Extending Phylogenetic Studies of Coevolution: Secondary Brooks Parsimony Analysis, Parasites, and the Great Apes

Cladistics 19 (2003) 104–119 www.elsevier.com/locate/yclad

Extending phylogenetic studies of coevolution: secondary Brooks parsimony analysis, parasites, and the Great Apes

Daniel R. Brooks* and Deborah A. McLennan

Department of Zoology, University of Toronto, 25 Harbord Street, Toronto, Ont., Canada M5S 3G5

Accepted 10 February 2003

Abstract

Dowling recently compared the empirical properties of Brooks parsimony analysis (BPA) and the leading method for studying phylogenetic aspects of coevolution, reconciled tree analysis (using the computer program TreeMap), based on a series of simulations. Like the majority of authors who have compared BPA with other methods, however, Dowling considered only the form of BPA proposed in 1981 and did not take into account various modiﬁcations of the method proposed from 1986 to 2002. This leaves some doubt as to the robustness of his assessments of both the superiority of BPA and its shortcomings. We provide a preecis of the principles of contemporary BPA, including ways to implement it algorithmically, using either Wagner algorithm-based or Hennigian argumentation-based approaches, followed by an empirical example. Our study supports DowlingÕs fundamental conclusions about the superiority of primary BPA relative to TreeMap. However, his conclusions about the shortcomings of BPA due to inclusive ORing (i.e., the production of ghost taxa) are incorrect, as secondary BPA eliminates inclusive ORing from the method. Secondary BPA provides a more complete account of the evolutionary associations between the parasite groups and their hosts than does primary BPA, without sacriﬁcing any indirectly generated information about host phylogeny. Secondary BPA of two groups of nematodes inhabiting Great Apes shows that TreeMap analysis underestimated the amount of cospeciation in the evolution of the nematode genus Enterobius. Ó 2003 The Willi Hennig Society. Published by Elsevier Science (USA). All rights reserved.

Parasites became important model systems in evolu- monophyletic group from those in which they do not. tionary biology when orthogenetic evolution became Brooks (1979) showed that parasites could have plesio- fashionable in the early 20th century. Orthogeneticists morphic, synapomorphic, autapomorphic, or even ho- believed that once a lineage became parasitic, it became moplasious host associations, supporting HennigÕs so dependent on its host that it no longer had any in- objection. He coined the term cospeciation to refer to the dependent evolutionary existence, becoming a wraith- congruent portions of host and parasite phylogenies. like shadow of the hostÕs evolution. Even when Although recognizing that a variety of processes could NeoDarwinism replaced orthogenesis as the dominant produce such macroevolutionary patterns, he tended to theory of evolution, many biologists continued to as- think that such congruence was most likely a by-product sume that the phylogenetic relationships of parasites of vicariant cospeciation (see also Brooks and McLen- exhibiting pronounced host specificity must parallel the nan, 1991, 1993, 2002; Dowling, 2002). phylogenetic relationships of their hosts. Hennig (1950, Existing models of coevolution all deal with coac- 1966) referred to this assumption as ‘‘the parasitological commodation (Brooks, 1979), later called coadaptation method,’’ which he rejected on the basis that there were (Brooks and McLennan, 1991, 1993), or various forms no objective criteria for distinguishing cases in which of mutual evolutionary modification between hosts and two or more hosts inhabited by a parasite species form a parasites which are anagenetic rather than cladogenetic processes. For this reason, Brooks (1979) proposed that assessments of host specificity (coaccommodation) were * Corresponding author. Fax: 416-978-8532. decoupled from assessments of the degree of phyloge- E-mail address: [email protected] (D.R. Brooks). netic association among host and parasite clades (co-

