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Macroevolutionary patterns of morphological diversification among parasitic fl atworms (platyhelminthes: Cercomeria)

Abstract. - Patterns of parasite morphological diversification were investigated using a morphological data base for the parasitic platyhelminths comprising 1,459 characters analyzed using phylogenetic systematic methods. Only 10.8% of the 1,882 character transformations are losses, casting doubt on views that parasites are secondarily simplified and exhibit degenerate evolution. Chi-squared analysis indicates that character loss in the Digenea and Monogenea occurs in proportion to total change and is disproportionately lower within the Eucestoda. In the Digenea fewerfemale characters and more male characters have been lost than expected by the total number of characters in that group, and more male and more nonreproductive characters have been lost in proportion to their distribution across groups. In the Monogenea fewer nonreproductive and more larval characters have been lost than expected within the group, and female character loss is high relative to other groups. In the Eucestoda fewer female and more larval characters have been lost than expected within the group, whereas loss of male and nonreproductive character is low, and loss of larval characters is high, compared to the other groups. Pattems of character loss result partially from characters that show repeated (homoplasious) loss in different groups. High consistency index and low homoplasy slope ratio values indicate that the parasitic platyheiminths show unusually low levels of homoplasy, casting doubt on views that parasite morphology is unusually adaptively plastic. Homoplasy within the monogeneans occurs in proportion to overall character change, is slightly higher than expected in the digeneans, and is much lower than expected within the eucestodes. Homoplasy occurs less often than expected in lar-val characters, and more often than expected in nonreproductive characters in the Digenea. Monogeneans show more homoplasy than expected for larval characters both within and among groups. Eucestodes show fewer homoplasious male and nonreproductive, and more homoplasious larval, characters than expected within the group, and higher homoplasy in larval characters and lower homoplasy in female and nonreproductive characters among groups.

Key words. - Adaptive plasticity, Cercomeria, Digenea, Eucestoda, evolutionary loss, macroevolution, Monogenea, morphological diversification, parasitic platyhelminths, phylogenetic system-

Parasites have not enjoyed a positive reputation among evolutionary biologists, and parasitologists have not participated extensively in evolutionary biology since the New Synthesis (Brooks and McLennan, 1993). This has led to an abundance of generalizations about parasite evolution that reinforce a persistent belief that parasite evolutionary biology is somehow different from the evolutionary biology of nonparasites. Consequently, parasites and parasitism are given either short shrift (Dodson and Dodson, 1985; Futuyma, 1986) or are not mentioned at all (Avers, 1989) in recent texts about evolutionary biology. One of the ways in which parasites are often thought to differ substantially from free-living organisms is in their pattems of morphological diversification. In particular, parasites are thought by many to exhibit unusually high degrees of reductive or degenerate evolution, signified by wholesale loss of characters, and to exhibit unusually high levels of homoplasy resulting from a combination of their adaptive plasticity, their evolutionary dependence on their hosts, and their convergent exposure to similar host environments.

These generalizations seem out of step with current evolutionary thinking in part because they emerged from theories of orthogenetic evolution in the early 20th century (Brooks and McLennan, 1993). The orthogenetic movement developed as a response to what many scientists saw as an overemphasis by Darwinians on the role of the environment in evolution. As an alternative to Darwinism, these researchers proposed that evolutionary change was internally, rather than externally or environmentally, driven. Among other things, this internal drive always led to progressive functional specializations, dependence on other species, a loss of evolutionary independence, and finally to self-imposed extinction (for an extended discussion in an historical context, see Bowler, 1983). Orthogeneticists coupled their hypothesis of evolutionary process with assumptions of particular patterns of morphological change throughout phylogeny, such as extensive reductive evolution and homoplasious change. Parasites, with their presumed evolutionarily degenerate nature, overspecialization, and dependence on their hosts, were thus considered key examples of orthogenesis. No longer masters of their own destiny, their evolutionary fate was sealed; they were totally dependent upon and molded by their hosts. The belief that parasites are secondarily simplified and degenerate in their morphology is problematical because parasites appear to have enjoyed a long history on this planet. By their persistence and numbers, they are an evolutionary success story (Price, 1980). This observation led some researchers to question the prevailing views of parasite evolution. For example, based upon his work with sensory structures, Rohde (see 1989 and references therein) has long championed the hypothesis that parasites are not secondarily simplified organisms. Searcy and MacInnis (1970) used evidence from differential rates of DNA renaturation to postulate that the genomes of some parasitic helminths were more complex than those of some free-living relatives. Kuris and Norton (1985) pointed out that overspecialization can be coupled with an increase in complexity. Despite these studies, the notion that parasites exhibit extensive morphological simplification, which is a form of degenerate evolution, is widespread even among recent authors (e.g., Dodson and Dodson, 1985). In free-living organisms, such as smelts and eels among teleostean fishes, caecilians among amphibians, and snakes among amniotes, secondary loss of characters and the resulting simplification in morphology is called evolutionary specialization, not degenerate evolution. Only for parasites has such evolutionary loss been termed degenerate (O'Grady, 1989). Thus, the notion that parasites exhibit degenerate evolution becomes tautological, stemming from a priori, and outmoded, assumptions about the evolutionary nature of parasites.

