The role of body size in host specificity: reciprocal transfer experiments with feather lice

Although most parasites show at least some degree of host specificity, factors governing the evolution of specificity remain poorly understood. Many different groups of host-specific parasites show a striking correlation between parasite and host body size, suggesting that size reinforces specificity. We tested this hypothesis by measuring the relative fitness of host-specific feather lice transferred to pigeons and doves that differ in size by an order of magnitude. To test the general influence of size, we transferred unrelated groups of wing and body lice, which are specialized for different regions of the host. Lice were transferred in both directions, from a large native host species, the rock pigeon (Columba livia), to several progressively smaller hosts, and from a small native host species, the common ground dove (Columbina passerina), to several larger hosts. We measured the relative fitness (population size) of lice transferred to these novel host species after two louse generations. Neither wing lice nor body lice could survive on novel host species that were smaller in size than the native host. However, when host defense (preening behavior) was blocked, both groups survived and reproduced on all novel hosts tested. Thus, host defense interacted with host size to govern the ability of lice to establish on small hosts. Neither wing lice nor body lice could survive on larger hosts, even when preening was blocked. In summary, host size influenced the fitness of both types of feather lice, but through different mechanisms, depending on the direction of the transfer. Our results indicate that host switching is most likely between hosts of similar body size. This finding has important implications for studies of host-parasite coevolution at both the micro- and macroevolutionary scales.     

Residence time of the sea louse, Lepeophtheirus salmonis K., on Atlantic salmon, Salmo salar L., after immersion in fresh water

Returning adult salmon caught at the mouth of the River Dee, Aberdeenshire, were transferred to tanks in the laboratory. For fish placed in fresh water, sea lice remained attached for up to 6 days, though most lice were lost in the first 48 hours. Few lice were lost from salmon maintained in sea water. The experiments were conducted in water within a temperature range of 12·8 to 16° C, equivalent to summer river temperatures in the Aberdeenshire Dee.     

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.     

Phoretic dispersal influences parasite population genetic structure

Dispersal is a fundamental component of the life history of most species. Dispersal influences fitness, population dynamics, gene flow, genetic drift and population genetic structure. Even small differences in dispersal can alter ecological interactions and trigger an evolutionary cascade. Linking such ecological processes with evolutionary patterns is difficult, but can be carried out in the proper comparative context. Here, we investigate how differences in phoretic dispersal influence the population genetic structure of two different parasites of the same host species. We focus on two species of host‐specific feather lice (Phthiraptera: Ischnocera) that co‐occur on feral rock pigeons (Columba livia). Although these lice are ecologically very similar, “wing lice” (Columbicola columbae) disperse phoretically by “hitchhiking” on pigeon flies (Diptera: Hippoboscidae), while “body lice” (Campanulotes compar) do not. Differences in the phoretic dispersal of these species are thought to underlie observed differences in host specificity, as well as the degree of host–parasite cospeciation. These ecological and macroevolutionary patterns suggest that body lice should exhibit more genetic differentiation than wing lice. We tested this prediction among lice on individual birds and among lice on birds from three pigeon flocks. We found higher levels of genetic differentiation in body lice compared to wing lice at two spatial scales. Our results indicate that differences in phoretic dispersal can explain microevolutionary differences in population genetic structure and are consistent with macroevolutionary differences in the degree of host–parasite cospeciation.     

Host defence mediates interspecific competition in ectoparasites

1. Interspecific competition influences which, how many and where species coexist in biological communities. Interactions between species in different trophic levels can mediate interspecific competition; e.g. predators are known to reduce competition between prey species by suppressing their population sizes. A parallel phenomenon may take place in host-parasite systems, with host defence mediating competition between parasite species. 2. We experimentally investigated the impact of host defence (preening) on competitive interactions between two species of feather-feeding lice: 'wing' lice Columbicola columbae and 'body' lice Campanulotes compar. Both species are host-specific parasites that co-occur on rock pigeons Columba livia. 3. We show that wing lice and body lice compete and that host defence mediates the magnitude of this competitive interaction. 4. Competition is asymmetrical; wing louse populations are negatively impacted by body lice, but not vice versa. This competitive asymmetry is consistent with the fact that body lice predominate in microhabitats on the host's body that offer the most food and the most space. 5. Our results indicate that host-defence-mediated competition can influence the structure of parasite communities and may play a part in the evolution of parasite diversity.     

