Highly Resolved Genomes of Two Closely Related Lineages of the Rodent Louse Polyplax serrata with Different Host Specificities.

Sucking lice of the parvorder Anoplura are permanent ectoparasites with specific lifestyle and highly derived features. Currently, genomic data are only available for a single species, the human louse Pediculus humanus. Here, we present genomes of two distinct lineages, with different host spectra, of a rodent louse Polyplax serrata. Genomes of these ecologically different lineages are closely similar in gene content and display a conserved order of genes, with the exception of a single translocation. Compared with P. humanus, the P. serrata genomes are noticeably larger (139 vs. 111 Mbp) and encode a higher number of genes. Similar to P. humanus, they are reduced in sensory-related categories such as vision and olfaction. Utilizing genome-wide data, we perform phylogenetic reconstruction and evolutionary dating of the P. serrata lineages. Obtained estimates reveal their relatively deep divergence (∼6.5 Mya), comparable with the split between the human and chimpanzee lice P. humanus and Pediculus schaeffi. This supports the view that the P. serrata lineages are likely to represent two cryptic species with different host spectra. Historical demographies show glaciation-related population size (Ne) reduction, but recent restoration of Ne was seen only in the less host-specific lineage. Together with the louse genomes, we analyze genomes of their bacterial symbiont Legionella polyplacis and evaluate their potential complementarity in synthesis of amino acids and B vitamins. We show that both systems, Polyplax/Legionella and Pediculus/Riesia, display almost identical patterns, with symbionts involved in synthesis of B vitamins but not amino acids.

Chewing lice of Bearded Reedling (Panurus biarmicus) and diversity of louse-host associations of birds in reed beds in Slovakia.

A total of 1,621 wild birds representing 34 species were examined for chewing lice in reed beds in southwestern Slovakia during the pre-breeding migration 2008-2009 and 2016-2019. A total of 377 (23.3%) birds representing 15 species were parasitized by 26 species of chewing lice of 12 genera. Dominant genera were Penenirmus (with dominance 32.6%) and Menacanthus (29.4%), followed by Brueelia (12.6%), Acronirmus (10.8%), Philopterus (7.7%), and Myrsidea (4.2%). We evaluated 33 host-louse associations including both 1) host-generalist, parasitizing more than one host species and host-specific lice, occurring only on a single host species, and 2) lice species with large range geographic distribution, reported across the range of the distribution of their hosts and lice species with only occasional records from a limited area within the range of their hosts. The Bearded Reedling, Panurus biarmicus (Linnaeus, 1758), was parasitized by two species of chewing lice, Menacanthus brelihi Balát, 1981 and Penenirmus visendus (Zlotorzycka, 1964), with conspicuously different prevalences (5.6% vs. 58.2%, respectively; n = 251). New material enabled us to redescribe both species of lice: the first one is resurrected from previous synonymy as a valid species. A fragment of the mitochondrial cytochrome oxidase I gene was sequenced from these two species in order to assess their relative phylogenetic position within their genera. Our study demonstrates the importance of an adequate identification of parasites, especially on rarely examined and endangered hosts.

Title: Mallophages de la Panure à moustaches (Panurus biarmicus) et diversité des associations mallophages-hôtes des oiseaux dans les roselières en Slovaquie. Abstract: Au total, 1 621 oiseaux sauvages représentant 34 espèces ont été examinés à la recherche de mallophages dans les roselières du sud-ouest de la Slovaquie au cours de la migration de pré-reproduction 2008­2009 et 2016­2019. Parmi ceux-ci, 377 oiseaux (23,3 %), représentant 15 espèces, étaient parasités par 26 espèces de mallophages de 12 genres. Les genres dominants étaient Penenirmus (avec une dominance de 32,6 %) et Menacanthus (29,4 %), suivis de Brueelia (12,6 %), Acronirmus (10,8 %), Philopterus (7,7 %) et Myrsidea (4,2 %). Nous avons évalué 33 associations mallophage-hôte comprenant à la fois 1) des espèces de mallophages généralistes, parasitant plus d'une espèce hôte, et des mallophages spécifiques, présents uniquement sur une seule espèce hôte et 2) des espèces de mallophages ayant une large répartition géographique, signalées à travers l'étendue de la répartition de leurs hôtes, et des espèces de mallophages avec seulement des observations occasionnelles dans une zone limitée à l'intérieur de l'aire de répartition de leurs hôtes. La Panure à moustaches, Panurus biarmicus (Linnaeus, 1758), était parasitée par deux espèces de mallophages, Menacanthus brelihi Balát, 1981 et Penenirmus visendus (Zlotorzycka, 1964), avec des prévalences nettement différentes (respectivement 5,6 % et 58,2 %, n = 251). Du nouveau matériel nous a permis de redécrire les deux espèces de mallophages, la première étant ressuscitée de la synonymie précédente en tant qu'espèce valide. Un fragment du gène mitochondrial de la cytochrome oxydase I a été séquencé à partir de ces deux espèces afin d'évaluer leur position phylogénétique relative au sein de leurs genres. Notre étude démontre l'importance d'une identification adéquate des parasites, en particulier sur les hôtes rarement examinés et menacés.

