Basal ischnoceran louse phylogeny (Phthiraptera: Ischnocera: Goniodidae and Heptapsogasteridae)

A phylogenetic analysis of generic relationships for avian chewing lice of families Goniodidae and Heptapsogasteridae (Phthiraptera: Ischnocera) is presented. These lice, hosted by galliform, columbiform and tinamiform birds are reputedly basal in the phylogeny of Ischnocera. A cladistic analysis of sixty‐two adult morphological characters from thirty‐one taxa revealed thirty equally parsimonious cladograms. The phylogeny is well resolved within Heptap‐sogasteridae and supports the monophyly of subfamily Strongylocotinae (sensu Eichler 1963 ). Resolution within Goniodidae is lower but suggests that the genera hosted by Columbiformes are largely monophyletic. Mapping host taxonomy on to the phylogeny of the lice reveals a consistent pattern which is largely congruent down to the rank of host family, although at lower taxonomic levels the association appears to be more complex. The inclusion of more louse taxa may help considerably to unravel the coevolutionary history of both the hosts and their parasites.     

Remarkable levels of avian louse (Insecta: Phthiraptera) diversity in the Congo Basin

Although the Democratic Republic of the Congo is considered a megadiverse country, the Congo Basin is not recognized as a conservation priority because of gross underestimates of species diversity and endemism, especially for invertebrate taxa. Examining ectoparasitic chewing lice parasitizing birds in this region could provide valuable information pertaining to the diversity of invertebrate taxa as well as host–parasite interactions within the Congo Basin. In this study, we used molecular and morphological data to examine avian louse diversity. From 60 parasitized birds, we documented 39 new host associations, and at least 12 and 17 species of amblyceran and ischnoceran chewing lice, respectively. Morphologically, we identified a minimum of 13 new species. Due to a lack of available reference material, we were unable to identify some specimens and it is likely many, if not all of these, represent new species. Our sampling efforts, morphological examinations and molecular analyses reveal an astounding amount of louse diversity in the Congo Basin.     

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.     

Phylogeny and classification, origins, and evolution of host associations of lice

Lice are highly successful ectoparasites. Most species of mammals and birds are infested by at least 1 but up to 6 species of lice. Current opinion is that lice evolved from free-living Psocoptera (booklice, barklice and psocids). It is generally agreed that there are 4 main groups of lice: Anoplura, Amblycera, Ischnocera and Rhyncophthirina. In contrast, there is no agreement on the phylogenetic relationships of these groups and their classification. In particular, there is much debate over the validity of the taxon Mallophaga, which is almost certainly paraphyletic. For many years the sister-group of the Boopiidae, which almost exclusively infest Australasian marsupials, was thought to be a group of lice that now infest marsupials in South America. This, however, is almost certainly incorrect; the sister-group of the Boopiidae probably contains bird-infesting lice from the Menoponidae (Amblycera). Thus, menoponid lice transferred from birds to mammals and from these arose the Boopiidae. Transfers of lice between mammals and birds have occurred on other occasions during the evolution of the lice; 2 of the 4 main groups of lice, the Ischnocera and Amblycera, contain families that infest birds and families that infest mammals. Strict cospeciation and coevolution was thought to predominate among the lice; however, detailed studies indicate this to be incorrect. Consequently, the axiom that lice and their hosts invariably coevolve should be abandoned. Ironically, biologists may learn more about the evolutionary biology of hosts when host-switching has occurred. Some evidence exists for competition between species of lice; this interaction may determine whether or not the transfer of a species of louse to an atypical hose (a potential host-switch) is successful. Thus, the extincion of populations of lice (that result in uninfested hosts) may facilitate host-switching and perhaps the evolution of new taxa of lice. In contrast, extinction of hosts unfortunately often leads to the extinction of species of lice.     

Multiple genes and the monophyly of Ischnocera (Insecta: Phthiraptera).

