Molecular evolution of Pediculus humanus and the origin of clothing

The human head louse (Pediculus humanus capitis) and body louse (P. humanus corporis or P. h. humanus) are strict, obligate human ectoparasites that differ mainly in their habitat on the host : the head louse lives and feeds exclusively on the scalp, whereas the body louse feeds on the body but lives in clothing. This ecological differentiation probably arose when humans adopted frequent use of clothing, an important event in human evolution for which there is no direct archaeological evidence. We therefore used a molecular clock approach to date the origin of body lice, assuming that this should correspond with the frequent use of clothing. Sequences were obtained from two mtDNA and two nuclear DNA segments from a global sample of 40 head and body lice, and from a chimpanzee louse to use as an outgroup. The results indicate greater diversity in African than non-African lice, suggesting an African origin of human lice. A molecular clock analysis indicates that body lice originated not more than about 72,000 +/- 42,000 years ago; the mtDNA sequences also indicate a demographic expansion of body lice that correlates with the spread of modern humans out of Africa. These results suggest that clothing was a surprisingly recent innovation in human evolution.     

Pyrethroid resistance mechanisms in the head louse Pediculus capitis from Israel: implications for control

In Israel, the head louse, Pediculus capitis, developed resistance to DDT through the extensive use of this insecticide until the 1980s. In 1991, permethrin was introduced for control of DDT resistant P. capitis in Israel, leading to control failure of this pyrethroid insecticide by 1994. Pyrethroid resistance of P. capitis in Israel extends to phenothrin, which has not been used for louse control. We identified a glutathione S-transferase(GST)-based mechanism of DDT resistance in the Israeli head lice. This GST mechanism occurred before 1989, while permethrin resistance in P. capitis developed after 1994, suggesting that the main GST resistance mechanism selected by DDT use does not confer any pyrethroid cross-resistance. Esterase activity levels were equivalent in pyrethroid resistant and susceptible P. capitis field-collected in Israel, and in a susceptible strain of P. humanus, the body louse, indicating no involvement of any esterase-based mechanism in resistance. A weak monooxygenase-based permethrin metabolism resistance mechanism was the only factor identified which could account for any of the observed pyrethroid resistance in P. capitis. However, the lack of synergism of phenothrin resistance by piperonyl butoxide suggests that a non-oxidative mechanism is also present in the resistant lice. Therefore it seems probable that pyrethroid resistance in Israeli P. capitis is due to a combination of nerve insensitivity (knockdown resistance or 'kdr') and monooxygenase resistance mechanisms.     

Genotyping of Human Lice Suggests Multiple Emergences of Body Lice from Local Head Louse Populations

Background

Genetic analyses of human lice have shown that the current taxonomic classification of head lice (Pediculus humanus capitis) and body lice (Pediculus humanus humanus) does not reflect their phylogenetic organization. Three phylotypes of head lice A, B and C exist but body lice have been observed only in phylotype A. Head and body lice have different behaviours and only the latter have been involved in outbreaks of infectious diseases including epidemic typhus, trench fever and louse borne recurrent fever. Recent studies suggest that body lice arose several times from head louse populations.

Methods and Findings

By introducing a new genotyping technique, sequencing variable intergenic spacers which were selected from louse genomic sequence, we were able to evaluate the genotypic distribution of 207 human lice. Sequence variation of two intergenic spacers, S2 and S5, discriminated the 207 lice into 148 genotypes and sequence variation of another two intergenic spacers, PM1 and PM2, discriminated 174 lice into 77 genotypes. Concatenation of the four intergenic spacers discriminated a panel of 97 lice into 96 genotypes. These intergenic spacer sequence types were relatively specific geographically, and enabled us to identify two clusters in France, one cluster in Central Africa (where a large body louse outbreak has been observed) and one cluster in Russia. Interestingly, head and body lice were not genetically differentiated.

Conclusions

We propose a hypothesis for the emergence of body lice, and suggest that humans with both low hygiene and head louse infestations provide an opportunity for head louse variants, able to ingest a larger blood meal (a required characteristic of body lice), to colonize clothing. If this hypothesis is ultimately supported, it would help to explain why poor human hygiene often coincides with outbreaks of body lice. Additionally, if head lice act as a reservoir for body lice, and that any social degradation in human populations may allow the formation of new populations of body lice, then head louse populations are potentially a greater threat to humans than previously assumed.     

