A priori and a posteriori methods in comparative evolutionary studies of host–parasite associations

Brooks parsimony analysis (BPA) and reconciliation methods in studies of host–parasite associations differ fundamentally, despite using the same null hypothesis. Reconciliation methods may eliminate or modify input data to maximize fit of single parasite clades to a null hypothesis of cospeciation, by invoking different a priori assumptions, including a known host phylogeny. By examining the degree of phylogenetic congruence among multiple parasite clades, using hosts as analogs of taxa but not presuming a host phylogeny or any degree of cospeciation a priori, BPA modifies the null hypothesis of cospeciation if necessary to maintain the integrity of the input data. Two exemplars illustrate critical empirical differences between reconciliation methods and BPA: (1) reconciliation methods rather than BPA may select the incorrect general host cladogram for a set of data from different clades of parasites, (2) BPA rather than reconciliation methods provides the most parsimonious interpretation of all available data, and (3) secondary BPA, proposed in 1990, when applied to data sets in which host‐switching produces hosts with reticulate histories, provides the most parsimonious and biologically realistic interpretations of general host cladograms. The extent to which these general host cladograms, based on cospeciation among different parasite clades inhabiting the same hosts, correspond to host phylogeny can be tested, a posteriori, by comparison with a host phylogeny generated from nonparasite data. These observations lead to the conclusion that BPA and reconciliation methods are designed to implement different research programs based on different epistemologies. BPA is an a posteriori method that is designed to assess the host context of parasite speciation events, whereas reconciliation methods are a priori methods that are designed to fit parasite phylogenies to a host phylogeny. Host‐switching events are essential for explaining complex histories of host–parasite associations. BPA assumes coevolutionary complexity (historical contingency), relying on parsimony as an a posteriori explanatory tool to summarize complex results, whereas reconciliation methods, which embody formalized assumptions of maximum cospeciation, are based on a priori conceptual parsimony. Modifications of basic reconciliation methods, embodied in TreeMap 1.0 and TreeMap 2.02, represent the addition of weighting schemes in which the researcher specifies allowed departures from cospeciation a priori, with the result that TreeMap results more closely agree with BPA results than do reconciled tree analysis results.     

Ending a decade of deception: a valiant failure, a not-so-valiant failure, and a success story

Prior studies involving two methods, Brooks Parsimony Analysis (BPA) and TreeMap, have found BPA to be the more reliable method. Recent criticisms leveled at these studies argue that the tests were unfairly created and biased in favor of BPA. The authors of a recent critique offered new exemplars to demonstrate flaws in BPA, plus a simple fix to correct the flaws found in TreeMap. A re‐evaluation of their exemplars clearly shows that the authors' calculations are incorrect, their understanding of the methods is lacking, and that their simple fix does not work. Additional analyses using TreeMap 2.02 are run to show that TreeMap 2.02, like TreeMap 1.0, cannot adequately deal with widespread parasites, contrary to the claims of its supporters. Furthermore, the exemplars corroborate previous findings that BPA, when calculated correctly, is more reliable than TreeMap1.0 and TreeMap 2.02 and therefore the method of choice in coevolutionary and biogeographic studies.     

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

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 précis 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 Dowling's 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.     

Computational aspects of host-parasite phylogenies

Computational aspects of host-parasite phylogenies form part of a set of general associations between areas and organisms, hosts and parasites, and species and genes. The problem is not new and the commonalities of exploring vicariance biogeography (organisms tracking areas) and host-parasite co-speciation (parasites tracking hosts) have been recognised for some time. Methods for comparing host-parasite phylogenies are now well established and fall within two basic categories defined in terms of the way the data are interpreted in relation to the comparison of host-parasite phylogenies, so-called a posteriori, eg Brooks' Parsimony Analysis (BPA), or a priori, eg reconciled trees and other model-based methods, as implemented in the program TreeMap; the relative merits of the two philosophies inherent in these two approaches remain hotly debated. This paper reviews the computational methods currently available to analyse host-parasite relationships.     