Whereas most traditional classifications identify Ischnocera as a major suborder of lice in the order Phthiraptera, a recent molecular study based on one gene did not recover monophyly of Ischnocera. In this study we test the monophyly of Ischnocera using sequences of portions of three different genes: two nuclear (EF1 alpha and 18S) and one mitochondrial (COI). Analysis of EF1 alpha and COI sequences did not recover monophyly of Ischnocera, but these genes provided little support for ischnoceran paraphyly because homoplasy is high among the divergent taxa included in this study. Analysis of 18S sequences recovered ischnoceran monophyly with strong support. Sequences from these three gene regions showed significant conflict with the partition homogeneity test, but this heterogeneity probably arises from the dramatic differences in substitution rates. In support of this conclusion, Kishino-Hasegawa tests of the EF1 alpha and COI genes did not reject several trees containing ischnoceran monophyly. Combined analysis of all three gene regions supported monophyly of Ischnocera, although not as strongly as analysis of 18S by itself. In sum, although rapidly evolving genes can retain some phylogenetic signal for deep phylogenetic relationships, strong support for such relationships is likely to come from more slowly evolving genes.     

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.     

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.     

Molecular systematics of Goniodidae (Insecta: Phthiraptera)

The higher level phylogenetic relationships within the avian feather lice (Insecta: Phthiraptera: Ischnocera) are extremely problematic. Here we investigate the relationships of 1 family (Goniodidae), sometimes recognized as distinct within Ischnocera, using parsimony and likelihood analyses of nuclear and mitochondrial DNA sequences. These data support monophyly for a restricted definition of traditional Goniodidae, but recognition of this family would result in paraphyly of the large heterogeneous family Philopteridae. We show that the New World Chelopistes is not related to other members of Goniodidae, despite similarities in morphology, but rather is the sister taxon to Oxylipeurus. Within Goniodidae, genera are divided into those occurring on Galliformes (the Goniodes complex) and those occurring on Columbiformes (the Coloceras complex). Within the well-sampled Coloceras complex, or Physconelloidinae, several groups are identified. However, traditionally recognized genera such as Coloceras and Phvsconelloides appear to be paraphyletic. Whereas the phylogeny of Goniodidae reflects some aspects of host relationships, biogeography also influences coevolutionary history.     

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.     

There and back again: switching between host orders by avian body lice (Ischnocera: Goniodidae)

Studies of major switches by parasites between highly divergent host lineages are important for understanding new opportunities for parasite diversification. One such major host switch is inferred for avian feather lice (Ischnocera) in the family Goniodidae, which parasitize two distantly‐related groups of birds: Galliformes (pheasants, quail, partridges, etc.) and Columbiformes (pigeons and doves). Although there have been several cophylogenetic studies of lice at the species level, few studies have focused on such broad evolutionary patterns and major host‐switching events. Using a phylogeny based on DNA sequences for goniodid feather lice, we investigated the direction of this major host switch. Unexpectedly, we found that goniodid feather lice have switched host orders, not just once, but twice. A primary host switch occurred from Galliformes to Columbiformes, leading to a large radiation of columbiform body lice. Subsequently, there was also a host switch from Columbiformes back to Galliformes, specifically to megapodes in the Papua–Australasian region. The results of the present study further reveal that, although morphologically diagnosable lineages are supported by molecular data, many of the existing genera are not monophyletic and a revision of generic limits is needed. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 614–625.     

Cophylogenetic assessment of New World warblers (Parulidae) and their symbiotic feather mites (Proctophyllodidae)