Orthogenesis aside, one of the major stumbling blocks to the study of parasite evolution has been the easily observable and striking difference in complexity between parasites and their (usually vertbrate) hosts. Such striking dissimilarity between two intimately associated species begs comparison (Price, 1980). While this comparison might provide information about patterns of increasing complexity through macroevolutionary time, it does not address the question of evolutionary simplification within parasites. To answer this, we need to investigate differences in character loss and in character innovation among related parasite groups and between parasites and their free living sister groups. At the moment, the phylogenetic data base for those free-living sister groups is not extensive enough to allow such comparisons. In addition, phylogeneticists have yet to undertake an analysis of free-living groups to determine what constitutes "usual" levels of evolutionary loss, beyond noting that some groups appear to exhibit more derived character loss than others (e.g., osmeroid fishes: Begle, 1991).

The picture is brighter on the parasitological side, where two decades of phylogenetic investigations have resulted in the development of a large morphological data base for the parasitic platyhelminths (superclass Cercomeria). Given the absence of a comparable data base for free-living organisms, the best we can do now is to examine the patterns of character loss and convergence within and among the major cercomerian clades. In so doing, we hope to highlight the possibilities for comparative studies with free-living groups and to indicate a number of interesting avenues for exploration within more mainstream aspects of evolutionary biology.

We investigated generalizations concerning evolutionary simplification and adaptive plasticity using a morphological (anatomical and ultrastructural) data base for the parasitic platyhelminths comprising 1,459 characters and 1,882 character transformations postulated by phylogenetic systematic analyses (Bandoni and Brooks, 1987a, 1987b; Beverly-Burton and Klassen, 1990; Boeger and Kritsky, 1988, 1989, 1993; Bray, 1986, 1987, 1988; Brooks, 1977, 1982, 1989a, 1989b, 1990, 1993a, 1993b; Brooks and Amato, 1992; Brooks et al., 1989; Brooks et al., 1992; Brooks and Deardorff, 1988; Brooks et al., 199 1; Brooks, and Holcman, 1993; Brooks and Macdonald, 1986; Brooks et al., 1981; Brooks et al., 1985a, 1985b; Brooks and Overstreet, 1978; Carney and Brooks, 1991; Cribb, 1988; Ehlers, 1984, 1985a, 1985b, 1986; Gibson, 1987; Hoberg, 1986, 1989; Hoberg and Adams, 1992; Justine, 1991a, 1991b; Klassen and Beverly-burton, 1987, 1988; Lotz, 1986; Macdonald and Brooks, 1989a, 1989b; Measures et al., 1990; O'Grady, 1987; Platt, 1988, 1992; Shoop, 1989; Van Every and Kritsky, 1992; Weekes, 1993; Wheeler and Beverly-Burton, 1989; Wirth, 1984; Xylander, 1986, 1987a, 1987b, 1987c, 1987d, 1988, 1989, 1990; see Brooks and McLennan, 1993, for a complete listing and updates). The characters represent a broad range of attributes that have formed the basis of traditional parasite taxonomic and morphological studies, and thus traditional views about parasite evolution. As an example, Figure I depicts the current phylogenetic hypothesis best supported by 154 characters requiring 157 character transformations; Appendix 1 lists the characters indicated by each number, and provides notations about homoplasies and losses.

