An annotated checklist of chewing lice (Phthiraptera: Amblycera, Ischnocera) from Slovakia

This checklist includes taxa of chewing lice from published records, old collections, and recently collected material from birds and mammals in Slovakia. Data from established collections correspond to five different periods: (1) 1925–1939, collection of Karel Pfleger; (2) 1946–1978, collection of František Balát; (3) 1974–1985, collection of Vladimír Straka; (4) 1997–2012, collection of Ján Krištofík; and (5) 2008–2019, a collection made by the authors of this paper. A total of 255 species of feather lice—67 amblyceran species in 22 genera of families Laemobothriidae, Menoponidae and Ricinidae, and 188 ischnoceran species in 54 genera of the family Philopteridae—and 366 host-louse associations are listed from 171 bird species in 21 orders. In addition, eight species of chewing lice in five genera of the family Trichodectidae are listed from eight species of mammals. Species of chewing lice are reported from about 240 different locations throughout the territory of Slovakia. Also, 43 species of lice and 20 host-louse associations for Slovakia, as well as four host-louse associations for the world, are included as new records. A host-louse list of recorded species is also given.

The reduced genome of a heritable symbiont from an ectoparasitic feather feeding louse

Background Feather feeding lice are abundant and diverse ectoparasites that complete their entire life cycle on an avian host. The principal or sole source of nutrition for these lice is feathers. Feathers appear to lack four amino acids that the lice would require to complete development and reproduce. Several insect groups have acquired heritable and intracellular bacteria that can synthesize metabolites absent in an insect’s diet, allowing insects to feed exclusively on nutrient-poor resources. Multiple species of feather feeding lice have been shown to harbor heritable and intracellular bacteria. We expected that these bacteria augment the louse’s diet with amino acids and facilitated the evolution of these diverse and specialized parasites. Heritable symbionts of insects often have small genomes that contain a minimal set of genes needed to maintain essential cell functions and synthesize metabolites absent in the host insect’s diet. Therefore, we expected the genome of a bacterial endosymbiont in feather lice would be small, but encode pathways for biosynthesis of amino acids. Results We sequenced the genome of a bacterial symbiont from a feather feeding louse (Columbicola wolffhuegeli) that parasitizes the Pied Imperial Pigeon (Ducula bicolor) and used its genome to predict metabolism of amino acids based on the presence or absence of genes. We found that this bacterial symbiont has a small genome, similar to the genomes of heritable symbionts described in other insect groups. However, we failed to identify many of the genes that we expected would support metabolism of amino acids in the symbiont genome. We also evaluated other gene pathways and features of the highly reduced genome of this symbiotic bacterium. Conclusions Based on the data collected in this study, it does not appear that this bacterial symbiont can synthesize amino acids needed to complement the diet of a feather feeding louse. Our results raise additional questions about the biology of feather chewing lice and the roles of symbiotic bacteria in evolution of diverse avian parasites.

Comparing rates of introgression in parasitic feather lice with differing dispersal capabilities

Organisms vary in their dispersal abilities, and these differences can have important biological consequences, such as impacting the likelihood of hybridization events. However, there is still much to learn about the factors influencing hybridization, and specifically how dispersal ability affects the opportunities for hybridization. Here, using the ecological replicate system of dove wing and body lice (Insecta: Phthiraptera), we show that species with higher dispersal abilities exhibited increased genomic signatures of introgression. Specifically, we found a higher proportion of introgressed genomic reads and more reticulated phylogenetic networks in wing lice, the louse group with higher dispersal abilities. Our results are consistent with the hypothesis that differences in dispersal ability might drive the extent of introgression through hybridization.