Host–symbiont relationships are ubiquitous in nature, yet evolutionary and ecological processes that shape these intricate associations are often poorly understood. All orders of birds engage in symbioses with feather mites, which are ectosymbiotic arthropods that spend their entire life on hosts. Due to their permanent obligatory association with hosts, limited dispersal and primarily vertical transmission, we hypothesized that the cospeciation between feather mites and hosts within one avian family (Parulidae) would be perfect (strict cospeciation). We assessed cophylogenetic patterns and tested for congruence between species in two confamiliar feather mite genera (Proctophyllodidae: Proctophyllodes, Amerodectes) found on 13 species of migratory warblers (and one other closely related migratory species) in the eastern United States. Based on COI sequence data, we found three Proctophyllodes lineages and six Amerodectes lineages. Distance‐ and event‐based cophylogenetic analyses suggested different cophylogenetic trajectories of the two mite genera, and although some associations were significant, there was little overall evidence supporting strict cospeciation. Host switching is likely responsible for incongruent phylogenies. In one case, we documented prairie warblers Setophaga discolor harboring two mite species of the same genus. Most interestingly, we found strong evidence that host ecology may influence the likelihood of host switching occurring. For example, we documented relatively distantly related ground‐nesting hosts (ovenbird Seiurus aurocapilla and Kentucky warbler Geothlypis formosa) sharing a single mite species, while other birds are shrub/canopy or cavity nesters. Overall, our results suggest that cospeciation is not the case for feather mites and parulid hosts at this fine phylogenetic scale, and raise the question if cospeciation applies for other symbiotic systems involving hosts that have complex life histories. We also provide preliminary evidence that incorporating host ecological traits into cophylogenetic analyses may be useful for understanding how symbiotic systems have evolved.     

Flyway homogenisation or differentiation? Insights from the phylogeny of the sandpiper (Charadriiformes: Scolopacidae: Calidrinae) wing louse genus Lunaceps (Phthiraptera: Ischnocera)

The wing louse genus Lunaceps, is the most speciose chewing louse (Phthiraptera) genus inhabiting sandpipers (Charadriiformes: Calidrinae) and is known from almost all sandpiper species. The hosts follow specific flyways from the Arctic breeding grounds to wintering locations in the southern hemisphere, and often form large mixed-species flocks during migration and wintering. We estimated a phylogeny of Lunaceps based on three mitochondrial loci, supporting monophyly of the genus but revealing extensive paraphyly at the species level. We also evaluated the relative importance of flyway differentiation (same host species having different lice along different flyways) and flyway homogenisation (different host species having the same lice along the same flyway). We found that while the lice of smaller sandpipers and stints show some evidence of flyway homogenisation, those of larger sandpipers do not. No investigated host species migrating along more than one flyway showed any evidence of flyway differentiation. The host-parasite associations within Lunaceps are in no case monophyletic, rejecting strict cospeciation.     

Clever birds are lousy: co-variation between avian innovation and the taxonomic richness of their amblyceran lice

Lice (Insecta: Phthiraptera) are ectoparasites that reduce host life expectancy and sexual attractiveness. Their taxonomic richness varies considerably among their hosts. Previous studies have already explored some important factors shaping louse diversity. An unexplored potential correlate of louse taxonomic richness is host behavioural flexibility. In this comparative study, we examine the relationship between louse generic richness, innovative capabilities (as a proxy for behavioural flexibility), and brain size while controlling for host species diversity, phylogeny, body size and research effort. Using data for 108 avian families, we found a highly significant positive relationship between host innovative capabilities and the taxonomic richness of amblyceran lice, but a lack of a similar relationship in ischnoceran lice. Host brain size had only a marginal impact on amblyceran diversity and no correlation with ischnoceran diversity. This suggests that the effect in Amblycera is not mediated by metabolic limitations due to the energetic costs of brain size and maintenance, rather directly caused by the ecological differences between hosts with differing cognitive capabilities. We propose four alternative and mutually non-exclusive hypotheses that may explain this phenomenon.     