Louse infestations of tree shrews (Tupaia glis)

Nine adult tree shrews, Tupaia glis, recently imported from West Malaysia were visually examined for ectoparasites while under general anesthesia. Three shrews were infested by the sucking louse, Sathrax durus , and six shrews had louse ova belonging to this species; two shrews had neither lice nor ova. A total of 20 adult female, 10 adult male, and three third instar nymphal lice was collected. Lice were located on the head, flanks, and dorsal body of shrews while ova were recorded mainly from the anterior flanks but also from some adjacent host sites. The tree shrews appeared to tolerate the lice well although louse vector capacity was not assessed. The last date that lice were recorded from shrews was 22 days after colony set-up, and the last date on which seemingly viable ova were recorded was 64 days after set-up showing that the infestations were ultimately lost.     

Community structure of lice (Insecta: Phthiraptera) from two sympatric gull species: kelp gull (Larus dominicanus) and Franklin's gull (Larus pipixcan) in Talcahuano, Chile

A total of 1,177 lice of four species were collected from 124 kelp gulls (Larus dominicanus) and 137 lice of the same four species from 60 Franklin's gulls (Larus pipixcan). The louse Saemundssonia lari (O Fabricius) (Phthiraptera: Philopteridae) was the most numerous on both gull species, with infestation rates of 4.9 on kelp gulls and 1.8 on Franklin's gulls. The second most abundant louse was Quadraceps punctatus (Burmeister), with a high infestation rate but low prevalence on kelp gulls; those parameters were much lower among lice from Franklin's gulls. The composition and community structure of the lice were similar on both host species, but not their infestation rates. In addition, the feather mite Zachvatkinia larica Mironov (Acari: Avenzoariidae) is recorded from kelp gulls and Franklin's gulls for the first time, while the gamasid mite Larinyssus sp. is recorded from kelp gulls, also for the first time. The population parameters of all species of ectoparasites are discussed.     

The head and body lice of humans are genetically distinct (Insecta: Phthiraptera, Pediculidae): evidence from double infestations

Little is known about the population genetics of the louse infestations of humans. We used microsatellite DNA to study 11 double infestations, that is, hosts infested with head lice and body lice simultaneously. We tested for population structure on a host, and for population structure among seven hosts that shared sleeping quarters. We also sought evidence of migration among louse populations. Our results showed that: (i) the head and body lice on these individual hosts were two genetically distinct populations; (ii) each host had their own populations of head and body lice that were genetically distinct to those on other hosts; and (iii) lice had migrated from head to head, and from body to body, but not between heads and bodies. Our results indicate that head and body lice are separate species.     

Ancient Human Genomes and Environmental DNA from the Cement Attaching 2,000-Year-Old Head Lice Nits

Over the past few decades, there has been a growing demand for genome analysis of ancient human remains. Destructive sampling is increasingly difficult to obtain for ethical reasons, and standard methods of breaking the skull to access the petrous bone or sampling remaining teeth are often forbidden for curatorial reasons. However, most ancient humans carried head lice and their eggs abound in historical hair specimens. Here we show that host DNA is protected by the cement that glues head lice nits to the hair of ancient Argentinian mummies, 1,500–2,000 years old. The genetic affinities deciphered from genome-wide analyses of this DNA inform that this population migrated from north-west Amazonia to the Andes of central-west Argentina; a result confirmed using the mitochondria of the host lice. The cement preserves ancient environmental DNA of the skin, including the earliest recorded case of Merkel cell polyomavirus. We found that the percentage of human DNA obtained from nit cement equals human DNA obtained from the tooth, yield 2-fold compared with a petrous bone, and 4-fold to a bloodmeal of adult lice a millennium younger. In metric studies of sheaths, the length of the cement negatively correlates with the age of the specimens, whereas hair linear distance between nit and scalp informs about the environmental conditions at the time before death. Ectoparasitic lice sheaths can offer an alternative, nondestructive source of high-quality ancient DNA from a variety of host taxa where bones and teeth are not available and reveal complementary details of their history.     

