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.     

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 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.     

Site,process and mechanism of active uptake of water vapour from the atmosphere in the Psocoptera

In the Psocoptera, occlusion of the anus or extended areas of the thorax and abdomen with paraffin wax does not interfere with the active uptake of water vapour from subsaturated atmospheres. However, blocking the mouth or impairing the mobility of the mouthparts with wax prevents watervapour absorption. Observations of the animals synchronized with continuous weight recordings, confirm an oral site of water-vapour uptake in this insect order, and reveal some details of the uptake mechanism. During uptake, paired lingual sclerites of the ventral hypopharyngeal surface are brought into a typical absorbing position. Water-vapour condensation proceeds onto a fluid layer covering this surface. The fluid presumably originates from a pair of dorsal labial glands. The condensed water vapour is transferred from the site of condensation to the gut entrance via a paired or branched sclerotized tubule traversing the hypopharynx. Propulsion of the fluid is achieved by a cibarial sucking pump. Below the critical equilibrium humidity the fluid layer dries up, the salivarium is closed and absorption ceases.     

Occurrence,properties and biological implications of the active uptake of water vapour from the atmosphere in Psocoptera

Water vapour absorption is shown to occur in 22 species of Psocoptera inhabiting diverse environments and representing all major groups of this insect order. Evidently the faculty is a common feature of the whole order and it seems not to be related to specific environmental conditions. For the first time water vapour uptake could be demonstrated in fully winged and flying insects. The critical equilibrium humidities vary considerably among different species ranging from 58 to 85% r.h. Marked interspecific differences are also observed in water loss and uptake rates but no clear correlation with habitat or systematic group is recognizable. The uptake rates of Psocoptera are among the highest of all arthropods investigated so far. From weight recordings with a sensitive microbalance it could be seen that continuous operation of the uptake mechanism is restricted to limited periods of time of less than 1 hr regardless of the water status of the animals. Initiation and termination of the uptake process are abrupt and continuous uptake proceeds at a constant rate at a given relative humidity. Uptake rates are humidity-dependent decreasing with falling relative humidity whereas the adjustment of the equilibrium level of body water is independent of ambient humidity. Equilibrium is maintained by intermittent operation of the uptake mechanism within ca. 3% of body water mass. The uptake mechanism exhibits marked sensitivity to starvation in most members of the Psocomorpha. Some features of the uptake process of Psocoptera are in close agreement with those of Mallophaga reflecting the close relationship between the two groups.     

The taxonomy of Brazilian insects vectors of transmissible diseases (1900-2000)--then and now

A brief historical overview is given of the most relevant taxonomic studies of insect groups vectors of transmissible diseases in Brazil, from the "heroic" times of the foundation of the Instituto Oswaldo Cruz in Rio de Janeiro up to the present. The following orders are considered: Phthiraptera (Anoplura, Amblycera and Ischnocera), Hemiptera (Reduviidae: Triatominae), Siphonaptera and Diptera (Culicidae, Ceratopogonidae, Psychodidae: Phlebotominae, Simuliidae, Tabanidae, Chloropidae and Muscidae). The most important Brazilian collections of each group are cited.     

Morphology of male genitalia in lice and their relatives and phylogenetic implications

Abstract.  Lice (Insecta: Phthiraptera) have long been considered to compose a monophyletic group of insects on the basis of external morphological characteristics. However, a recent phylogenetic analysis of 18S rDNA sequences suggested that 'Phthiraptera' have arisen twice within the order Psocoptera (booklice and barklice). The external features of lice are highly specialized to a parasitic lifestyle, and convergence may be frequent for such characters. To provide a further test between traditional and recent molecular-based phylogenetic hypotheses, a phylogenetic analysis of lice and relatives based on morphological characters that are independent from the selective pressures of a parasitic lifestyle is needed. Here, we examined the morphology of the male phallic organ in lice and relatives ('Psocoptera': suborders Troctomorpha and Psocomorpha) and detected some novel modifications that were stable within each group and useful for higher level phylogenetic reconstruction. Phylogenetic analysis based on these characters provided a concordant result with the 18S-based phylogeny. In particular, the apomorphic presence of articulations between the basal plate, mesomere and ventral plate (= sclerite on the permanently everted endophallus) is observed consistently throughout the psocid families Pachytroctidae and Liposcelididae and the louse suborder Amblycera, providing support for a clade composed of these three groups, although possible homoplasy was detected in some Ischnocera. This is the first study to provide morphological support for the polyphyly of lice.     

