The perils of using host relationships in parasite taxonomy: phylogeny of the Degeeriella complex

The taxonomy of lice (Insecta: Phthiraptera) is often heavily influenced by host taxonomy. The use of host information to define genera of avian lice in the widespread Degeeriella complex has been prevalent but has created problems. Several workers have suggested that genera defined on the basis of host association are not monophyletic. We used sequences of nuclear (elongation factor-1alpha) and mitochondrial (cytochrome oxidase I) genes to test the monophyly of several genera in the Degeeriella complex. Parsimony and likelihood analyses of these data indicated that many genera in the Degeeriella complex are not monophyletic, such that species occurring on the same host groups do not form monophyletic groups. Biological features of hosts (including predaceous habits, brood parasitism, and hole nesting) for species in the Degeeriella complex likely provide opportunities for switching of lice between host groups. In addition, dispersal of lice via phoresy on hippoboscid flies also likely provides opportunities for host switching in the Degeeriella complex. This study indicates that the overuse of host taxonomy in louse taxonomy can result in classifications that do not reflect phylogenetic history.     

Correlated evolution of host and parasite body size: tests of Harrison's rule using birds and lice

Large-bodied species of hosts often harbor large-bodied parasites, a pattern known as Harrison's rule. Harrison's rule has been documented for a variety of animal parasites and herbivorous insects, yet the adaptive basis of the body-size correlation is poorly understood. We used phylogenetically independent methods to test for Harrison's rule across a large assemblage of bird lice (Insecta: Phthiraptera). The analysis revealed a significant relationship between louse and host size, despite considerable variation among taxa. We explored factors underlying this variation by testing Harrison's rule within two groups of feather-specialist lice that share hosts (pigeons and doves). The two groups, wing lice (Columbicola spp.) and body lice (Physconelloidinae spp.), have similar life histories, despite spending much of their time on different feather tracts. Wing lice showed strong support for Harrison's rule, whereas body lice showed no significant correlation with host size. Wing louse size was correlated with wing feather size, which was in turn correlated with overall host size. In contrast, body louse size showed no correlation with body feather size, which also was not correlated with overall host size. The reason why body lice did not fit Harrison's rule may be related to the fact that different species of body lice use different microhabitats within body feathers. More detailed measurements of body feathers may be needed to explore the precise relationship of body louse size to relevant components of feather size. Whatever the reason, Harrison's rule does not hold in body lice, possibly because selection on body size is mediated by community-level interactions between body lice.     

Biogeography and comparative ecology of testate amoebae inhabiting Sphagnum-dominated peatlands in the Great Lakes and Rocky Mountain regions of North America

Testate amoebae (Protozoa: Rhizopoda) are common inhabitants of peatlands. Strong relationships between community composition and substrate moisture in Sphagnum‐dominated peatlands have made them particularly useful as hydrological proxies in environmental and palaeoenvironmental research. However, stability of these relationships in geographical space is important for widespread applicability. In this study, we compared testate amoeba communities inhabiting Sphagnum‐dominated peatlands of the Great Lakes and Rocky Mountain regions of North America. Our primary objectives were to describe patterns of community composition in the two regions, develop hypotheses to explain differences, and determine if taxa occupy similar ecological niches with respect to substrate moisture in both places. Our results indicated that testate amoeba communities are relatively different in the two regions, and these differences are probably caused by differences in climate and peatland trophic status, although other factors may also play a role. However, many taxa do occur in both regions and these taxa had comparable moisture preferences in each region, suggesting that the ecological niches of taxa with respect to substrate moisture are similar even within communities of relatively different composition.     

