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.     

Differentiating between hypotheses of lineage sorting and introgression in New Zealand alpine cicadas (Maoricicada Dugdale)

Lineage sorting and introgression can lead to incongruence among gene phylogenies, complicating the inference of species trees for large groups of taxa that have recently and rapidly radiated. In addition, it can be difficult to determine which of these processes is responsible for this incongruence. We explore these issues with the radiation of New Zealand alpine cicadas of the genus Maoricicada Dugdale. Gene trees were estimated from four putative independent loci: mitochondrial DNA (2274 nucleotides), elongation factor 1-alpha (1275 nucleotides), period (1709 nucleotides), and calmodulin (678 nucleotides). We reconstructed phylogenies using maximum likelihood and Bayesian methods from 44 individuals representing the 19 species and subspecies of Maoricicada and two outgroups. Species-level relationships were reconstructed using a novel extension of gene tree parsimony, whereby gene trees were weighted by their Bayesian posterior probabilities. The inferred gene trees show marked incongruence in the placement of some taxa, especially the enigmatic forest and scrub dwelling species, M. iolanthe. Using the species tree estimated by gene tree parsimony, we simulated coalescent gene trees in order to test the null hypothesis that the nonrandom placement of M. iolanthe among gene trees has arisen by chance. Under the assumptions of constant population size, known generation time, and panmixia, we were able to reject this null hypothesis. Furthermore, because the two alternative placements of M. iolanthe are in each case with species that share a similar song structure, we conclude that it is more likely that an ancient introgression event rather than lineage sorting has caused this incongruence.     

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.     

Cophylogeny on a fine scale: Geomydoecus chewing lice and their pocket gopher hosts, Pappogeomys bulleri

Many species of pocket gophers and their ectoparasitic chewing lice have broadly congruent phylogenies, indicating a history of frequent codivergence. For a variety of reasons, phylogenies of codiverging hosts and parasites are expected to be less congruent for more recently diverged taxa. This study is the first of its scale in the pocket gopher and chewing louse system, with its focus entirely on comparisons among populations within a single species of host and 3 chewing louse species in the Geomydoecus bulleri species complex. We examined mitochondrial DNA from a total of 46 specimens of Geomydoecus lice collected from 11 populations of the pocket gopher host, Pappogeomys bulleri. We also examined nuclear DNA from a subset of these chewing lice. Louse phylogenies were compared with a published pocket gopher phylogeny. Contrary to expectations, we observed a statistically significant degree of parallel cladogenesis in these closely related hosts and their parasites. We also observed a higher rate of evolution in chewing louse lineages than in their corresponding pocket gopher hosts. In addition, we found that 1 louse species (Geomydoecus burti) may not be a valid species, that subspecies within G. bulleri are not reciprocally monophyletic, and that morphological and genetic evidence support recognition of a new species of louse, Geomydoecus pricei.     

The dynamics of preferential host switching: Host phylogeny as a key predictor of parasite distribution*

Parasites often jump to and become established in a new host species. There is much evidence that the probability of such host shifts decreases with increasing phylogenetic distance between donor and recipient hosts, but the consequences of such preferential host switching remain little explored. We develop a computational model to investigate the dynamics of parasite host shifts in the presence of this phylogenetic distance effect. In this model, a clade of parasites evolves on an evolving clade of host species where parasites can cospeciate with their hosts, switch to new hosts, speciate within hosts or become extinct. Our model predicts that host phylogenies are major determinants of parasite distributions across trees. In particular, we predict that trees consisting of few large clades of host species and those with fast species turnover should harbor more parasites than trees with many small clades and those that diversify more slowly. Within trees, large clades are predicted to exhibit a higher fraction of infected species than small clades. We discuss our results in the light of recent cophylogenetic studies in a wide range of host–parasite systems.     