0748-3007/03/$ - see front matter Ó 2003 The Willi Hennig Society. Published by Elsevier Science (USA). All rights reserved. doi:10.1016/S0748-3007(03)00018-5 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 105 speciation); hence, one could not use degree of host to identify the parasite clades most likely to exhibit specificity as a guide to determining which parasite clades cospeciation patterns and then provide the maximum were ‘‘likely’’ to have cospeciated with their hosts. The- degree of fit between the phylogenies of those parasites oretical and experimental studies of coevolving systems and their hosts. Dowling (2002) recently compared the of many kinds have supported this proposal (for a re- empirical properties of BPA and the leading method for view and references, see Brooks and McLennan (2002)). determining maximum cospeciation, reconciled tree Instead, Brooks (1979) supported the view that parasites analysis (using the computer program TreeMap), based could be treated as analogous to taxonomic characters of on a series of simulations. His results indicated that BPA their hosts, with the proviso that, like all characters, not was preferable to TreeMap for two reasons: ‘‘First, all parasites provided information about host phylog- TreeMap grossly overestimates duplications and sorting eny. Brooks (1981) extended this analogy, proposing a events when widespread taxa due to host switching are direct application of the inclusion/exclusion rule in present in the associations between the host and parasite phylogenetic systematics for studies of cospeciation: phylogenies. Second, the ghost taxa that BPA mistakenly treat parasite phylogenetic trees as ordered and polar- produces do not cause any topological changes in the ized multistate transformation series, treat the hosts as tree, are readily recognizable, and are easy to interpret.’’ terminal taxa, run a phylogenetic systematic analysis of Like the majority of authors who have compared BPA the data, and compare the resultant host cladogram with other methods (e.g., Morrone and Carpenter, 1994; (analogous to an area cladogram) with the host phy- Morrone and Crisci, 1995; Page, 1990; Page and logenetic tree. Congruence between the two ‘‘trees’’ Charleston, 1998; Ronquist, 1995, 1996, 1997a,b, 1998), corroborates a hypothesis of cospeciation between the Dowling considered only the form of BPA proposed in parasite clades, while incongruence falsifies it. Brooks 1981, and did not take into account modifications of the also came to a radical conclusion: if parasites are evo- method (Brooks, 1990; Brooks and McLennan, 1991, lutionarily independent entities, like free living organ- 1993, 2002; Brooks et al., 2001; Green et al., 2002; Van isms, then members of different parasite clades need not Veller and Brooks, 2001; Wiley, 1986, 1988a,b). This show identical patterns of evolutionary diversification leaves some doubt as to the robustness of DowlingÕs with respect to host relationships, except in the default conclusions about both the superiority of BPA and its case of association by common ancestry (possibly indi- shortcomings. In this paper, therefore, we provide a cating simply common episodes of vicariant speciation). preecis of contemporary BPA, followed by an empirical He argued that even if each parasite clade included some example using pinworm–roundworm–Great Ape inter- species which did not cospeciate with their hosts, si- actions, to assess DowlingÕs conclusions in light of con- multaneous analysis of multiple parasite clades inhab- temporary BPA. iting a given host group should provide evidence of host phylogeny as a byproduct of assessing the unique coevolutionary history of each parasite clade. Comparing the Methodology host cladogram produced by phylogenetic analysis of parasites with a host phylogeny generated using other Part 1: Starting points data can test this hypothesis. Points of congruence between the two trees corroborate the hypothesis that the (Assumption 0). All species and all host distributions parasites and the hosts have cospeciated; points of in- in each input parasite phylogeny must be considered congruence falsify that hypothesis. This proposal echoed without modification, and the final analysis must be the then emerging phylogenetic systematic view that logically consistent with all input data. This assumption homology was determined a posteriori by character is important because it mandates a minimum of con- congruence (Patterson, 1981, 1982, 1987; Wiley, 1981). straints on any analysis by prohibiting the researcher After this approach was applied to historical biogeog- from eliminating, modifying, or weighting data a priori raphy (Brooks, 1985), it was dubbed Brooks parsimony (Wiley, 1986, 1988a,b; Zandee and Roos, 1987). Page analysis or BPA (Wiley, 1986, 1988a,b). (1990) coined the term ‘‘Assumption 0 Analysis’’ for the Not all phylogeneticists are convinced that BrooksÕ methodological approach that codes hosts from which Hennigian solution to the question of ‘‘the parasitolog- members of a parasite clade are missing as primitively ical method’’ is adequate. For example, the ‘‘maximum lacking the parasite clade. This shortcoming in the ori- cospeciation’’ research program (Page, 2002; Page and ginal BPA formulation (Brooks, 1981) occurred because Charleston, 1998 and references therein) is based upon computer programs at the time did not accept missing the traditional assumption that cospeciation lies at the data entries. Five years later, the computer programs core of many specialized associations, rejecting Brooks’ had been modified and Wiley (1986, 1988a,b) solved this (1979) argument that cospeciation and coaccommoda- particular problem by suggesting that ‘‘absence’’ be tion were decoupled evolutionarily. Advocates of this coded a priori as ‘‘missing’’ (?) and interpreted a pos- approach have developed a variety of methods designed teriori as either primitive absence or secondary loss 106 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119

(extinction). We term this the Missing Data Coding or for the study groups in particular. Two additional Protocol: all cases of ‘‘absence’’ should be coded a priori evolutionary phenomena produce patterns that are al- as ‘‘missing.’’ By coding all absences as ‘‘missing’’ a ways logically consistent with any general cospeciation priori, BPA requires the investigator to account for such pattern. These are (1) cases in which single species are missing data codes a posteriori, i.e., after the host widespread in two or more hosts because they did not cladogram has been produced. This is done by character respond to a vicariance event that produced sister spe- optimization (see Fig. 9 and associated discussion be- cies of hosts (Fig. 2) and (2) episodes of sympatric spe- low). ‘‘Assumption 0 Analysis’’ of Page (1990), imple- ciation (sometimes called ‘‘lineage duplication’’), which mented in various computer programs, is thus not BPA, produce replicate pairs of sister species of the same clade which relies on both the original Assumption 0 and the in the same host species (Fig. 3). Missing Data Coding Protocol. A number of evolutionary phenomena produce special or unique coevolutionary elements that do not Part 2: Distinguish general and special elements conﬂict with the general cospeciation patterns but indicate novel host relationships; e.g., host switching by Cospeciation between hosts and parasites as a by- members of one clade to a host not inhabited by other product of vicariance should be the null hypothesis for members of its clade or by any members of the clades studies of coevolution because it is the only mode of being analyzed. Such dispersal may take the form of speciation that will always produce episodes of congru- host switching without speciation (postspeciation dis- ent host and parasite speciation (Brooks, 1981, 1985; persal) (Fig. 4), which increases host range, or of host Brooks and McLennan, 1993, 2002; Dowling, 2002). switching with speciation (peripheral isolates speciation) Other modes of parasite speciation (e.g., sequential (Fig. 5), which does not increase host range (for a dis- colonization of hosts) may, but need not, produce co- cussion of speciation by host switching as a form of speciation patterns (see Brooks and McLennan (2002)). peripheral isolates allopatric speciation see Brooks and Therefore, whenever we ﬁnd pairs of sister species of McLennan, 1993, 2002; Funk et al., 1995; Funk, 1998). parasites representing at least two clades that show the In the latter case, clade 1 is absent from host E because same host relationships (Fig. 1), we invoke cospeciation its members were never associated with that host. This even in the absence of an independent host phylogeny, means that we would not expect host E to be the sister because we have evidence that the two parasite groups species of host D, hence E is not represented in the host share a common history of speciation. Requiring two or phylogeny (Fig. 5d). There is, however, an additional more congruent speciation events is simply the meth- interpretation of Fig. 5. If species 11 and 12 have been odological ‘‘cost’’ of invoking vicariance and does not produced as the result of a cospeciation event (meaning, imply a priori assumptions about the probability or among other things, that host E might be the sister likelihood of the occurrence of cospeciation in general species of host D), then it is possible that the same event

