PARALLEL PHYLOGENIES: RECONSTRUCTING THE HISTORY OF HOST-PARASITE ASSEMBLAGES

Abstract— A method for reconstructing the history of a host-parasite assemblage is described. This method has the advantage of making explicit the relationship between the host and parasite trees, and it allows a visually intuitive representation of that history. It also enables host switches to be incorporated as an explanation of the observed pattern of host-parasite associations, without the spurious overestimates of the number of host switches that can be obtained using Brooks parsimony analysis (BPA). Reconstructions that maximize the number of cospeciation events have the greatest explanatory power and are hence preferred over reconstructions with fewer cospeciation events. A heuristic algorithm to find a single maximal reconstruction, and an exact algorithm to find all such reconstructions are presented. Two empirical applications of the method are given.     

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.     

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.     

Evolutionary relationships, cospeciation, and host switching in avian malaria parasites

We used phylogenetic analyses of cytochrome b sequences of malaria parasites and their avian hosts to assess the coevolutionary relationships between host and parasite lineages. Many lineages of avian malaria parasites have broad host distributions, which tend to obscure cospeciation events. The hosts of a single parasite or of closely related parasites were nonetheless most frequently recovered from members of the same host taxonomic family, more so than expected by chance. However, global assessments of the relationship between parasite and host phylogenetic trees, using Component and ParaFit, failed to detect significant cospeciation. The event-based approach employed by TreeFitter revealed significant cospeciation and duplication with certain cost assignments for these events, but host switching was consistently more prominent in matching the parasite tree to the host tree. The absence of a global cospeciation signal despite conservative host distribution most likely reflects relatively frequent acquisition of new hosts by individual parasite lineages. Understanding these processes will require a more refined species concept for malaria parasites and more extensive sampling of parasite distributions across hosts. If parasites can disperse between allopatric host populations through alternative hosts, cospeciation may not have a strong influence on the architecture of host-parasite relationships. Rather, parasite speciation may happen more often in conjunction with the acquisition of new hosts followed by divergent selection between host lineages in sympatry. Detailed studies of the phylogeographic distributions of hosts and parasites are needed to characterize these events.     

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.     

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.     

Plant-insect interactions: double-dating associated insect and plant lineages reveals asynchronous radiations

An increasing number of plant-insect studies using phylogenetic analysis suggest that cospeciation events are rare in plant-insect systems. Instead, nonrandom patterns of phylogenetic congruence are produced by phylogenetically conserved host switching (to related plants) or tracking of particular resources or traits (e.g., chemical). The dominance of host switching in many phytophagous insect groups may make the detection of genuine cospeciation events difficult. One important test of putative cospeciation events is to verify whether reciprocal speciation is temporally plausible. We explored techniques for double-dating of both plant and insect phylogenies. We use dated molecular phylogenies of a psyllid (Hemiptera)-Genisteae (Fabaceae) system, a predominantly monophagous insect-plant association widespread on the Atlantic Macaronesian islands. Phylogenetic reconciliation analysis suggests high levels of parallel cladogenesis between legumes and psyllids. However, dating using molecular clocks calibrated on known geological ages of the Macaronesian islands revealed that the legume and psyllid radiations were not contemporaneous but sequential. Whereas the main plant radiation occurred some 8 million years ago, the insect radiation occurred about 3 million years ago. We estimated that >60% of the psyllid speciation has resulted from host switching between related hosts. The only evidence for true cospeciation is in the much more recent and localized radiation of genistoid legumes in the Canary Islands, where the psyllid and legume radiations have been partially contemporaneous. The identification of specific cospeciation events over this time period, however, is hindered by the phylogenetic uncertainty in both legume and psyllid phylogenies due to the apparent rapidity of the species radiations.     

Inferring processes of coevolutionary diversification in a community of Panamanian strangler figs and associated pollinating wasps*

The fig and pollinator wasp obligate mutualism is diverse (～750 described species), ecologically important, and ancient (～80 Ma). Once thought to be an example of strict one‐to‐one cospeciation, current thinking suggests genera of pollinator wasps codiversify with corresponding sections of figs, but the degree to which cospeciation or other processes contribute to the association at finer scales is unclear. Here, we use genome‐wide sequence data from a community of Panamanian strangler figs and associated wasp pollinators to estimate the relative contributions of four evolutionary processes generating cophylogenetic patterns in this mutualism: cospeciation, host switching, pollinator speciation, and pollinator extinction. Using a model‐based approach adapted from the study of gene family evolution, our results demonstrate the importance of host switching of pollinator wasps at this fine phylogenetic and regional scale. Although we estimate a modest amount of cospeciation, simulations reveal the number of putative cospeciation events to be consistent with what would be expected by chance. Additionally, model selection tests identify host switching as a critical parameter for explaining cophylogenetic patterns in this system. Our study demonstrates a promising approach through which the history of evolutionary association between interacting lineages can be rigorously modeled and tested in a probabilistic phylogenetic framework.     