Phylogenetic congruence of mealybugs and their primary endosymbionts

Tight interactions between unrelated organisms such as is seen in plant-insect, host-parasite, or host-symbiont associations may lead to speciation of the smaller partners when their hosts speciate. Totally congruent phylogenies of interacting taxa have not been observed often but a number of studies have provided evidence that various hemipteran insect taxa and their primary bacterial endosymbionts share phylogenetic histories. Like other hemipterans, mealybugs (Pseudococcidae) harbour multiple intracellular bacterial symbionts, which are thought to be strictly vertically inherited, implying codivergence of hosts and symbionts. Here, robust estimates of phylogeny were generated from four fragments of three nuclear genes for mealybugs of the subfamily Pseudococcinae, and a substantial fragment of the 16S-23S rDNA of their P-endosymbionts. Phylogenetic congruence was highly significant, with 75% of nodes on the two trees identical, and significant correlation of branch lengths indicated coincident timing of cladogenesis. It is suggested that the low level of observed incongruence was influenced by uncertainty in phylogenetic estimation, but evolutionary outcomes other than congruence, including host shifts, could not be rejected.     

Codivergence in heteromyid rodents (Rodentia: heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: anoplura)

Although most studies of codivergence rely primarily on topological comparisons of host and parasite phylogenies, temporal assessments are necessary to determine if divergence events in host and parasite trees occurred contemporaneously. A combination of cophylogenetic analyses and comparisons of branch lengths are used in this study to understand the host-parasite association between heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura). Cophylogenetic comparisons based on nucleotide substitutions in the mitochondrial COI gene reveal a significant, but not perfect, pattern of cophylogeny between heteromyids and their sucking lice. Regression analyses show a significant functional relationship between the lengths of analogous branches in the host and parasite trees, indicating that divergence events in hosts and parasites were approximately contemporaneous. Thus, the topological similarity observed between heteromyids and their lice is the result of codivergence. These analyses also show that the COI gene in lice is evolving two to three times faster than the same gene in their hosts (similar to the results of studies of other lice and their vertebrate hosts) and that divergence events in lice occurred shortly after host divergence. We recommend that future studies of codivergence include temporal comparisons and, when possible, use the same molecular marker(s) in hosts and parasites to achieve the greatest insight into the history of the host-parasite relationship.     

Testing hybridization hypotheses based on incongruent gene trees

Hybridization is an important evolutionary mechanism in plants and has been increasingly documented in animals. Difficulty in reconstruction of reticulate evolution, however, has been a long-standing problem in phylogenetics. Consequently, hybrid speciation may play a major role in causing topological incongruence between gene trees. The incongruence, in turn, offers an opportunity to detect hybrid speciation. Here we characterized certain distinctions between hybridization and other biological processes, including lineage sorting, paralogy, and lateral gene transfer, that are responsible for topological incongruence between gene trees. Consider two incongruent gene trees with three taxa, A, B, and C, where B is a sister group of A on gene tree 1 but a sister group of C on gene tree 2. With a theoretical model based on the molecular clock, we demonstrate that time of divergence of each gene between taxa A and C is nearly equal in the case of hybridization (B is a hybrid) or lateral gene transfer, but differs significantly in the case of lineage sorting or paralogy. After developing a bootstrap test to test these alternative hypotheses, we extended the model and test to account for incongruent gene trees with numerous taxa. Computer simulation studies supported the validity of the theoretical model and bootstrap test when each gene evolved at a constant rate. The computer simulation also suggested that the model remained valid as long as the rate heterogeneity was occurring proportionally in the same taxa for both genes. Although the model could not test hypotheses of hybridization versus lateral gene transfer as the cause of incongruence, these two processes may be distinguished by comparing phylogenies of multiple unlinked genes.     