虱目裂化线粒体基因组研究进展

虱目是哺乳类和鸟类体表的专性寄生虫。在虱科、阴虱科、长角鸟虱科和兽羽虱科的某些寄生虱种中发现了线粒体基因组裂化现象, 其线粒体基因组裂化成了多个环状的线粒体染色体, 如体虱(Pediculus humanus)、头虱(pediculus capitis)和阴虱(Pthirus pubis)的线粒体基因组分别裂化形成20个、20个和14个微环染色体。微环染色体可能是基因删除和同源重组的结果, 关于线粒体基因组裂化的具体原因和机制, 目前并不清楚, 推测可能是进化选择或随机遗传漂变的结果或与线粒体单链DNA结合蛋白的缺失有关。鉴于线粒体基因组裂化研究对于深入理解线粒体的起源和进化方面具有重要意义, 文章以虱目裂化线粒体基因组为主线, 列举了动物裂化线粒体基因组和裂化特征, 阐述了虱目裂化线粒体基因组的研究现状, 分析了虱目线粒体基因组裂化的类型、原因和机制, 并对该领域未来的研究方向进行了展望。     

Geographic distributions and origins of human head lice (Pediculus humanus capitis) based on mitochondrial data

Human head lice (Pediculus humanus capitis) are subdivided into 3 deeply divergent mitochondrial clades (Clades A, B, and C), each having unique geographical distributions. Determining the evolutionary history and geographic distribution of these mitochondrial clades can elucidate the evolutionary history of the lice as well as their human hosts. Previous data suggest that lice belonging to mitochondrial Clade B may have originated in North America or Asia; however, geographic sampling and sample sizes have been limited. With newly collected lice, we calculate the relative frequency, geographic distribution, and genetic diversity of louse mitochondrial clades to determine the geographic origin of lice belonging to Clade B. In agreement with previous studies, genetic diversity data support a North American origin of Clade B lice. It is likely that lice belonging to this mitochondrial clade recently migrated to other geographic localities, e.g., Europe and Australia, and, if not already present, may disperse further to occupy all geographic regions.     

Nuclear Genetic Diversity in Human Lice (Pediculus humanus) Reveals Continental Differences and High Inbreeding among Worldwide Populations

Understanding the evolution of parasites is important to both basic and applied evolutionary biology. Knowledge of the genetic structure of parasite populations is critical for our ability to predict how an infection can spread through a host population and for the design of effective control methods. However, very little is known about the genetic structure of most human parasites, including the human louse (Pediculus humanus). This species is composed of two ecotypes: the head louse (Pediculus humanus capitis De Geer), and the clothing (body) louse (Pediculus humanus humanus Linnaeus). Hundreds of millions of head louse infestations affect children every year, and this number is on the rise, in part because of increased resistance to insecticides. Clothing lice affect mostly homeless and refugee-camp populations and although they are less prevalent than head lice, the medical consequences are more severe because they vector deadly bacterial pathogens. In this study we present the first assessment of the genetic structure of human louse populations by analyzing the nuclear genetic variation at 15 newly developed microsatellite loci in 93 human lice from 11 sites in four world regions. Both ecotypes showed heterozygote deficits relative to Hardy–Weinberg equilibrium and high inbreeding values, an expected pattern given their parasitic life history. Bayesian clustering analyses assigned lice to four distinct genetic clusters that were geographically structured. The low levels of gene flow among louse populations suggested that the evolution of insecticide resistance in lice would most likely be affected by local selection pressures, underscoring the importance of tailoring control strategies to population-specific genetic makeup and evolutionary history. Our panel of microsatellite markers provides powerful data to investigate not only ecological and evolutionary processes in lice, but also those in their human hosts because of the long-term coevolutionary association between lice and humans.     