Testing the accuracy of TreeMap and Brooks parsimony analyses of coevolutionary patterns using artificial associations

Brooks parsimony analysis and TreeMap are the two most commonly used methods and are tested using artificially evolved host–parasite associations with varying amounts of coevolutionary events occurring between the two “phylogenies.” The purpose is to test the precision with which each method recovers the true coevolutionary history. The reconstructions recovered by each method are compared against the original test case to determine how closely the reconstruction resembles the artificially created coevolutionary history. Brooks parsimony analysis is found to be consistently less prone to gross overestimation of coevolutionary events and misleading results. Brooks parsimony analysis performs better overall because it is more adept at dealing with host-switching events, both between and within lineages leading to widespread parasite taxa, which provides enough evidence for implementing Brooks parsimony analysis instead of TreeMap in coevolutionary studies.     

Comparing host and parasite phylogenies: gyrodactylus flatworms jumping from goby to goby

The combination of exceptionally high species diversity, high host specificity, and a complex reproduction system raises many questions about the underlying mechanisms triggering speciation in the flatworm genus Gyrodactylus. The coevolutionary history with their goby hosts was investigated using both topology- and distance-based approaches; phylogenies were constructed of the V4 region of the 18S rRNA and the complete ITS rDNA region for the parasites, and 12S and 16S mtDNA fragments for the hosts. The overall fit between both trees was significant according to the topology-based programs (TreeMap 1.0, 2.0 beta and TreeFitter), but not according to the timed analysis in TreeMap 2.0 beta and the distance-based method (ParaFit). An absolute timing of speciation events in host and parasite ruled out the possibility of synchronous speciation for the gill parasites, favouring the distance-based result. Based on this information together with the biological background of host and parasite, the following TreeMap solution was selected. The group of gill parasites evolved from a host switch from G. arcuatus, parasitizing the three-spined stickleback onto the gobies, followed by several host-switching events among the respective goby hosts. The timing of these events is estimated to date back to the Late Pleistocene, suggesting a role for refugia-mediated mixing of parasite species. In contrast, it is suggested that co-speciation in the fin-parasites resulted in several host-associated species complexes. This illustrates that phylogenetically conserved host-switching mimics the phylogenetic signature of co-speciation, confounding topology-based programs.     

Have chondracanthid copepods co-speciated with their teleost hosts?

Chondracanthid copepods parasitise many teleost species and have a mobile larval stage. It has been suggested that copepod parasites, with free-living infective stages that infect hosts by attaching to their external surfaces, will have co-evolved with their hosts. We examined copepods from the genus Chondracanthus and their teleost hosts for evidence of a close co-evolutionary association by comparing host and parasite phylogenies using TreeMap analysis. In general, significant co-speciation was observed and instances of host switching were rare. The prevalence of intra-host speciation events was high relative to other such studies and may relate to the large geographical distances over which hosts are spread.     

A Bayesian framework for the analysis of cospeciation

Abstract.— Information on the history of cospeciation and host switching for a group of host and parasite species is contained in the DNA sequences sampled from each. Here, we develop a Bayesian framework for the analysis of cospeciation. We suggest a simple model of host switching by a parasite on a host phylogeny in which host switching events are assumed to occur at a constant rate over the entire evolutionary history of associated hosts and parasites. The posterior probability density of the parameters of the model of host switching are evaluated numerically using Markov chain Monte Carlo. In particular, the method generates the probability density of the number of host switches and of the host switching rate. Moreover, the method provides information on the probability that an event of host switching is associated with a particular pair of branches. A Bayesian approach has several advantages over other methods for the analysis of cospeciation. In particular, it does not assume that the host or parasite phylogenies are known without error; many alternative phylogenies are sampled in proportion to their probability of being correct.     

Escaping the matrix: a new algorithm for phylogenetic comparative studies of co-evolution

An algorithm for generating host cladograms from parasite‐host cladograms derived from parasite phylogenies, Phylogenetic Analysis for Comparing Trees (PACT), is described. PACT satisfies Assumption 0, that all the information in each parasite‐host cladogram must be used in a co‐evolutionary analysis, and that the host relationships depicted in the final host cladogram must be logically consistent with the phylogenetic relationships depicted in every part of every parasite‐host cladogram used to construct the host cladogram. It accounts for cases of speciation by host switching and expansion of host range, and reticulated host relationships, in addition to co‐speciation, sympatric speciation, and extinction in all input parasite‐host cladograms, and does so without a priori weighting schemes and without a posteriori manipulation of the data.     