Supergroup F Wolbachia with extremely reduced genome: transition to obligate insect symbionts.

BACKGROUND: Wolbachia belong to highly abundant bacteria which are frequently found in invertebrate microbiomes and manifest by a broad spectrum of lifestyles from parasitism to mutualism. Wolbachia supergroup F is a particularly interesting clade as it gave rise to symbionts of both arthropods and nematodes, and some of its members are obligate mutualists. Investigations on evolutionary transitions among the different symbiotic stages have been hampered by a lack of the known diversity and genomic data for the supergroup F members. RESULTS: Based on amplicon screening, short- and long-read WGS approaches, and laser confocal microscopy, we characterize five new supergroup F Wolbachia strains from four chewing lice species. These strains reached different evolutionary stages and represent two remarkably different types of symbiont genomes. Three of the genomes resemble other known members of Wolbachia F supergroup, while the other two show typical signs of ongoing gene inactivation and removal (genome size, coding density, low number of pseudogenes). Particularly, wMeur1, a symbiont fixed in microbiomes of Menacanthus eurysternus across four continents, possesses a highly reduced genome of 733,850 bp. The horizontally acquired capacity for pantothenate synthesis and localization in specialized bacteriocytes suggest its obligate nutritional role. CONCLUSIONS: The genome of wMeur1 strain, from the M. eurysternus microbiome, represents the smallest currently known Wolbachia genome and the first example of Wolbachia which has completed genomic streamlining as known from the typical obligate symbionts. This points out that despite the large amount and great diversity of the known Wolbachia strains, evolutionary potential of these bacteria still remains underexplored. The diversity of the four chewing lice microbiomes indicates that this vast parasitic group may provide suitable models for further investigations. Video Abstract.

Phylogeography of the parasitic mite Laelaps agilis in Western Palearctic shows lineages lacking host specificity but possessing different demographic histories.

BACKGROUND: Laelaps agilis C.L. Koch, 1836 is one the most abundant and widespread parasitic mite species in the Western Palearctic. It is a permanent ectoparasite associated with the Apodemus genus, which transmits Hepatozoon species via the host's blood. Phylogenetic relationships, genealogy and host specificity of the mite are uncertain in the Western Palearctic. Here, we investigated the population genetic structure of 132 individual mites across Europe from their Apodemus and Clethrionomys hosts. Phylogenetic relationships and genetic variation of the populations were analyzed using cytochrome c oxidase subunit I (COI) gene sequences. RESULTS: We recovered three main mtDNA lineages within L. agilis in the Western Palearctic, which differentiated between 1.02 and 1.79 million years ago during the Pleistocene period: (i) Lineage A, including structured populations from Western Europe and the Czech Republic, (ii) Lineage B, which included only a few individuals from Greece and the Czech Republic; and (iii) Lineage C, which comprised admixed populations from Western and Eastern Europe. Contrary to their population genetic differentiation, the lineages did not show signs of specificity to different hosts. Finally, we confirmed that the sympatric congener L. clethrionomydis is represented by a separated monophyletic lineage. CONCLUSION: Differences in the depth of population structure between L. agilis Lineages A and C, corroborated by the neutrality tests and demographic history analyses, suggested a stable population size in the structured Lineage A and a rapid range expansion for the geographically admixed Lineage C. We hypothesized that the two lineages were associated with hosts experiencing different glaciation histories. The lack of host specificity in L. agilis lineages was in contrast to the co-occurring highly host-specific lineages of Polyplax serrata lice, sharing Apodemus hosts. The incongruence was attributed to the differences in mobility between the parasites, allowing mites to switch hosts more often.