Mitochondrial genomes of Columbicola feather lice are highly fragmented, indicating repeated evolution of minicircle-type genomes in parasitic lice

Most animals have a conserved mitochondrial genome structure composed of a single chromosome. However, some organisms have their mitochondrial genes separated on several smaller circular or linear chromosomes. Highly fragmented circular chromosomes (“minicircles”) are especially prevalent in parasitic lice (Insecta: Phthiraptera), with 16 species known to have between nine and 20 mitochondrial minicircles per genome. All of these species belong to the same clade (mammalian lice), suggesting a single origin of drastic fragmentation. Nevertheless, other work indicates a lesser degree of fragmentation (2–3 chromosomes/genome) is present in some avian feather lice (Ischnocera: Philopteridae). In this study, we tested for minicircles in four species of the feather louse genus Columbicola (Philopteridae). Using whole genome shotgun sequence data, we applied three different bioinformatic approaches for assembling the Columbicola mitochondrial genome. We further confirmed these approaches by assembling the mitochondrial genome of Pediculus humanus from shotgun sequencing reads, a species known to have minicircles. Columbicola spp. genomes are highly fragmented into 15–17 minicircles between ∼1,100 and ∼3,100 bp in length, with 1–4 genes per minicircle. Subsequent annotation of the minicircles indicated that tRNA arrangements of minicircles varied substantially between species. These mitochondrial minicircles for species of Columbicola represent the first feather lice (Philopteridae) for which minicircles have been found in a full mitochondrial genome assembly. Combined with recent phylogenetic studies of parasitic lice, our results provide strong evidence that highly fragmented mitochondrial genomes, which are otherwise rare across the Tree of Life, evolved multiple times within parasitic lice.

The role of scratching in the control of ectoparasites on birds

Grooming by birds is thought to serve essential anti-parasite functions. While preening has been well studied, little is known about the function of scratching in birds. We conducted a series of experiments to determine the effectiveness of scratching for controlling feather lice (Columbicola columbae) on Rock Pigeons (Columba livia). First, we used a hobbling technique to impair scratching. After 6 mo, hobbled birds had significantly more lice than controls that could scratch. In addition, lice on hobbled birds were concentrated on the birds’ heads and necks (i.e. the regions that birds scratch). Secondly, we tested the role the claw plays in scratching by declawing nestlings. Once mature, declawed pigeons had significantly more lice than control birds with claws. Moreover, lice on declawed birds were concentrated on the head and neck. Next, we tested whether the flange found on the middle claw of many bird species enhances scratching. We experimentally manipulated the flange; however, the number and location of lice on birds without flanges was not significantly different than that on control birds with intact flanges. Finally, we tested whether scratching removes parasites directly or indirectly by “flushing” them onto body regions where they can be preened. When we impaired scratching (with hobbles) and preening (with “bits”) we found that scratching no longer reduced the number of lice on birds. Our results indicated that scratching and preening work synergistically; scratching reduces parasite load by flushing lice onto regions of the body where they can be eliminated by preening.

Extensive in situ radiation of feather lice on tinamous

Tinamous host the highest generic diversity of lice of any group of birds, as well as hosting representatives of all four avian feather louse ecomorphs. Although the generic diversity of tinamou feather lice is well documented, few attempts have been made to reconstruct the phylogenetic relationships among these lice. To test whether tinamou feather lice form a monophyletic group as a whole, we used whole-genome sequencing to estimate a higher-level phylogeny of tinamou feather lice, together with a broad diversity of other avian feather louse groups. In total, we analysed sequences from over 1000 genes for 48 genera of avian lice using both concatenated and coalescent approaches to estimate the phylogeny of this diverse group of avian feather lice. Although the body louse ecomorph of tinamou feather lice formed a monophyletic group, they did not strictly form a monophyletic group together with the other three ecomorphs of tinamou feather lice. In particular, a clade comprised of several feather louse genera, mainly from South America, is nested phylogenetically within tinamou lice, which also have their main centre of diversity in South America. These results suggest in situ radiation of these parasites in South America.

Extensive host-switching of avian feather lice following the Cretaceous-Paleogene mass extinction event

Nearly all lineages of birds host parasitic feather lice. Based on recent phylogenomic studies, the three major lineages of modern birds diverged from each other before the Cretaceous-Paleogene (K-Pg) mass extinction event. In contrast, studies of the phylogeny of feather lice on birds, indicate that these parasites diversified largely after this event. However, these studies were unable to reconstruct the ancestral avian host lineage for feather lice. Here we use genome sequences of a broad diversity of lice to reconstruct a phylogeny based on 1,075 genes. By comparing this louse evolutionary tree to the avian host tree, we show that feather lice began diversifying on the common ancestor of waterfowl and landfowl, then radiated onto other avian lineages by extensive host-switching. Dating analyses and cophylogenetic comparisons revealed that two of three lineages of birds that diverged before the K-Pg boundary acquired their feather lice after this event via host-switching.

