Macroparasites of introduced parakeets in Italy: a possible role for parasite-mediated competition.

Alien species are considered a cause of biodiversity loss throughout the world. An important but often overlooked form of competition with native species is the parasite-mediated one. Introduced species may bring their own parasites from their native ranges (spillover) or get native parasites from native species, thus increasing the parasites' spread and transmission risk (spillback). Thus, a complete knowledge of parasites hosted by introduced species is important to assess and to possibly prevent impacts. Ring-necked and monk parakeets have been introduced in many European countries, where they established a number of alien reproductive populations. We sampled 21 ring-necked parakeets and 7 monk parakeets from Italy and identified 35 arthropod ectoparasites belonging to five species. Amongst those, one species was native to India (Neopsittaconirmus lybartota), where alien populations of ring-necked parakeet may have been originated, and one species from South America (Paragoniocotes fulvofasciatus), which is typically found of the monk parakeet in its native range. The other three species of arthropod parasites were native to Italy and commonly found on native species, suggesting the possibility of spillback processes.

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.

Repeated adaptive divergence of microhabitat specialization in avian feather lice.

BACKGROUND: Repeated adaptive radiations are evident when phenotypic divergence occurs within lineages, but this divergence into different forms is convergent when compared across lineages. Classic examples of such repeated adaptive divergence occur in island (for example, Caribbean Anolis lizards) and lake systems (for example, African cichlids). Host-parasite systems in many respects are analogous to island systems, where host species represent isolated islands for parasites whose life cycle is highly tied to that of their hosts. Thus, host-parasite systems might exhibit interesting cases of repeated adaptive divergence as seen in island and lake systems.The feather lice of birds spend their entire life cycle on the body of the host and occupy distinct microhabitats on the host: head, wing, body and generalist. These microhabitat specialists show pronounced morphological differences corresponding to how they escape from host preening. We tested whether these different microhabitat specialists were a case of repeated adaptive divergence by constructing both morphological and molecular phylogenies for a diversity of avian feather lice, including many examples of head, wing, body and generalist forms. RESULTS: Morphological and molecular based phylogenies were highly incongruent, which could be explained by rampant convergence in morphology related to microhabitat specialization on the host. In many cases lice from different microhabitat specializations, but from the same group of birds, were sister taxa. CONCLUSIONS: This pattern indicates a process of repeated adaptive divergence of these parasites within host group, but convergence when comparing parasites across host groups. These results suggest that host-parasite systems might be another case in which repeated adaptive radiations could be relatively common, but potentially overlooked, because morphological convergence can obscure evolutionary relationships.

A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites.

BACKGROUND: Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galápagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms. RESULTS: Mitochondrial DNA sequences were obtained for four species of Galápagos mockingbirds and three sympatric species of ectoparasites--two louse and one mite species. These data were complemented with nuclear EF1α sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands. CONCLUSIONS: The gene genealogies of Galápagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galápagos mockingbirds and their parasites.

Multiple lineages of lice pass through the K-Pg boundary.

For modern lineages of birds and mammals, few fossils have been found that predate the Cretaceous-Palaeogene (K-Pg) boundary. However, molecular studies using fossil calibrations have shown that many of these lineages existed at that time. Both birds and mammals are parasitized by obligate ectoparasitic lice (Insecta: Phthiraptera), which have shared a long coevolutionary history with their hosts. Evaluating whether many lineages of lice passed through the K-Pg boundary would provide insight into the radiation of their hosts. Using molecular dating techniques, we demonstrate that the major louse suborders began to radiate before the K-Pg boundary. These data lend support to a Cretaceous diversification of many modern bird and mammal lineages.

Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura).