A priori assumptions about characters as a cause of incongruence between molecular and morphological hypotheses of primate interrelationships

When molecules and morphology produce incongruent hypotheses of primate interrelationships, the data are typically viewed as incompatible, and molecular hypotheses are often considered to be better indicators of phylogenetic history. However, it has been demonstrated that the choice of which taxa to include in cladistic analysis as well as assumptions about character weighting, character state transformation order, and outgroup choice all influence hypotheses of relationships and may positively influence tree topology, so that relationships between extant taxa are consistent with those found using molecular data. Thus, the source of incongruence between morphological and molecular trees may lie not in the morphological data themselves but in assumptions surrounding the ways characters evolve and their impact on cladistic analysis. In this study, we investigate the role that assumptions about character polarity and transformation order play in creating incongruence between primate phylogenies based on morphological data and those supported by multiple lines of molecular data. By releasing constraints imposed on published morphological analyses of primates from disparate clades and subjecting those data to parsimony analysis, we test the hypothesis that incongruence between morphology and molecules results from inherent flaws in morphological data. To quantify the difference between incongruent trees, we introduce a new method called branch slide distance (BSD). BSD mitigates many of the limitations attributed to other tree comparison methods, thus allowing for a more accurate measure of topological similarity. We find that releasing a priori constraints on character behavior often produces trees that are consistent with molecular trees. Case studies are presented that illustrate how congruence between molecules and unconstrained morphological data may provide insight into issues of polarity, transformation order, homology, and homoplasy.     

A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites

Background

Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galápagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms.

Results

Mitochondrial DNA sequences were obtained for four species of Galápagos mockingbirds and three sympatric species of ectoparasites - two louse and one mite species. These data were complemented with nuclear EF1α sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands.

Conclusions

The gene genealogies of Galápagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galápagos mockingbirds and their parasites.     

Comparing tree shapes: beyond symmetry

This paper describes two types of problems related to tree shapes, as well as algorithms that can be used to solve these problems. The first problem is that of comparing the similarity of the unlabelled shapes instead of merely their degree of balance, in a manner analogous to that routinely used to compare topologies for labelled trees. There are possible practical applications for this comparison, such as determining, based on tree shape similarity alone, whether the taxa in two phylogenies are likely to have a correspondence (e.g. hosts and parasites with high specificity). It is shown that tree balance is insufficient for this task and that standard measures of topological difference (Robinson–Foulds distances, SPR distances or retention indices of the matrices representing the trees, MRPs) can be easily adapted to the problem. The second type of problem is to determine whether taxa of uncertain matching unique to two different phylogenies could correspond to each other (e.g. the same species in larvae and adults of metamorphic animals, fossils known from different body parts). This second problem can be solved by either relabelling taxa in such a way that the number of consensus nodes is maximized, or relabelling taxa in such a way that the sum of the number of steps in the MRP of each tree mapped onto the other is minimum.     

Cophylogeny of the Ficus microcosm

The various mutualistic and antagonistic symbioses between fig trees (Ficus: Moraceae) and chalcid wasps comprise a community in microcosm. Phylogenetic estimates of figs and fig wasps show general topological correspondence, making the microcosm a model system for cophylogeny. Incongruence between phylogenies from associated organisms can be reconciled through a combination of evolutionary events. Cophylogeny mapping reconciles phylogenies by embedding an associate tree into a host tree, finding the optimal combinations of events capable of explaining incongruence and evaluating the level of codivergence. This review addresses the results of cophylogeny analysis concerning Ficus and discusses the plausibility of different evolutionary events. Five different associations encompassing fig-pollinator, fig-parasite and pollinator-parasitoid interactions are reconciled. The method improves on previous comparisons by employing 'jungles' to provide an exhaustive and quantitative analysis of cophylogeny. A jungle is a mechanism for inferring host switches and obtaining all potentially optimal solutions to the reconciliation problem. The results support the consensus that figs codiverge significantly with pollinators but not non-pollinators. However, pollinators still appear to have switched between hosts in contradiction to the traditional model of faithful codivergence. This emphasises the growing realisation that evolutionary transitions in the microcosm are more flexible than previously thought and host specificity is necessary but not sufficient for codivergence. The importance of sampling strategy is emphasised by the influence of taxon set on the fig-pollinator and fig-parasite jungles. Spurious significant results for fig-parasite and fig-parasitoid jungles indicate that the choice of congruence measure influences significance; the total number of events required to reconcile two trees ('total cost') is not a good measure of congruence when switches cannot be realistically weighted.     