We use only the results of phylogenetic systematic studies because nonphylogenetic studies might include paraphyletic groups. Paraphyletic groups are diagnosed by plesiomorphic characters, and because plesiomorphic characters are also used in the diagnoses of other, monophyletic, taxa such duplication of trait biases the mean in any statistical analysis of evolutionary phenomena (Wiley, 1981; Harvey and Pagel, 1991). In addition, critical investigation of the hypothesis that parasites exhibit unusual degrees of secondary simplification requires assessing the proportion of total apomorphic changes that result in character loss, not just an enumeration of lost traits. For example, Rogers I 962) stated that "the loss of sense organs is a common feature of parasitism." and that "These organs are replaced by mechanisms which allow the infective stage to "recognize" its host." Rohde (1989), in a complementary vein, demonstrated the existence of eight types of sensory receptors in a single species of endoparasitic flatworm (and postulated that there might be more), leading us to wonder if there might actually be a net gain of sense organs in the evolution of these parasites. Finally, to examine the postulate that parasites show high rates of homoplasious changes, we must utilize a method that provides a strong test of homoplasy, and phylogenetic systematics fulfills that requirement (Hennig, 1966; Wiley, 1981; Brooks and McLennan, 1991; Wiley et al., 1991).

Parasites Are Not Morphologically

Simplified and Degenerate

We begin this section with three questions: (1) How much character loss has occurred within the Cercomeria? (2) Are particular types of characters more susceptible to being lost? (3) Are the same characters lost repeatedly? To examine (2) and (3), we divided characters into four categories: male reproductive, female reproductive, adult nonreproductive, and larval. Table 1 summarizes our results. We did not include separate columns for the species-poor groups Aspidobothrea, Gyrocotylidea, and Amphilinidea because so few characters have been described for these taxa that analysis of each group is uninformative. The data for these groups, however, are included in the "totals" column in Table 1.

[TABULAR DATA OMITTED]

The observation of prime importance is that only 10.8% of the 1,882 character transformations displayed by the parasitic flatworms in the current data base are evolutionary losses. Thus, character innovation far outstrips character loss in these organisms. Because we do not yet have comparable information about proportions of losses in free-living organisms, especially in the rhabdocoels that are the closest relatives of the cercomerians, we do not know if the proportion of losses exhibited by the parasitic flatworms is significantly higher than that found in free-living platyhelminths. Judging from phylogenetic systematic studies of other free-living groups, we do not think this is the case. Nevertheless, we do believe that this result casts serious doubt on the traditional perspective that parasites are highly simplified through secondary loss of characters.

We next investigated the proportion of character types lost versus the proportion of change (Table 2 depicts the results of the chi-squared analyses) for all characters within groups (columns in Table 1) and for individual character categories among groups (rows in Table 1) to see if there were any generalizations about the types of characters that are lost in these organisms. The total amount of character loss is not distributed among the three major cercomerian groups (the Digenea, Monogenea, and Eucestoda) in proportion to the amount of character change in each group ([X.sup.2] = 8.95, P < 0.025; Table 2). Character loss in the Digenea and Monogenea occurs in proportion to total change, while character loss is disproportionately lower than total change within the Eucestoda. This is counter-intuitive because tapeworms are often cited as one of the best examples of degenerate evolution in parasites.

The three most species-rich groups appear to have followed different evolutionary "character loss" pathways. In the Digenea fewer female characters and more male characters have been lost than would be expected by the total amount of male and female characters in that group, and more male and more nonreproductive characters have been lost in proportion to their distribution across groups. In the Monogenea fewer nonreproductive and more larval characters have been lost than would be expected, and the loss of female characters is high relative to the other groups. Finally, in the Eucestoda fewer female and more larval characters have been lost than would be expected, and the loss of male and nonreproductive characters is low, while the loss of larval characters is high, compared to the other groups. These descriptions can be summarized as follows: the monogeneans show no strong overall trends, the digeneans have a strong propensity to lose male characters, and the eucestodes have a tendency to lose larval characters and to preserve adult characters. These complex pattems of character loss demonstrate that no group shows an overall trend towards secondary simplification. In addition, as discussed above, the group that shows the strongest resistance to evolutionary loss is the Eucestoda.