Host sympatry and body size influence parasite straggling rate in a highly connected multihost,multiparasite system

Parasite lineages commonly diverge when host lineages diverge. However, when large clades of hosts and parasites are analyzed, some cases suggest host switching as another major diversification mechanism. The first step in host switching is the appearance of a parasite on an atypical host, or “straggling.” We analyze the conditions associated with straggling events. We use five species of colonially nesting seabirds from the Galapagos Archipelago and two genera of highly specific ectoparasitic lice to examine host switching. We use both genetic and morphological identification of lice, together with measurements of spatial distribution of hosts in mixed breeding colonies, to test: (1) effects of local host community composition on straggling parasite identity; (2) effects of relative host density within a mixed colony on straggling frequency and parasite species identity; and (3) how straggling rates are influenced by the specifics of louse attachment. Finally, we determine whether there is evidence of breeding in cases where straggling adult lice were found, which may indicate a shift from straggling to the initial stages of host switching. We analyzed more than 5,000 parasite individuals and found that only ~1% of lice could be considered stragglers, with ~5% of 436 host individuals having straggling parasites. We found that the presence of the typical host and recipient host in the same locality influenced straggling. Additionally, parasites most likely to be found on alternate hosts are those that are smaller than the typical parasite of that host, implying that the ability of lice to attach to the host might limit host switching. Given that lice generally follow Harrison's rule, with larger parasites on larger hosts, parasites infecting the larger host species are less likely to successfully colonize smaller host species. Moreover, our study supports the general perception that successful colonization of a novel host is extremely rare, as we found only one nymph of a straggling species, which may indicate successful reproduction.     

Host resources govern the specificity of swiftlet lice: size matters

1. An important component of parasite diversity is the specificity for particular host taxa shown by many parasites. Specificity is often assumed to imply adaptive specialization by the parasite to its host, such that parasites are incapable of surviving and reproducing on 'foreign' hosts.
2. Specificity, however, need not be due to adaptation to particular hosts. Some parasites may be specific simply because they are incapable of dispersing among host taxa. For example, 'permanent' parasites like chewing lice spend their entire lifecycle on the body of the host and require direct contact between hosts for dispersal.
3. The role of adaptive constraints in parasite host-specificity has seldom been tested in natural populations. We conducted such a test by comparing the relative fitness of host-specific lice experimentally transferred among closely related species of cave swiftlets in northern Borneo.
4. The survival of lice in most of these transfers was significantly reduced in proportion to the mean difference in feather barb size between the donor and recipient species of hosts. Thus, adaptation to a particular resource on the body of the host does appear to govern the specificity of swiftlet lice.
5. In transfers where lice survived, microhabitat shifting on the body of the host was observed, whereby the mean barb diameter of the feathers on which the lice occurred was held 'constant'.     

Evidence That Head and Body Lice on Homeless Persons Have the Same Genotype

Human head lice and body lice are morphologically and biologically similar but have distinct ecologies. They were shown to have almost the same basic genetic content (one gene is absent in head lice), but differentially express certain genes, presumably responsible for the vector competence. They are now believed to be ecotypes of the same species (Pediculus humanus) and based on mitochondrial studies, body lice have been included with head lice in one of three clades of human head lice (Clade A). Here, we tested whether head and body lice collected from the same host belong to the same population by examining highly polymorphic intergenic spacers. This study was performed on lice collected from five homeless persons living in the same shelter in which Clade A lice are prevalent. Lice were individually genotyped at four spacer loci. The genetic identity and diversity of lice from head and body populations were compared for each homeless person. Population genetic structure was tested between lice from the two body regions and between the lice from different host individuals.We found two pairs of head and body lice on the same homeless person with identical multi locus genotypes. No difference in genetic diversity was found between head and body louse populations and no evidence of significant structure between the louse populations was found, even after controlling for a possible effect of the host individual. More surprisingly, no structure was obvious between lice of different homeless persons.We believe that the head and body lice collected from our five subjects belong to the same population and are shared between people living in the same shelter. These findings confirm that head and body lice are two ecotypes of the same species and show the importance of implementing measures to prevent lice transmission between homeless people in shelters.     

被动式电子标签用于花鼠种群动态研究的可行性

在野生动物研究过程中经常需要对动物个体进行标记。传统的标记方法存在着标记物易脱落、可能影响被标记动物的生理和行为、难于进行个体识别等缺点。被动式电子标签(passive integrated transponder, PIT)是基于射频识别技术的电子标签,可用于体内标记,具有不易脱落消失且能够进行个体识别的优点。我们在凉水国家级自然保护区以PIT标签为标记物,采用标志重捕技术开展花鼠(Eutamias sibiricus)的种群动态研究,同时对应用PIT标签的可靠性进行了研究。2011年秋季至2012年春季共标记花鼠个体140只,其中86只被重捕至少1次。2011年秋季标记的72只个体中有38只在2012年春季被重捕。重捕的花鼠个体注射口愈合完好,体重无明显降低。结果表明PIT标签是一种安全可靠、识别迅速、数据准确、不易丢失、可循环使用的体内标记电子标签,适用于基于个体识别的小型哺乳动物生态学研究。     