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.     

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.     

Patterns of host–parasite associations in tropical lice and their passerine hosts in Cameroon

Coevolutionary processes that drive the patterns of host–parasite associations can be deduced through congruence analysis of their phylogenies. Feather lice and their avian hosts have previously been used as typical model systems for congruence analysis; however, such analyses are strongly biased toward nonpasserine hosts in the temperate zone. Further, in the Afrotropical region especially, cospeciation studies of lice and birds are entirely missing. This work supplements knowledge of host–parasite associations in lice using cospeciation analysis of feather lice (genus Myrsidea and the Brueelia complex) and their avian hosts in the tropical rainforests of Cameroon. Our analysis revealed a limited number of cospeciation events in both parasite groups. The parasite–host associations in both louse groups were predominantly shaped by host switching. Despite a general dissimilarity in phylogeny for the parasites and hosts, we found significant congruence in host–parasite distance matrices, mainly driven by associations between Brueelia lice and passerine species of the Waxbill (Estrildidae) family, and Myrsidea lice and their Bulbul (Pycnonotidae) host species. As such, our study supports the importance of complex biotic interactions in tropical environments.     

Host shift and cospeciation rate estimation from co‐phylogenies

Host shifts can cause novel infectious diseases, and is a key process in diversification. Disentangling the effects of host shift vs. those of cospeciation is non‐trivial as both can result in phylogenic congruence. We develop a new framework based on network analysis and Approximate Bayesian Computation to quantify host shift and cospeciation rates in host‐parasite systems. Our method enables estimation of the expected time to the next host shift or cospeciation event. We then apply it to avian haemosporidian parasite systems and to the pocket gophers‐chewing lice system, and demonstrate that both host shift and cospeciation can be reliably estimated by our method. We confirm that host shifts have shaped the evolutionary history of avian haemosporidian parasites and have played a minor role in the gopher–chewing lice system. Our method is promising for predicting the rate of potential host shifts and thus the emergence of novel infectious diseases.     

Monogeneans of West African cichlid fish: evolution and cophylogenetic interactions

The goals of this paper were to investigate phylogenetic and evolutionary patterns of cichlid fish from West Africa and their Cichlidogyrus and Scutogyrus monogenean parasites, to uncover the presence of host-parasite cospeciation and to assess the level of morphological adaptation in parasites. This required the following steps, each one representing specific objectives of this paper: (1) to build phylogenetic trees for Cichlidogyrus and Scutogyrus species based on ribosomal DNA sequences, (2) to investigate phylogenetic relationships within West African cichlid fish based on the analysis of mitochondrial cytochrome b DNA sequences, (3) to investigate host-parasite cophylogenetic history to gain clues on parasite speciation process, and (4) to investigate the link between the morphology of the attachment apparatus and parasite phylogeny. Phylogenetic analyses supported the monophyletic origin of the Cichlidogyrus/Scutogyrus group, and suggested that Cichlidogyrus is polyphyletic and that Scutogyrus is monophyletic. The phylogeny of Cichlidae supported the separation of mouthbrooders and substrate-brooders and is consistent with the hypothesis that the mouthbrooding behavior of Oreochromis and Sarotherodon evolved from substrate-brooding behavior. The mapping of morphological characters of the haptor onto the parasite phylogenetic tree suggests that the attachment organ has evolved from a very simple form to a more complex one. The cophylogenetic analyses indicated a significant fit between trees using distance-based tests, but no significant cospeciation signal using tree-based tests, suggesting the presence of parasite duplications and host switches on related host species. This shed some light on the diversification process of Cichlidogyrus species parasitizing West African cichlids.     

Diversification and host switching in avian malaria parasites

The switching of parasitic organisms to novel hosts, in which they may cause the emergence of new diseases, is of great concern to human health and the management of wild and domesticated populations of animals. We used a phylogenetic approach to develop a better statistical assessment of host switching in a large sample of vector-borne malaria parasites of birds (Plasmodium and Haemoproteus) over their history of parasite-host relations. Even with sparse sampling, the number of parasite lineages was almost equal to the number of avian hosts. We found that strongly supported sister lineages of parasites, averaging 1.2% sequence divergence, exhibited highly significant host and geographical fidelity. Event-based matching of host and parasite phylogenetic trees revealed significant cospeciation. However, the accumulated effects of host switching and long distance dispersal cause these signals to disappear before 4% sequence divergence is achieved. Mitochondrial DNA nucleotide substitution appears to occur about three times faster in hosts than in parasites, contrary to findings on other parasite-host systems. Using this mutual calibration, the phylogenies of the parasites and their hosts appear to be similar in age, suggesting that avian malaria parasites diversified along with their modern avian hosts. Although host switching has been a prominent feature over the evolutionary history of avian malaria parasites, it is infrequent and unpredictable on time scales germane to public health and wildlife management.     