Larval habits, host-plant associations, and speciation in nematine sawflies (Hymenoptera: Tenthredinidae)

Adaptive radiations consist of two intertwined processes, diversification of species and diversification of their ecological niches, but it is unclear whether there is a causal link between the processes. In phytophagous insects, ecological diversification mainly involves shifts in host-plant associations and in larval feeding habits (internal or external) on different plant parts, and several observations indicate that speciation is facilitated by host shifts. Data on host use in individual species suggest that internal feeders are less likely to colonize new hosts than external-feeding taxa and, consequently, increases in collective host ranges and species numbers should be slowed down in endophagous lineages. We tested these related hypotheses by using phylogenetic information to reconstruct the evolutionary history of larval resource use in the sawfly subfamily Nematinae, a group of 1000 plus species with a broad range of niches: the subfamily's combined host range includes over 20 plant families, and larvae may feed externally on leaves or needles, or internally, for example, in buds, fruits, leaves, or galls. The results show that: (1) Most internally feeding groups have evolved independently from external-feeding ancestors, but several distinct internal habits have appeared convergently multiple times; (2) Shifts among host taxa are clearly more common than changes in larval habits; (3) The majority of host switches have occurred among phylogenetically close plant groups, but many shifts are manifest among distantly related, ecologically proximate hosts; (4) Although external feeding characteristic of the common ancestor of Nematinae is associated with relatively high rates of host-shifting, internal feeders are very conservative in their host use; (5) In contrast, the effect of endophagy on speciation probabilities is more variable: net speciation rates are lowered in most internal-feeding groups, but a striking exception is found in species that induce galls on Salicaceae. The loose connection between collective host ranges and species diversity provides empirical support for theoretical models suggesting that speciation rates are a function of a complex interplay between "intrinsic" niche width and resource heterogeneity.     

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.     

Unexpected distribution patterns of Carduiceps feather lice (Phthiraptera: Ischnocera: Philopteridae) on sandpipers (Aves: Charadriiformes: Scolopacidae)

The louse genus Carduiceps Clay & Meinertzhagen, 1939 is widely distributed on sandpipers and stints (Calidrinae). The current taxonomy includes three species on the Calidrinae (Carduiceps meinertzhageni, Carduiceps scalaris, Carduiceps zonarius) and four species on noncalidrine hosts. We estimated a phylogeny of four of the seven species of Carduiceps (the three mentioned above and Carduiceps fulvofasciatus) from 13 of the 29 hosts based on three mitochondrial loci, and evaluated the relative importance of flyway differentiation (same host species has different lice along different flyways) and flyway homogenization (different host species have the same lice along the same flyway). We found no evidence for either process. Instead, the present, morphology‐based, taxonomy of the genus corresponds exactly to the gene‐based phylogeny, with all four included species monophyletic. Carduiceps zonarius is found both to inhabit a wider range of hosts than wing lice of the genus Lunaceps occurring on the same group of birds, and to occur on Calidris sandpipers of all sizes, both of which are unexpected for a body louse. The previously proposed family Esthiopteridae is found to be monophyletic with good support. The concatenated dataset suggests that the pigeon louse genus Columbicola may be closely related to the auk and diver louse genus Craspedonirmus. These two genera share some morphological characters with Carduiceps, but no support was obtained for grouping these three genera together. Based on mitochondrial data alone, the relationships among genera within this proposed family cannot be properly assessed, but some previously suggested relationships within this proposed family are confirmed.     

Phylogenomics and host-switching patterns of Philopteridae (Psocodea: Phthiraptera) feather lice

Philopteridae feather lice are a group of ectoparasitic insects which have intimate relationships with their avian hosts. Feather lice include an enormous number of described species; however, the relationships of major lineages have been clouded by homoplasious characters due to convergent evolution. In this study, a comprehensive phylogenomic analysis of the group is performed which includes 137 feather louse species. Several other analyses are also completed including dating analysis, cophylogenetic reconstructions, and ancestral character estimation to understand the evolution of complex morphological and ecological traits. Phylogenetic results recover high support for the placement of major feather louse lineages, but with lower support for long-branched enigmatic genera found at the base of the tree. The results of dating analyses suggest modern feather lice began to diversify approximately 49 million years ago following the adaptive radiation of their avian hosts. Cost-based cophylogenetic reconstructions recover a high frequency of host switching, while congruence-based methods indicate a significant level of congruence between host and parasite trees. Ancestral state reconstructions favour a generalist ancestor and water bird host at the root. The analyses completed provide insight into the evolution of a diverse group of ectoparasitic insects which infest a wide variety of avian hosts. The results represent the most comprehensive phylogenetic hypothesis of the group to date and provide a framework for future classification of the family into natural groupings.     

Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura)

Background  

Sucking lice (Phthiraptera: Anoplura) are obligate, permanent ectoparasites of eutherian mammals, parasitizing members of 12 of the 29 recognized mammalian orders and approximately 20% of all mammalian species. These host specific, blood-sucking insects are morphologically adapted for life on mammals: they are wingless, dorso-ventrally flattened, possess tibio-tarsal claws for clinging to host hair, and have piercing mouthparts for feeding. Although there are more than 540 described species of Anoplura and despite the potential economical and medical implications of sucking louse infestations, this study represents the first attempt to examine higher-level anopluran relationships using molecular data. In this study, we use molecular data to reconstruct the evolutionary history of 65 sucking louse taxa with phylogenetic analyses and compare the results to findings based on morphological data. We also estimate divergence times among anopluran taxa and compare our results to host (mammal) relationships.     

Molecular systematics of the bark lice infraorder Caeciliusetae (Insecta: Psocodea)

The phylogenetic relationships of bark lice and parasitic lice (Insecta: Psocodea) have been studied in a number of recent molecular phylogenetic analyses based on DNA sequences. Many of these studies have focused on the position of parasitic lice within the free‐living bark lice. However, fewer such studies have examined the relationships among major groups of free‐living bark lice and their implications for classification. In this study we focus on the infraorder Caeciliusetae, a large group of bark lice (?1000 species) within the suborder Psocomorpha. Using sequences of two mitochondrial and two nuclear genes, we estimated the phylogeny for relationships among the five recognized families within the infraorder Caeciliusetae. Based on the results, the sister‐group relationship and respective monophyly of Stenopsocidae and Dasydemellidae is strongly supported. Monophyly of the larger families Amphipsocidae and Caeciliusidae was not supported, although the causes of this were the placement of two distinct subfamilies (Paracaeciliinae and Calocaeciliinae). The monophyly of Asiopsocidae could not be tested because it was sampled only by one species. Based on these results and consideration of morphological characters, we propose a new classification for Caeciliusetae, recognizing six families: Amphipsocidae, Stenopsocidae, Dasydemellidae, Asiopsocidae, Paracaeciliidae and Caeciliusidae. We expect that this new classification will stabilize the higher‐level taxonomy of this group and help to identify groups in need of further work among these insects.     

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.     

Avian louse phylogeny (Phthiraptera: Ischnocera): a cladistic study based on morphology

The louse suborder Ischnocera (Phthiraptera) contains 3060 currently described species from over 150 genera. These lice are permanent obligatory ectoparasites of a diverse selection of birds and mammals with a worldwide distribution. Historically, they have played a major role in the development of our ideas on coevolution, and species hosted by mammals have been used extensively as model organisms for the study of cospeciation. In contrast, avian taxa comprising 90% of ischnoceran species have been neglected due to a lack of data on their wider systematics. A comparative study based on the adult and nymphal instar morphology of avian lice yielded 138 characters from 56 species (51 genera), all of which are illustrated or discussed here for the first time. A further five outgroup taxa were examined from the mammalian ischnoceran family Trichodectidae. Phylogenetic analyses of these data produced three most parsimonious cladograms, the strict consensus of which is highly resolved and broadly consistent with previous classifications. Morphological character variation is extensive, and nymphal character traits are useful in identifying instances of convergent evolution in adult morphology. The role of ontogeny in the development of the major character complexes of the head and abdomen is discussed, and its implications for further work on the phylogeny of avian Ischnocera is considered. Comparison with host taxonomy reveals a series of complex host-parasite associations that do not support a hypothesis of strict one to one cospeciation. However, extrapolation of these associations is compromised by the low sample size. The role of niche specialization to explain the presence of multiple unrelated lineages on the same host taxon is considered.     