Fig. 1. Minimal support for cospeciation: two parasite clades supporting the same host relationships indicate episodes of mutual speciation by the parasite clades. The default expectation is that these host relationships are congruent with host phylogeny, which can be tested if an independently derived estimate of host phylogeny is available. Open circles highlight putative instances of vicariant speciation (the default speciation mode)/cospeciation events. D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 107

Fig. 2. Nonresponse to host speciation produces parasite species acting as synapomorphies of two or more host species.

Fig. 3. Sympatric speciation (lineage duplication) of parasite lineage in ancestral member of host lineage produces two cospeciating lineages in some descendant hosts. fragmented clade 1, producing species 4 (in host D) and three clades inhabiting the same host group must be its sister species (in host E), which later became extinct. analyzed. If we examine only two clades we can identify the For example, suppose there is a third group of problem of missing taxa, but we cannot determine a so- parasites with representatives in all ﬁve hosts shown in lution to that problem because we do not know whether Fig. 5. The new host cladogram (Fig. 6) indicates that the ambiguity is caused by the presence or absence of the presence of species 12 and species 21 in host E species in the unusual host (in this case host E). In other conforms to a general pattern. It is thus the absence of words, we do not know which alternative represents the the sister to species 4 (clade 1) in host E that is the general pattern. This leads to the ‘‘ThreeÕs Rule’’ rule: to unique element, and it is most parsimonious to invoke distinguish between general and special patterns of his- an episode of secondary extinction to explain that torical association based solely on the data at hand, in absence. In the absence of other information, we particular to determine when absence from a host is due would also expect that host E is the sister species of to secondary extinction or primitive absence, at least host D. 108 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119

Fig. 4. Postspeciation host switching, indicated by dotted lines and airplanes, to enlarge host range involving novel host species. Such occurrencesdo not aﬀect the detection of cospeciation events.

Fig. 5. Peripheral isolates speciation, indicated by open circle (ancestor) and closed circle (new descendant species), by host switching into novel host species. Such occurrences may aﬀect the detection of cospeciation events if only two clades of parasites are examined because cospeciation with secondary extinction cannot be diﬀerentiated from peripheral isolates speciation by host switching.

Part 3: Recognize hosts that have reticulate histories of isolates speciation by host switching create more than association with their parasites one set of relationships for the same host species (i.e., some host species have reticulate histories with respect A number of evolutionary phenomena produce co- to their parasite faunas). The only way to satisfy As- evolutionary elements that conﬂict with cospeciation sumption 0 in such cases is to duplicate the hosts with patterns, e.g., host switching among members of one reticulate histories until all such speciation events in- parasite clade to hosts already inhabited by other volving those hosts are accounted for (Figs. 7 and 8). members of that parasite clade or by any members of the This is called the Host Duplication Convention: whenever other parasite clades being analyzed. Such episodes of hosts have reticulate histories with respect to the parasite postspeciation expansion of host range and peripheral species inhabiting them, Assumption 0 will be violated D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 109

Fig. 6. Peripheral isolates speciation by host switching into novel hosts can be distinguished from cospeciation with secondary extinction if at least three diﬀerent parasite clades are examined (the ‘‘ThreeÕs Rule’’ rule).

Fig. 7. Postspeciation dispersal enlarging host range involving colonization of a host utilized by another member of the parasite clade. Such reticulate host relationships can be detected using the Host Duplication Convention. unless those hosts are represented as separate entities for When all available data (total evidence) falsify that null each separate historical episode. In this case the ambigu- hypothesis, BPA duplicates hosts to indicate the exact ous hosts should be duplicated until Assumption 0 is sat- departures from (falsifications of) the null hypothesis isfied. but does not multiply hosts beyond necessity (logical The host duplication convention is an extension of parsimony: Wiley, 1975; see also Kluge, 1997, 1998, the principles of total evidence, logical parsimony, and 1999). falsification embodied in Assumption 0. Our null hy- Brooks (1981) proposed that when two or more pothesis is that all hosts have a single history with re- members of the same parasite clade occur in the same spect to all the species of parasites that inhabit them. host, the binary codes representing each species and its 110 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119

Fig. 8. Peripheral isolates speciation by host switching into a host utilized by another member of the parasite clade. Such reticulate host relationships can be detected using the Host Duplication Convention.

