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.     

Phylogeny and classification of the Psocodea, with particular reference to the lice (Psocodea: Phthiraptera)

ABSTRACT. Apomorphies that have been proposed for the Psocodea, Psocoptera, Phthiraptera and superfamilial groups within the Phthiraptera are enumerated and evaluated. The Psocodea and Phthiraptera are considered to be holophyletic, but the sister-group of the Phthiraptera lies within the Psocoptera. Within the Phthiraptera the Anoplura and Rhyncophthirina form a holophyletic group whose sister-group is the Ischnocera, and the Amblycera is the sister-group of this assemblage. The common ancestor of the Phthiraptera is suggested to have been parasitic, and all lice are believed to have evolved under environmental constraints similar to those operating today. On the evidence provided by host relationships the origin of the lice is dated as the Cretaceous, but the host of the ancestor of the order is not identified. The lice of marsupials in South America and Australia are not considered to comprise a holophyletic group.     

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.     

Ectoparasites, uropygial glands and hatching success in birds

The uropygial gland of birds secretes wax that is applied to the plumage, where the secretions are hypothesized to eliminate fungi and bacteria, thereby potentially providing important benefits in terms of plumage maintenance. We analyzed variation in size of the uropygial gland in 212 species of birds to determine the function and the ecological correlates of variation in gland size. Bird species with larger uropygial glands had more genera of chewing lice of the sub-order Amblycera, but not of the sub-order Ischnocera, and more feather mites. There was a fitness advantage associated with relatively large uropygial glands because such species had higher hatching success. These findings are consistent with the hypothesis that the uropygial gland functions to manage the community of microorganisms, and that certain taxa of chewing lice have diverged as a consequence of these defenses.     

Ectoparasites of northern fulmars Fulmarus glacialis (Procellariiformes: Procellariidae) from the Canadian Arctic

We studied the prevalence and intensity of infestation of ectoparasites on northern fulmars (Fulmarus glacialis L.) from a breeding colony in Arctic Canada in June–August 2003. No fleas or ticks were found on any fulmars, but three species of chewing lice (Phthiraptera) were recorded: Ischnocera: Perineus nigrolimbatus (Giebel 1874), Ischnocera: Saemundssonia occidentalis (Kellogg 1896), and Amblycera: Ancistrona vagelli (Fabricius 1787). Non-breeding birds had a higher prevalence of lice than breeding birds, and prevalence varied markedly among louse species. Our study is an important baseline for the occurrence of ectoparasites on northern fulmars in the high Arctic, a region undergoing extensive environmental change due to global warming, and an area where parasites are expected to extend ranges or increase in prevalence under changing annual temperature regimes.     

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.     

Chewing lice from high‐altitude and migrating birds in Yunnan,China, with descriptions of two new species of Guimaraesiella

In total, 366 birds representing 55 species in 24 families and eight orders, were examined for chewing lice (Phthiraptera: Amblycera, Ischnocera) in two high‐altitude localities in Yunnan Province, China. In Ailaoshan, almost all of the birds examined were resident passeriforms, of which 36% were parasitized by chewing lice. In Jinshanyakou, most birds were on migration, and included both passerine and non‐passerine birds. Of the passerine birds caught in Jinshanyakou, only one bird (0.7%) was parasitized by chewing lice. The prevalence of Myrsidea and Brueelia‐complex lice on birds caught in Ailaoshan was higher than in previous reports. Of the chewing lice identifiable to species level, three represent new records for China: Actornithophilus hoplopteri (Mjöberg, 1910), Maculinirmus ljosalfar Gustafsson & Bush, 2017 and Quadraceps sinensis Timmermann, 1954. In total, 17 new host records are included, of which we describe two as new species in the Brueelia‐complex: Guimaraesiella (Cicchinella) ailaoshanensis sp. nov. ex Schoeniparus dubius dubius (Hume, 1874) and G. (C.) montisodalis sp. nov. ex Fulvetta manipurensis tonkinensis Delacour & Jabouille, 1930. This published work has been registered in ZooBank, http://zoobank.org/urn:lsid:zoobank.org:pub:9FC3D8EE‐2CED‐4DBE‐A1DB‐471B71260D27 .     