A new symbiotic lineage related to Neisseria and Snodgrassella arises from the dynamic and diverse microbiomes in sucking lice.

The phylogenetic diversity of symbiotic bacteria in sucking lice suggests that lice have a complex history of symbiont acquisition, loss, and replacement throughout their evolution. These processes have resulted in the establishment of different, phylogenetically distant bacteria as obligate mutualists in different louse groups. By combining metagenomics and amplicon screening across several populations of three louse species (members of the genera Polyplax and Hoplopleura) we describe a novel louse symbiont lineage related to Neisseria and Snodgrassella, and show its independent origin in the two louse genera. While the genomes of these symbionts are highly similar, their respective distributions and status within lice microbiomes indicate that they have different functions and history. In Hoplopleura acanthopus, the Neisseriaceae-related bacterium is a dominant obligate symbiont present across several host populations. In contrast, the Polyplax microbiomes are dominated by the obligate symbiont Legionella polyplacis, with the Neisseriaceae-related bacterium co-occurring only in some samples and with much lower abundance. The results thus support the view that compared to other exclusively blood feeding insects, Anoplura possess a unique capacity to acquire symbionts from diverse groups of bacteria.

"Parasite turnover zone" at secondary contact: A new pattern in host-parasite population genetics.

We describe here a new pattern of population genetic structure in a host-parasite system that can arise after secondary contact of previously isolated populations. Due to different generation times, and therefore different tempos of molecular evolution, the host and parasite populations reach different degrees of genetic differentiation during their separation (e.g., in refugia). Consequently, upon secondary contact, the host populations are able to re-establish a single panmictic population across the area of contact, while the parasite populations stop their dispersal at the secondary contact zone and create a narrow hybrid zone. From the host's perspective, the parasite's hybrid zone functions on a microevolutionary scale as a "parasite turnover zone": while the hosts are passing from area A to area B, their parasites turn genetically from the area A genotypes to the area B genotypes. We demonstrate this novel pattern with a model composed of Apodemus mice and Polyplax lice by comparing maternally inherited markers (complete mitochondrial genomes, and complete genomes of the vertically transmitted symbiont Legionella polyplacis) with single nucleotide polymorphisms derived from louse genomic data. We discuss the circumstances that may lead to this pattern and possible reasons why it has been overlooked in studies of host-parasite population genetics.

Host specificity driving genetic structure and diversity in ectoparasite populations: Coevolutionary patterns in Apodemus mice and their lice.

A degree of host specificity, manifested by the processes of host-parasite cospeciations and host switches, is assumed to be a major determinant of parasites' evolution. To understand these patterns and formulate appropriate ecological hypotheses, we need better insight into the coevolutionary processes at the intraspecific level, including the maintenance of genetic diversity and population structure of parasites and their hosts. Here, we address these questions by analyzing large-scale molecular data on the louse Polyplax serrata and its hosts, mice of the genus Apodemus, across a broad range of European localities. Using mitochondrial DNA sequences and microsatellite data, we demonstrate the general genetic correspondence of the Apodemus/Polyplax system to the scenario of the postglacial recolonization of Europe, but we also show several striking discrepancies. Among the most interesting are the evolution of different degrees of host specificity in closely related louse lineages in sympatry, or decoupled population structures of the host and parasites in central Europe. We also find strong support for the prediction that parasites with narrower host specificity possess a lower level of genetic diversity and a deeper pattern of interpopulation structure as a result of limited dispersal and smaller effective population size.

Mysteries of host switching: Diversification and host specificity in rodent-coccidia associations.

