Mitochondrial genome fragmentation is correlated with increased rates of molecular evolution.

While mitochondrial genome content and organization is quite diverse across all Eukaryotes, most bilaterian animal mitochondrial genomes (mitogenomes) exhibit highly conserved gene content and organisation, with genes typically encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) are among the notable exceptions, having mitogenomes fragmented into multiple circular chromosomes. To better understand the process of mitogenome fragmentation, we conducted a large-scale genomic study of a major group of lice, Amblycera, with extensive taxon sampling. Analyses of the evolution of mitogenome structure across a phylogenomic tree of 90 samples from 53 genera revealed evidence for multiple independent origins of mitogenome fragmentation, some inferred to have occurred less than five million years ago. We leveraged these many independent origins of fragmentation to compare the rates of DNA substitution and gene rearrangement, specifically contrasting branches with fragmented and non-fragmented mitogenomes. We found that lineages with fragmented mitochondrial genomes had significantly higher rates of mitochondrial sequence evolution. In addition, lineages with fragmented mitochondrial genomes were more likely to have mitogenome gene rearrangements than those with single-chromosome mitochondrial genomes. By combining phylogenomics and mitochondrial genomics we provide a detailed portrait of mitogenome evolution across this group of insects with a remarkably unstable mitogenome structure, identifying processes of molecular evolution that are correlated with mitogenome fragmentation.

First record of Cebidicola armatus (Phthiraptera: Trichodectidae) on the Brachyteles hypoxanthus (Primate: Atelidae) in Brazil.

This study reports for the first time the infestation of Cebidicola armatus in Brachyteles hypoxanthus. In total, 14 lice were recovered of an individual in Minas Gerais, Brazil. These were subjected to a microscopic analysis and the identification of C. armatus was carried out through its very characteristic morphology.

Association between louse abundance and MHC II supertypes in Galápagos mockingbirds.

Major histocompatibility complex class II (MHC II) is an essential molecule triggering the adaptive immune response by the presentation of pathogens to helper T cells. The association between individual MHC II variants and various parasites has become a frequent finding in studies of vertebrate populations. However, although bird ectoparasites have a significant effect on their host's fitness, and the host's immune system can regulate ectoparasitic infections, no study has yet investigated the association between MHC II polymorphism and ectoparasite infection in the populations of free-living birds. Here, we test whether an association exists between the abundance of a chewing louse (Myrsidea nesomimi) and MHC II polymorphism of its hosts, the Galápagos mockingbirds (Mimus). We have found that the presence of two MHC II supertypes (functionally differentiated clusters) was significantly associated with louse abundance. This pattern supports the theory that a co-evolutionary interaction stands behind the maintenance of MHC polymorphism. Moreover, we have found a positive correlation between louse abundance and heterophil/lymphocyte ratio (an indicator of immunological stress) that serves as an additional piece of evidence that ectoparasite burden is affected by immunological state of Galápagos mockingbirds.

Two lineages of kingfisher feather lice exhibit differing degrees of cospeciation with their hosts.

Unlike most bird species, individual kingfisher species (Aves: Alcedinidae) are typically parasitized by only a single genus of louse (Alcedoffula, Alcedoecus, or Emersoniella). These louse genera are typically specific to a particular kingfisher subfamily. Specifically, Alcedoecus and Emersoniella parasitize Halcyoninae, whereas Alcedoffula parasitizes Alcedininae and Cerylinae. Although Emersoniella is geographically restricted to the Indo-Pacific region, Alcedoecus and Alcedoffula are geographically widespread. We used DNA sequences from two genes, the mitochondrial COI and nuclear EF-1α genes, to infer phylogenies for the two geographically widespread genera of kingfisher lice, Alcedoffula and Alcedoecus. These phylogenies included 47 kingfisher lice sampled from 11 of the 19 currently recognized genera of kingfishers. We compared louse phylogenies to host phylogenies to reconstruct their cophylogenetic history. Two distinct clades occur within Alcedoffula, one that infests Alcedininae and a second that infests Cerylinae. All species of Alcedoecus were found only on host species of the subfamily Halcyoninae. Cophylogenetic analysis indicated that Alcedoecus, as well as the clade of Alcedoffula occurring on Alcedininae, do not show evidence of cospeciation. In contrast, the clade of Alcedoffula occurring on Cerylinae showed strong evidence of cospeciation.