Marine Area Relationships from Twenty Sponge Phylogenies. A Comparison of Methods and Coding Strategies

Published phylogenies of 20 marine sponge groups are used to build general area cladograms of marine areas of endemism under three different methods for which algorithms adapted for personal computers are available, viz. COMPONENT, BPA and TAS, and two different coding strategies, Assumption 0 (A0) and "no assumption" (NA). The latter is a recently proposed procedure for handling the distributions of widespread taxa by treating these as separate areas of endemism, rather than as suites of smaller constituent areas. The 20 phylogenies contained large numbers of problem data which prevented an exhaustive search for all possible equally "best" general area cladograms. The Nelson consensus trees and their equivalents in parsimony analysis for all six attempts (viz. three different methodologies under two different coding strategies) were compared using their fit with the 20 sponge phylogenies as a measure of quality. Fit was determined using the number of "cospeciations" between a general area cladogram and a taxon area cladogram computed with TreeMap 1.0. No single method or coding strategy yielded a clearly better fit, each cladogram fitting variously better or worse with various phylogenies. In general, fit with NA coding was higher than with A0 coding, but random tree tests failed to generate statistically significant support for the conclusion that NA coding improves fit. Assuming that available sponge phylogenies are representative of marine benthic groups, software and hardware limitations are serious obstacles to a successful development of marine general area cladograms under any method or coding strategy.     

Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly

Studies of cophylogenetic associations between hosts and parasites have become increasingly common. Historically, congruence between host and parasite phylogenies has been seen as evidence for cospeciation. Analyses of such coevolutionary relationships, however, are made extremely difficult by the complex interplay of cospeciation, host switching, sorting (extinction), duplication (intrahost speciation) and inertia (lack of parasite speciation) events, all of which may produce incongruence between host and parasite phylogenies. Here we review several methods of analysing cospeciation. We illustrate these methods with an example from a Procellariiformes (seabird) and chewing louse (Halipeurus) association.     

Phylogenetic analysis of European species of Proteocephalus (Cestoda: Proteocephalidea): compatibility of molecular and morphological data, and parasite-host coevolution.

The phylogeny of European species of the tapeworm genus Proteocephalus was studied, based on partial 18S rDNA and morphological data. The group was found to be monophyletic. The analysis showed a low informative value of available morphological characters in comparison with molecular data. The morphological matrix resulted in a poorly resolved tree which is, however, compatible with the topology (Proteocephalus osculatus (Proteocephalus torulosus (Proteocephalus macrocephalus, Proteocephalus filicollis) (Proteocephalus tetrastomus, Proteocephalus percae, Proteocephalus longicollis))) based on the 18S rDNA data. A comparison performed by the program TreeMap showed a lack of significant congruency between parasite and host phylogenies. Therefore, the distribution of species in their hosts appears to be independent of the phylogeny and it is likely to be a result of host-switching, rather than co-speciation events.     

Multiple cophylogenetic analyses reveal frequent cospeciation between pelecaniform birds and Pectinopygus lice

Lice in the genus Pectinopygus parasitize a single order of birds (Pelecaniformes). To examine the degree of congruence between the phylogenies of 17 Pectinopygus species and their pelecaniform hosts, sequences from mitochondrial 12S rRNA, 16S rRNA, COI, and nuclear wingless and EF1-alpha genes (2290 nucleotides) and from mitochondrial 12S rRNA, COI, and ATPases 8 and 6 genes (1755 nucleotides) were obtained for the lice and the birds, respectively. Louse data partitions were analyzed for evidence of incongruence and evidence of long-branch attraction prior to cophylogenetic analyses. Host-parasite coevolution was studied by different methods: TreeFitter, TreeMap, ParaFit, likelihood-ratio test, data-based parsimony method, and correlation of coalescence times. All methods agree that there has been extensive cospeciation in this host-parasite system, but the results are sensitive to the selection of different phylogenetic hypotheses and analytical methods for evaluating cospeciation. Perfect congruence between phylogenies is not found in this association, probably as a result of occasional host switching by the lice. Errors due to phylogenetic reconstruction methods, incorrect or incomplete taxon sampling, or to different loci undergoing different evolutionary histories cannot be rejected, thus emphasizing the need for improved cophylogenetic methodologies.     

When do parasites fail to speciate in response to host speciation?