Finally, we asked whether particular types of characters have a propensity to be lost repeatedly; this is reflected in phylogenetic analyses by homoplasious apomorphic losses (Table 3). Overall, this is a trend towards decreasing homoplasious loss from the digeneans to the eucestodes, which once again emphasizes the conservative nature of tapeworm evolution. Among character categories, the amount of homoplasious loss is 49%, indicating that a fair number of characters tend to be lost repeatedly. The distribution of that homoplasious loss, however, and the types of characters that show homoplasious losses within each of these groups differ among clades. In the Digenea, the highest proportion of homoplasious loss is found in male reproductive and adult nonreproductive characters, and the lowest proportion is found in female reproductive characters. Of the male characters, the genital sac and male intromittent organs are lost most often. On the nonreproductive side, the homoplasy is divided between the body surface (the acetabulum has been lost at least eight times and body spines have been lost at least five times) and the digestive system (the pharynx has been lost at least four times, the esophagus at least four times, and one of the two ceca at least four times). The distribution of homoplasy parallels the distribution of overall losses depicted in Table 2. The digenean pattern is reversed in the Monogenea, which show the highest proportion of homoplasious loss in female characters and the lowest proportion in male and larval traits. Within the female characters, the vagina and egg filaments appear to have been lost most often. The moderate proportion of nonreproductive homoplasy centers around the loss of hooks and hooklets. The Eucestoda show very few homoplasious losses. Of these, the loss of an axoneme in the sperm's tail (male) and the loss of cilia on hexacanths and tails on plerocercoids (larval) occur more than once.

[TABULAR DATA OMITTED]

This analysis provides three generalizations about the current morphological data base for parasitic platyhelminths: (1) these parasites do not show high levels of character loss; (2) the types of characters that are lost show different distribution patterns among the three major clades; and (3) these patterns are partially the result of differences in which characters show repeated (homoplasious) loss in the different groups.

Parasites Do Not Exhibit

High Levels of Adaptive

Plasticity in Morphology

The above conclusions lead to another commonly held view about parasite evolution: success is due, in part, to parasites' ability to adapt rapidly to an ever changing set of challenges posed by the environment, which in the case of parasites generally means the host(s) (Price, 1980). One form of evidence of this adaptability might be unusually high levels of homoplasious evolution in morphology, the result of convergent adaptive responses to similar hosts. In extreme forms, we might even expect the amount of homoplasy to obscure, and possibly to swamp, the genealogical information available in homologous characters.

Once again, to investigate this problem we need information from two sources; the amount of homoplasy within free-living groups in general, and within the free-living sister groups of the parasitic clades in particular. Also once again, we do not have the necessary sister-group data. We do, however, have evidence that high levels of morphological homoplasy exist among a variety of groups of free-living organisms, including prokaryotes (Bremer and Bremer, 1989); fungi (Hoiland, 1987; Crisci et al., 1988); angiosperms (Crane, 1985; Freire, 1987; Bremer, 1987); opisthobranch molluscs (Gosliner and Ghiselin, 1984); amphipods (Myers, 1988); nemerteans (Sundberg, 1989); insects (Throckmorton, 1965; Saether, 1977); and vertebrates (Hecht and Edwards, 1976; Butler, 1982; Begle, 1991). Thus, while we cannot make the precise comparisons we would like, we can assess whether the parasitic platyhelminths fall into the "high homoplasy" group of taxa.

We have used two measures for estimating the amount of homoplasious evolution in our data base, and for evaluating its significance. The first of these is the consistency index (CI; see Wiley et al., 1991), a ratio of the number of character transitions needed to account for the different character states in a data set divided by the total number of character changes on the final phylogenetic tree. Each episode of homoplasious evolution adds a character change that was not recognized in the original assessment of character evolution. That is, the CI is an indicator of the proportion of mistaken hypotheses of homology made by the researcher prior to performing a phylogenetic analysis of an entire data set. There are problems with using the CI as a very strong indicator. For example, the inclusion of autapomorphies or symplesiomorphies in the calculation of the CI inflates the value of the measure based on characters that do not in fact affect the robustness of the phylogenetic hypothesis under consideration; hence, it has been suggested that the CI should be calculated using only putative synapomorphies (Sanderson and Donoghue, 1989). In addition, the CI is not strictly comparable across data sets, because it is insensitive to the number of characters or the number of taxa involved in any study.

