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.     

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.     

Cophylogenetic relationships between penguins and their chewing lice

It is generally thought that the evolution of obligate parasites should be linked intimately to the evolution of their hosts and that speciation by the hosts should cause speciation of their parasites. The penguins and their chewing lice present a rare opportunity to examine codivergence between a complete host order and its parasitic lice. We estimated a phylogeny for all 15 species of lice parasitising all 17 species of penguins from the third domain of the mitochondrial 12S ribosomal rRNA gene, a portion of the mitochondrial cytochrome oxidase subunit 1 gene and 55 morphological characters. We found no evidence of extensive cospeciation between penguins and their chewing lice using TreeMap 2.02beta. Despite the paucity of cospeciation, there is support for significant congruence between the louse and penguin phylogenies due to possible failure to speciate events (parasites not speciating in response to their hosts speciating).     

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.     

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.     

Linking coevolutionary history to ecological process: doves and lice

Abstract Many host-specific parasites are restricted to a limited range of host species by ecological barriers that impede dispersal and successful establishment. In some cases, microevolutionary differentiation is apparent on top of host specificity, as evidenced by significant parasite population genetic structure among host populations. Ecological barriers responsible for specificity and genetic structure can, in principle, reinforce macroevolutionary processes that generate congruent host-parasite phylogenies. However, few studies have explored both the micro- and macroevolutionary ramifications of close association in a single host-parasite system. Here we compare the macroevolutionary histories of two genera of feather lice (Phthiraptera: Ischnocera) that both parasitize New World pigeons and doves (Aves: Columbiformes). Earlier work has shown that dove body lice (genus Physconelloides ) are more host specific and have greater population genetic structure than dove wing lice ( Columbicola ). We reconstructed phylogenies for representatives of the two genera of lice and their hosts, using nuclear and mitochondrial DNA sequences. The phylogenies were well resolved and generally well supported. We compared the phylogenies of body lice and wing lice to the host phylogeny using reconciliation analyses. We found that dove body lice show strong evidence of cospeciation whereas dove wing lice do not. Although the ecology of body and wing lice is very similar, differences in their dispersal ability may underlie these joint differences in host specificity, population genetic structure, and coevolutionary history.     

Phylogenetic approaches in coevolution and biogeography

I review phylogenetic approaches to problems in coevolution and biogeography, illustrating with case studies. In coevolution, genealogical trees are essential in differentiating between ancient and recent associations, in identifying cospeciation events, and in studying host-switching patterns. Cospeciating associations are of particular interest because they allow powerful tests of molecular clocks and accurate comparison of evolutionary rates across groups of organisms. In biogeography, phylogenies can help reconstruct the distribution history of individual groups and identify past geological events that have affected the evolution of entire communities. Parsimony analysis in coevolution and biogeography should be based on identification of different types of events, each of which is associated with a specific cost. Similar event-based methods are applicable to coevolutionary and biogeographic inference, as well as in the mapping of gene trees onto organism trees. The discussed examples span a variety of organisms and spatiotemporal scales: primate pin worms, HIV, pocket gophers and their lice, aphids and their bacterial symbionts, gall wasps and their host plants, the root of the tree of life, the historical biogeography of the Holarctic, and the geographical origin of our own species.     

Clade-limited colonization in brood parasitic finches (Vidua spp.)

The African brood parasitic finches (Vidua spp.) are host specialists that mimic the songs and nestling mouth markings of their finch hosts (family Estrildidae). Although recent molecular analyses suggest rapid speciation associated with host switches in some members of this group, the association of different Vidua lineages with particular host genera suggests the possibility of cospeciation at higher levels in the host and parasite phylogenies. We compared a phylogeny of all Vidua species with a phylogeny of their estrildid finch hosts and compared divergence time estimates for the two groups. Basal divergences among extant members of the Vidulidae and among Vidua species are more recent than those among host genera and species, respectively, allowing a model of cospeciation to be rejected at most or all levels of the Vidua phylogeny. Nonetheless, some tests for cospeciation indicated significant congruence between host and parasite tree topologies. This result may be an artifact of clade-limited colonization. Host switches in parasitic finches have most often involved new hosts in the same or a closely related genus, an effect that increases the apparent congruence of host and parasites trees.     

Phoretic dispersal influences parasite population genetic structure

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host‐specific feather lice (Phthiraptera: Ischnocera) that co‐occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, “wing lice” (Columbicola columbae) disperse phoretically by “hitchhiking” on pigeon flies (Diptera: Hippoboscidae), while “body lice” (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host–parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of 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.     

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.     

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.     

Seabird and louse coevolution: complex histories revealed by 12S rRNA sequences and reconciliation analyses

We investigated the coevolutionary history of seabirds (orders Procellariiformes and Sphenisciformes) and their lice (order Phthiraptera). Independent trees were produced for the seabirds (tree derived from 12S ribosomal RNA, isoenzyme, and behavioral data) and their lice (trees derived from 12S rRNA data). Brook's parsimony analysis (BPA) supported a general history of cospeciation (consistency index = 0.84, retention index = 0.81). We inferred that the homoplasy in the BPA was caused by one intrahost speciation, one potential host-switching, and eight or nine sorting events. Using reconciliation analysis, we quantified the cost of fitting the louse tree onto the seabird tree. The reconciled trees postulated one host-switching, nine cospeciation, three or four intrahost speciation, and 11 to 14 sorting events. The number of cospeciation events was significantly more than would be expected from chance alone (P < 0.01). The sequence data were used to test for rate heterogeneity for both seabirds and lice. Neither data set displayed significant rate heterogeneity. An examination of the codivergent nodes revealed that seabirds and lice have cospeciated synchronously and that lice have evolved at approximately 5.5 times the rate of seabirds. The degree of sequence divergence supported some of the postulated intrahost speciation events (e.g., Halipeurus predated the evolution of their present hosts). The sequence data also supported some of the postulated host-switching events. These results demonstrate the value of sequence data and reconciliation analyses in unraveling complex histories between hosts and their parasites.     