Fig. 9. A posteriori explanations for ‘‘missing’’ parasites. The absence of any member of clade 1 in host A is not due to extinction, because the most parsimonious interpretation of the data is that clade 1 did not become associated with the host clade until the common ancestor of BCD. The absence of any member of clade 3 in host C, however, is most parsimoniously explained as an extinction event, because clade 3 became associated with the host clade in the common ancestor of ABCD and because clades 1 and 2 have sister species occurring in sister hosts C and D. phylogenetic relationships should be combined in the the method. BPA not using the host duplication con- binary matrix used to generate the host cladogram. vention has been called ‘‘primary BPA,’’ while that in- Cressey et al. (1983) first noted that this protocol, which voking the duplication convention has been called they called inclusive ORing, produced the ‘‘ghost taxa’’ ‘‘secondary BPA’’ (Brooks and McLennan, 2002; to which Dowling (2002) referred. Brooks (1990) pro- Brooks et al., 2001; Green et al., 2002). Van Veller and posed the Duplication Convention (in a biogeographic Brooks (2001) suggested that reconciled tree analysis is context) specifically to eliminate inclusive ORing from more closely analogous to secondary BPA than to pri- D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 111 mary BPA (e.g., reconciled tree analysis permits clade 4. Perform parsimony analysis on the data matrix (this duplications, whereas secondary BPA permits host du- is primary BPA): If the result is a single most parsi- plications), and thus empirical comparisons between the monious host cladogram in which there is no homo- methods in studies of historical biogeography should use plasy, the default explanation is that the host secondary BPA. We suggest that the same holds true for cladogram is congruent with the host phylogeny, comparisons between the methods in studies of coevo- and cospeciation, nonresponse to host speciation, lution. and sympatric speciation [ ¼ lineage duplication] ex- Note also that we have used the ‘‘ThreeÕs Rule’’ rule plains the observed host–parasite associations. In in Figs. 7 and 8 to determine which version of host A other words, all notations for parasites on the belongs to the general (cospeciation) pattern and which host cladogram will correspond to the patterns does not. BPA assesses cospeciation patterns among shown in Figs. 1–3. If the results are otherwise, go different clades of parasites. Only when different parasite to step 5. clades exhibit cospeciation patterns due to a common 5. Account for all host taxa coded as ‘‘missing’’ for history of speciation events also involving their hosts particular parasites a posteriori. This means distin- will those patterns correspond to host phylogeny. guishing cases in which the parasite group was never associated with particular host taxa from those in which the parasite group has been secondarily lost. Performing BPA This can be done by a simple optimization proce- dure—locate the code for the basal branch of each BPA is not a model, so there are no a priori costs, given parasite clade on the host cladogram (if pri- probabilities, or weights associated with different co- mary BPA has produced more than one equally par- evolutionary phenomena. Rather, BPA is a discovery- simonious tree, this part of the analysis can be done based approach, in which different coevolutionary phe- using any of the alternatives). This indicates the nomena are inferred from the analysis a posteriori, in point at which the parasite clade became associated accordance with the most parsimonious description of with the host clade (Fig. 9). Absence of the parasite the data. This does not mean that BPA is nonalgorith- clade in taxa above that point on the host clado- mic, however, because BPA is a direct application of the gram is the result of extinction (Figs. 6 and 9). If principles of phylogenetic systematics. This can be done the result of a primary BPA is a single most parsi- in two ways, which we outline below. monious host cladogram in which there is homoplasy due to inferred reversals ( ¼ loss of the parasite clade in a particular host taxon), the default Wagner algorithm explanation is that the host cladogram is congruent with the host phylogeny, and a single history of 1. Convert all parasite phylogenetic trees into parasite– cospeciation (and possibly sympatric speciation host cladograms by replacing parasite identities with [ ¼ lineage duplication]) plus parasite extinctions ex- host identities on the terminal branches of each par- plains the observed host–parasite associations. In asite phylogenetic tree and then numbering each other words, all notations for parasites on the host branch of each parasite–host cladogram for binary cladogram will correspond to the patterns shown coding. in Figs. 1–3 and 6. 2. Construct a data matrix in which the rows corre- 6. If the result is one or more most parsimonious host spond to host taxa (each host taxon is listed once) cladograms that include nonreversal homoplasy, the and the columns correspond to the total number of default explanation is that the nonreversal homo- branches in all parasite–host cladograms being con- plasy indicates episodes of host switching. In such sidered. cases, notations for parasites on the host cladogram 3. Convert each parasite–host cladogram into additive will correspond to the patterns shown in Figs. 4 binary codes and fill in the matrix: (a) for each case and 5. in which a host taxon is not inhabited by a member 7. Eliminate the ghost lineages from the host cladogram of a given parasite–host cladogram, list that host tax- by duplicating hosts for each instance of nonreversal on as ‘‘missing’’ (?) for the parasite clade; (b) for each homoplasy (Figs. 7 and 8). case in which a parasite taxon occurs in more than 8. Check the analysis by producing a new binary matrix, one host taxon, combine the information from each this time including duplicated taxa as separate en- of those cases (inclusive ORing); and (c) for each case tries. The result should be a single host cladogram in which more than one parasite taxon occurs in the (which may include polytomies, because unique speci- same host, combine the binary codes representing ation by host switching events can produce hard each species and its phylogenetic relationships in the polytomies: Brooks and McLennan, 2002) with no binary matrix (inclusive ORing). homoplasy except for inferred extinction events. 112 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119

