decade. In addition, only a handful platyhelminths and fundamentals of cestode clas- of those remaining active include these new ad- sification. In Parasites-Their world and ours, D. vances, such as phylogenetics, in their programs. F. Mettrick and S. S. Desser (eds.). Elsevier Biomedical, Amsterdam, pp. 189-193. for to It would indeed be a shame parasitology 1984. What's going on in evolution?: A brief be under-represented in these exciting times. guide to some new ideas in evolutionary theory. Canadian Journal of Zoology 61: 2637-2645. 1985. Historical ecology: A new approach to ACKNOWLEDGMENTS ? study in the evolution of ecological associations. I would like to extend my appreciation to Dr. Annals of the Missouri Botanical Garden 72: 660- D. F. Mettrick, editor, and to the members of 680. , AND J. N. CAIRA. 1982. Atrophecaecumlob- the editorial and consulting board for inviting acetabulare sp. n. (Digenea: Cryptogonimidae: me to contribute this article. My thanks also to Acanthostominae) with discussion of the generic those many parasitologists who have kindly suf- statusof ParacanthostomumFischthal and Kuntz, fered my professional growing pains over the past 1965 and AteuchocephalaCoil and Kuntz, 1960. of debts of to Proceedings of the Biological Society Washing- 12 years. I owe particular gratitude ton 95: 223-231. Janine N. Caira, Ronald A. Campbell, Murray , , T. R. PLATT,AND M. H. PRITCHARD. D. Dailey, Donald W. Duszynski, Gerald W. 1984. Principles and methods of cladistic anal- Esch, William F. Font, John C. Holmes, John ysis. A workbook. Special Publication No. 12, of the Museum of Natural University of Janovy, Jr., J. Ralph Lichtenfels, John S. Mac- History, Kansas, Lawrence, Kansas. 92 p. Ro- kiewicz, Monte A. Mayes, Brent B. Nichol, , AND D. R. GLEN. 1982. Pinworms and pri- bin M. Overstreet, Thomas R. Platt, Mary H. mates: A case study in coevolution. Proceedings Pritchard, Robert L. Rausch, Gerald D. Schmidt, of the Helminthological Society of Washington 49: and Horace W. Stunkard. My thanks also to the 76-85. M. A. MAYES,AND T. B. THORSON. 1981. Sciences and Council , Natural Engineering Systematic review of cestodes infecting freshwater (NSERC) Population Biology Committee which, stingrays (Chondrichthyes: Potamotrygonidae) in- in these times of financial hardships, has pro- cluding four new species from Venezuela. Pro- BROOKS-PHYLOGENETICSAND HELMINTHSYSTEMATICS 727

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