The water-vapour uptake system of the phthiraptera

The occurrence of active water-vapour uptake was examined in 16 Phthirapteran species representing the two groups of biting lice or Mallophaga (Amblycera and Ischnocera) and the sucking lice or Anoplura. Water-vapour uptake could not be demonstrated in the Anoplura and although it is frequently encountered in the biting lice, some members of both the Ischnocera and Amblycera lack the faculty. Uptake performance in the absorbing species of biting lice is exceptionally efficient showing higher rates and lower thresholds than other absorbing arthropods. The critical equilibrium humidities were found to range between 43 and 52% r.h., 43% being the lowest value so far reported. The uptake rates, expressed as a percentage of total body water mass, by far surpass those of all other arthropods investigated. The Phthirapteran uptake pattern closely resembles that of the Psocoptera, showing abrupt initiation and termination of the uptake process, limitation of continuous absorption to relatively short periods of time and constancy of the absorption rate over the entire period of continuous uptake. Studies on the uptake site and mechanism in Phthiraptera revealed an oral-uptake system which is congruous with that of the Psocoptera. The structural components of the uptake device, like a pair of oval lingual sclerites, representing the site of water-vapour condensation and a cibarial sucking pump which is connected by a paired or branching selerotized tubule to the lingual selerites and is responsible for the transfer of the condensed water to the gut, are unique acquisitions of the Psocodea.In those members of the biting lice which have lost the faculty of water-vapour uptake the structural components of the uptake system are modified or reduced.     

Arthropods--the pelage of mammals as an environment

The problem of lousiness in nature is usually not why are a few hosts heavily infested, it is why does the majority of the host population carry so few lice. The reproductive potentials described have probably been selected to enable these survivals. Anoplura have exploited the pelage of mammals the best. Their food, blood, is available over just about the whole body, and is a diet that supplies sufficient water for the increases in egg production only seen in this group. At least 70% of an egg is water. They have also a great capacity to change their generation time. The Trichodectidae feed at the epidermals surface on keratin, skin gland secretions and bacteria. These change in quality and abundance over the body and seasonally. The diet is limited in free moisture which together with the small size of the louse apparently restricts daily egg production. Parthenogenic reproduction is found in this group. Aspects of the biology of the Boopiidae on marsupials appear to parallel both anopluran and ischnoceran lice.Several species may infest one host, and they or their strains may infest different parts of the same host. Their ecology is not the same, and what may be catastrophic to one is not necessarily catastrophic to another. Although it is convenient to consider a population of lice as that found on a single host, the evolutionary unit is a population of hosts. The environments within the pelages of a population of hosts are not identical, so some lice may survive catastrophies, the surviving populations providing the insects for subsequent dispersal and repopulation.     

Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts

Antagonistic host-parasite interactions lead to coevolution of host defenses and parasite virulence. Such adaptation by parasites to host defenses may occur to the detriment of the ability of parasites to exploit alternative hosts, causing parasite specialization and speciation. We investigated the relationship between level of anti-parasite defense in hosts and taxonomic richness of two chewing louse suborders (Phthiraptera: Amblycera, Ischnocera) on birds. While Amblyceran lice tend to occur in contact with host skin, feed on host skin and chew emerging tips of developing feathers to obtain blood, Ischnoceran lice live on feathers and feed on the non-living keratin of feather barbules. We hypothesized that Amblyceran abundance and richness would have evolved in response to interaction with the immune system of the host, while Ischnoceran taxonomic richness would have evolved independently of immunological constraints. In an interspecific comparison, the abundance of Ischnocerans was positively related to host body size, while host body mass and Ischnoceran taxonomic richness accounted for the abundance of Amblycerans. Amblyceran taxonomic richness was predicted by the intensity of T-cell mediated immune response of nestling hosts, while the T-cell response of adults had no significant effect. In contrast, Ischnoceran taxonomic richness was not predicted by host T-cell responses. These results suggest that the taxonomic richness of different parasite taxa is influenced by different host defenses, and they are consistent with the hypothesis that increasing host allocation to immune defense increases Amblyceran biodiversity.Electronic Supplementary Material Supplementary material is available for this article at     

The chewing lice (Phthiraptera: Ischnocera,Amblycera) of the great cormorant (Phalacrocorax carbo)

The Great Cormorant is a widespread bird species with almost worldwide distribution. Accordingly, its general biology has been investigated thoroughly. Less well known, however, are the chewing lice that live inside the plumage of this diving bird. We examined the two known species of Great Cormorant chewing lice, Eidmanniella pellucida (Rudow, 1869) (Amblycera: Menoponidae) and Pectinopygus gyricornis (Denny, 1842) (Ischnocera: Philopteridae). Taking advantage of the autofluorescence of the cuticle, confocal laser scanning microscopy (CLSM) was used to explore the external morphology of all developmental stages of P. gyricornis. Morphometric analyses revealed a standard increase in body size from first larval instar to the adult. In addition, all instars exhibited increasing body segment differentiation, especially in the abdomen and the head. A total of 277 individuals of Pectinopygus gyricornis and 2 individuals of Eidmanniella pellucida were collected from eleven Great Cormorants from Mecklenburg-Western Pomerania, Germany, in 2015.     