Phylogenomics using Target-Restricted Assembly Resolves Intrageneric Relationships of Parasitic Lice (Phthiraptera: Columbicola).

Parasitic "wing lice" (Phthiraptera: Columbicola) and their dove and pigeon hosts are a well-recognized model system for coevolutionary studies at the intersection of micro- and macroevolution. Selection on lice in microevolutionary time occurs as pigeons and doves defend themselves against lice by preening. In turn, behavioral and morphological adaptations of the lice improve their ability to evade host defense. Over macroevolutionary time wing lice tend to cospeciate with their hosts; yet, some species of Columbicola have switched to new host species. Understanding the ecological and evolutionary factors that influence coadaptation and codiversification in this system will substantially improve our understanding of coevolution in general. However, further work is hampered by the lack of a robust phylogenetic framework for Columbicola spp. and their hosts. Previous attempts to resolve the phylogeny of Columbicola based on sequences from a few genes provided limited support. Here, we apply a new approach, target restricted assembly, to assemble 977 orthologous gene sequences from whole-genome sequence data generated from very small, ethanol-preserved specimens, representing up to 61 species of wing lice. Both concatenation and coalescent methods were used to estimate the species tree. These two approaches yielded consistent and well-supported trees with 90% of all relationships receiving 100% support, which is a substantial improvement over previous studies. We used this new phylogeny to show that biogeographic ranges are generally conserved within clades of Columbicola wing lice. Limited inconsistencies are probably attributable to intercontinental dispersal of hosts, and host switching by some of the lice. [aTRAM; coalescent; coevolution; concatenation; species tree.].

Simultaneous radiation of bird and mammal lice following the K-Pg boundary.

The diversification of parasite groups often occurs at the same time as the diversification of their hosts. However, most studies demonstrating this concordance only examine single host-parasite groups. Multiple diverse lineages of ectoparasitic lice occur across both birds and mammals. Here, we describe the evolutionary history of lice based on analyses of 1107 single-copy orthologous genes from sequenced genomes of 46 species of lice. We identify three major diverse groups of lice: one exclusively on mammals, one almost exclusively on birds and one on both birds and mammals. Each of these groups radiated just after the Cretaceous-Paleogene (K-Pg) boundary, the time of the mass extinction event of the dinosaurs and rapid diversification of most of the modern lineages of birds and mammals.

Ectoparasites of small-mammals: determinants of community structure in South American savannah.

This study aimed to assess the contribution of hosts characteristics (rodents and marsupials) in the organization of ectoparasite communities present in woodland patches in western central Brazil. We verified the effect of host species, sex, body mass and vertical strata in addition to the role of seasonality on the ectoparasite composition, richness and abundance. The total sampling effort was 22 032 trap-nights equally distributed in 54 woodland patches. Variance partition and principal coordinate analysis were used to verify the existence of significant relationships between response variables and predictors. As expected, host species was the most important variable in ectoparasite community assembly. The composition, richness and abundance of mites and lice were highly influenced by host species, although higher for mites than for lice. Host body mass had a determining role on the richness and abundance of tick species. Vertical stratification and seasonality had weak influence, while the sex of the host had no influence on the organization of these communities. The results are closely related to the evolutionary characteristics of the species involved, as well as with local environmental characteristics of the study area.

Unlocking the black box of feather louse diversity: A molecular phylogeny of the hyper-diverse genus Brueelia.

Songbirds host one of the largest, and most poorly understood, groups of lice: the Brueelia-complex. The Brueelia-complex contains nearly one-tenth of all known louse species (Phthiraptera), and the genus Brueelia has over 300 species. To date, revisions have been confounded by extreme morphological variation, convergent evolution, and periodic movement of lice between unrelated hosts. Here we use Bayesian inference based on mitochondrial (COI) and nuclear (EF-1α) gene fragments to analyze the phylogenetic relationships among 333 individuals within the Brueelia-complex. We show that the genus Brueelia, as it is currently recognized, is paraphyletic. Many well-supported and morphologically unified clades within our phylogenetic reconstruction of Brueelia were previously described as genera. These genera should be recognized, and the erection of several new genera should be explored. We show that four distinct ecomorphs have evolved repeatedly within the Brueelia-complex, mirroring the evolutionary history of feather-lice across the entire order. We show that lice in the Brueelia-complex, with some notable exceptions, are extremely host specific and that the host family associations and geographic distributions of these lice are significantly correlated with our understanding of their phylogenetic history. Several ecological phenomena, including phoresis, may be responsible for the macroevolutionary patterns in this diverse group.