In the past few years, a number of systematic theorists have begun investigating the problem of providing a statistically robust means of assessing the results of phylogenetic analyses (e.g., Sanderson and Donoghue, 1989; Archie, 1989; Farris, 1989; Meier et al., 1991). These studies have produced some interesting, and in some cases counter-intuitive, findings. For example, the minimum significant value for the CI decreases as one adds taxa and characters to a study; that is, a study using 50 characters for 20 taxa and reporting a CI of 60% may actually be more robust than one using 10 characters for 7 taxa and reporting a CI of 80%. This is because there are often apomorphic character changes that occur once within a given taxon that also occur once in another taxon. If someone were to expand the scope of a study to include both taxa, the estimate of homoplasy would increase even if the hypothesized phylogenetic relationships of the (now) subgroups did not change. That is, "global" phylogenetic analysis may discover homoplasy that two local" analyses failed to recognize.

Among the recent proposals for additional measures of homoplasy is the homoplasy slope ratio (HSR), a measure that is independent of number of characters or number of taxa and which compares the CI of a real data set, also taking into consideration the number of characters and taxa used, with the results of a randomly generated data set of the same number of characters for the same number of taxa (see Meier et al., 1991 for details of the calculations). An HSR of 0.35 means that the observed homoplasy is 35% of the homoplasy that would be expected for a randomly generated data set of the same number of characters for the same number of taxa. This measure behaves in a manner complementary to the homoplasy excess ratio (HER) proposed by Archie (1989) (a value of 0.35 for the HSR is comparable to a value of 0.65 for the HER) but is easier for a working systematist to implement, because it does not require one to perform a series of randomizations of the data set. In addition to producing a standard of comparison based on simulations of randomly generated data sets, Meier et al. (1991) performed a regression analysis based on a set of published phylogenetic studies, so that one could begin to assess the expected significant HSR values for real data sets. They also noted that the HSR does not take into account the internal structure of an individual data set, which may have a pronounced influence on the robustness of a phylogenetic tree, but this is a problem for all such measures at the moment (for example, the HSR may be overly sensitive to multi-state characters; A. Kluge, pers. comm.).

The HSR seems to be more sensitive than the CI to increasing robustness of a phylogenetic hypothesis provided by the addition of corroborating characters. For example, Meier et al. (1991) reported an HSR of 0.04 for an early study of the relationships among the major groups of cercomerians (Brooks et al., 1985a). That study was based on 39 characters, 2 of which were homoplasious, giving a CI of 0.951. The current data base for those taxa is 154 character, three of which are homoplasious, giving a CI of 0.981. Intuitively, we would think that adding 115 characters, only 1 of which is homoplasious, would increase the robustness of our phylogenetic hypothesis by more than 3%. The HSR value for the current data is 0.014, or 65% lower than the previous estimate. This accords more with our intuitions about the increase in robustness of the phylogenetic hypothesis resulting from a substantial increase in characters that corroborate the original tree.

We have calculated both the CI and the HSR for the major groups of cercomerians, based on both local and global homoplasy searches (Table 4). The only group for which the HSR value falls above the regression line for HSR values generated from real data sets by Meier et al. (1991) is the Aspidobothrea, a group which has a high CI value but very few characters. All other values fall well below the regression line, suggesting that we are dealing with a highly nonrandom data set; in fact, the lowest HSR value reported for a real data set by Meier et al. was 0.03.

[TABULAR DATA OMITTED]

Examination of homoplasy levels and distribution among the cercomerians supports the theoretical predictions: homoplasy on a global level is higher than that seen on a more local scale of investigation (Table 4). Most of the increase in homoplasy that resulted from the global search occurs within the digeneans, which experienced a drop in the overall consistency index from 90.8% to 71.6%. The consistency indices for the monogeneans, gyrocotylideans, amphilinideans, and eucestodes did not change appreciably when character evolution was examined among higher taxonomic levels. Despite the drop in Cl resulting from the increased homoplasy found in global considerations, the HSR values for the digeneans indicate that the data are not substantially less robust when considered globally (and, perhaps more importantly, none of the phylogenetic relationships postulated on the basis of local parsimony change when global parsimony is considered). Much of the digenean homoplasy appears to be spread among groups, whereas with the other cercomerian taxa most of the homoplasy occurs within groups (see Sanderson and Donoghue, 1989, for discussion of homoplasy distribution among taxa on phylogenetic trees). This is an example of global homoplasy considerations not having much of an influence on the robustness of local phylogenetic trees (see also Wilkinson, 1991).