Hennig argumentation Second, for cases in which a given host taxon appears only once in each of the two parasite–host clado- Hennigian argumentation is an approach in which grams, assume a priori that this is the result of com- transformation series are combined sequentially, using mon ancestral associations. If this assumption is the inclusion/exclusion rule (see Brooks and McLennan, violated, the inclusion/exclusion rule will also be vio- 2002; Wiley et al., 1991, 2003). In standard phylogenetic lated, producing nonreversal homoplasy in a stan- analysis, homoplasy produces violations of the inclu- dard parsimony analysis of the combined data for sion/exclusion rule. In BPA, each parasite–host clado- the two parasite–host cladograms (host code 18 ap- gram is used as a transformation series, and host pears twice in Fig. 11c). This is resolved by invoking switching produces violations of the inclusion/exclusion the host duplication convention (see hosts D1 and D2 rule. in Fig. 11d). 1. Convert all parasite phylogenetic trees into parasite– 4. Calculate a new matrix for Fig. 11d, and use it in host cladograms by replacing parasite identities with combining the third parasite–host cladogram. Con- host identities on the terminal branches of each par- tinue this process iteratively until all parasite–host asite phylogenetic tree, and then numbering each cladograms are incorporated. This should result in branch of each parasite–host cladogram for binary a single host cladogram with a consistency index of coding. 100%. 2. Begin with one of the parasite–host cladograms (Fig. 5. Assess missing data a posteriori as with the Wagner 10a). Convert it to a binary matrix without inclusive algorithm to obtain the final host cladogram. If there ORing; this may produce duplicated hosts (Fig. 10b). are absences most parsimoniously interpreted as sec- Standard parsimony analysis of this matrix should re- ondary losses, the final host cladogram will have a produce the parasite–host cladogram exactly, and consistency index of less than 100%. with a consistency index of 100%. 3. Take a second parasite–host cladogram (Fig. 11a). Convert to an additive binary matrix for combination Results with the data from the first parasite–host cladogram (Fig. 10b). There are two coding protocols that need Brooks and Glen (1982) presented the first phyloge- to be observed at this point. First, if the second par- netic systematic analysis examining the relationship be- asite–host cladogram has a species occurring in a host tween the Great Apes and their parasites based on the that has already been duplicated, treat the host for pinworm (nematodes) genus Enterobius. Subsequently, a the second parasite clade as a separate occurrence group of hookworms [Oesophagostomum (Conoweberia); and duplicate it (host A3 in Fig. 11b). [Note: when Glen and Brooks (1985); see both Brooks and Glen making a data matrix combining the information (1985) and Glen and Brooks (1982) for discussions of for both clades, in this case host A3 should be coded host records including the extreme ambiguity of zoo- as ‘‘missing’’ for clade 1–11 and hosts A1 and A2 based data] was added to the database, followed by a should be coded as ‘‘missing’’ for clade 12–20]. If new phylogenetic analysis of Enterobius and relatives the duplication is unnecessary, standard parsimony (Hugot, 1999). Hugot (1999) examined the coevolu- analysis will result in the same hosts appearing either tionary relationship between the Enterobiinae and their as sister groups or in a polytomy with a third host primate hosts. In this analysis we will focus on a subset (see hosts A2 and A3 in Fig. 11c). In these cases, com- of HugotÕs study, the relationship between the Entero- bine the duplicated hosts (see host A2 in Fig. 11d). bius pinworms and the Great Apes. Reanalysis of Hu-

Fig. 10. Secondary BPA using Hennigian Argumentation Coding I. (a) Phylogenetic tree for parasite clade comprising terminal taxa 1–6 inhabiting host groups ABCDE, with host taxa superimposed above numbers representing diﬀerent parasite species. (b) Phylogenetic tree for parasite clade comprising terminal taxa 1–6, coded for BPA without inclusive ORing; note that host ‘‘A’’ is listed twice, once as host for parasite species 1 and once as host for parasite species 4. D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 113

Fig. 11. Secondary BPA using Hennigian Argumentation coding II. (a) Parasite–host cladogram for a second clade of parasites inhabiting host group ABCDE, comprising species 12–16, with host taxa superimposed above numbers representing different parasite species. (b) Phylogenetic tree for parasite clade comprising terminal taxa 12–16, coded for BPA without inclusive ORing; host A is listed as A3, because host A has been duplicated in the previous step (see Fig. 10) and we do not know whether the presence of parasite species 15 in host A is part of the pattern represented by host A1 or host A2 in the previous step or represents a third historical utilization of host A. (c) Initial host cladogram produced by using the inclusion/ exclusion rule to combine the host information from the parasite clade comprising species 1–6 and 12–16. Note the double occurrence of ancestor 18, nonreversal homoplasy indicating host switching. Note also that hosts A2 and A3 occur in a polytomy with the ancestor of hosts D þ E. (d) Final host cladogram produced by using the inclusion/exclusion rule to combine the host information from the parasite clade comprising species 1–6 and 12–16. The homoplasy for ancestor 18 has been resolved by duplicating host D and host A3 has been combined with A2. gotÕs data matrix indicated that there were three equally nately there are currently only two resolved parasite parsimonious trees for Enterobius, differing only in the clades for the Great Apes, so the results presented in placement of E. lerouxi with respect to the E. buckleyi this paper represent the best hypothesis that we can clade and E. anthropopitheci. In his study, Hugot used erect based on the data in hand. Bearing this caveat in the topology that gave the best fit to the host phylogeny. mind, we compare both the results of primary BPA We have used the consensus tree showing a polytomy with those of secondary BPA and the results of the among these three taxa. Our interpretation of coevolu- secondary BPA with those of the Tree map-based tionary relationships within this subclade may thus results discussed by Hugot (1999), for the relevant change if the polytomy is resolved by the addition of species. further characters. On the other hand, the polytomy 1. Because we are interested only in the relationships be- may represent a ‘‘real’’ evolutionary phenomenon (e.g., tween the worms and their Great Ape hosts, we have peripheral isolates species; see discussion in Brooks and simplified the phylogenetic trees for the parasites by McLennan, 2002), in which case the addition of further collapsing each monophyletic group that inhabits data will corroborate the interpretation presented in this other hosts into a single lineage. This does not change study. BPA does not differ from any other phylogenetic the phylogenetic tree for the parasites and thus will systematics-based method; its conclusions are based not affect our interpretations about parasite and upon the most parsimonious interpretation of the data Great Ape coevolution. The phylogenetic tree for at hand and may thus change with the addition of new the pinworms (Fig. 12) depicts three such lineages: information. the E. brevicauda + E. bipapillatus + E. macaci clade Here we use both the pinworm and the hookworm (6) whose members inhabit cercopithecines, the Colo- phylogenetic trees to demonstrate how BPA is properly benterobius clade (7) whose members inhabit colo- performed for coevolutionary studies. The use of only bines, and the Trypanoxyuris clade (8) whose two trees violates the ‘‘ThreeÕs Rule’’ rule, which means members plesiomorphically inhabit New World mon- that some unique events may have two equally parsi- keys. The phylogenetic tree for the hookworms (Fig. monious explanations (e.g., extinction versus peripheral 13) depicts one such lineage: O. xeri + O. susannae isolates speciation, see discussion of Fig. 5). Unfortu- clade (20) whose members inhabit rodents. 114 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119