Unintentional parasite conservation success: chewing lice recovered from Crested Ibis,Nipponia nippon,in breeding program facilities in Shaanxi,China

The crested ibis has survived a dramatic population decline during the twentieth century, declining from a range across much of China, Japan, the Korean peninsula and nearby Russia, to a known world population of seven individuals. These formed the basis of a successful breeding program in Shaanxi, China. We examined ibises in this breeding program for ectoparasites, to establish whether any of the three chewing louse species known from this host had survived this severe host population bottleneck. We recovered representatives of three species of lice, identified as the same species as those previously known from the wild populations: Ardeicola nippon, Colpocephalum nipponi, and Ibidoecus meinertzhageni. Of these, the two first species were recovered from almost all examined hosts, whereas I. meinertzhageni was more rare. As these lice are host specific, this implies that all three louse species remarkably survived this bottleneck, and are now thriving in both the reintroduced and captive populations of crested ibis. This constitutes an unintentional success story in the conservation of parasitic species. We provide the first photos of all three species, as well as a preliminary assessment of their conservation status, and discuss the future of chewing louse conservation.

     

The Ectoparasites of the European Badger, Meles meles, and the Behavior of the Host-Specific Flea, Paraceras melis

The badger-specific flea, Paraceras melis, jumps repeatedly when separated from its host Meles meles; thereafter fleas settled into sheltered positions. After separation from badgers, some 42% of fleas (n = 63) voided their gut contents; this was associated with a significant increase in mean jumping distance. The maximum longevity of fleas away from the host was 89 days, with 50% mortality at around 35 days. Badger lice, Trichodectes melis, survived for up to 3 days postcapture. We conclude that the badger's habit of frequently swapping dens with a mean period of return of 6 days is unlikely to bring about significant mortality of adult fleas but may effectively eradicate lice. Fleas abandoned in bedding in a simulated badger sett were mobile, being drawn toward light and moving upward. This response would draw the fleas to the den entrance, which may be a suitable site to intercept returning badgers. The fleas responded to stimuli which might signal the proximity of the host: they jumped toward sources of carbon dioxide and of carbon dioxide in air current directed at the flea. The strongest response was seen when a mixture of stimuli consisting of carbon dioxide, a dark circle of card, and movement were tested; the majority of fleas jumped toward the mixed stimulus. Finally, fleas separated from the host responded to exhaled air by running and jumping; this is in marked contrast to their response to those stimuli when on the host, when fleas run downward and very rarely jump. These contrasting observations find adaptive explanation in the two contexts.     

Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France

By serving as hosts for native vectors, introduced species can surpass native hosts in their role as major reservoirs of local pathogens. During a 4-year longitudinal study, we investigated factors that affected infestation by ixodid ticks on both introduced Siberian chipmunks Tamias sibiricus barberi and native bank voles Myodes glareolus in a suburban forest (Forêt de Sénart, Ile-de-France). Ticks were counted on adult bank voles and on adult and young chipmunks using regular monthly trapping sessions, and questing ticks were quantified by dragging. At the summer peak of questing Ixodes ricinus availability, the average tick load was 27-69 times greater on adult chipmunks than on adult voles, while average biomass per hectare of chipmunks and voles were similar. In adult chipmunks, individual effects significantly explained 31% and 24% of the total variance of tick larvae and nymph burdens, respectively. Male adult chipmunks harboured significantly more larvae and nymphs than adult females, and than juveniles born in spring and in summer. The higher tick loads, and more specifically the ratio of nymphs over larvae, observed in chipmunks may be caused by a higher predisposition - both in terms of susceptibility and exposure - to questing ticks. Tick burdens were also related to habitat and seasonal variation in age- and sex-related space use by both rodents. Introduced chipmunks may thus have an important role in the dynamics of local vector-borne pathogens compared with native reservoir hosts such as bank voles.     