Implications of a Dating Analysis of Hippoboscoidea (Diptera) for the Origins of Phoresis in Feather Lice (Psocodea: Phthiraptera: Philopteridae)

Hippoboscidae (Samouelle 1819) is a family of blood feeding Diptera, which can be phoretic vectors for parasitic feather lice (Philopteridae Burmeister 1838). Hippoboscid flies are understood to provide opportunities for increased instances of dispersal and host-switching for feather lice. This intimate relationship between hippoboscid fly and feather louse may have hypothetically existed since the origin of avian-specialized Hippoboscidae. Thus, phoretic dispersal may have affected patterns of diversification in feather lice over millions of years. To test this, a dating analysis of a previously published Hippoboscoidea data set was performed using known fossil calibrations. The results of the dating analysis suggest Hippoboscoidea diversified shortly after the K-Pg boundary, similar to their modern vertebrate hosts. A maximum age of the avian feeding Ornithomyini is estimated to have occurred around the origin of parasitic feather lice. This maximum divergence date suggest this phoretic relationship could have existed for much of the diversification of avian feather lice and had the potential to influence patterns of diversification due to dispersal and host-switching among avian hosts.

Mitochondrial genomes ofColumbicolafeather lice are highly fragmented, indicating repeated evolution of minicircle-type genomes in parasitic lice

ABSTRACTMost animals have a conserved mitochondrial genome structure composed of a single chromosome. However, some organisms have their mitochondrial genes separated on several smaller circular or linear chromosomes. Highly fragmented circular chromosomes (“minicircles”) are especially prevalent in parasitic lice (Insecta: Phthiraptera), with 16 species known to have between 9 and 20 mitochondrial minicircles per genome. All of these species belong to the same clade (mammalian lice), suggesting a single origin of drastic fragmentation. Nevertheless, other work indicates a lesser degree of fragmentation (2-3 chromosomes/genome) is present in some avian feather lice (Ischnocera: Philopteridae). In this study, we tested for minicircles in four species of the feather louse genusColumbicola(Philopteridae). Using whole genome shotgun sequence data, we applied three different bioinformatic approaches for assembling theColumbicolamitochondrial genome. We further confirmed these approaches by assembling the mitochondrial genome ofPediculus humanusfrom shotgun sequencing reads, a species known to have minicircles. All three methods indicatedColumbicolaspp. genomes are highly fragmented into 15-17 minicircles between 1,119 and 3,173 bp in length, with 1-4 genes per minicircle. Subsequent annotation of the minicircles indicated that tRNA arrangements of minicircles varied substantially between species. These mitochondrial minicircles for species ofColumbicolarepresent the first feather lice (Philopteridae) for which minicircles have been found in a full mitochondrial genome assembly. Combined with recent phylogenetic studies of parasitic lice, our results provide strong evidence that highly fragmented mitochondrial genomes, which are otherwise rare across the Tree of Life, evolved multiple times within parasitic lice.

Rapid experimental evolution of reproductive isolation from a single natural population

Ecological speciation occurs when local adaptation generates reproductive isolation as a by-product of natural selection. Although ecological speciation is a fundamental source of diversification, the mechanistic link between natural selection and reproductive isolation remains poorly understood, especially in natural populations. Here, we show that experimental evolution of parasite body size over 4 y (approximately 60 generations) leads to reproductive isolation in natural populations of feather lice on birds. When lice are transferred to pigeons of different sizes, they rapidly evolve differences in body size that are correlated with host size. These differences in size trigger mechanical mating isolation between lice that are locally adapted to the different sized hosts. Size differences among lice also influence the outcome of competition between males for access to females. Thus, body size directly mediates reproductive isolation through its influence on both intersexual compatibility and intrasexual competition. Our results confirm that divergent natural selection acting on a single phenotypic trait can cause reproductive isolation to emerge from a single natural population in real time.