Molecular phylogeny and novel host associations of avian chewing lice (Insecta: Phthiraptera) from South Africa

Compared with Europe and the Americas, the ectoparasites of African birds are poorly understood, despite the avian fauna being relatively well known. Notably, previous studies documenting the host associations and genetic diversity of parasitic chewing lice of southern African birds have been limited in geographic and taxonomic scope. Recent field expeditions exploring the avian diversity in South Africa facilitated an opportunity to obtain louse specimens from a taxonomically diverse host assemblage. This study is the first to investigate avian louse host associations and diversity across a large portion of South Africa encompassing several distinct habitat types, while incorporating molecular genetic data (from portions of the mitochondrial COI and nuclear EF‐1α genes) for ectoparasite phylogenetic analyses. From 1105 South African bird individuals and 170 species examined for lice, a total of 105 new louse–host associations were observed. Morphological and genetic examination of lice with these new host associations reveals a maximum of 66 louse species new to science. Results of this study support the observation that examining museum specimens is a useful way to investigate louse diversity and host associations.     

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.     

River barriers and cryptic biodiversity in an evolutionary museum

The Riverine Barriers Hypothesis (RBH) posits that tropical rivers can be effective barriers to gene flow, based on observations that range boundaries often coincide with river barriers. Over the last 160 years, the RBH has received attention from various perspectives, with a particular focus on vertebrates in the Amazon Basin. To our knowledge, no molecular assessment of the RBH has been conducted on birds in the Afrotropics, despite its rich avifauna and many Afrotropical bird species being widely distributed across numerous watersheds and basins. Here, we provide the first genetic evidence that an Afrotropical river has served as a barrier for birds and for their lice, based on four understory bird species collected from sites north and south of the Congo River. Our results indicate near‐contemporaneous, Pleistocene lineage diversification across the Congo River in these species. Our results further indicate differing levels of genetic variation in bird lice; the extent of this variation appears linked to the life‐history of both the host and the louse. Extensive cryptic diversity likely is being harbored in Afrotropical forests, in both understory birds and their lice. Therefore, these forests may not be “museums” of old lineages. Rather, substantial evolutionary diversification may have occurred in Afrotropical forests throughout the Pleistocene, supporting the Pleistocene Forest Refuge Hypothesis. Strong genetic variation in birds and their lice within a small part of the Congo Basin forest indicates that we may have grossly underestimated diversity in the Afrotropics, making these forests home of substantial biodiversity in need of conservation.     

Influence of host ecology and morphology on the diversity of Neotropical bird lice

Host‐parasite systems can be powerful arenas in which to explore factors influencing community structure. We used a comparative approach to examine the influence of host ecology and morphology on the diversity of chewing lice (Insecta: Phthiraptera) among 52 species of Peruvian birds. For each host species we calculated two components of parasite diversity: 1) cumulative species richness, and 2) mean abundance. We tested for correlations between these parasite indices and 13 host ecological and morphological variables. Host ecological variables included geographic range size, local population density, and microhabitat use. Host morphological variables included body mass, plumage depth, and standard dimensions of bill, foot and toenail morphology, all of which could influence the efficiency of anti‐parasite grooming. Data were analysed using statistical and comparative methods that control for sampling effort and host phylogeny. None of the independent host variables correlated with louse species richness when treated as a dependent variable. When richness was treated as an independent variable, however, it was positively correlated with mean louse abundance. Host body mass was also positively correlated with mean louse abundance. When louse richness and host body mass were held constant, mean louse abundance correlated negatively with the degree to which the upper mandible of the host's bill overhangs the lower mandible. This correlation suggests that birds with longer overhangs are better at controlling lice during preening. We propose a specific functional hypothesis in which preening damages lice by exerting a shearing force between the overhang and the tip of the lower mandible. This study is the first to suggest a parasite‐control function of such a detailed component of bill morphology across species. Avian biologists have traditionally focused almost exclusively on bills as tools for feeding. We suggest that the adaptive radiation of bill morphology should be reinterpreted with both preening and feeding in mind.     

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.     

Rodent louse diversity,phylogeny, and cospeciation in the Manu Biosphere Reserve,Peru

We investigated the diversity, cophylogenetic relationships, and biogeography of hoplopleurid sucking lice (Phthiraptera: Anoplura) parasitizing rodents (Muridae: Sigmodontinae) in the Manu National Park and Biosphere Reserve. Our morphological and molecular studies reveal that 15 distinct louse species parasitize 19 rodent species. Three of these louse species are new to science, and all but two of the host associations were previously unknown. We find that hoplopleurid lice in South America parasitize multiple host species across a large geographic area, and that Peru represents a new geographic locality for almost all the louse species collected in the present study. Phylogenetic analyses of mitochondrial and nuclear data reveal that the louse family Hoplopleuridae and the genera Hoplopleura and Pterophthirus are not monophyletic, and lice do not appear to group by host tribe, collecting locality, or collection elevation. The lack of monophyly for these apparently natural groups (taxonomic, locality, and elevation) indicates that host switching with or without parasite speciation may be prevalent among hoplopleurid lice. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 598–610.     