Cophylogenetic analysis of New World ground-doves (Aves: Columbidae) and their parasitic wing lice (Insecta: Phthiraptera: Columbicola).

Hosts-parasite interactions are plentiful and diverse, and understanding the patterns of these interactions can provide great insight into the evolutionary history of the organisms involved. Estimating the phylogenetic relationships of a group of parasites and comparing them to that of their hosts can indicate how factors such as host or parasite life history, biogeography, or climate affect evolutionary patterns. In this study we compare the phylogeny generated for a clade of parasitic chewing lice (Insecta: Phthiraptera) within the genus Columbicola to that of their hosts, the small New World ground-doves (Aves: Columbidae). We sampled lice from the majority of host species, including samples from multiple geographic locations. From these samples we sequenced mitochondrial and nuclear loci for the lice, and used these data to estimate phylogenetic trees and population networks. After estimating the appropriate number of operational taxonomic units (OTUs) for the lice, we used cophylogenetic analyses to compare the louse phylogeny to an existing host phylogeny. Our phylogenetic analysis recovered significant structure within the louse clade, including evidence for potentially cryptic species. All cophylogenetic analyses indicated an overall congruence between the host and parasite trees. However, we only recovered a single cospeciation event. This finding suggests that certain branches in the trees are driving the signal of congruence. In particular, lice with the highest levels of congruence are associated with high Andean species of ground-doves that are well separated altitudinally from other related taxa. Other host-parasite associations are not as congruent, and these often involved widespread louse taxa. These widespread lice did, however, have significant phylogeographic structure, and their phylogenetic relationships are perhaps best explained by biogeographic patterns. Overall these results indicate that both host phylogeny and biogeography can be simultaneously important in influencing the patterns of diversification of parasites.

Chewing Lice of Swan Geese (Anser cygnoides): New Host-Parasite Associations.

Chewing lice (Phthiraptera) that parasitize the globally threatened swan goose Anser cygnoides have been long recognized since the early 19th century, but those records were probably biased towards sampling of captive or domestic geese due to the small population size and limited distribution of its wild hosts. To better understand the lice species parasitizing swan geese that are endemic to East Asia, we collected chewing lice from 14 wild geese caught at 3 lakes in northeastern Mongolia. The lice were morphologically identified as 16 Trinoton anserinum (Fabricius, 1805), 11 Ornithobius domesticus Arnold, 2005, and 1 Anaticola anseris (Linnaeus, 1758). These species are known from other geese and swans, but all of them were new to the swan goose. This result also indicates no overlap in lice species between older records and our findings from wild birds. Thus, ectoparasites collected from domestic or captive animals may provide biased information on the occurrence, prevalence, host selection, and host-ectoparasite interactions from those on wild hosts.

[THE FAUNA AND POPULATION OF CHEWING LICE (INSECTA, PHTHIRAPTERA) PARASITIZING SEDENTARY PASSERINE BIRDS (AVES, PASSERIFORMES) IN YAKUTIA].

The data on the fauna, abundance and prevalence of chewing lice collected from 360 specimens of 13 sedentary species of passerine birds in Yakutia are given. A total of 3206 chewing lice specimens belonging to 27 species of 6 genera were found. Most explored bird species were infested with several chewing lice species. We assume exchanges of parasites could take place between some bird species in the region explored.

Six new species of Myrsidea Waterston, 1915 (Phthiraptera: Menoponidae) from New World jays of the genus Cyanocorax Boie (Passeriformes: Corvidae), with notes on the chorionic structure of eggs.