The high CI and low HSR values indicate that homoplasy in morphological evolution is not unusually high in these parasites. Furthermore, we believe the same can be said for the other groups of parasites, although the data bases for those taxa are not as extensive as for the platyhelminths (see data for protists and nematodes in Brooks and McLennan, 1993). If anything, this particular group of parasites shows unusually high levels of phylogenetic constraint in morphological diversification. Just as with the fall of the myth of rampant character loss, the fall of the myth of rampant homoplasy has left several interesting problems in its place.

Homoplasious characters, like character losses, among the four types of characters within and among the major groups of cercomerians (Table 5) are not distributed among the three major cercomerian groups in proportion to the amount of character change in each group ([X.sup.2] = 11.3; P < 0.005; Table 6). The picture is similar to that depicted for evolutionary character losses: homoplasy within the monogeneans occurs in proportion to overall character change, while homoplasy is slightly higher than expected in the digeneans and much lower than expected within the eucestodes. Once again, this supports the hypothesis that eucestodes are the most evolutionarily conservative group within the Cercomeria.

[TABULAR DATA OMITTED]

In general, the trends shown for homoplasy parallel those uncovered for losses, with some notable exceptions. Homoplasy in the digeneans occurs less often than expected in larval characters within and among groups, and more often than expected in nonreproductive characters within and among groups. Digeneans do not show an unusual amount of homoplasy in male character. They do show a high level of male character loss, most of which is homoplasious loss. Monogeneans show unusually high levels of homoplasy in larval characters both within and across groups. In conjunction with the observed trend towards increased loss, it appears that larval characters are extremely flexible within the Mongenea. Finally, within the Eucestoda, there are fewer homoplasious male and nonreproductive, and more homoplasious larval, characters than would be expected. When eucestodes are compared with other cercomerian groups, levels of homoplasious larval characters are higher and levels of homoplasious female and nonreproductive characters are lower than expected.

SUMMARY

We can combine the information on homoplasy with the data on character loss to begin developing a picture of morphological character evolution within the three species-rich groups of cercomerians. In general, the "digenean profile" is one of tightly constrained larval characters (lower than expected levels of loss and homoplasy), constrained female characters (slightly above average homoplasy and very low levels of loss), flexible male characters (above average loss, average homoplasy), and very flexible nonreproductive characters (higher than expected levels of both loss and homoplasy). The "monogenean profile" presents constrained nonreproductive characters (lower than expected levels of loss and average homoplasy), unremarkable male characters (average amount of loss and homoplasy), flexible female characters (higher than expected levels of loss and average homoplasy), and very flexible larval characters (higher than expected levels of both loss and homoplasy). Finally, the "eucestode profile" shows tightly constrained female and nonreproductive characters (lower than expected levels of loss and homoplasy), constrained male characters (lower than expected levels of loss, slightly above average homoplasy), and very flexible larval characters (higher than expected levels of loss and homoplasy).

As anticipated by some earlier workers using a limited data base, the most widely accepted theories of parasite morphological evolution are not supported by evidence from a large data base. Those refuted theories were based on assumptions about homoplasious and reductive evolution that stemmed originally from orthogenetic thinking. Therefore, we do not have an extensive set of explanations for the patterns that we do observe, or for additional interesting questions that remain to be investigated at lower phylogenetic levels within each group. If the current data base is representative of overall morphological evolution in this group, parasitic flatworms are among the most constrained, rather than among the most plastic, organisms in their patterns of morphological evolution. Alternatively, the current data base could indicate only that parasite systematists using phylogenetic systematic methods have been unusually successful in recognizing a highly nonrandom subset of informative and unambiguous characters. In addition, although we believe this is the largest phylogenetically analyzed morphological data base used in evolutionary studies to date, it is by no means exhaustive. In fact, the data base represents only phylogenetic analysis to family level for all cercomerians, with some more detailed (generic level and species level) studies sprinkled throughout the groups.

The discovery that levels of character loss and homoplasy are not unusually high within the parasitic flatworms causes us to rethink our theories about parasite evolution by providing evidence that the evolution of parasites does not differ from that of free-living species. This suggests that in rethinking theories about parasite evolution we should pay attention to current theories in general evolutionary biology rather than continuing to develop special theories about parasite evolution. For example, it would be interesting to investigate questions such as the types of characters that show the highest level of homoplasy and the degree to which the origins of any of those homoplasious characters might be correlated with changes in the environment (such as predictable host switches or changes in life cycle patterns), one approach to studies of adaptation (Brooks and McLennan, 1991; Harvey and Pagel, 1991, and references therein). At the moment we have evidence for the existence of homoplasy, but we have no evidence about which of those characters might serve an adaptive function. In the future, we should search for the mechanisms that actually cause character loss or homoplasious evolution to occur, in addition to mechanisms that preserve homoplasious characters once they appear.