Fig. 12. Simpliﬁed phylogenetic tree for the pinworm genus Enterobius and relatives (consensus of three trees) coded for coevolutionary analysis; 6, the monophyletic group Enterobius brevicauda þ E. bipapillatus þ E. macaci (modiﬁed from Hugot, 1999).

Fig. 13. Phylogenetic tree for the hookworm genus Oesophagostomum (Conoweberia); 20, O. xeri and O. susannae (modiﬁed from Glen and Brooks, 1985).

2. The current estimate of anthropoid phylogeny cercopithecines). Fig. 16 depicts the host cladogram (Goodman et al., 1998) is shown in Fig. 14. Primary derived by maintaining the phylogenetic relationships BPA (Table 1) produces two equally parsimonious of O. bifurcum in accordance with the requirements of host cladograms (the consensus is shown in Fig. Assumption 0. It diﬀers from the computer (i.e., 15), which depict substantial, but not complete, con- Wagner algorithm)-generated host cladogram only gruence with the phylogenetic relationships among in the placement of Homo2 and Pan2 (PAUP places the Great Apes and between the Great Apes and their these two taxa into a polytomy at the base of sister groups (Old and New World monkeys; com- CO þ CE1) and in having a CI of 100%, which indi- pare the host cladogram with the host phylogeny cates the truly most parsimonious representation of shown in Fig. 14). the data. 3. Secondary BPA (Table 2) produces one most parsimonious host cladogram with a CI of 97%, but that host cladogram places O. bifurcum (species 23) as Discussion the ancestor to species 31, rather than as its sister, vi- olating Assumption 0. This misplacement occurs be- Hugot used Using TreeMap to ﬁt the Enterobius cause of the widespread distribution of O. bifurcum phylogeny to the phylogeny of the Great Apes (missing (it is the only species to inhabit Homo, Pan, and the Hylobates) þ sister group (Old World monkeys). Tree D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 115

Fig. 14. Phylogenetic tree for the Great Apes (Hominidae) and their relatives. The Old World monkey clade includes the Cercopithecinae (e.g., baboons, macaques) and the Colobinae (e.g., colobines, langurs). The New World monkeys include such famous representatives as the howler monkeys and tamarins.

Table 1 Primary matrix listing the distribution of pinworm and hookworm clades among their primate hosts, with the binary codes representing the phylogenetic relationships for both clades Host Species Binary code New World monkeys 8, 24 0000000100 0001000000 0001000000 001 Cercopithecines 6, 16, 21, 23 0000010000 1111010000 1010111111 111 Colobines 7, 21, 22, 23 0000001000 0011000000 1110000001 111 Hylobates 17, 18 ?????????? ????001100 0000011111 111 Pongo 5, 19 0000100000 1111000010 0000000111 111 Gorilla 4, 15 0001000000 0111100000 0000111111 111 Pan 3, 15, 23 0010000001 0111100000 0010111111 111 Homo 1, 2, 15, 23 1100000011 0111100000 0010111111 111 Rodents 20 ?????????? ????000001 0000000011 111 Species 1–8, Enterobius; species 15–24, Oesophagostomum; ?, species missing from the host group. For explanations of parasite species numbers see Figs. 12 and 13.

Fig. 15. Primary BPA of the parasite data. Bold lines, historical backbone of association between the primates and their pinworms and hookworms; dashed lines, host misplaced on the tree, indicating interactions other than cospeciation. 116 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119

Table 2 Secondary BPA matrix listing the distribution of pinworm and hookworm clades among their primate hosts, with binary codes representing the phylogenetic relationships for both clades Host Species Binary code New World monkeys 8, 24 0000000100 0001000000 0001000000 001

Cercopithecines1 21, 23 ?????????? ????000000 1010000001 111 Cercopithecines2 6 0000010000 1111?????? ?????????? ??? Cercopithecines3 16 ?????????? ????010000 0000111111 111 Colobines 7, 21, 22, 23 0000001000 0011000000 1110000001 111

Hylobates1 18 ?????????? ????000100 0000001111 111 Hylobates2 17 ?????????? ????001000 0000011111 111 Pongo 5, 19 0000100000 1111000010 0000000111 111 Gorilla 4, 15 0001000000 0111100000 0000111111 111

Pan1 3, 15 0010000001 0111100000 0000111111 111 Pan2 23 ?????????? ????000000 0010000000 011 Homo1 1, 2, 15 1100000011 0111100000 0000111111 111 Homo2 23 ?????????? ????000000 0010000000 011 Rodents 20 ?????????? ????000001 0000000011 111 The Cercopithecines are listed as three separate taxa, while Hylobates, Pan, and Homo are each listed as two separate taxa. Species 1–8, Enterobius; species 15–24, Oesophagostomum; ?, species missing from the host group. For explanations of parasite species numbers see Figs. 12 and 13.