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.     

吸虱亚目非典型线粒体基因组研究进展

吸虱是真兽类哺乳动物体表的专性寄生虫,在全世界广泛分布,物种数量高达540种。近年来随着分子生物学的飞速发展,在NCBI中已收录15种吸虱线粒体基因组序列,其独特的非典型线粒体基因组发生剧烈的裂化现象,形成数目不等的微环染色体。本文综述了15种吸虱线粒体基因组的结构和组成、RNA基因、非编码区以及对吸虱祖先线粒体核型推测的方法和结果。探讨了不同种属间以及与其它昆虫的差异,提出今后对吸虱亚目线粒体基因组研究的展望。     

云南省吸虱昆虫区系及物种多样性

吸虱是寄生于真兽类哺乳动物体表的专性吸血寄生虫,广布于世界各地。云南省已知吸虱昆虫9科13属44种,分别占中国已知吸虱科、属、种的81.82%,59.09%,45.83%。文章参考大量相关文献,从分类阶元、特有物种、动物地理区划和宿主动物4个方面分析云南省吸虱的物种多样性。云南省吸虱特有种有13种,占云南省已知吸虱种类的29.55%,27种为东洋种,15种为古北和东洋两界兼有种,广布种9种。吸虱在5个地理小区的分布,以横断山中部和横断山南部2个地理小区的吸虱物种多样性较高,其它3个区的物种多样性较低。相对于全国而言,云南省吸虱物种多样性较高,吸虱的宿主动物种类丰富。但蚤、恙螨和革螨等其它体表寄生虫相比较,兽类宿主动物体表吸虱的物种多样性明显低于其它体表寄生虫,1科(属)阶元的吸虱其宿主多为相对一致的1个科(属)动物阶元,反映了吸虱宿主特异性较高的事实,吸虱昆虫与其对应的宿主动物已经形成了比较稳定的"一对一"的寄生关系,这是吸虱昆虫与其宿主动物协同进化的生态学表现。     

Epidemiological prediction of the distribution of insects of medical significance: comparative distributions of fleas and sucking lice on the rat host Rattus norvegicus in Yunnan Province, China

Determining the distribution patterns of ectoparasites is important for predicting the spread of vector-borne diseases. A simple epidemiological model was used to compare the distributions of two different taxa of ectoparasitic insects, sucking lice (Insecta: Siphonaptera) and fleas (Insecta: Anoplura), on the same rodent host, Rattus norvegicus Berkenhout (Rodentia: Muridae), in Yunnan Province, China. Correlations between mean abundance and prevalence were determined. Both fleas and sucking lice were aggregated on their hosts, and sucking lice showed a higher degree of aggregation than fleas. The prevalence of both fleas and sucking lice increased with log-transformed mean abundance and a highly linear correlation and modelling efficiency of predicted prevalence against observed prevalence were obtained. The results demonstrate that prevalence can be explained simply by mean abundance.     

中国吸虱昆虫区系及物种多样性研究

吸虱是寄生于真兽类哺乳动物体表的专性吸血寄生虫,广布于世界各地.我国已知吸虱11科22属96种.分别占世界已知科、属、种的64.71%、45.83%、17.14%.从分类阶元、特有物种、动物地理区划和宿主动物4个方面分析了我国吸虱的物种多样性.中国特有种吸虱27种.中国横跨古北和东洋两界,吸虱分布以东洋界和占北界共有属级分布型最丰富,有13属29种;其次为东洋界特有分布型,有6属41种,种类丰富;古北界特有分布型仅2属,但种类丰富,有24种.吸虱在7个地理区分布,以华中区、华南区、西南区3个地理区的吸虱物种多样性较高,其它4个区的物种多样性较低.我国吸虱物种多样性较为丰富,吸虱的物种分布受宿主动物地域分布的影响较大.吸虱的宿主动物种类丰富,但宿主动物体表吸虱的物种多样性低,一科(属)阶元的吸虱其宿主多为相对应的一科(亚科)动物阶元,反映了吸虱宿主特异性较高的事实,是吸虱与其宿主协同进化的生态学表现.     

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.     