Appendix

An example of the characters used to examine the amounts of evolutionary character loss and homoplasy in parasitic platyhelminths. The numbers refer to numbers on the phylogenetic tree shown in Figure 1. Notations: * and H = homoplasy; L = loss; M = male; F = female; La = larval (life cycle patterns included here as well); N = nonreproductive adult features. Characters concerning pores or openings for genitalia of both sexes are assigned to the female reproductive character class; life cycle pattern characters are assigned to the larval character class. The number of homoplasious characters is half the number of homoplasious changes listed. Characters listed as reductions or fusions are not counted because we do not have adequate evidence that there is no compensatory change (e.g., one large unicellular protonephridium versus a small multicellular protonephridium). Paedomorphic characters are not listed as lost characters.

no vagina (1) F single ovary (2) F paired testes (3) M paired lateral excretory vesicles (4) N doliiform pharynx (5) N saccate gut (6) N

copulatory stylet (7) M without locomotory cilia in adults (8) L-N posterior adhesive organ formed by an expansion of

the parenchyma into, minimally, an external pad (9)

N terminal or subterminal mouth (10) N reduction of dual-gland adhesive system (11) N amphistomous juvenile (12) La one-host life cycle with arthropod host (13) La ectoparasitic* (14) H-La genital aperture midline (15) F cephalic tentacles (16) N peripheral layer of microtubules in spermatozoa spirally

arranged (17) M genital pores in anterior half of body (18) F single ventro-lateral vagina connecting with oviduct

(19) F Mehlis' gland (20) F vitellaria in adults lateral and follicular (21) F no dictyosomes or endoplasmic reticulum in larval epidermis

(22) L-La cytoplasmic granules lacking in spermatozoa (23) L-M larval epidermis shed at end of larval stage (24) La protonephridia with two-cell weir (25) N syncitial post-larval neodermis (26) N cilia of larval epidermis with only 1 rostrally directed

rootlet (27) La epithelial sensory cells with EM-dense collars (28) N epidermal cells in larvae separated by neodermis material

(29) La copulatory stylet lacking (30) L-M secondary protonephridial system of canals and pores

(31) N giant paranephrocytes (32) N arthropod host itself is parasitic on vertebrate (33) La male genital pore and uterus proximate (34) M oral sucker present (35) N uterus with lateral coiling (36) F adult intestine bifurcate (37) N spermiogenesis with a proximal-distal fusion, resulting

in dorsal and ventral microtubules present in the

principal region of the spermatozoon (38) M two-host life cycle involving an arthropod and a vertebrate

(39) La endoparasitic (40) La muscular cirrus (41) M oviduct straight, intercecal (42) F dorsal vagina a Laurer's canal (43) F posterior adhesive organ a sucker (44) N male genitalia consisting of cirrus sac, pars prostatica,

and internal seminal vesicle (45) M male genital pore opening into genital atrium independent

of uterine opening (46) M operculate eggs usually longer than 50 [mu]m (47) La adults with pharynx near oral sucker (48) N lamellated walls in protonephridia (49) N cercomer shifted to ventral surface (50) N single medial excretory vesicle opening postero-dorsally

(51) N two-host cycle involving a molluscan and a vertebrate

(52) La vaginal opening lost (53) L-F specialized micro-villi and microtubules in neodermis

(54) N posterior suckers fused anteriorly (55) N hypertrophy and linear subdivision of posterior sucker

by tranverse septa (56) N atrophy or oral sucker (57) N first larval stage a miracidium (58) La miracidium hatches from egg and swims to snail host

(59) La miracidium with one pair of flame cells (60) La saclike sporocyst stage ("mother sporocyst") in snail

host follows miracidium (61) La cercaria stage developing in snail follows mother sporocyst