Allee effects may slow the spread of parasites in a coastal marine ecosystem

Allee effects are thought to mediate the dynamics of population colonization, particularly for invasive species. However, Allee effects acting on parasites have rarely been considered in the analogous process of infectious disease establishment and spread. We studied the colonization of uninfected wild juvenile Pacific salmon populations by ectoparasitic salmon lice (Lepeophtheirus salmonis) over a 4-year period. In a data set of 68,376 fish, we observed 85 occurrences of precopular pair formation among 1,259 preadult female and 613 adult male lice. The probability of pair formation was dependent on the local abundance of lice, but this mate limitation is likely offset somewhat by mate-searching dispersal of males among host fish. A mathematical model of macroparasite population dynamics that incorporates the empirical results suggests a high likelihood of a demographic Allee effect, which can cause the colonizing parasite populations to die out. These results may provide the first empirical evidence for Allee effects in a macroparasite. Furthermore, the data give a rare detailed view of Allee effects in colonization dynamics and suggest that Allee effects may dampen the spread of parasites in a coastal marine ecosystem.     

Linking coevolutionary history to ecological process: doves and lice

Abstract Many host-specific parasites are restricted to a limited range of host species by ecological barriers that impede dispersal and successful establishment. In some cases, microevolutionary differentiation is apparent on top of host specificity, as evidenced by significant parasite population genetic structure among host populations. Ecological barriers responsible for specificity and genetic structure can, in principle, reinforce macroevolutionary processes that generate congruent host-parasite phylogenies. However, few studies have explored both the micro- and macroevolutionary ramifications of close association in a single host-parasite system. Here we compare the macroevolutionary histories of two genera of feather lice (Phthiraptera: Ischnocera) that both parasitize New World pigeons and doves (Aves: Columbiformes). Earlier work has shown that dove body lice (genus Physconelloides ) are more host specific and have greater population genetic structure than dove wing lice ( Columbicola ). We reconstructed phylogenies for representatives of the two genera of lice and their hosts, using nuclear and mitochondrial DNA sequences. The phylogenies were well resolved and generally well supported. We compared the phylogenies of body lice and wing lice to the host phylogeny using reconciliation analyses. We found that dove body lice show strong evidence of cospeciation whereas dove wing lice do not. Although the ecology of body and wing lice is very similar, differences in their dispersal ability may underlie these joint differences in host specificity, population genetic structure, and coevolutionary history.     

Infection of wild fishes by the parasitic copepod Caligus elongatus on the south east coast of Norway

Natural Caligus elongatus Nordmann infections of wild coastal fishes on the Norwegian south east coast were monitored at various times of the year from 2002 to 2004. The prevalence for all coastal fish (n = 4427) pooled was 15%, and there were great differences between fish species and seasons. Lumpfish Cyclopterus lumpus L. spawners were the most infected fish, with a prevalence of 61% and a median intensity of 4 lice fish(-1), whereas gadids had a mean prevalence of 19% and a median infection of 1 to 2 lice fish(-1). Sea trout Salmo trutta L. and herring Clupea harengus L. carried C. elongatus at prevalence values of 29 and 21%, respectively. The results were compared with infection data for immature North Sea lumpfish. Lumpfish spawners caught on the coast in March to April had fewer lice than North Sea lumpfish in July. Spawners carried mostly adult lice, as did coastal fish hosts in May to June. The low development rates of lice at low spring temperatures and new genetic data suggest that the May to June adult lice could not have been offspring of the March to April lice, indicating transfer of adult lice to coastal fish. Most coastal fish species appeared to acquire new C. elongatus infections between May to June and September. The relatively high numbers of chalimii on North Sea lumpfish suggest that offshore fish sustain an oceanic population of this louse species.     

Size variation in chewing lice <Emphasis Type="Italic">Docophorulus coarctatus</Emphasis>: how host size and louse population density vary together

Chewing lice of the species Docophorulus coarctatus were extracted from museum specimens of their host, the great grey shrike Lanius excubitor, by combing feathers from 36 freshly shot birds (shot between 1962 and 1974), and samples of ten individual lice (five female, five male) were randomly collected for measurements from each bird. Female lice were bigger than males for all studied measurements (P < 0.001 in all cases), although the size of both sexes obtained from individual hosts was positively correlated. The overall size of lice (derived from a principal components analysis) was positively correlated with the overall size of the avian host, and also with the population density of lice on the individual host. We suggest that variation in louse morphology is due to differences in selection pressure exerted by each host and by intraspecific competition due to conspecifics. This is, to the best of our knowledge, the first evidence that Harrison’s rule (parasites on larger host species are often bigger than those on smaller hosts) not only works in a multispecies comparison but also within a single host–single parasite system as well.