Ecological niches of ectoparasites

On mammals and birds communities of ectoparasites are present, which can include scores of ticks, mites and insects species. The parasitizing of arthropods terrestrial vertebrates appeared as far back a the Cretaceous period, and after 70-100 mil. years of the coevolution ectoparasites have assimilated all food resources and localities of the hosts' bodies. To the present only spatial and (to the less extent) trophic niches of parasitic insects, ticks and mites are studied completely enough. The main results these investigations are discussed in the present paper. A high abundance of the communities is reached because of their partition into the number of ecological niches. Host is complex of ecological niches for many ectoparasites species. These niches reiterate in the populations of a species closely related species of hosts and repeat from generation to generation. The each part of host (niche) being assimilated be certain parasite species is available potentially for other species. The partition of host into ecological niches is clearer than the structure of ecosystems including free-living organisms. A real extent of the ecological niches occupation by different species of ticks, mites and insects is considerably lower than a potential maximum. The degree of ecological niches saturation depends on the history of the coevolution of parasites community components, previous colonization be new ectoparasite species and many other ecological factors affecting host-parasite system. The use of the ecological niche conception in parasitology is proved to be rather promising. Ectoparasites communities because of their species diversity, different types of feeding and a number of habitats on host represent convenient models and study of them can contribute significantly to the developmeht of the general conception of ecological niche.     

Cryptic diversity in the genus <Emphasis Type="Italic">Adineta</Emphasis> Hudson &; Gosse, 1886 (Rotifera: Bdelloidea: Adinetidae): a DNA taxonomy approach

Cryptic species are continuously discovered in rotifers using different methods to delineate these units of diversity. DNA taxonomy is the most effective method taxonomists have to untie potential cryptic taxa. Here, we estimate hidden diversity in a genus of bdelloid rotifers, Adineta. We analyse cryptic diversity using a coalescent approach to infer evolutionarily significant units from a phylogenetic tree obtained from cytochrome oxidase I sequences. Cryptic diversity was measured for eight traditional species and from several additional undetermined populations. Taxonomic inflation of up to 36 taxa was found in A. vaga from DNA taxonomy. As observed in other microscopic organisms, cryptic taxa within each traditional species were not geographically isolated, but had significantly narrower ecological niches than expected by chance alone.     

Independent origins of the feather lice (Insecta: Degeeriella) of raptors

Although diurnal birds of prey have historically been placed in a single order due to a number of morphological characters, recent molecular phylogenies have suggested that this is a case of convergence rather than homology, with hawks (Accipitridae) and falcons (Falconidae) forming two distantly related groups within birds. The feather lice of birds have often been used as a model for comparing host and parasite phylogenies, and in some cases there is significant congruence between the two. Thus, studying the phylogeny of the lice of diurnal raptors may be of particular interest with respect to the independent evolution of hawks vs. falcons. Using one mitochondrial gene and three nuclear genes, we inferred a phylogeny for the feather louse genus Degeeriella (which are all obligate raptor ectoparasites) and related genera. This phylogeny indicated that Degeeriella is polyphyletic, with lice from falcons vs. hawks forming two distinct clades. Falcon lice were sister to lice from African woodpeckers, whereas Capraiella, a genus of lice from rollers lice, was embedded within Degeeriella from hawks. This phylogeny showed significant geographical structure, with host geography playing a larger role than host taxonomy in explaining louse phylogeny, particularly within clades of closely related lice. However, the louse phylogeny does reflect host phylogeny at a broad scale; for example, lice from the hawk genus Accipiter form a distinct clade. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 837–847.     

Non-lichenized Antarctic fungi: transient visitors or members of a cryptic ecosystem?

To date over 1 000 non-lichenized fungal species have been recorded by collection or isolation from Antarctica, and additional taxa are now being identified by molecular studies. The number and variety of species recorded so far suggest that the fungi may be the most diverse biota in the Antarctic, and the additional taxa identified by molecular surveys suggest that the true diversity may be far greater than is currently estimated. Fungi occupy many different ecological niches in the Antarctic, and their significance in these niches is only poorly understood. The majority of species described from the region have been identified as members of broadly cosmopolitan groups, but there is some evidence for both endemic strains and populations. This review brings together the current broad systematic and ecological findings for the non-lichenized Antarctic fungi.     