Phylogeny of the lice (Insecta, Phthiraptera) inferred from small subunit rRNA

There has been much argument about the phylogenetic relationships of the four suborders of lice (Insecta: Phthiraptera). Lyal's study of the morphology of lice indicated that chewing/biting lice (Mallophaga) are paraphyletic with respect to sucking lice (Anoplura). To test this hypothesis we inferred the phylogeny of 33 species of lice from small subunit (SSU) rRNA sequences (18S rRNA). Liposcelis sp. from the Liposcelididae (Psocoptera) was used for outgroup reference. Phylogenetic relationships among the four suborders of lice inferred from these sequences were the same as those inferred from morphology. The Amblycera is apparently the sister-group to all other lice whereas the Rhynchophthirina is apparently sister to the Anoplura; these two suborders are sister to the Ischnocera, i.e. (Amblycera (Ischnocera (Anoplura, Rhynchophthirina))). Thus, the Mallophaga (Amblycera, Ischnocera, Rhynchophthirina) is apparently paraphyletic with respect to the Anoplura. Our analyses also provide evidence that: (i) each of the three suborders of lice that are well represented in our study (the Amblycera, Ischnocera, and Anoplura) are monophyletic; (ii) the Boopiidae is monophyletic; (iii) the genera Heterodoxus and Latumcephalum (Boopiidae) are more closely related to one another than either is to the genus Boopia (also Boopiidae); (iv) the Ricinidae and Laemobothridae may be sister-taxa; (v) the Philopteridae may be paraphyletic with respect to the Trichodectidae; (vi) the genera Pediculus and Pthirus are more closely related to each other than either is to the genus Pedicinus ; and (vii) in contrast to published data for mitochondrial genes, the rates of nucleotide substitution in the SSU rRNA of lice are not higher than those of other insects, nor do substitution rates in the suborders differ substantially from one another.     

Ecology of congruence: past meets present

Phylogenetic congruence is governed by various macroevolutionary events, including cospeciation, host switching, sorting, duplication, and failure to speciate. The relative frequency of these events may be influenced by factors that govern the distribution and abundance of the interacting groups; i.e., ecological factors. If so, it may be possible to predict the degree of phylogenetic congruence between two groups from information about their ecology. Unfortunately, adequate comparative ecological data are not available for many of the systems that have been subjected to cophylogenetic analysis. An exception is provided by chewing lice (Insecta: Phthiraptera), which parasitize birds and mammals. For a few genera of these lice, enough data have now been published to begin exploring the relationship between ecology and congruence. In general, there is a correspondence between important ecological factors and the degree of phylogenetic congruence. Careful comparison of these genera suggests that dispersal is a more fundamental barrier to host switching among related hosts than is establishment. Transfer experiments show that host-specific lice can survive and reproduce on novel hosts that are similar in size to the native host as long as the lice can disperse to these hosts. To date, studies of parasite dispersal have been mainly inferential. A better understanding of the role of dispersal will require more direct data on dispersal frequency and distances.     

A morphological phylogeny for four families of amblyceran lice (Phthiraptera: Amblycera: Menoponidae, Boopiidae, Laemobothriidae, Ricinidae)

The suborder Amblycera (Insecta: Phthiraptera) comprises seven recognized families of parasitic lice. Three of these families (the Menoponidae, Laemobothriidae and Ricinidae) are present on a wide range of avian hosts. The four remaining families are restricted to a small section of mammals (the Boopiidae are parasites of Australian and New Guinean marsupials, and the Gyropidae, Trimenoponidae and Abrocomophagidae parasitize South and Central American rodents). This study uses a morphological approach to examine the evolutionary relationships between the genera from four amblyceran families: the Menoponidae, Boopiidae, Laemobothriidae and Ricinidae. Genera are represented by exemplars and a total of 44 louse taxa and one outgroup taxon were included. A cladistic analysis of 147 unordered characters recovered six equally parsimonious trees. Bootstrap, jackknife and Bremer support analyses were undertaken to assess the level of support for each resolved node in the strict consensus topology. Strong support was found for deep branch relationships between the families and in some cases for supra-generic groupings within families. The clades present in the strict consensus tree are discussed with reference to supra-generic and interfamily relationships, character choice, morphological convergence and host distribution. This study is the first phylogeny presented solely for amblyceran genera.  © 2003 The Linnean Society of London, Zoological Journal of the Linnean Society , 2003, 138 , 39–82.     

Phylogeny of "Philoceanus complex" seabird lice (Phthiraptera: Ischnocera) inferred from mitochondrial DNA sequences

The Philoceanus complex is a large assemblage of lice that parasitise procellariiform seabirds (petrels, albatrosses, and their relatives). We obtained mitochondrial 12S rRNA and cytochrome oxidase I DNA sequences from 39 species from diverse hosts and localities. Resolution of deeper relationships between genera was limited, however there is evidence for two major clades, one hosted by albatrosses, the other by petrels. Based on our results, the genera hosted by albatrosses are excellent candidates for detailed analysis of cospeciation. Our results also suggest that a previous estimate of a 5-fold difference in the relative rate of sequence evolution in lice and their avian hosts is an artefact of limited taxonomic sampling.     