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.     

Comparative body size relationships in pocket gophers and their chewing lice

In this paper, we use the method of independent contrasts to study body size relationships between pocket gophers and their chewing lice, a host-parasite system in which both host and parasite phylogcnies are well studied. The evolution of body size of chewing lice appears to be dependent only on the body size of their hosts, which confirms the 1991 findings of Harvey and Keymer. We show that there is a positive relationship between body size and hair-shaft diameter in pocket gophers, and that there is also a positive relationship between body size and head-groove width in chewing lice. Finally, we show a positive relationship between gopher hair-shaft diameter and louse head-groove width. We postulate that changes in body size of chewing lice are driven by a mechanical relationship between the parasite's head-groove dimension and the diameter of the hairs of its host. Louse species living"on larger host species may be larger simply because their hosts have thicker hairs, which requires that the lice have a wider head groove. Our study of gopher hair-shaft diameter and louse head-groove dimensions suggest that there is a 'lock-and-key' relationship between these two anatomical features.     

Dispersal ecology versus host specialization as determinants of ectoparasite distribution in brood parasitic indigobirds and their estrildid finch hosts

Brood parasitic birds offer a unique opportunity to examine the ecological and evolutionary determinants of host associations in avian feather lice (Phthiraptera). Brood parasitic behaviour effectively eliminates vertical transfer of lice between parasitic parents and offspring at the nest, while at the same time providing an opportunity for lice associated with the hosts of brood parasites to colonize the brood parasites as well. Thus, the biology of brood parasitism allows a test of the relative roles of host specialization and dispersal ecology in determining the host-parasite associations of birds and lice. If the opportunity for dispersal is the primary determinant of louse distributions, then brood parasites and their hosts should have similar louse faunas. In contrast, if host-specific adaptations limit colonization ability, lice associated with the hosts of brood parasites may be unable to persist on the brood parasites despite having an opportunity for colonization. We surveyed lice on four brood parasitic finch species (genus Vidua), their estrildid finch host species, and a few ploceid finches. While Brueelia lice were found on both parasitic and estrildid finches, a molecular phylogeny showed that lice infesting the two avian groups belong to two distinct clades within Brueelia. Likewise, distinct louse lineages within the amblyceran genus Myrsidea were found on estrildid finches and the parasitic pin-tailed whydah (Vidua macroura), respectively. Although common on estrildid finches, Myrsidea lice were entirely absent from the brood parasitic indigobirds. The distribution and relationships of louse species on brood parasitic finches and their hosts suggest that host-specific adaptations constrain the ability of lice to colonize new hosts, at least those that are distantly related.     

A hitchhiker’s guide to parasite transmission: The phoretic behaviour of feather lice

Transmission to new hosts is a fundamental challenge for parasites. Some species meet this challenge by hitchhiking on other, more mobile parasite species, a behaviour known as phoresis. For example, feather-feeding lice that parasitise birds disperse to new hosts by hitchhiking on parasitic louse flies, which fly between individual birds. Oddly, however, some species of feather lice do not engage in phoresis. For example, although Rock Pigeon (Columba livia) “wing” lice (Columbicola columbae) frequently move to new hosts phoretically on louse flies (Pseudolynchia canariensis), Rock Pigeon “body” lice (Campanulotes compar) do not. This difference in phoretic behaviour is puzzling because the two species of lice have very similar life cycles and are equally dependent on transmission to new hosts. We conducted a series of experiments designed to compare the orientation, locomotion and attachment capabilities of these two species of lice, in relation to louse flies. We show that wing lice use fly activity as a cue in orientation and locomotion, whereas body lice do not. We also show that wing lice are more capable of remaining attached to active flies that are walking, grooming or flying. The superior phoretic ability of wing lice may be related to morphological adaptations for life on wing feathers, compared to body feathers.     