Transmission ratio distortion in the human body louse, Pediculus humanus (Insecta: Phthiraptera)

We studied inheritance at three microsatellite loci in eight F, and two F2 families of the body (clothes) louse of humans, Pediculus humanus. The alleles of heterozygous female-parents were always inherited in a Mendelian fashion in these families. Alleles from heterozygous male-parents, however, were inherited in two different ways: (i) in a Mendelian fashion and (ii) in a non-Mendelian fashion, where males passed to their offspring only one of their two alleles, that is, 100% nonrandom transmission. In male body lice, where there was non-Mendelian inheritance, the paternally inherited set of alleles was eliminated. We interpret this pattern of inheritance as evidence for extreme transmission ratio distortion of paternal alleles in this species.     

Evidence from double infestations for the specific status of human head lice and body lice (Anoplura)

Abstract Samples of head lice and body lice obtained from Ethiopians suffering from double infestations were mounted onto microscope slides and measured. The mean length of body lice (♀ 4.4mm; ♂ 3.8mm) was greater than that of head lice (♀ 3.5 mm; ♂ 2.9mm), but the best discriminant was the length of the tibia of the middle leg (♀ 425/296 μ♂421/291 μ). No intermediate specimens were found in these double infestations, although intermediates can can be produced experimentally by cross-mating. Since populations of head lice and body lice remain distinct it is concluded that they represent two distinct species, Pediculus capitis De Geer and P. humanus Linneaus.     

Permethrin resistance in the head louse Pediculus capitis from Israel

Head lice, Pediculus capitis , were collected from children aged 3–12 years in Maale Adumin, a town near Jerusalem, after reports of control failure with the pyrethroid insecticide permethrin. A total of 1516 children were examined: living lice and eggs were found on 12.1% of the children; or another 22.8% of the children only nits were found. Twice as many girls as boys (8.1% v 4%) were infested with lice and or nits. Head lice collected from infested children were exposed to permethrin impregnated filter-papers. Log time probit mortality (ltp) regression lines were calculated for mortality data and compared to ltp lines for a similar collection of head lice made in 1989. The regression lines for the two years were significantly different, with a 4-fold decrease in susceptibility at the LT50 level between 1989 and 1994. The slopes of the lines also suggested that the 1994 population was more heterogenous in its response to permethrin than the 1989 population. In contrast, a laboratory population of body lice (Pediculus humanus) tested with the same batch of permethrin-impregnated papers showed a slight but non-significant increase in susceptibility between 1989 and 1994. The results suggest that resistance to pyrethroids has developed rapidly among head lice since permethrin was introduced in 1991 as a pediculicide in Israel.     

Immunization of rabbits with a midgut extract of the human body louse Pediculus humanus humanus: the effect of induced resistance on the louse population

Abstract. Resistance to human body lice, Pediculus humanus humanus L, induced by feeding on rabbits immunized with an extract of louse gut was studied. The mortality of lice fed on immunized rabbits was 73%, significantly higher than that of lice fed on control rabbits (52%) ( P < 0.01). The proportion of dead nymphs and female lice with ruptured guts was significantly higher in lice fed on immunized rabbits (P<0.01). The size of the bloodmeal was 35% greater in female lice fed on control rabbits than on immunized rabbits. Lice fed on immunized rabbits laid 40% less eggs than those fed on the controls, they also demonstrated a significant decrease in the number of eggs per female over time ( P < 0.01). 86% of the eggs laid by lice fed on immunized animals hatched, compared with 92% hatching of eggs laid by the lice fed on control animals (P< 0.01). With the exception of the first bloodmeal the percentage of hatched eggs which were laid between any two bloodmeals was significantly smaller (p<0.01) in the lice fed on immunized rabbits than in the control group. The first nymphal stage of lice fed on immunized rabbits took an average of 5.2 days to moult to the second stage, compared with 4 days for those fed on control rabbits.     

Evolutionary relationships of "Candidatus Riesia spp.," endosymbiotic enterobacteriaceae living within hematophagous primate lice