(62) La cercariae with simple tails (63) La cercariae amphistomous (64) La cercarial excretory system anepitheliocystid (65) La cercarial excretory ducts stenostomatous (66) La cercariae with secondary dorsal excretory pore (67) La cercariae with primary excretory pore at posterior end

of tail (68) La cercariae remain in sporocyst until snail host is ingested

(69) La cercarial intestine bifurcate (70) La uteri in adults passing postovarian, then anteriorly to

just post-bifurcal (71) F gut development paedomorphic (does not appear until

redial or cercarial stage) (72) La tiers of epidermal cells in miracidium (73) La no evidence of endoderm in embryos* (74) H-La/L-La vitellogenic cells with only one kind of electron-dense

vesiculated inclusions* (75) H-F/L-F posterior adhesive organ armed with hooks, called a

cercomer (76) La cerebral commissures doubled (77) N posterior nervous system commissures doubled (78) N 12 to 16 hooks on cercomer in larvae (79) La three rows of ciliary epidermal bands in oncomiracidium

larva (one at each end, one in middle) (80) La four rhabdomeric eye-spots (81) N one-host life cycle involving a vertebrate (loss of arthropod

host) (82) L-La ectoparasitic* (83) H-La single testis (84) L-M testes postovarian (85) M sperm microtubules lying along entire cell periphery

(86) M cirrus spinose (87) M cirrus ovate (88) M single egg filament (89) La no anchors on oncomiracidium (90) La 16 marginal hooks on oncomiracidium (91) La haptor disk-shaped (92) N 16 marginal hooks in adult (93) N dactylogyrid hook shape (94) N anchors present in at least one stage of development

(95) N one pair of ventral anchors (96) N osmoregulatory system becomes reticulate in late ontogeny

(97) N intestine lacking (98) L-N posterior body invagination present (99) N cercomer paedomorphic, reduced in size and at least

partially invaginated (100) N male genital pore not proximate to uterine opening

(101) F oral sucker/pharynx complex small (102) N ovary follicular (103) F ovary bilobed (104) F testes multiple, in two lateral bands (105) M 10 equal-sized hooks on cercomer in larvae (106) L-La larval epidermis syncitial (107) La vitelloducts syncitial (108) F neodermis does not protrude to surface between epidermal

cells (109) N no desmosomes in the passage of the first excretory

canal cells (110) L-N no evidence of endoderm in embryos* (111) H-La/L-La vitellogenic cells with only one kind of electron-dense

vesiculated inclusions* (112) H-F/L-F inner longitudinal muscle layer well developed (113)

N rosette at posterior end of body (114) N funnel connecting with rosette short (115) N funnel narrow (116) N antero-lateral genital notch present (117) F body margins crenulate (118) N body spines small over most of body, large at pharyngeal

level (119) N large body spines long and narrow (120) N testes extending posteriorly only to level of metraterm

(121) M vitellaria encircling entire body, extending along entire

body length (122) F no nuclei in larval epidermis (123) La no multi-ciliary nervous receptors (124) L-N neodermis not extending into intercellular space between

epidermis and basal lamina (125) N copulatory papilla present (126) M male genital pore and vagina proximate (127) F cercomer totally invaginated during ontogeny (128) La excretory system opens posteriorly in later ontogeny

(129) N hooks on larval cercomer in two size classes (6 large

and 4 small) (130) La protonephridial ducts lined with microvilli (131) N subepidermal ciliary receptors with true photoreceptor

functions lacking in larvae (132) L-la protonephridia in larvae in posterior end of body (133)

La genital pores marginal (134) F uterine pore and genital pores not proximate (135) F male pore at posterior end (136) M vaginal pore at posterior end (137) F tegument of adults with irregular ridges and depressions

(138) N uterus "N"-shaped (139) F uterine pore proximal to vestigial pharynx (140) F inner longitudinal muscle layer weakly developed (141)

N adults parasitic in body cavity (142) N body of adults polyzoic (143) N cercomer lost during ontogeny (144) L-La six hooks on larval cercomer (145) L-La excretory system reticulate in early ontogeny (146) La medullary portion of proglottids restricted (147) N hexacanth embryo hatches from egg, is ingested in water

(148) La second larval stage a procercoid (149) La third larval stage a plerocercoid (150) La protein embedments in epidermis of hexacanth (151)

La tegument covered with microtriches (152) N sperm lacking mitochondria (153) L-M cerebral development paedomorphic, none seen in larvae

(154) La "polylecithal" eggs (a large component of vitelline material forming a true shell that is quinone tanned)

(155) La one embryonic membrane formed by the embryo (with

the consequent lack of an embryophore) (156) La hexacanth larvae with unicellular protonephridium

(157) La

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Date:Apr 1, 1993
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