Fig. 16. Secondary BPA of the parasite data. Bold lines, historical backbone of association between the primates and their pinworms and hookworms; dashed lines and airplanes, postspeciation dispersal by the parasite into new hosts; open circle (ancestor) þ solid circle (peripheral isolate), instance of peripheral isolates speciation via host switching; numbers accompanying slash marks, species codes (from Figs. 12 and 13); gray box, lineage duplication; CE, cercopithecines; CO, colobines; Hylo, Hylobates.

Map found 12 different reconstructions in which the monkeys, and one speciation event within the same host number of posited extra evolutionary events (sorting, (Homo). duplication, host switching) ranged from 11 to 6, indi- Secondary BPA analysis, on the other hand, posits cating that the relationship between the Great Apes and that hookworms and pinworms were already jointly their pinworms is an extremely complex one. Hugot associated in the common ancestor of the anthropoid preferred the hypothesis invoking 6 events because it primates (ancestors 14 and 33 on Fig. 16). There is a was the scenario requiring the fewest events that was strong historical backbone of cospeciation among these consistent with the assumption that the pinworms of organisms (bold lines in Fig. 16). In terms of Enterobius, Gorilla þ Pan þ Homo were monophyletic. This scenario BPA corroborates HugotÕs proposal of a cospeciation posited one sorting event at the base of the Great Ape event occurring with (1) the Pan þ Homo bifurcation tree, two cospeciation events (the Gorilla þ [Pan, Homo] (ancestor 10 giving rise to species 3 and ancestor 9 in and Pan þ Homo splits), one host switch from Gorilla to Fig. 16) and (2) the Gorilla þ sister-group split (ancestor Pongo, one host switch from Gorilla to the Old World 12 giving rise to species 4 and ancestor 10 in Fig. 16). It D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 117 is relevant to note at this point that BPA resolves the this problem further, we need a detailed phylogeny for trichotomous placement of E. lerouxi in favor of the the Old World monkeys and intensive inventories of the cospeciation pattern adopted by Hugot, but does so parasites of all primate species. without an a priori assumption of maximum cospecia- Because BPA treats hosts and parasites as directly tion. BPA, however, places a third co-speciation event at analogous to geographic areas and the species living in the Pongo þ sister group split. The presence of species 5 them, it is relatively easy to add historical biogeo- in Pongo is thus hypothesized to be the result of co- graphical information to coevolutionary findings. Geo- speciation and not of a host switch from Gorilla. There graphic distribution data for these two parasite groups are three apparent cases of lineage duplication in the suggest complex, and as yet incompletely resolved, ancestor of the Old World monkeys þ Great Apes (de- movements of primates throughout the tropical regions noted by the joint occurrence of ancestors 30, 31, and of the Old World. O. bifurcum and O. brumpti occur in 32). As with all lineage duplications, these may represent both Africa and Asia, while O. aculeatum is endemic to ancient cases of sympatric speciation. No lineage du- Asia, possibly suggesting dispersal from Africa to Asia plications are postulated for Enterobius. The secondary (although O. xeri þ O. susannae are endemic to South BPA suggests that there have been six episodes of host Africa). O. blanchardi (species 19), O. raillieti (species switching. The most obvious of these is the occurrence 18), and O. ovatum (species 17) are Asian endemics, of the hookworms O. xeri þ O. susannae (20) in South while O. pachycephalum (species 16) and O. stephano- African rodents, which represents an episode of specia- stomum (species 15) are African endemics, suggesting tion by host switching from apes to rodents. This type of dispersal from Asia to Africa by the common ances- exchange is not unique; Hugot (1999) documented in- tor(s) of, not surprisingly, the African Great Apes (Go- stances of other pinworms (Trypanoxyuris) speciating rilla, Pan, and Homo). As early hominids moved out of after they had transferred from New World monkeys to the African forest into the African savannah, our direct squirrels. The occurrence of O. pachycephalum (species ancestors may have added O. bifurcum (remember, 16) in cercopithecines and of O. ovatum (species 17) and O. bifurcum may have been acquired by the ancestor of O. raillieti (species 18) in Hylobates also appear to rep- humans and chimpanzees) to their parasite repertoire resent episodes of peripheral isolates speciation by host through host switches from Old World monkeys. The switching from one or more species ancestral to the parasites then indicate that Homo moved to Asia, leav- African Great Apes. The only pinworm to host switch ing O. stephanostomum behind in Africa (humans in was species 6 (recall that ‘‘6’’ actually refers to the an- Asia do not have this hookworm). The occurrence of cestor of a monophyletic group of three species in cer- O. bifurcum in humans in Africa and Asia is not sur- copithecines; see Fig. 12). Ancestor 6 appears to have prising; the host cladogram suggests that O. bifurcum colonized the cercopithecines from the Pongo lineage occurred in Old World monkeys on both continents long and not from Gorilla as suggested by Hugot, where it before Homo arrived in Asia. This period may also have subsequently diversified in the new host group. seen the differentiation of the pinworms E. vermicularis The occurrence of O. bifurcum (species 23) in Pan and (species 2) and E. gregorii (species 1), sister species in the Homo represents postspeciation dispersal by the parasite same host produced in the absence of host speciation. from Old World