Molecular phylogenies of fig wasps: partial cocladogenesis of pollinators and parasites

Figs (Ficus spp., Moraceae) and their pollinating wasps form an obligate mutualism, which has long been considered a classic case of coevolution and cospeciation. Figs are also exploited by several clades of nonpollinating wasps, which are parasites of the mutualism and whose patterns of speciation have received little attention. We used data from nuclear and mitochondrial DNA regions to estimate the phylogenies of 20 species of Pleistodontes pollinating wasps and 16 species of Sycoscapter nonpollinating wasps associated with Ficus species in the section Malvanthera. We compare the phylogenies of 15 matched Pleistodontes/Sycoscapter species pairs and show that the level of cospeciation is significantly greater than that expected by chance. Our estimates of the maximum level of cospeciation (50 to 64% of nodes) are very similar to those obtained in other recent studies of coevolved parasitic and mutualistic associations. However, we also show that there is not perfect congruence of pollinator and parasite phylogenies (for any substantial clade) and argue that host plant switching is likely to be less constrained for Sycoscapter parasites than for Pleistodontes pollinators. There is perfect correspondence between two terminal clades of two sister species in the respective phylogenies, and rates of molecular evolution in these pairs are similar.     

Speciation in fig pollinators and parasites

Here we draw on phylogenies of figs and fig wasps to suggest how modes of speciation may be affected by interspecific interactions. Mutualists appear to have cospeciated with their hosts to a greater extent than parasites, which showed evidence of host shifting. However, we also repeatedly encountered a pattern not explained by either cospeciation or host switching. Sister species of fig parasites often attack the same host in sympatry, and differences in ovipositor length suggest that parasite speciation could result from divergence in the timing of oviposition with respect to fig development. These observations on fig parasites are consistent with a neglected model of sympatric speciation.     

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.     

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.     

COSPECIATION ANALYSIS OF AN OBLIGATE POLLINATION MUTUALISM: HAVEGLOCHIDION TREES (EUPHORBIACEAE) AND POLLINATING EPICEPHALA MOTHS(GRACILLARIIDAE) DIVERSIFIED IN PARALLEL?

Species-specific obligate pollination mutualism between Glochidion trees (Euphorbiaceae) and Epicephala moths (Gracillariidae) involves a large number of interacting species and resembles the classically known fig-fig wasp and yucca-yucca moth associations. To assess the extent of parallel cladogenesis in Glochidion-Epicephala association, we reconstruct phylogenetic relationships of 18 species of Glochidion using nuclear ribosomal DNA sequences (internal and external transcribed spacers) and those of the corresponding 18 Epicephala species using mitochondrial (the cytochrome oxidase subunit I gene) and nuclear DNA sequences (the arginine kinase and elongation factor-1alpha genes). Based on the obtained phylogenies, we determine whether Glochidion and Epicephala have undergone parallel diversification using several different methods for investigating the level of cospeciation between phylogenies. These tests indicate that there is generally a greater degree of correlation between Glochidion and Epicephala phylogenies than expected in a random association, but the results are sensitive to selection of different phylogenetic hypotheses and analytical methods for evaluating cospeciation. Perfect congruence between phylogenies is not found in this association, which likely resulted from host shift by the moths. The observed significant discrepancy between Glochidion and Epicephala phylogenies implies that the one-to-one specificity between the plants and moths has been maintained through a complex speciation process or that there is an underestimated diversity of association between Glochidion trees and Epicephala moths.     

Host behaviour drives parasite genetics at multiple geographic scales: population genetics of the chewing louse,Thomomydoecus minor

Pocket gophers and their symbiotic chewing lice form a host–parasite assemblage known for a high degree of cophylogeny, thought to be driven by life history parameters of both host and parasite that make host switching difficult. However, little work to date has focused on determining whether these life histories actually impact louse populations at the very fine scale of louse infrapopulations (individuals on a single host) at the same or at nearby host localities. We used microsatellite and mtDNA sequence data to make comparisons of chewing‐louse (Thomomydoecus minor) population subdivision over time and over geographic space where there are different potential amounts of host interaction surrounding a zone of contact between two hybridizing pocket‐gopher subspecies. We found that chewing lice had high levels of population isolation consistent with a paucity of horizontal transmission even at the very fine geographic scale of a single alfalfa field. We also found marked genetic discontinuity in louse populations corresponding with host subspecies and little, if any, admixture in the louse genetic groups even though the lice are closely related. The correlation of louse infrapopulation differentiation with host interaction at multiple scales, including across a discontinuity in pocket‐gopher habitat, suggests that host behaviour is the primary driver of parasite genetics. This observation makes sense in light of the life histories of both chewing lice and pocket gophers and provides a powerful explanation for the well‐documented pattern of parallel cladogenesis in pocket gophers and chewing lice.     

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.