The primary endosymbiotic bacteria from three species of parasitic primate lice were characterized molecularly. We have confirmed the characterization of the primary endosymbiont (P-endosymbiont) of the human head/body louse Pediculus humanus and provide new characterizations of the P-endosymbionts from Pediculus schaeffi from chimpanzees and Pthirus pubis, the pubic louse of humans. The endosymbionts show an average percent sequence divergence of 11 to 15% from the most closely related known bacterium "Candidatus Arsenophonus insecticola." We propose that two additional species be added to the genus "Candidatus Riesia." The new species proposed within "Candidatus Riesia" have sequence divergences of 3.4% and 10 to 12% based on uncorrected pairwise differences. Our Bayesian analysis shows that the branching pattern for the primary endosymbionts was the same as that for their louse hosts, suggesting a long coevolutionary history between primate lice and their primary endosymbionts. We used a calibration of 5.6 million years to date the divergence between endosymbionts from human and chimpanzee lice and estimated an evolutionary rate of nucleotide substitution of 0.67% per million years, which is 15 to 30 times faster than previous estimates calculated for Buchnera, the primary endosymbiont in aphids. Given the evidence for cospeciation with primate lice and the evidence for fast evolutionary rates, this lineage of endosymbiotic bacteria can be evaluated as a fast-evolving marker of both louse and primate evolutionary histories.     

Susceptibility of British head lice, Pediculus capitis, to imidacloprid and fipronil

The head louse, Pediculus capitis De Geer (Phthiraptera: Pediculidae) has developed resistance to organochlorines, the organophosphate malathion and to pyrethroids in the U.K. Therefore, headlice from Bristol school children were bioassayed against two new insecticides, fipronil and imidacloprid. Pediculus capitis was fully susceptible to imidacloprid, but it required a relatively high dose and acted slowly. Fipronil acted faster at lower dose, but seemed to be affected by cross-resistance in a small proportion of P. capitis.     

Resistance and the control of lice on humans and production animals

Phthiraptera (lice) are specialised insects adapted to parasitise many warm-blooded vertebrates, including domestic animals and humans. Often, attempts by the host to alleviate the irritation created by lice, causes derangement of the hair/fur coat. Unless treated, this derangement may cause economic losses due to hide damage and/or downgrading of wool/hair/fur. In 1981, application of aqueous insecticide solutions (dipping) for the control of sheep body lice (Bovicola ovis) was largely superseded by off-shears pyrethroid "pour-on" treatments. By 1985, several field failures with these products were found to be due to low-level (20x) insecticide resistance. In 1990, high-level (640x) resistance was diagnosed in a New South Wales population. However, despite 30+years use, organophosphate-based products are still usually effective. Until recently, cattle lice caused little concern. Treatments were applied mainly for aesthetic reasons when cattle were to be presented for sale, and also to prevent damage to fences by rubbing cattle. However, the introduction of quality-management programmes have raised awareness of the economic losses due to hide damage associated with lice infestations. Emerging industries such as emu and alpaca farming have raised the pest status of other louse species, and necessitated insecticidal intervention. In humans, attempts to control head lice, Pediculus humanus capitis, infestations have repeatedly failed around the world.     

The fumigant and repellent activity of aliphatic lactones against Pediculus humanus capitis (Anoplura: Pediculidae)

New alternative insecticides are necessary for the chemical control of head lice. In this study the fumigant knockdown time 50% (KT50) and repellency index (RI) of three aliphatic lactones was compared with two essential oils and DDVP, against permethrin-resistance Pediculus humanus capitis from Argentina. In the fumigant assay, none of the lactones were effective compared to the highest activity of eucalyptus (KT50 15.53 m). In the repellency test, the three lactones were equally or more effective (RI ranging from 60.50 to 76.68) than the positive control (piperonal). These lactones are promising as head lice repellents.     

Determination of Knockdown Resistance (kdr) Allele Frequencies (T929I mutation) in Head Louse Populations from Mexico,Canada, and Peru

The head louse Pediculus humanus capitis (De Geer) is a hematophagous ectoparasite that inhabits the human scalp. The infestations are asymptomatic; however, skin irritation from scratching occasionally may cause secondary bacterial infections. The present study determined the presence and frequency of the knockdown resistance (kdr) mutation T929I in 245 head lice collected from Mexico, Peru, and Canada. Head lice were collected manually using a comb in the private head lice control clinic. Allele mutation at T9291 was present in 100% of the total sampled populations (245 lice) examined. In addition, 4.89% of the lice were homozygous susceptible, whereas 6.93% heterozygous and 88.16% homozygous were resistant, respectively. This represents the second report in Mexico and Quebec and fist in Lima.     