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.     

Evolutionary relationships between digeneans of the family Brachycladiidae Odhner, 1905 and their marine mammal hosts: A cophylogenetic study

Cophylogenetic studies examine the congruence between host and parasite phylogenies. There are few studies that quantify the relative contribution of coevolutionary events, i.e. duplication, loss, failure-to-diverge, host-switching and spreading in trophically-transmitted parasites at the marine realm. We addressed this issue in the Brachycladiidae, a cosmopolitan digenean family specific to marine mammals. We used, for the first time, distance-based and event-based methods to explicitly test the coevolutionary events that have shaped the current brachycladiid-marine mammal associations. Parasite phylogeny was constructed using mtDNA ND3 sequences of nine brachycladiid species, and host phylogeny using cytochrome b sequences of 104 mammalian species. A total of 50 host-parasite links were identified. Distance-based methods supported the hypothesis of a global non-random association of host and parasite phylogenies. Significant individual links (i.e., 24 out of 50) were those related to Campula oblonga, Nasitrema delphini, N. globicephalae and Brachycladium atlanticum and their associated taxa from the Delphinoidea. Regarding event-based methods, we explored 54 schemes using different combinations of costs for each potential coevolutionary event. Three coevolutionary scenarios were identified across all schemes and in all cases the number of loss events (87–156) was the most numerous, followed by failure-to-diverge (40), duplication (3–6), host-switching (0–3) and cospeciation (0–2). We developed a framework to interpret the evolution of this host-parasite system and confirmed that failure-to-diverge and colonization with or without subsequent diversification could have been decisive in the establishment of the associations between brachycladiids and marine mammals.     

Pseudocospeciation of the mycoparasite Cosmospora with their fungal hosts

Species of Cosmospora are parasites of other fungi (mycoparasites), including species belonging to the Xylariales. Based on prior taxonomic work, these fungi were determined to be highly host specific. We suspected that the association of Cosmospora and their hosts could not be a result of random chance, and tested the cospeciation of Cosmospora and the their hosts with contemporary methods (e.g., ParaFit, PACo, and Jane). The cophylogeny of Cosmospora and their hosts was found to be congruent, but only host‐parasite links in more recent evolutionary lineages of the host were determined as coevolutionary. Reconciliation reconstructions determined at least five host‐switch events early in the evolution of Cosmospora. Additionally, the rates of evolution between Cosmospora and their hosts were unequal. This pattern is more likely to be explained by pseudocospeciation (i.e., host switches followed by cospeciation), which also produces congruent cophylogenies.     

STATISTICAL TESTS OF HOST-PARASITE COSPECIATION

A history of cospeciation (synchronous speciation) among ecologically associated, but otherwise distantly related, species is often revealed by a strong correspondence of their phylogenies. In this paper, we present several tests of cospeciation that use maximum-likelihood and Bayesian methods of phylogenetic estimation. The hypotheses tested include: (1) topological agreement of phylogenies for coevolving groups; (2) identical speciation times of associated species; and (3) identical evolutionary rates in genes of associated species. These tests are applied to examine a possible instance of host-parasite coevolution among pocket gophers and lice using mitochondrial COI DNA sequences. The observed differences between gopher and louse trees cannot be explained by sampling error and are consistent with a rate of host switching about one-third the host speciation rate. A subset of the gopher-louse data is consistent with a common history of evolution (i.e., the topologies and speciation times are identical). However, the relative rate of nucleotide substitution is two to four times higher in the lice than in the gophers.     

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.     

Evolutionary history of nematodes associated with sweat bees

Organisms that live in close association with other organisms make up a large part of the world’s diversity. One driver of this diversity is the evolution of host-species specificity, which can occur via reproductive isolation following a host-switch or, given the correct circumstances, via cospeciation. In this study, we explored the diversity and evolutionary history of Acrostichus nematodes that are associated with halictid bees in North America. First, we conducted surveys of bees in Virginia, and found six halictid species that host Acrostichus. To test the hypothesis of cospeciation, we constructed phylogenetic hypotheses of Acrostichus based on three genes. We found Acrostichus puri and Acrostichus halicti to be species complexes comprising cryptic, host-specific species. Although several nodes in the host and symbiont phylogenies were congruent and tests for cospeciation were significant, the host’s biogeography, the apparent patchiness of the association across the host’s phylogeny, and the amount of evolution in the nematode sequence suggested a mixture of cospeciation, host switching, and extinction events instead of strict cospeciation. Cospeciation can explain the relationships between Ac. puri and its augochlorine hosts, but colonization of Halictus hosts is more likely than cospeciation. The nematodes are vertically transmitted, but sexual transmission is also likely. Both of these transmission modes may explain host-species specificity and congruent bee and nematode phylogenies. Additionally, all halictid hosts come from eusocial or socially polymorphic lineages, suggesting that sociality may be a factor in the suitability of hosts for Acrostichus.