Multiple origins of parasitism in lice

A major fraction of the diversity of insects is parasitic, as herbivores, parasitoids or vertebrate ectopara sites. Understanding this diversity requires information on the origin of parasitism in various insect groups. Parasitic lice (Phthiraptera) are the only major group of insects in which all members are permanent parasites of birds or mammals. Lice are classified into a single order but are thought to be closely related to, or derived from, book lice and bark lice (Psocoptera). Here, we use sequences of the nuclear 18S rDNA gene to investigate the relationships among Phthiraptera and Psocoptera and to identify the origins of parasitism in this group (termed Psocodea). Maximum-likelihood (ML), Bayesian ML and parsimony analyses of these data indicate that lice are embedded within the psocopteran infraorder Nanopsocetae, making the order Psocoptera paraphyletic (i.e. does not contain all descendants of a single common ancestor). Furthermore, one family of Psocoptera, Liposcelididae, is identified as the sister taxon to the louse suborder Amblycera, making parasitic lice (Phthiraptera) a polyphyletic order (i.e. descended from two separate ancestors). We infer from these results that parasitism of vertebrates arose twice independently within Psocodea, once in the common ancestor of Amblycera and once in the common ancestor of all other parasitic lice.     

SPECIES DIVERSITY AND COMMUNITY STRUCTURE OF SUCKING LICE IN YUNNAN, CHINA

Abstract  On the basis of investigating 9 counties (towns) in Yunnan Province of China, the species diversity and community structure of sucking lice on the body surface of small mammal hosts are studied in the paper. Species richness ( S ) is used to stand for the species diversity. The calculation of community diversity index and evenness are based on Shannon-Wiener's method. 2 745 small mammals captured from the investigated sites belong to 10 families, 25 genera and 41 species in 5 orders (Rodentia, Insectivora, Scandentia, Logomorpha and Carnivora) while 18165 individuals of sucking lice collected from the body surface of the small mammal hosts are identified into 4 families, 6 genera and 22 species. The species of sucking lice are much less than the species of their hosts. Most species of small mammals have their fixed sucking lice on their body surface. One species of small mammals usually have few species of sucking lice (1 to 4 species). The close species of the hosts in the taxonomy are found to have the same or similar dominant species of sucking lice on their body surface. The results reveal that the species diversity of sucking lice on small mammals is very low with a very simple community structure. The results also imply there may be a close co-evolution relationship between the lice and the hosts.     

Successful Rearing of <Emphasis Type="Italic">Colpocephalum turbinatum</Emphasis>(Phthiraptera)

SEVERAL attempts have been made to rear avian lice in vitro but in most cases they have been maintained for only one generation^{1, 2}. Stenram³, however, seems to have reared a species of the suborder Ischnocera, Columbicola columbae (Linn.) in culture for several generations without difficulty and I report here that a species of the suborder Amblycera has been colonized successfully in vitro. I also report the first definitive evidence of predation by lice, for this species feeds on its own eggs and nymphs.     

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.     

Host-parasite relationships of the genus Hyalomma Koch, 1844 (Acari, Ixodidae) and their connection with microevolutionary process

Host-parasite relationships of Hyalomma species of the world fauna are analyzed. The majority of species infests predominately various mammals. Birds and reptiles are used as preferred hosts by several Hyalomma species, and only on certain stage: adults of H. aegyptium parasitize tortoises; immature stages of H. marginatum parasitize birds. It is hypothesized that relationships of H. aegyptium adults (subgenus Hyalomma s. str.) with reptiles are secondarily in origin. Immature stages of H. aegyptium retain the primary wide diapason of hosts, which are various small mammals, birds and reptiles. The life cycle of this species is the three-host type that is considered as a primary type in ixodid ticks. A typical scheme of relationships with their hosts in all well-examined Hyalommina species has following features: the adult stage parasitize large and medium sized mammals, immature stages parasitize small mammals, three-host life cycle. A variety of preferred hosts and types of life cycle is observed in the subgenus Euhyalomma. All species of this subgenus can be arranged into two groups. In the first group, the immature stages infest only small mammals and birds, and the adults parasitize large mammals; this type of host preferences is probably primary host-parasite relationships of Hyalomma. This group includes: H. albiparmatum, H. asiaticum, H. excavatum, H. franchinii, H. impeltatum, H. impressum, H. lusitanicum, H. marginatum, H. nitidum, H. schulzei, and H. truncatum. Hyalomma marginatum and H. schulzei are two-host species; H. excavatum is two- or three-host tick. All the remaining species (except H. albiparmatum, which life cycle is unknown) are three-host ticks. In the second group, the immature stages as well as the adult stage parasitize large mammals. This group includes: H. dromedarii, H. anatolicum, and H. scupense. These species are two- or one-host ticks.     