Cospeciation generally increases the similarity between host and parasite phylogenies. Incongruence between host and parasite phylogenies has previously been explained in terms of host switching, sorting, and duplication events. Here, we describe an additional process, failure of the parasite to speciate in response to host speciation, that may be important in some host-parasite systems. Failure to speciate is likely to occur when gene flow among parasite populations is much higher than that of their hosts. We reconstructed trees from mitochondrial and nuclear DNA sequences for pigeons and doves (Aves: Columbiformes) and their feather lice in the genus Columbicola (Insecta: Phthiraptera). Although comparisons of the trees from each group revealed a significant amount of cospeciation, there was also a significant degree of incongruence. Cophylogenetic analyses generally indicated that host switching may be an important process in the history of this host-parasite association. Using terminal sister taxon comparisons, we also identified three apparent cases where the host has speciated but the associated parasite has not. In two of these cases of failure to speciate, these comparisons involve allopatric sister taxa of hosts whose lice also occur on hosts sympatric with both of the allopatric sisters. These additional hosts for generalist lice may promote gene flow with lice on the allopatric sister species. Relative rate comparisons for the mitochondrial cytochrome oxidase I gene indicate that molecular substitution occurs about 11 times faster in lice than in their avian hosts.     

Biogeography explains cophylogenetic patterns in toucan chewing lice

Historically, comparisons of host and parasite phylogenies have concentrated on cospeciation. However, many of these comparisons have demonstrated that the phylogenies of hosts and parasites are seldom completely congruent, suggesting that phenomena other than cospeciation play an important role in the evolution of host-parasite assemblages. Other coevolutionary phenomena, such as host switching, parasite duplication (speciation on the host), sorting (extinction), and failure to speciate can also influence host-parasite assemblages. Using mitochondrial and nuclear protein-coding DNA sequences, I reconstructed the phylogeny of ectoparasitic toucan chewing lice in the Austrophilopterus cancellosus subspecies complex and compared this phylogeny with the phylogeny of the hosts, the Ramphastos toucans, to reconstruct the history of coevolutionary events in this host-parasite assemblage. Three salient findings emerged. First, reconstructions of host and louse phylogenies indicate that they do not branch in parallel, and their cophylogenetic history shows little or no significant cospeciation. Second, members of monophyletic Austrophilopterus toucan louse lineages are not necessarily restricted to monophyletic host lineages. Often, closely related lice are found on more distantly related but sympatric toucan hosts. Third, the geographic distribution of the hosts apparently plays a role in the speciation of these lice. These results suggest that for some louse lineages biogeography may be more important than host associations in structuring louse populations and species, particularly when host life history (e.g., hole nesting) or parasite life history (e.g., phoresis) might promote frequent host switching events between syntopic host species. These findings highlight the importance of integrating biogeographic information into cophylogenetic studies.     

Integrating phylogenomic and population genomic patterns in avian lice provides a more complete picture of parasite evolution

Parasite diversity accounts for most of the biodiversity on earth, and is shaped by many processes (e.g., cospeciation, host switching). To identify the effects of the processes that shape parasite diversity, it is ideal to incorporate both deep (phylogenetic) and shallow (population) perspectives. To this end, we developed a novel workflow to obtain phylogenetic and population genetic data from whole genome sequences of body lice parasitizing New World ground‐doves. Phylogenies from these data showed consistent, highly resolved species‐level relationships for the lice. By comparing the louse and ground‐dove phylogenies, we found that over long‐term evolutionary scales their phylogenies were largely congruent. Many louse lineages (both species and populations) also demonstrated high host‐specificity, suggesting ground‐dove divergence is a primary driver of their parasites’ diversity. However, the few louse taxa that are generalists are structured according to biogeography at the population level. This suggests dispersal among sympatric hosts has some effect on body louse diversity, but over deeper time scales the parasites eventually sort according to host species. Overall, our results demonstrate that multiple factors explain the patterns of diversity in this group of parasites, and that the effects of these factors can vary over different evolutionary scales. The integrative approach we employed was crucial for uncovering these patterns, and should be broadly applicable to other studies.     