monkeys (dotted lines þ airplanes in This apparently is not an isolated case in the evolu- Fig. 16). Because Homo and Pan are sister groups, it is tion of human parasites. Hoberg et al. (2000) recently actually most parsimonious to postulate that O. bifur- discovered evidence that two cases of speciation by host cum colonized the common ancestor of Pan þ Homo,in switching, correlated with the shift from scavenging to which case a single host switch explains the observed predation (hunting) more than a million years ago in increase in host range. Once there, the hookworm did Africa, explained the association between humans and not speciate again, even though its new host did, pro- tapeworms in the genus Taenia that infect humans (in- ducing the Pan and Homo lineages. The presence of cluding the beef tapeworm, T. saginata, and the pork another hookworm, O. stephanostomum (species 15) in tapeworm, T. solium). Furthermore, they found that Gorilla, Pan, and Homo also represents a case of the T. saginata and T. asiatica, sister species occurring in parasite failing to speciate with its host. In other words, Africa and Asia, respectively, diverged from each other the expanded host ranges of O. stephanostomum and between 750,000 and 1,700,000 years ago, perhaps at the O. bifurcum were gained not by rampant host switching same time that E. vermicularis and E. gregorii were but rather by the parasite species not speciating when its differentiating (but in different parts of the host). host did. O. bifurcum, O. brumpti (species 22), and O. aculeatum (species 21) inhabit various Old World monkeys. At this level of analysis we cannot tell whether Conclusions this large host range was achieved through association by descent (hosts continued to speciate while the para- TreeMap, using the Enterobius þ Great Ape data, sites did not) or widespread colonization. To investigate identified one sorting event at the base of the Great Ape 118 D.R. Brooks, D.A. McLennan / Cladistics 19 (2003) 104–119 tree, two cospeciation events (the Gorilla þ [Pan, Homo] discussions about the issues addressed in this contribu- and Pan þ Homo splits), one host switch from Gorilla to tion. This research was supported by research funding Pongo, one host switch from Gorilla to the Old World from the Natural Sciences and Engineering Research monkeys and one speciation event within the same host Council (NSERC) of Canada to D.R.B. and to D.A.M. (Homo) (six events). Secondary BPA posited three cospeciation events, one host switch, and one speciation event within the same host (five events), providing a more References parsimonious explanation of the data without having to invoke any a priori assumptions about the monophyly of Brooks, D.R., 1979. Testing the context and extent of host–parasite the parasites inhabiting the hosts or the likelihood of coevolution. Syst. Zool. 28, 299–307. cospeciation occurring. It is also noteworthy that, in this Brooks, D.R., 1981. HennigÕs parasitological method: a proposed case, BPA postulates more cospeciation events than does solution. Syst. Zool. 30, 229–249. TreeMap. Our study thus corroborates DowlingÕs (2002) Brooks, D.R., 1985. Historical ecology: a new approach to studying the evolution of ecological associations. Ann. Mo. Bot. Garden 72, fundamental conclusions about the merits of primary 660–680. BPA relative to TreeMap; if the only objective is to pro- Brooks, D.R., 1990. Parsimony analysis in historical biogeography vide a parasite-based estimate of host phylogeny, primary and coevolution: methodological and theoretical update. Syst. BPA should be the preferred method of analysis. This Zool. 39, 14–30. parallels findings by Van Veller and Brooks (2001) that Brooks, D.R., Glen, D.R., 1982. Pinworms and primates: a case study in coevolution. Proc. Helminthol. Soc. Wash. 49, 76–85. primary BPA is better than TreeMap at finding the gen- Brooks, D.R., McLennan, D.A., 1991. Phylogeny, Ecology and eral biogeographic pattern when there have been sub- Behavior: A Research Program in Comparative Biology. Univer- stantial amounts of dispersal. However, DowlingÕs study, sity of Chicago Press, Chicago. like most previous studies purportedly comparing BPA Brooks, D.R., McLennan, D.A., 1993. Parascript: Parasites and the and other methods in a biogeographic context (Morrone Language of Evolution. Smithsonian Inst. Press, Washington, DC. Brooks, D.R., McLennan, D.A., 2002. The Nature of the Organism: and Carpenter, 1994; Morrone and Crisci, 1995; Page, An Evolutionary Voyage Through Space and Time. University of 1990; Page and Charleston, 1998; Ronquist, 1995, 1996, Chicago Press, Chicago. 1997a,b, 1998), failed to consider secondary BPA. As a Brooks, D.R., Van Veller, M.G.P., McLennan, D.A., 2001. How to do result, his conclusions about the shortcomings of BPA BPA, really. J. Biogeogr. 28, 343–358. due to inclusive ORing (i.e., the production of ghost taxa) Cressey, R.F., Collette, B., Russo, J., 1983. Copepods and scombrid fishes: a study in host–parasite relationships. Fish. Bull. 81, 227– are incorrect, as secondary BPA eliminates inclusive 265. ORing from the method (Van Veller and Brooks, 2001). Dowling, A.P.G., 2002. A rigorous test of accuracy between Brooks In addition, secondary BPA provides a more complete Parsimony Analysis and TREEMAP, the two most commonly used account of the evolutionary associations between the methods for determining coevolutionary patterns. Cladistics 18, parasite groups and their hosts than does either TreeMap 416–435. Funk, D.J., 1998. Isolating a role for natural selection in speciation: or primary BPA, without sacrificing any indirectly gen- host adaptation and sexual isolation in Neochlamisus bebbianae leaf erated information about host phylogeny. Our analysis of beetles. 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