The only species of previously named Myrsidea Waterston, 1915 from Neotropical jays of the genus Cyanocorax Boie (Passeriformes: Corvidae), Myrsidea fallax Kéler, 1938 (type-host Cyanocorax cyanomelas Vieillot), is redescribed and six new species of lice in the genus Myrsidea are described: Myrsidea pseudofallax n. sp. [type-host C. c. chrysops (Vieillot)]; M. moriona n. sp. [type-host C. m. morio (Wagler)]; Myrsidea daleclaytoni n. sp. [type-host C. v. violaceus Du Bus de Gisignies]; Myrsidea lindolphoi n. sp. [type-host C. caeruleus (Vieillot)]; Myrsidea melanocyanei n. sp. [type-host C. melanocyaneus chavezi (Miller & Griscom)]; and Myrsidea cristatelli n. sp. [type-host C. cristatellus (Temminck)]. A key to the identification of both sexes of these seven species is provided. Immature stages of M. daleclaytoni n. sp. (all instars) and M. cristatelli n. sp. (nymph III) are described. External chorionic architecture of the eggs is described and illustrated for six Myrsidea spp. from corvine birds: M. picae (Linnaeus, 1758) ex Pica p. pica L.; M. cornicis (DeGeer, 1778) ex Corvus c. corone L.; M. isostoma (Nitzsch in Giebel, 1866) ex Co. f. frugilegus L.; M. interrupta (Osborn, 1896) ex Co. brachyrhynchus Brehm; M. fallax ex Cy. cyanomelas; and M. moriona n. sp. ex Cy. m. morio. This is the first review of the data on Myrsidea spp. infesting Neotropical Corvidae.

Population genetics of bisexual and unisexual populations of the scaly-winged bark louse Echmepteryx hageni (Insecta: Psocoptera).

The scaly-winged bark louse, Echmepteryx hageni, exhibits a unique pattern of co-existence of apparently differnt reproductive modes. Unisexuality is widespread in eastern North America, while sexual populations are restricted to isolated rock out-croppings in southern Illinois and eastern Kentucky. Three of the four nuclear loci examined show greater genetic diversity in the unisexual form compared to the sexual form of E. hageni, in accordance with the pattern previously shown in mitochondrial genetic data. Neutrality tests of the nuclear loci indicate a consistent signal of demographic expansion in asexual populations, but not in sexual populations. There was evidence of inbreeding in the isolated sexual populations at three of the nuclear loci, and one locus had signs of gene specific balancing selection. However, there is no significant genetic differentiation between bisexual and unisexual populations, possibly due to the greater effective population size of nuclear loci relative to mitochondrial loci. The mitochondrial differentiation of E. hageni populations in the northwestern part of their range (Minnesota and Wisconsin) was also not reflected in the nuclear data. We present three hypotheses that may explain the disparity in observed nuclear and mitochondrial genetic diversity between the reproductive forms of E. hageni.

Comparisons of host specificity in feather louse genera (Insecta: Phthiraptera: Philopteridae) parasitizing gulls (Aves: Laridae: Larus).

Data from gene sequences and morphological structures were collected for the gull feather lice, Saemundssonia lari, Quadraceps punctatus, and Q. ornatus, parasitizing Larus crassirostris and L. schistisagus. Saemundssonia lari was collected from both gull species, and no detectable morphological and genetic differences were found between lice collected from the two different hosts. In contrast, Q. punctatus was only collected from L. crassirostris, whereas Q. ornatus was only collected from L. schistisagus. The two Quadraceps species were genetically highly divergent, and body-size differences corresponding to the gull's body size (Harrison's rule) were also detected between them. Both Quadraceps species were collected from the interbarb of the remex or rectrix, and a match in body size between the louse and the interbarb space may be important in escape from host preening defenses. In contrast, Saemundssonia is a head louse, inhabiting the finer feathers of the head and neck, which the bird cannot preen. A close match to host body size may be less important for lice in the head microhabitat. The differences in the pattern of host-specificity between Saemundssonia and Quadraceps on the two focal host species of this study were probably due to their different microhabitat preferences. More broadly, comparisons of the gene sequences of S. lari and Q. punctatus to those from other gull hosts showed that genetically almost undifferentiated populations of both species were distributed on wide range of gull species. Frequent interspecific hybridization of gulls is one possible factor that may allow these lice to maintain gene flow across multiple host species.

Community interactions govern host-switching with implications for host-parasite coevolutionary history.