BACKGROUND: Sucking lice (Phthiraptera: Anoplura) are obligate, permanent ectoparasites of eutherian mammals, parasitizing members of 12 of the 29 recognized mammalian orders and approximately 20% of all mammalian species. These host specific, blood-sucking insects are morphologically adapted for life on mammals: they are wingless, dorso-ventrally flattened, possess tibio-tarsal claws for clinging to host hair, and have piercing mouthparts for feeding. Although there are more than 540 described species of Anoplura and despite the potential economical and medical implications of sucking louse infestations, this study represents the first attempt to examine higher-level anopluran relationships using molecular data. In this study, we use molecular data to reconstruct the evolutionary history of 65 sucking louse taxa with phylogenetic analyses and compare the results to findings based on morphological data. We also estimate divergence times among anopluran taxa and compare our results to host (mammal) relationships. RESULTS: This study represents the first phylogenetic hypothesis of sucking louse relationships using molecular data and we find significant conflict between phylogenies constructed using molecular and morphological data. We also find that multiple families and genera of sucking lice are not monophyletic and that extensive taxonomic revision will be necessary for this group. Based on our divergence dating analyses, sucking lice diversified in the late Cretaceous, approximately 77 Ma, and soon after the Cretaceous-Paleogene boundary (ca. 65 Ma) these lice proliferated rapidly to parasitize multiple mammalian orders and families. CONCLUSIONS: The diversification time of sucking lice approximately 77 Ma is in agreement with mammalian evolutionary history: all modern mammal orders are hypothesized to have diverged by 75 Ma thus providing suitable habitat for the colonization and radiation of sucking lice. Despite the concordant timing of diversification events early in the association between anoplurans and mammals, there is substantial conflict between the host and parasite phylogenies. This conflict is likely the result of a complex history of host switching and extinction events that occurred throughout the evolutionary association between sucking lice and their mammalian hosts. It is unlikely that there are any ectoparasite groups (including lice) that tracked the early and rapid radiation of eutherian mammals.

Scratchpads: a data-publishing framework to build, share and manage information on the diversity of life.

BACKGROUND: Natural History science is characterised by a single immense goal (to document, describe and synthesise all facets pertaining to the diversity of life) that can only be addressed through a seemingly infinite series of smaller studies. The discipline's failure to meaningfully connect these small studies with natural history's goal has made it hard to demonstrate the value of natural history to a wider scientific community. Digital technologies provide the means to bridge this gap. RESULTS: We describe the system architecture and template design of "Scratchpads", a data-publishing framework for groups of people to create their own social networks supporting natural history science. Scratchpads cater to the particular needs of individual research communities through a common database and system architecture. This is flexible and scalable enough to support multiple networks, each with its own choice of features, visual design, and constituent data. Our data model supports web services on standardised data elements that might be used by related initiatives such as GBIF and the Encyclopedia of Life. A Scratchpad allows users to organise data around user-defined or imported ontologies, including biological classifications. Automated semantic annotation and indexing is applied to all content, allowing users to navigate intuitively and curate diverse biological data, including content drawn from third party resources. A system of archiving citable pages allows stable referencing with unique identifiers and provides credit to contributors through normal citation processes. CONCLUSION: Our framework http://scratchpads.eu/ currently serves more than 1,100 registered users across 100 sites, spanning academic, amateur and citizen-science audiences. These users have generated more than 130,000 nodes of content in the first two years of use. The template of our architecture may serve as a model to other research communities developing data publishing frameworks outside biodiversity research.

The Natural History Museum Data Portal.

The Natural History Museum, London (NHM), generates and holds some of the largest global data sets relating to the biological and geological diversity of the natural world. A majority of these data were, until 2015, not widely accessible, and, even when published, were typically hard to find, poorly documented and in formats that impede discovery and integration. To better serve the bespoke needs of user communities outside and within the NHM, a dedicated data portal was developed to surface these data sets and provide a sustainable platform to encourage their citation and reuse. This paper describes the technical development of the data portal, from its inception to beta launch in December 2015, its first 2 years of operation, and future plans for the project. It outlines the development principles adopted for this prototypical project, which subsequently informed new digital project management methodologies at the NHM. The process of developing the data portal acted as a driver to implement policies necessary to encourage a culture of data sharing at the NHM.

A Novel Automated Mass Digitisation Workflow for Natural History Microscope Slides.

The Natural History Museum, London (NHM) has embarked on an ambitious programme to digitise its collections. One aim of the programme has been to improve the workflows and infrastructure needed to support high-throughput digitisation and create comprehensive digital inventories of large scientific collections. This paper presents the workflow developed to digitise the entire Phthiraptera (parasitic lice) microscope slide collection (70,663 slides). Here we describe a novel process of semi-automated mass digitisation using both temporary and permanent barcode labels applied before and during slide imaging. By using a series of barcodes encoding information associated with each slide (i.e. unique identifier, location in the collection and taxonomic name), we can run a series of automated processes, including file renaming, image processing and bulk import into the NHM's collection management system. We provide data on the comparative efficiency of these processes, illustrating how simple activities, like automated file renaming, reduces image post-processing time, minimises human error and can be applied across multiple collection types.