Congruence of Morphological and Molecular Phylogenies

When phylogenetic trees constructed from morphological and molecular evidence disagree (i.e. are incongruent) it has been suggested that the differences are spurious or that the molecular results should be preferred a priori. Comparing trees can increase confidence (congruence), or demonstrate that at least one tree is incorrect (incongruence). Statistical analyses of 181 molecular and 49 morphological trees shows that incongruence is greater between than within the morphological and molecular partitions, and this difference is significant for the molecular partition. Because the level of incongruence between a pair of trees gives a minimum bound on how much error is present in the two trees, our results indicate that the level of error may be underestimated by congruence within partitions. Thus comparisons between morphological and molecular trees are particularly useful for detecting this incongruence (spurious or otherwise). Molecular trees have higher average congruence than morphological trees, but the difference is not significant, and both within- and between-partition incongruence is much lower than expected by chance alone. Our results suggest that both molecular and morphological trees are, in general, useful approximations of a common underlying phylogeny and thus, when molecules and morphology clash, molecular phylogenies should not be considered more reliable a priori.     

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.     

Shared geographic histories and dispersal contribute to congruent phylogenies between amphipods and their microsporidian parasites at regional and global scales

In parasites that strongly rely on a host for dispersal, geographic barriers that act on the host will simultaneously influence parasite distribution as well. If their association persists over macroevolutionary time it may result in congruent phylogenetic and phylogeographic patterns due to shared geographic histories. Here, we investigated the level of congruent evolutionary history at a regional and global scale in a highly specialised parasite taxon infecting hosts with limited dispersal abilities: the microsporidians Dictyocoela spp. and their amphipod hosts. Dictyocoela can be transmitted both vertically and horizontally and is the most common microsporidian genus occurring in amphipods in Eurasia. However, little is known about its distribution elsewhere. We started by conducting molecular screening to detect microsporidian parasites in endemic amphipod species in New Zealand; based on phylogenetic analyses, we identified nine species‐level microsporidian taxa including six belonging to Dictyocoela. With a distance‐based cophylogenetic analysis at the regional scale, we identified overall congruent phylogenies between Paracalliope, the most common New Zealand freshwater amphipod taxon, and their Dictyocoela parasites. Also, hosts and parasites showed similar phylogeographic patterns suggesting shared biogeographic histories. Similarly, at a global scale, phylogenies of amphipod hosts and their Dictyocoela parasites showed broadly congruent phylogenies. The observed patterns may have resulted from covicariance and/or codispersal, suggesting that the intimate association between amphipods and Dictyocoela may have persisted over macroevolutionary time. We highlight that shared biogeographic histories could play a role in the codiversification of hosts and parasites at a macroevolutionary scale.     

When can host shifts produce congruent host and parasite phylogenies? A simulation approach

Congruence between host and parasite phylogenies is often taken as evidence for cospeciation. However, 'pseudocospeciation', resulting from host-switches followed by parasite speciation, may also generate congruent trees. To investigate this process and the conditions favouring its appearance, we here simulated the adaptive radiation of a parasite onto a new range of hosts. A very high congruence between the host tree and the resulting parasite trees was obtained when parasites switched between closely related hosts. Setting a shorter time lag for speciation after switches between distantly related hosts further increased the degree of congruence. The shape of the host tree, however, had a strong impact, as no congruence could be obtained when starting with highly unbalanced host trees. The strong congruences obtained were erroneously interpreted as the result of cospeciations by commonly used phylogenetic software packages despite the fact that all speciations resulted from host-switches in our model. These results highlight the importance of estimating the age of nodes in host and parasite phylogenies when testing for cospeciation and also demonstrate that the results obtained with software packages simulating evolutionary events must be interpreted with caution.     

Fossils of parasites: what can the fossil record tell us about the evolution of parasitism?