Data incongruence and the problem of avian louse phylogeny

Smith, V. S., Page, R. D. M. & Johnson, K. P. (2004). Data incongruence and the problem of avian louse phylogeny. — Zoologica Scripta, 33 , 239 –259.
Recent studies based on different types of data (i.e. morphological and molecular) have supported conflicting phylogenies for the genera of avian feather lice (Ischnocera: Phthiraptera). We analyse new and published data from morphology and from mitochondrial (12S rRNA and COI) and nuclear (EF1-α) genes to explore the sources of this incongruence and explain these conflicts. Character convergence, multiple substitutions at high divergences, and ancient radiation over a short period of time have contributed to the problem of resolving louse phylogeny with the data currently available. We show that apparent incongruence between the molecular datasets is largely attributable to rate variation and nonstationarity of base composition. In contrast, highly significant character incongruence leads to topological incongruence between the molecular and morphological data. We consider ways in which biases in the sequence data could be misleading, using several maximum likelihood models and LogDet corrections. The hierarchical structure of the data is explored using likelihood mapping and SplitsTree methods. Ultimately, we concede there is strong discordance between the molecular and morphological data and apply the conditional combination approach in this case. We conclude that higher level phylogenetic relationships within avian Ischnocera remain extremely problematic. However, consensus between datasets is beginning to converge on a stable phylogeny for avian lice, at and below the familial rank.     

Phylogenetic analysis of partial sequences of elongation factor 1alpha identifies major groups of lice (Insecta: Phthiraptera)

As a first attempt to use molecular data to resolve the relationships between the four suborders of lice and within the suborder Ischnocera, we sequenced a 347-bp fragment of the elongation factor 1alpha gene of 127 lice (Insecta: Phthiraptera) as well as outgroup taxa from the order Psocoptera. A number of well-supported monophyletic groups were found but the relationships among many of these groups could not be resolved. While it is probable that multiple substitutions at high divergences and ancient radiation over a short period of time have contributed to the problem, we attribute most of this lack of resolution to the high ratio of taxa to characters. Nevertheless, the sequence data unequivocally support a number of important relationships that are at variance with the conclusions of morphological taxonomy. These include the sister group relationship of Chelopistes and Oxylipeurus, two lice occupying different ecological niches on the same host, which have previously been assigned to different families. These results provide evidence in support of the hypothesis that lice have speciated in situ on the host in response to niche specialization and that this has given rise to convergent morphologies in the lice of different host groups which share similar ecological niches. We discuss our attempts to overcome the limitations of this large data set, including the use of leaf stability analysis, a new method for analyzing the stability of taxa in a phylogenetic tree, and examine a number of hypotheses of relationships based on both traditional taxonomy and host associations.     

AVIAN BROOD PARASITISM AND ECTOPARASITE RICHNESS–SCALE‐DEPENDENT DIVERSITY INTERACTIONS IN A THREE‐LEVEL HOST–PARASITE SYSTEM

Brood parasitic birds, their foster species and their ectoparasites form a complex coevolving system composed of three hierarchical levels. However, effects of hosts’ brood parasitic life‐style on the evolution of their louse (Phthiraptera: Amblycera, Ischnocera) lineages have never been tested. We present two phylogenetic analyses of ectoparasite richness of brood parasitic clades. Our hypothesis was that brood parasitic life‐style affects louse richness negatively across all avian clades due to the lack of vertical transmission routes. Then, narrowing our scope to brood parasitic cuckoos, we explored macroevolutionary factors responsible for the variability of their louse richness. Our results show that taxonomic richness of lice is lower on brood parasitic clades than on their nonparasitic sister clades. However, we found a positive covariation between the richness of cuckoos’ Ischnoceran lice and the number of their foster species, possibly due to the complex and dynamic subpopulation structure of cuckoo species that utilize several host species. We documented diversity interactions across a three‐level host parasite system and we found evidence that brood parasitism has opposing effects on louse richness at two slightly differing macroevolutionary scales, namely the species richness and the genera richness.