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.

Genetic analysis of lice supports direct contact between modern and archaic humans.

Parasites can be used as unique markers to investigate host evolutionary history, independent of host data. Here we show that modern human head lice, Pediculus humanus, are composed of two ancient lineages, whose origin predates modern Homo sapiens by an order of magnitude (ca. 1.18 million years). One of the two louse lineages has a worldwide distribution and appears to have undergone a population bottleneck ca. 100,000 years ago along with its modern H. sapiens host. Phylogenetic and population genetic data suggest that the other lineage, found only in the New World, has remained isolated from the worldwide lineage for the last 1.18 million years. The ancient divergence between these two lice is contemporaneous with splits among early species of Homo, and cospeciation analyses suggest that the two louse lineages codiverged with a now extinct species of Homo and the lineage leading to modern H. sapiens. If these lice indeed codiverged with their hosts ca. 1.18 million years ago, then a recent host switch from an archaic species of Homo to modern H. sapiens is required to explain the occurrence of both lineages on modern H. sapiens. Such a host switch would require direct physical contact between modern and archaic forms of Homo.

Actionable, long-term stable and semantic web compatible identifiers for access to biological collection objects.

With biodiversity research activities being increasingly shifted to the web, the need for a system of persistent and stable identifiers for physical collection objects becomes increasingly pressing. The Consortium of European Taxonomic Facilities agreed on a common system of HTTP-URI-based stable identifiers which is now rolled out to its member organizations. The system follows Linked Open Data principles and implements redirection mechanisms to human-readable and machine-readable representations of specimens facilitating seamless integration into the growing semantic web. The implementation of stable identifiers across collection organizations is supported with open source provider software scripts, best practices documentations and recommendations for RDF metadata elements facilitating harmonized access to collection information in web portals. Database URL: : http://cetaf.org/cetaf-stable-identifiers.

Wild turkey (Meleagris gallopavo) as a host of ixodid ticks, lice, and Lyme disease spirochetes (Borrelia burgdorferi sensu lato) in California state parks.

Rio Grande wild turkeys (Meleagris gallopavo intermedia) were evaluated as potential hosts of ixodid ticks, lice, and Lyme disease spirochetes (Borrelia burgdorferi sensu lato [s.l.]) in three state parks in Sonoma County, California, USA, during 2003 and 2004. In total, 113 birds were collected, 50 (44.2%) of which were found to be infested by 361 ixodid ticks representing three species: the western black-legged tick (Ixodes pacificus, n=248), the rabbit tick (Haemaphysalis leporispalustris, n=112), and one American dog tick (Dermacentor variabilis). Year-round the prevalence of all ticks combined was unrelated to the age or sex of turkeys, and the prevalence of infestation by I. pacificus (35.4%) was significantly higher than it was for either H. leporispalustris (14.2%) or D. variabilis (0.9%). The proportion of the two prevalent tick species differed significantly by life stage with 86.3% of the I. pacificus and 82.1% of the H. leporispalustris enumerated being nymphs and larvae, respectively. Three species of lice were collected, including the chicken body louse Menacanthus stramineus (12.5% of total), Chelopistes meleagridis (37.5% of total), and Oxylipeurus polytrapezius (50% of total). The records for all three ticks are the first ever from wild turkeys, and those for the lice are the first from this host in the far-western United States. Wild turkeys potentially were exposed to the feeding activities of I. pacificus nymphs infected with B. burgdorferi s.l. as 15% of host-seeking nymphs (n=200) collected in woodlands used by turkeys as roosting or foraging areas were infected mainly with B. burgdorferi sensu stricto (s.s.). However, only one (1%) of 90 turkey blood specimens tested by PCR contained B. burgdorferi s.s., and four in vitro, complement-protein assays demonstrated that domestic turkey serum is moderately bacteriolytic for this spirochete. Taken together, these findings indicate that wild turkeys are important avian hosts of I. pacificus nymphs, but they appear to be inconsequential hosts of B. burgdorferi s.l.

BioAcoustica: a free and open repository and analysis platform for bioacoustics.