Comparative phylogenetic histories of two louse genera found on Catharus thrushes and other birds

The louse genera Brueelia (Ischnocera) and Myrsidea (Amblycera) are broadly codistributed on songbirds (Passeriformes), but differ in a variety of life history characteristics. We used mitochondrial and nuclear DNA sequences to assess levels of genetic divergence and reconstruct phylogenies of these 2 genera, focusing especially on Catharus thrushes in North America. We then qualitatively compared the phylogenies and levels of divergence within these 2 genera of codistributed parasites. Neither Brueelia nor Myrsidea appears to cospeciate with Catharus thrushes or passerine birds in general. The Myrsidea phylogeny exhibits significant levels of biogeographic structure, whereas the Brueelia phylogeny does not. Myrsidea and Brueelia also differ in their levels of intra-generic genetic divergence, with Myrsidea showing higher levels of genetic divergence and host specificity than Brueelia. Our genetic data support traditional morphology-based taxonomy in several instances in which the same species of Brueelia has been reported on multiple host taxa, e.g., all migrant Catharus spp. carry B. antiqua, with little haplotype divergence. Myrsidea found on each Catharus sp. are in general genetically distinct, except for M. incerta, which parasitizes both Catharus ustulatus and Catharus minimus. The strong biogeographic signal in the Myrsidea phylogeny and higher relative levels of host specificity of Myrsidea spp. suggest that infrequent host-switching, followed by speciation, is shaping the evolutionary history of this group. In contrast, the relatively lower host specificity of Brueelia spp. suggests that host-switching, combined with more frequent ongoing dispersal, has been more important in the evolutionary history of Brueelia.     

中国云南吸虱昆虫物种多样性及群落结构研究(英文)

在对云南省9个县(市)抽样调查的基础上,本文对境内小型哺乳动物(小兽)体表吸虱昆虫物种多样性及群落结构进行了研究。物种多样性用物种丰富度表示,多样性指数及均匀度计算采用Shannon-Wiener方法。所捕获的2745只小兽经分类鉴定隶属啮齿目、食虫目、攀目、兔形目和食肉目5个目中的10科、25属、41种。从各种小兽宿主体表共采集到吸虱昆虫18165只,经分类鉴定隶属4科、6属、22种,其种类明显少于宿主种类。几乎每种小兽宿主体表都有固定的吸虱种类寄生,但吸虱种类数很少(1-4种)。动物分类上接近的宿主,其体表的优势吸虱种类基本相同。研究结果表明,小型哺乳动物体表吸虱昆虫的物种多样性很低,群落结构十分简单。研究同时提示,吸虱昆虫与小兽宿主之间可能存在高度一致的协同进化关系。     

Impact of feather molt on ectoparasites: looks can be deceiving

Animals possess a variety of well-documented defenses against ectoparasites, including morphological, behavioral, and immune responses. Another possible defense that has received relatively little attention is the shedding of the host's exterior. The conventional wisdom is that ectoparasite abundance is reduced when birds molt their feathers, mammals molt their hair, and reptiles shed their skin. We carried out an experimental test of this hypothesis for birds by manipulating molt in feral pigeons (Columba livia) infested with feather lice (Phthiraptera: Ischnocera). We used two standard methods, visual examination and body washing, to quantify the abundance of lice on the birds. The visual data indicated a significant effect of molt on lice. However, the more robust body washing method showed that molt had no effect on louse abundance. Two factors caused visual examination to underestimate the number of lice on molting birds. First, molt replaces worn feathers with new, lush plumage that obscures lice during visual examination. Second, we discovered that lice actively seek refuge inside the sheath that encases developing feathers, where the lice cannot be seen. The apparent reduction in louse abundance caused by these factors may account for the conventional wisdom that feather molt reduces ectoparasite abundance in birds. In light of our experimental results, we argue that it is necessary to reinterpret the conclusions of previous studies that were based on observational data. Additional experiments are needed to test whether shedding of the host's exterior reduces ectoparasites in other birds, mammals, and reptiles, similar to the impact of facultative leaf drop on herbivorous insects on trees.

     

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.