Recent studies show that host switching is much more frequent than originally believed and constitutes an important driver in evolution of host-parasite associations. However, its frequency and ecological mechanisms at the population level have been rarely investigated. We address this issue by analyzing phylogeny and population genetics of an extensive sample, from a broad geographic area, for commonly occurring parasites of the genus Eimeria within the abundant rodent genera Apodemus, Microtus and Myodes, using two molecular markers. At the most basal level, we demonstrate polyphyletic arrangement, i.e. multiple origin, of the rodent-specific clusters within the Eimeria phylogeny, and strong genetic/phylogenetic structure within these lineages determined at least partially by specificities to different host groups. However, a novel and the most important observation is a repeated occurrence of host switches among closely related genetic lineages which may become rapidly fixed. Within the studied model, this phenomenon applies particularly to the switches between the eimerians from Apodemus flavicollis/Apodemus sylvaticus and Apodemus agrarius groups. We show that genetic differentiation and isolation between A. flavicollis/A. sylvaticus and A. agrarius faunas is a secondary recent event and does not reflect host-parasite coevolutionary history. Rather, it provides an example of rapid ecology-based differentiation in the parasite population.

Characterisation of microsatellite loci in two species of lice, Polyplax serrata (Phthiraptera: Anoplura: Polyplacidae) and Myrsidea nesomimi (Phthiraptera: Amblycera: Menoponidae).

Polymorphic microsatellite loci were characterised for two louse species, the anopluran Polyplax serrata Burmeister, 1839, parasitising Eurasian field mice of the genus Apodemus Kaup, and the amblyceran Myrsidea nesomimi Palma et Price, 2010, found on mocking birds endemic to the Galápagos Islands. Evolutionary histories of the two parasites show complex patterns influenced both by their geographic distribution and through coevolution with their respective hosts, which renders them prospective evolutionary models. In P. serrata, 16 polymorphic loci were characterised and screened across 72 individuals from four European populations that belong to two sympatric mitochondrial lineages differing in their breadth of host-specificity. In M. nesomimi, 66 individuals from three island populations and two host species were genotyped for 15 polymorphic loci. The observed heterozygosity varied from 0.05 to 0.9 in P. serrata and from 0.0 to 0.96 in M. nesomimi. Deviations from the Hardy-Weinberg equilibrium were frequently observed in the populations of both parasites. Fst distances between tested populations correspond with previous phylogenetic data, suggesting the microsatellite loci are an informative resource for ecological and evolutionary studies of the two parasites.

Host generalists and specialists emerging side by side: an analysis of evolutionary patterns in the cosmopolitan chewing louse genus Menacanthus.

Parasites with wide host spectra provide opportunities to study the ecological parameters of speciation, as well as the process of the evolution of host specificity. The speciose and cosmopolitan louse genus Menacanthus comprises both multi-host and specialised species, allowing exploration of the ecological and historical factors affecting the evolution of parasites using a comparative approach. We used phylogenetic analysis to reconstruct evolutionary relationships in 14 species of Menacanthus based on the sequences of one mitochondrial and one nuclear gene. The results allowed us to validate species identification based on morphology, as well as to explore host distribution by assumed generalist and specialist species. Our analyses confirmed a narrow host use for several species, however in some cases, the supposed host specialists had a wider host spectrum than anticipated. In one case a host generalist (Menacanthus eurysternus) was clustered terminally on a clade almost exclusively containing host specialists. Such a clade topology indicates that the process of host specialisation may not be irreversible in parasite evolution. Finally, we compared patterns of population genetic structure, geographic distribution and host spectra between two selected species, M. eurysternus and Menacanthus camelinus, using haplotype networks. Menacanthus camelinus showed limited geographical distribution in combination with monoxenous host use, whereas M. eurysternus showed a global distribution and lack of host specificity. It is suggested that frequent host switching maintains gene flow between M. eurysternus populations on unrelated hosts in local populations. However, gene flow between geographically distant localities was restricted, suggesting that geography rather than host-specificity is the main factor defining the global genetic diversity of M. eurysternus.

Winter infestation of wild birds by ticks and chiggers (Acari: Ixodidae, Trombiculidae) in the Czech Republic.

In winter months during 2003-2006, wild birds were captured and examined for ticks and chiggers at two sites near Brno, Czech Republic. In total, 1,362 birds, mostly passerines, were examined. The tick Ixodes arboricola Schulze et Schlottke, 1929 was found on 47 (3%) birds of six species. Ixodes ricinus Linnaeus, 1758 was found on 11 (1%) birds of five species. Larvae of chiggers Ascoschoengastia latyshevi (Schluger 1955) were found on 13 (1%) birds of six species. I. arboricola and A. latyshevi associated with hole-nesting birds can appear on birds rather frequently even during winter months. I. ricinus occurs on birds in winter sporadically.