Reciprocal selective effects between coevolving species are often influenced by interactions with the broader ecological community. Community-level interactions may also influence macroevolutionary patterns of coevolution, such as cospeciation, but this hypothesis has received little attention. We studied two groups of ecologically similar feather lice (Phthiraptera: Ischnocera) that differ in their patterns of association with a single group of hosts. The two groups, "body lice" and "wing lice," are both parasites of pigeons and doves (Columbiformes). Body lice are more host-specific and show greater population genetic structure than wing lice. The macroevolutionary history of body lice also parallels that of their columbiform hosts more closely than does the evolutionary history of wing lice. The closer association of body lice with hosts, compared with wing lice, can be explained if body lice are less capable of switching hosts than wing lice. Wing lice sometimes disperse phoretically on parasitic flies (Diptera: Hippoboscidae), but body lice seldom engage in this behavior. We tested the hypothesis that wing lice switch host species more often than body lice, and that the difference is governed by phoresis. Our results show that, where flies are present, wing lice switch to novel host species in sufficient numbers to establish viable populations on the new host. Body lice do not switch hosts, even where flies are present. Thus, differences in the coevolutionary history of wing and body lice can be explained by differences in host-switching, mediated by a member of the broader parasite community.

Next-generation phylogenomics using a Target Restricted Assembly Method.

Next-generation sequencing technologies are revolutionizing the field of phylogenetics by making available genome scale data for a fraction of the cost of traditional targeted sequencing. One challenge will be to make use of these genomic level data without necessarily resorting to full-scale genome assembly and annotation, which is often time and labor intensive. Here we describe a technique, the Target Restricted Assembly Method (TRAM), in which the typical process of genome assembly and annotation is in essence reversed. Protein sequences of phylogenetically useful genes from a species within the group of interest are used as targets in tblastn searches of a data set from a lane of Illumina reads for a related species. Resulting blast hits are then assembled locally into contigs and these contigs are then aligned against the reference "cDNA" sequence to remove portions of the sequences that include introns. We illustrate the Target Restricted Assembly Method using genomic scale datasets for 20 species of lice (Insecta: Psocodea) to produce a test phylogenetic data set of 10 nuclear protein coding gene sequences. Given the advantages of using DNA instead of RNA, this technique is very cost effective and feasible given current technologies.

The sympatric occurrence of two genetically divergent lineages of sucking louse, Polyplax arvicanthis (Phthiraptera: Anoplura), on the four-striped mouse genus, Rhabdomys (Rodentia: Muridae).

Within southern Africa, the widely distributed four-striped mouse genus (Rhabdomys) is parasitized by, amongst others, the specific ectoparasitic sucking louse, Polyplax arvicanthis. Given the presence of significant geographically structured genetic divergence in Rhabdomys, and the propensity of parasites to harbour cryptic diversity, the molecular systematics of P. arvicanthis was investigated. Representatives of P. arvicanthis were sampled from Rhabdomys at 16 localities throughout southern Africa. Parsimony and Bayesian gene trees were constructed for the mitochondrial COI, 12S rRNA, 16S rRNA and nuclear CAD genes. Our findings support the existence of 2 genetic groups within P. arvicanthis separated by at least 25% COI sequence divergence, which is comparable to that observed among recognized Polyplax species. We therefore propose that these 2 genetic lineages probably represent distinct species and that the apparent absence of clear morphological differences may point to cryptic speciation. The 2 taxa have sympatric distributions throughout most of the sampled host range and also occasionally occur sympatrically on the same host individual. The co-occurrence of these genetically distinct lineages probably resulted from parasite duplication via host-associated allopatric divergence and subsequent reciprocal range expansions of the 2 parasite taxa throughout southern Africa.

The efficacy and safety of alphacypermethrin as a pour-on treatment for water buffalo (Bubalus bubalis) infested with Haematopinus tuberculatus (Phthiraptera: Haematopinidae).