Parasites are common in many ecosystems, yet because of their nature, they do not fossilise readily and are very rare in the geological record. This makes it challenging to study the evolutionary transition that led to the evolution of parasitism in different taxa. Most studies on the evolution of parasites are based on phylogenies of extant species that were constructed based on morphological and molecular data, but they give us an incomplete picture and offer little information on many important details of parasite–host interactions. The lack of fossil parasites also means we know very little about the roles that parasites played in ecosystems of the past even though it is known that parasites have significant influences on many ecosystems. The goal of this review is to bring attention to known fossils of parasites and parasitism, and provide a conceptual framework for how research on fossil parasites can develop in the future. Despite their rarity, there are some fossil parasites which have been described from different geological eras. These fossils include the free‐living stage of parasites, parasites which became fossilised with their hosts, parasite eggs and propagules in coprolites, and traces of pathology inflicted by parasites on the host's body. Judging from the fossil record, while there were some parasite–host relationships which no longer exist in the present day, many parasite taxa which are known from the fossil record seem to have remained relatively unchanged in their general morphology and their patterns of host association over tens or even hundreds of millions of years. It also appears that major evolutionary and ecological transitions throughout the history of life on Earth coincided with the appearance of certain parasite taxa, as the appearance of new host groups also provided new niches for potential parasites. As such, fossil parasites can provide additional data regarding the ecology of their extinct hosts, since many parasites have specific life cycles and transmission modes which reflect certain aspects of the host's ecology. The study of fossil parasites can be conducted using existing techniques in palaeontology and palaeoecology, and microscopic examination of potential material such as coprolites may uncover more fossil evidence of parasitism. However, I also urge caution when interpreting fossils as examples of parasites or parasitism‐induced traces. I point out a number of cases where parasitism has been spuriously attributed to some fossil specimens which, upon re‐examination, display traits which are just as (if not more) likely to be found in free‐living taxa. The study of parasite fossils can provide a more complete picture of the ecosystems and evolution of life throughout Earth's history.     

Of lice and men: The return of the ’comparative parasitology‘ debate

The question of whether or not parasite phylogeny provides information about host relationships (‘comparative parasitology’) reached a peak in 1957 in a vigorous debate between Gunther Timmermann and Ernst Mayr. Timmermann argued that parasites were associated with their hosts by descent and that this produced congruent host and parasite phylogenies. In contrast, Mayr argued that parasites were often associated by colonization and that this led to incongruence between host and parasite phylogenies. To test these differing views. Adrian Paterson, Russell Gray and Graham Wallis derived a procellaniform phylogeny. This tree is here compared with Timmermann's tree based on the relationships of feather lice. Timmermann's tree is more similar to the seabird phylogeny than would be expected by chance. Thus, support is found for the ‘comparative parasitology’ approach.     

Lousy grouse: Comparing evolutionary patterns in Alaska galliform lice to understand host evolution and host–parasite interactions

Understanding both sides of host–parasite relationships can provide more complete insights into host and parasite biology in natural systems. For example, phylogenetic and population genetic comparisons between a group of hosts and their closely associated parasites can reveal patterns of host dispersal, interspecies interactions, and population structure that might not be evident from host data alone. These comparisons are also useful for understanding factors that drive host–parasite coevolutionary patterns (e.g., codivergence or host switching) over different periods of time. However, few studies have compared the evolutionary histories between multiple groups of parasites from the same group of hosts at a regional geographic scale. Here, we used genomic data to compare phylogenomic and population genomic patterns of Alaska ptarmigan and grouse species (Aves: Tetraoninae) and two genera of their associated feather lice: Lagopoecus and Goniodes. We used whole‐genome sequencing to obtain hundreds of genes and thousands of single‐nucleotide polymorphisms (SNPs) for the lice and double‐digest restriction‐associated DNA sequences to obtain SNPs from Alaska populations of two species of ptarmigan. We found that both genera of lice have some codivergence with their galliform hosts, but these relationships are primarily characterized by host switching and phylogenetic incongruence. Population structure was also uncorrelated between the hosts and lice. These patterns suggest that grouse, and ptarmigan in particular, share habitats and have likely had historical and ongoing dispersal within Alaska. However, the two genera of lice also have sufficient dissimilarities in the relationships with their hosts to suggest there are other factors, such as differences in louse dispersal ability, that shape the evolutionary patterns with their hosts.