Heteroplasmy in the Mitochondrial Genomes of Human Lice and Ticks Revealed by High Throughput Sequencing

The typical mitochondrial (mt) genomes of bilateral animals consist of 37 genes on a single circular chromosome. The mt genomes of the human body louse, Pediculus humanus, and the human head louse, Pediculus capitis, however, are extensively fragmented and contain 20 minichromosomes, with one to three genes on each minichromosome. Heteroplasmy, i.e. nucleotide polymorphisms in the mt genome within individuals, has been shown to be significantly higher in the mt cox1 gene of human lice than in humans and other animals that have the typical mt genomes. To understand whether the extent of heteroplasmy in human lice is associated with mt genome fragmentation, we sequenced the entire coding regions of all of the mt minichromosomes of six human body lice and six human head lice from Ethiopia, China and France with an Illumina HiSeq platform. For comparison, we also sequenced the entire coding regions of the mt genomes of seven species of ticks, which have the typical mitochondrial genome organization of bilateral animals. We found that the level of heteroplasmy varies significantly both among the human lice and among the ticks. The human lice from Ethiopia have significantly higher level of heteroplasmy than those from China and France (P_t<0.05). The tick, Amblyomma cajennense, has significantly higher level of heteroplasmy than other ticks (P_t<0.05). Our results indicate that heteroplasmy level can be substantially variable within a species and among closely related species, and does not appear to be determined by single factors such as genome fragmentation.     

Immunization of rabbits with faecal extract of Pediculus humanus, the human body louse: effects on louse development and reproduction

Abstract Immunization of rabbits with a faecal extract of the human body louse (Pediculus humanus) induced a high titre of specific IgG. The mean weight of Wood taken by females fed on the immunized rabbits was significantly lower (29%) than taken by females fed on the control rabbits. The mean number of eggs per female fed on the immunized rabbits was significantly lower than for females fed on the control rabbits. The hatchability of the eggs laid by lice fed on immunized rabbits (91%) was significantly lower than of those fed on control rabbits (94%). The rate of development of nymphs fed on control rabbits was significantly higher than those fed on the immunized rabbits. There was no difference in survival rates of lice fed on immunized and control rabbits.     

In vitro efficacy of over-the-counter botanical pediculicides against the head louse Pediculus humanus var capitis based on a stringent standard for mortality assessment

Abstract.  Infestation of the head louse Pediculus humanus var capitis DeGeer (Phthiraptera: Pediculidae) is an important public health problem in Australia, with up to a third of children infested in some primary schools. Insecticide resistance and inadequate attention to the application instructions of topical pediculicides are common reasons for treatment failure. This study evaluated six popular Australian over-the-counter products against head lice, primarily comprised of different botanical extracts, and compared them with permethrin 1% (Quellada^®) and a non-treatment control in order to assess their in vitro efficacy. We also assessed commonly used criteria for evaluating pediculicide efficacy in vitro. All tested products failed to demonstrate high levels of efficacy with the exception of Tea Tree Gel^®, which outperformed 1% permethrin. Permethrin had a high level of efficacy, but using stringent criteria 18% of lice were not dead at 3 h, indicating some resistance to Quellada^®. Commonly used less stringent criteria were shown to overestimate mortality of head lice as a result of the protective phenomenon of stasis or sham death observed in exposed lice that may recover after some time. Using two different levels of stringency resulted in different rankings of efficacy for most products, with the exception of the first ranked product, Tea Tree Gel^®. Rankings of efficacy also varied over time, even within the different assessment criteria. Government regulatory agencies should require standard in vitro tests using stringent mortality criteria, with an observation period of ≥ 6 h, to determine the efficacy of new pediculicides, and only products that cause a minimum mortality rate (e.g. 80%) in head lice collected from the target population should be licensed for sale.     

Engorgement response of human body lice Pediculus humanus (Insecta: Anoplura) to blood fractions and their components

ABSTRACT. Fed through a synthetic membrane, 80% of females of the human body louse, Pediculus humanus de Geer, engorged on whole human blood compared to 30% on platelet poor plasma. Both the plasma albumin and small molecular weight components of the cellular fraction seemed to stimulate engorgement by lice. Known haemo-phagostimulants such as adenosine triphosphate and diphosphoglyceric acid when added to plasma, did not replace the small molecular weight components of the cellular fraction as feeding stimuli. Nymphs discriminated less than adults in selecting blood fractions.