A cophylogenetic perspective of RNA-virus evolution

The extent to which viruses and their hosts codiverge remains an open question, given that numerous cases of both "cospeciation" and horizontal switching have recently been documented. DNA viruses that form persistent infections are thought to be the most likely candidates for phylogenetic congruence. Phylogenetic reconciliation analysis was used to compare established phylogenies for four RNA viruses and their hosts. The analysis employs a cophylogeny mapping technique, implemented in TreeMap v2.0, to find the most parsimonious combinations of evolutionary events able to reconcile any incongruence. This technique is guaranteed to recover all potentially optimal solutions to the reconciled tree and specifically tests the null hypothesis that an associate phylogeny is no more congruent with a host phylogeny than would be a random tree with the same taxon set. Phylogenies for Hantavirus, Spumavirus, and avian sarcoma leukosis virus were found to be significantly similar to their host trees, whereas Lyssavirus and Arenavirus displayed no significant congruence. These results demonstrate that RNA viruses are able to form stable associations with their hosts over evolutionary time scales and that the details of such associations are consistent with persistent infection being a necessary but not sufficient precondition.     

Coevolution between Lamellodiscus (Monogenea: Diplectanidae) and Sparidae (Teleostei): the study of a complex host-parasite system

Abstract.— Host-parasite coevolution was studied between Sparidae (Teleostei) fishes and their parasites of the genus Lamellodiscus (Monogenea, Diplectanidae) in the northwestern Mediterranean Sea. Molecular phylogenies were reconstructed for both groups. The phylogenetic tree of the Sparidae was obtained from previously published 16S mitochondrial DNA (mtDNA) sequences associated with new cytochrome-b mtDNA sequences via a "total evidence" procedure. The phylogeny of Lamellodiscus species was reconstructed from 18S rDNA sequences that we obtained. Host-parasite coevolution was studied through different methods: TreeFitter, TreeMap, and a new method, ParaFit. If the cost of a host switch is not assumed to be high for parasites, all methods agree on the absence of widespread cospeciation processes in this host-parasite system. Host-parasite associations were interpreted to be due more to ecological factors than to coevolutionary processes. Host specificity appeared not to be related to host-parasite cospeciation.     

Co-evolutionary relationships between the nematode subfamily Cloacininae and its macropodid marsupial hosts

Morphologically based phylogenies of the cloacinine genera Cyclostrongylus, Macropostrongylus, Pharyngostrongylus, Popovastrongylus, Rugopharynx, Thallostonema, Wallabinema, and Zoniolaimus were constructed and compared with the phylogeny of their respective macropodid hosts. These comparisons show some evidence of co-speciation. However, there was little consistency among trees of different nematode genera, parasite species were scattered amongst hosts and basal parasite taxa were, in some instances, parasitic in hosts belonging to derived clades. A cladistic analysis, using as characters 208 cloacinine nematode species found in 23 species of host, produced a tree largely resembling that of the host tree but with significant differences explainable by host switching among macropodids occupying similar habitat. Nematodes were moderately host-specific, but some species occurred in three or more distantly related host species indicating a degree of host switching. The results are more consistent with the hypothesis of a colonisation of macropodid hosts by cloacinine nematodes rather than a prolonged period of co-speciation although alternative interpretations of the data are also considered.     

毛蚜属Chaitophorus蚜虫(半翅目:蚜科:毛蚜亚科)与初级内共生菌Buchnera的演化关系

【目的】蚜虫体内共生菌种类丰富,二者关系十分密切。几乎所有蚜虫都具有一类专性的初级内共生菌Buchnera aphidicola,二者的专性共生关系使蚜虫-Buchnera成为研究共生关系演化的理想模型。本研究对蚜虫-Buchnera在低级阶元水平上的"平行演化假说"进行了验证。【方法】选取在杨属Populus或柳属Salix植物上营同寄主全周期生活的毛蚜属Chaitophorus蚜虫作为研究对象,基于不同来源的分子标记(蚜虫线粒体基因、核基因和内共生菌基因),运用最大似然法和贝叶斯法重建蚜虫和Buchnera的系统树,并利用Tree Map、Jane和Para Fit检验二者是否具有协同系统发生关系。【结果】Tree Map和Jane分析检测到毛蚜属蚜虫与Buchnera具有显著的共成种信号,Para Fit分析结果表明二者的总体关联极为显著。【结论】毛蚜属蚜虫与其初级内共生菌Buchnera在种级及以下水平上符合"平行演化假说",并且二者的演化关系不会受到寄主植物差异的影响。