Cophylogenetic patterns are uncorrelated between two lineages of parasites on the same hosts

Free‐living organisms are often host to multiple lineages of closely related parasites. Different lineages of obligate parasites living on the same hosts might potentially be expected to display similar cophylogenetic patterns. However, there are also reasons why these lineages might have different evolutionary histories (e.g. host switching, host geography). In the present study, we use mitochondrial and nuclear DNA sequence data to evaluate the cophylogenetic patterns between doves and their wing and body lice. Previous studies have found that the wing and body lice of doves have different levels of congruence between their phylogenetic histories. However, these studies are limited in scope, either taxonomically or geographically. We used both new and existing data to generate a worldwide and taxonomically diverse data set for doves and two independent groups of lice: wing and body lice. Using event and topology‐based methods, we found that cophylogenetic patterns were not correlated between wing and body lice, even though both groups showed evidence of cospeciation with their hosts. These results indicate that external factors vary in their impact on different groups of parasites and also that broad sampling is critical for identifying patterns in cophylogenetic analyses.     

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.     

Revision of Dennyus (Collodennyus) lice (Phthiraptera: Menoponidae) from swiftlets, with descriptions of new taxa and a comparison of host–parasite relationships

Lice of the subgenus Dennyus ( Collodennyus ) are host specific, permanent parasites of swiftlets (Aves: Apodidae). As a prelude to a test of the hypothesis that these lice have cospeciated with their hosts, we revise the taxonomy of the subgenus, redescribing the seven previously recognized species, and adding thirteen new species and three new subspecies. All twenty-three of these louse taxa are found on swiftlets (Apodiformes: Apodidae), with four from hosts of the genus Collocalia , eighteen from Aerodramus , and one from Hydrochous . Successful identification is associated in most cases with females; males are only tenuously separable. A complete host–parasite list for the subgenus Collodennyus is provided, as well as a key for the identification of these taxa. Limited morphological variation within the subgenus has prevented ready extraction of discrete characters for cladistic analysis. In the absence of such characters, a cluster analysis of female and male lice is presented. Comparison of a dendrogram for Dennyus ( Collodennyus ) with a molecular phylogeny for the swiftlet hosts suggests that the history of the swiftlet–louse association has been complex, including episodes of host switching and independent speciation by the lice.     

Ecology and Feeding Habits Drive Infection of Water Bugs with <Emphasis Type="Italic">Mycobacterium ulcerans</Emphasis>

Mycobacterium ulcerans (MU), the causative agent of Buruli ulcer, is present in a wide spectrum of environments, including terrestrial and aquatic ecosystems in tropical regions. The most promising studies on the epidemiological risk of this disease suggest that some ecological settings may favor infection of animals with MU including human. A species’ needs and impacts on resources and the environment, i.e., its ecological niche, may influence its susceptibility to be infected by this microbial form. For example, some Naucoridae may dive in fresh waters to prey upon infected animals and thus may get infected with MU. However, these studies have rarely considered that inference on the ecological settings favoring infection and transmission may be confounded because host carrier sister species have similar ecological niches, and potentially the same host–microbe interactions. Hence, a relationship between the ecological niche of Naucoridae and its infection with MU may be due to a symbiotic relationship between the host and the pathogen, rather than its ecological niche. To account for this confounding effect, we investigated the relationships between surrogates of the ecological niche of water bug species and their susceptibility to MU, by performing phylogenetic comparative analyses on a large dataset of 11 families of water bugs collected in 10 different sites across Cameroon, central Africa. Our results indicate that MU circulates and infects a couple of host taxa, i.e., Belostomatidae, Naucoridae, living both in the aquatic vegetation and as predators inside the trophic network and sister species of water bugs have indeed similar host–microbe interactions with MU.