The multipartite mitochondrial genome of Liposcelis bostrychophila: insights into the evolution of mitochondrial genomes in bilateral animals

Booklice (order Psocoptera) in the genus Liposcelis are major pests to stored grains worldwide and are closely related to parasitic lice (order Phthiraptera). We sequenced the mitochondrial (mt) genome of Liposcelis bostrychophila and found that the typical single mt chromosome of bilateral animals has fragmented into and been replaced by two medium-sized chromosomes in this booklouse; each of these chromosomes has about half of the genes of the typical mt chromosome of bilateral animals. These mt chromosomes are 8,530 bp (mt chromosome I) and 7,933 bp (mt chromosome II) in size. Intriguingly, mt chromosome I is twice as abundant as chromosome II. It appears that the selection pressure for compact mt genomes in bilateral animals favors small mt chromosomes when small mt chromosomes co-exist with the typical large mt chromosomes. Thus, small mt chromosomes may have selective advantages over large mt chromosomes in bilateral animals. Phylogenetic analyses of mt genome sequences of Psocodea (i.e. Psocoptera plus Phthiraptera) indicate that: 1) the order Psocoptera (booklice and barklice) is paraphyletic; and 2) the order Phthiraptera (the parasitic lice) is monophyletic. Within parasitic lice, however, the suborder Ischnocera is paraphyletic; this differs from the traditional view that each suborder of parasitic lice is monophyletic.     

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.     

Lice and ticks of the eastern rufous mouse lemur, Microcebus rufus, with descriptions of the male and third instar nymph of Lemurpediculus verruculosus (Phthiraptera: Anoplura)

Sucking lice and ticks were collected from live-trapped eastern rufous mouse lemurs, Microcebus rufus Geoffroy, in and around the periphery of Ranomafana National Park, southeastern Madagascar, from 2007 to 2009. Samples of 53 sucking lice (Insecta: Phthiraptera: Anoplura) and 28 hard ticks (Acari: Ixodidae) were collected from 36 lemur captures representing 26 different host individuals. All of the lice were Lemurpediculus verruculosus (Ward) (6 males, 46 females, 1 third instar nymph). Only the holotype female was known previously for this louse and the host was stated to be a "mouse lemur." Therefore, we describe the male and third instar nymph of L. verruculosus and confirm M. rufus as a host (possibly the only host) of this louse. All of the ticks were nymphs and consisted of 16 Haemaphysalis lemuris Hoogstraal, 11 Haemaphysalis sp., and 1 Ixodes sp. The last 2 ticks listed did not morphologically match any of the Madagascar Haemaphysalis or Ixodes ticks for which nymphal stages have been described.     

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.     

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.     

Influence of bill and foot morphology on the ectoparasites of barn owls

Preening is the principle behavioral defense used by birds to combat ectoparasites. Most birds have a small overhang at the tip of their bills that is used to shear through the tough cuticle of ectoparasitic arthropods, making preening much more efficient. Birds may also scratch with their feet to defend against ectoparasites. This is particularly important for removing ectoparasites on the head, which birds cannot preen. Scratching may be enhanced by the comb-like serrations that are found on the claws of birds in many avian families. We examined the prevalence and intensity of ectoparasites of barn owls (Tyto alba pratincola) in southern Idaho in relation to bill hook length and morphological characteristics of the pectinate claw. The barn owls in our study were infested with 3 species of lice (Phthiraptera: Ischnocera): Colpocephalum turbinatum , Kurodaia subpachygaster, and Strigiphilus aitkeni . Bill hook length was associated with the prevalence of these lice. Owls with longer hooks were more likely to be infested with lice. Conventional wisdom suggests that the bill morphology of raptors has been shaped by selection for efficient foraging; our data suggest that hook morphology may also play a role in ectoparasite defense. The number of teeth on the pectinate claw was also associated with the prevalence of lice. Owls that had claws with more teeth were less likely to be infested with lice, which suggests that larger pectinate claws may offer relatively more protection against ectoparasitic lice. Experiments that manipulate the bill hook and pectinate claw are needed to confirm whether these host characters are involved in ectoparasite defense. Finally, we recovered mammalian ectoparasites from 4 barn owls. We recovered species of mammalian lice (Phthiraptera:Anoplura) and fleas (Siphonaptera) that are commonly found on microtine rodents. The owls probably acquired these parasites from recently eaten prey. This represents 1 of the few documented cases of parasites "straggling" from prey to predator.