The sucking louse Haematopinus tuberculatus (Burmeister 1839) is an ectoparasite of buffaloes, cattle, camels, and American bison. Alphacypermethrin (ACYP) is a pyrethroid insecticide commonly used to control arthropods of veterinary and public health interest. Therapeutics, such as antiparasitic compounds, is often administered to buffaloes based on dosage and intervals recommended for cattle because very few drugs have buffalo-specific label indications. A trial was conducted on 20 louse-infested buffaloes at a farm to assess the efficacy and safety of ACYP pour-on, at the manufacturer's recommended dose for cattle, on buffaloes naturally infested by H. tuberculatus. Ten animals were assigned to ACYP-treated group (ACYP-group) and ten to untreated control group (C-group). On day 0, all ACYP-group buffaloes received alphacypermethrin pour-on. Louse counts were performed on days -1, 7, 14, 21, 28, 35, 42, 49, and 56 at eight predilection sites on the skin of each buffalo. ACYP was completely effective (100%) at day 7, highly effective (99.8%) at day 14, and completely effective (100%) from day 21 until the end of the study (day 56 post-treatment). During the trial, ACYP was well tolerated by all animals as there were no observed clinically adverse reactions. The results of this trial suggest that ACYP is an effective, safe, and user-friendly compound suitable for treatment of buffaloes with natural louse infestations.

Ectoparasitic insects and mites on Yunnan red-backed voles (Eothenomys miletus) from a localized area in southwest China.

Ectoparasitic insects and mites on Yunnan red-backed voles (Eothenomys miletus) in Dali prefecture, Yunnan Province, southwest China, were studied between 2003 and 2004. In total, 34,389 individuals of 86 species of ectoparasitic insects (seven species of fleas and five species of sucking lice) and mites (23 species of gamasid mites and 51 species of chigger mites) were collected from 916 individual hosts. The diversity of ectoparasites on this single rodent species in such a small area was much higher than in previous reports, which concerned more host species and greater geographical areas. The majority of the ectoparasites were chigger mites, which accounted for 59.3% of the parasite species and 87.4% of the individual parasites. Most voles harbored parasites with an overall prevalence (P) of 82.5% and mean abundance (MA) of 37.5 parasites per host. The dispersion coefficient (C) and patchiness index (m*/m) were used to study the spatial patterns of the seven dominant parasite species, and all seven had aggregated distributions. The species abundance distribution of the ectoparasites on the vole was fitted by Preston's lognormal distribution (R (2) = 0.82), and the total expected parasite species was estimated from this plot as 167 species. Yunnan red-backed voles harbor many ectoparasites as revealed by examination of a large host population. Future field investigations should sample large numbers of host individuals to assess ectoparasite populations.

A drop in the bucket of the megadiverse chewing louse genus Myrsidea (Phthiraptera, Amblycera, Menoponidae): ten new species from Amazonian Brazil.

Ten new species of Myrsidea Waterston, 1915 parasitic on members of the avian families Formicariidae, Thraupidae, Tyrannidae, Troglodytidae and Icteridae are described herein. They and their type hosts are M. isacantha sp. n. ex Chamaeza nobilis Gould, M. circumsternata sp. n. ex Formicarius colma Boddaert (Formicariidae); M. cacioppoi sp. n. ex Lanio fulvus (Boddaert), M. brasiliensis sp. n. ex Tangara chilensis (Vigors), M. saviti sp. n. ex Tangara schrankii (Spix) (Thraupidae), M. rodriguesae sp. n. ex Cnipodectes subbrunneus (Sclater), M. cnemotriccola sp. n. ex Cnemotriccus fuscatus (Wied-Neuwied), M. lathrotriccola sp. n. ex Lathrotriccus euleri (Cabanis) (Tyrannidae), M. faccioae sp. n. ex Cyphorhinus arada transfluvialis (Todd) (Troglodytidae), and M. lampropsaricola sp. n. ex Lampropsar tanagrinus (Spix) (Icteridae). Among these are two new Myrsidea species described from the avian family Formicariidae, which previously had only a single described Myrsidea species, and a new host record for M. cinnamomei Dalgleish et Price, 2005 ex Attila citriniventris Sclater. Analysis of mitochondrial cytochrome oxidase I sequences for these and other neotropical Myrsidea species provides an assessment of their phylogenetic relationships and indicates that all of these newly described species are genetically distinct. We also put these descriptions into context by estimating the potential number of unnamed Myrsidea species in Brazil, given the known diversity of potential hosts and typical levels of host specificity for Myrsidea species. Our estimate indicates that Brazilian Myrsidea species diversity is likely more than an order of magnitude greater than the number of described Myrsidea species known from Brazil, highlighting the need for future work on this megadiverse ectoparasite genus.