We describe an online open repository and analysis platform, BioAcoustica (http://bio.acousti.ca), for recordings of wildlife sounds. Recordings can be annotated using a crowdsourced approach, allowing voice introductions and sections with extraneous noise to be removed from analyses. This system is based on the Scratchpads virtual research environment, the BioVeL portal and the Taverna workflow management tool, which allows for analysis of recordings using a grid computing service. At present the analyses include spectrograms, oscillograms and dominant frequency analysis. Further analyses can be integrated to meet the needs of specific researchers or projects. Researchers can upload and annotate their recordings to supplement traditional publication.

Inselect: Automating the Digitization of Natural History Collections.

The world's natural history collections constitute an enormous evidence base for scientific research on the natural world. To facilitate these studies and improve access to collections, many organisations are embarking on major programmes of digitization. This requires automated approaches to mass-digitization that support rapid imaging of specimens and associated data capture, in order to process the tens of millions of specimens common to most natural history collections. In this paper we present Inselect-a modular, easy-to-use, cross-platform suite of open-source software tools that supports the semi-automated processing of specimen images generated by natural history digitization programmes. The software is made up of a Windows, Mac OS X, and Linux desktop application, together with command-line tools that are designed for unattended operation on batches of images. Blending image visualisation algorithms that automatically recognise specimens together with workflows to support post-processing tasks such as barcode reading, label transcription and metadata capture, Inselect fills a critical gap to increase the rate of specimen digitization.

Scratching an ancient itch: an Eocene bird louse fossil.

Out of the 30 extant orders of insects, all but one, the parasitic lice (Insecta: Phthiraptera), have a confirmed fossil record. Here, we report the discovery of what appears to be the first bird louse fossil: an exceptionally well-preserved specimen collected from the crater of the Eckfeld maar near Manderscheid, Germany. The 44-million-year-old specimen shows close phylogenetic affinities with modern feather louse ectoparasites of aquatic birds. Preservation of feather remnants in the specimen's foregut confirms its association as a bird ectoparasite. Based on a phylogenetic analysis of the specimen and palaeoecological data, we suggest that this louse was the parasite of a large ancestor to modern Anseriformes (swans, geese and ducks) or Charadriiformes (shorebirds). The crown group position of this fossil in the phylogeny of lice confirms the group's long coevolutionary history with birds and points to an early origin for lice, perhaps inherited from early-feathered theropod dinosaurs.

Multiple origins of parasitism in lice.

A major fraction of the diversity of insects is parasitic, as herbivores, parasitoids or vertebrate ectopara sites. Understanding this diversity requires information on the origin of parasitism in various insect groups. Parasitic lice (Phthiraptera) are the only major group of insects in which all members are permanent parasites of birds or mammals. Lice are classified into a single order but are thought to be closely related to, or derived from, book lice and bark lice (Psocoptera). Here, we use sequences of the nuclear 18S rDNA gene to investigate the relationships among Phthiraptera and Psocoptera and to identify the origins of parasitism in this group (termed Psocodea). Maximum-likelihood (ML), Bayesian ML and parsimony analyses of these data indicate that lice are embedded within the psocopteran infraorder Nanopsocetae, making the order Psocoptera paraphyletic (i.e. does not contain all descendants of a single common ancestor). Furthermore, one family of Psocoptera, Liposcelididae, is identified as the sister taxon to the louse suborder Amblycera, making parasitic lice (Phthiraptera) a polyphyletic order (i.e. descended from two separate ancestors). We infer from these results that parasitism of vertebrates arose twice independently within Psocodea, once in the common ancestor of Amblycera and once in the common ancestor of all other parasitic lice.

Linking multiple biodiversity informatics platforms with Darwin Core Archives.

We describe an implementation of the Darwin Core Archive (DwC-A) standard that allows for the exchange of biodiversity information contained within the Scratchpads virtual research environment with external collaborators. Using this single archive file Scratchpad users can expose taxonomies, specimen records, species descriptions and a range of other data to a variety of third-party aggregators and tools (currently Encyclopedia of Life, eMonocot Portal, CartoDB, and the Common Data Model) for secondary use. This paper describes our technical approach to dynamically building and validating Darwin Core Archives for the 600+ Scratchpad user communities, which can be used to serve the diverse data needs of all of our content partners.