On the ubiquity and phylogeny of Wolbachia in lice

Wolbachia are intracellular bacteria that occur in an estimated 20% of arthropod species. They are of broad interest because they profoundly affect the reproductive fitness of diverse host taxa. Here we document the apparent ubiquity and diversity of Wolbachia in the insect orders Anoplura (sucking lice) and Mallophaga (chewing lice), by detecting single or multiple infections in each of 25 tested populations of lice, representing 19 species from 15 genera spanning eight taxonomic families. Phylogenetic analyses indicate a high diversity of Wolbachia in lice, as evidenced by the identification of 39 unique strains. Some of these strains are apparently unique to lice, whereas others are similar to strains that infect other insect taxa. Wolbachia are transmitted from infected females to their offspring via egg cytoplasm, such that similar species of lice are predicted to have similar strains of Wolbachia. This predicted pattern is not supported in the current study and may reflect multiple events of recent horizontal transmission between host species. At present, there is no known mechanism that would allow for this latter mode of transmission to and within species of lice.     

Integrating phylogenomic and population genomic patterns in avian lice provides a more complete picture of parasite evolution

Parasite diversity accounts for most of the biodiversity on earth, and is shaped by many processes (e.g., cospeciation, host switching). To identify the effects of the processes that shape parasite diversity, it is ideal to incorporate both deep (phylogenetic) and shallow (population) perspectives. To this end, we developed a novel workflow to obtain phylogenetic and population genetic data from whole genome sequences of body lice parasitizing New World ground‐doves. Phylogenies from these data showed consistent, highly resolved species‐level relationships for the lice. By comparing the louse and ground‐dove phylogenies, we found that over long‐term evolutionary scales their phylogenies were largely congruent. Many louse lineages (both species and populations) also demonstrated high host‐specificity, suggesting ground‐dove divergence is a primary driver of their parasites’ diversity. However, the few louse taxa that are generalists are structured according to biogeography at the population level. This suggests dispersal among sympatric hosts has some effect on body louse diversity, but over deeper time scales the parasites eventually sort according to host species. Overall, our results demonstrate that multiple factors explain the patterns of diversity in this group of parasites, and that the effects of these factors can vary over different evolutionary scales. The integrative approach we employed was crucial for uncovering these patterns, and should be broadly applicable to other studies.     

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).     

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.     

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.     

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.     

Chewing lice (Phthiraptera) from wild birds in southern Portugal

This study was carried out to determine chewing louse species of wild birds in the Ria Formosa Natural Park, located in southern Portugal. In addition, the hypothesis that bird age, avian migration and social behaviour have an impact on the louse prevalence was tested. Between September and December of 2013, 122 birds (belonging to 10 orders, 19 families, 31 genera and 35 species) captured in scientific ringing sessions and admitted to the Wildlife Rehabilitation and Investigation Centre of Ria Formosa were examined for lice. Twenty-six (21.3%) birds were found to be infested with at least one chewing louse species. The chewing lice identified include 18 species. Colonial birds (34.9%) and migratory birds (29.5%) had statistically significant higher prevalence than territorial birds (6.8%) and resident birds (13.1%), respectively. This paper records 17 louse species for the first time in southern Portugal: Laemobothrion maximum, Laemobothrion vulturis, Actornithophilus piceus lari, Actornithophilus umbrinus, Austromenopon lutescens, Colpocephalum heterosoma, Colpocephalum turbinatum, Eidmanniella pustulosa, Nosopon casteli, Pectinopygus bassani, Pseudomenopon pilosum, Trinoton femoratum, Trinoton querquedulae, Craspedorrhynchus platystomus, Degeeriella fulva, Falcolipeurus quadripustulatus, Lunaceps schismatus. Also a nymph of the genus Strigiphilus was collected from a Eurasian eagle-owl. These findings contribute to the knowledge of avian chewing lice from important birds areas in Portugal.     

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.     

Experimental evidence for costs due to chewing lice in the European bee-eater (Merops apiaster)

Animals frequently host organisms on their surface which can be beneficial, have no effect or a negative effect on their host. Ectoparasites, by definition, are those which incur costs to their host, but these costs may vary. Examples of avian ectoparasites are chewing lice which feed exclusively on dead feather or skin material; therefore, costs to their bird hosts are generally considered small. Theoretically, many possible proximate effects exist, like loss of tissue or food, infected bites, transmission of microparasitic diseases or reduced body insulation due to loss of feathers, which may ultimately also have fitness consequences. Here, we experimentally examined a possible negative impact of 2 feather-eating louse species (Meropoecus meropis and Brueelia apiastri) on male and female European bee-eaters (Merops apiaster) by removing or increasing louse loads and comparing their impact to a control group (lice removed and immediately returned) after 1 month. A negative effect of chewing lice was found on body mass and sedimentation rate and to a lesser extent on haematocrit levels. Males and females lost more weight when bearing heavy louse loads, and were more susceptible to infestations as indicated by the higher sedimentation rate. Our results further suggest differences in sex-specific susceptibility.