MicroCT illuminates the unique morphology of Shiinoidae (Copepoda: Cyclopoida), an unusual group of fish parasites.

The copepod family Shiinoidae Cressey, 1975 currently comprises nine species of teleost parasites with unusual morphology and a unique attachment mechanism. Female shiinoids possess greatly enlarged antennae that oppose a rostrum, an elongate outgrowth of cuticle that originates between the antennules. The antennae form a moveable clasp against the rostrum which they use to attach to their host. In this study, we use micro-computed tomography (microCT) to examine specimens of Shiinoa inauris Cressey, 1975 in situ attached to host tissue in order to characterize the functional morphology and specific muscles involved in this novel mode of attachment and to resolve uncertainty regarding the segmental composition of the regions of the body. We review the host and locality data for all reports of shiinoids, revise the generic diagnoses for both constituent genera Shiinoa Kabata, 1968 and Parashiinoa West, 1986, transfer Shiinoa rostrata Balaraman, Prabha & Pillai, 1984 to Parashiinoa as Parashiinoa rostrata (Balaraman, Prabha & Pillai, 1984) n. comb., and present keys to the females and males of both genera.

Resurrection and redescription of Clepsinepallida Verrill, 1872 (Hirudinida, Glossiphoniidae) with a phylogeny of the genus Alboglossiphonia.

Alboglossiphoniapallida (Verrill, 1872) comb. nov. is resurrected and redescribed based on morphological and molecular data from specimens of the type locality (New Haven County, Connecticut, USA) that demonstrate it is distinct from North American Alboglossiphoniaheteroclita, European Alboglossiphoniaheteroclita, and Alboglossiphoniapapillosa. Alboglossiphoniapallida is characterized by having dark chromatophores on the dorsal surface arranged lateral to patrilaterally and medially as a thin line or interrupted thin line along with three pairs of eye spots (with the first pair closest together), six pairs of crop ceca, and a united gonopore. Additional sampling of specimens of the genus Alboglossiphonia is needed to understand its phylogeny especially as many species have not been collected since their description.

What would it take to describe the global diversity of parasites?

How many parasites are there on Earth? Here, we use helminth parasites to highlight how little is known about parasite diversity, and how insufficient our current approach will be to describe the full scope of life on Earth. Using the largest database of host-parasite associations and one of the world's largest parasite collections, we estimate a global total of roughly 100 000-350 000 species of helminth endoparasites of vertebrates, of which 85-95% are unknown to science. The parasites of amphibians and reptiles remain the most poorly described, but the majority of undescribed species are probably parasites of birds and bony fish. Missing species are disproportionately likely to be smaller parasites of smaller hosts in undersampled countries. At current rates, it would take centuries to comprehensively sample, collect and name vertebrate helminths. While some have suggested that macroecology can work around existing data limitations, we argue that patterns described from a small, biased sample of diversity aren't necessarily reliable, especially as host-parasite networks are increasingly altered by global change. In the spirit of moonshots like the Human Genome Project and the Global Virome Project, we consider the idea of a Global Parasite Project: a global effort to transform parasitology and inventory parasite diversity at an unprecedented pace.

Leeches in the extreme: Morphological, physiological, and behavioral adaptations to inhospitable habitats.

With more than 700 described species, leeches include morphological, physiological, and behavioral diversity and occur in terrestrial and aquatic habitats, including freshwater, estuarine, and marine ecosystems. Leeches inhabit a number of extreme environments, including extremes in temperature, moisture, salinity, pressure, light, and pollution. In some cases, leeches in extreme environments have specialized morphological, physiological, or behavioral adaptations to survive these conditions, yet unique adaptations are not apparent in some species. Leeches that inhabit inhospitable habitats occur in more than one branch or family of leech phylogeny suggesting that there have been independent invasions of environments with extreme conditions. Herein, we review examples of leeches that live in extreme conditions and the exceptional biology that has contributed to leeches being the most extreme annelids.

Phylogenetic Position and Description of a New Species of Medicinal Leech from the Eastern United States.

A new species of medicinal leech, Macrobdella mimicus n. sp., is described from specimens collected in Maryland; this is the first description of a North American macrobdellid since 1975. Superficially, the new species resembles the well-known Macrobdella decora, as both species possess 4 accessory pores arranged symmetrically on the ventral surface, yet the new species is distinguished from M. decora in possessing 4-4½ annuli (rather than 3½) between the gonopores and 4 annuli (rather than 5 annuli) between the female gonopore and the first pair of accessory pores. Phylogenetic analyses, based on 2 mitochondrial and 2 nuclear loci for a set of closely related taxa, confirms the placement of the new species within the family Macrobdellidae and places it as the sister taxon to M. decora and M. diplotertia.

Phylogenomic Analysis of a Putative Missing Link Sparks Reinterpretation of Leech Evolution.

Leeches (Hirudinida) comprise a charismatic, yet often maligned group of organisms. Despite their ecological, economic, and medical importance, a general consensus on the phylogenetic relationships of major hirudinidan lineages is lacking. This absence of a consistent, robust phylogeny of early-diverging lineages has hindered our understanding of the underlying processes that enabled evolutionary diversification of this clade. Here, we used an anchored hybrid enrichment-based phylogenomic approach, capturing hundreds of loci to investigate phylogenetic relationships among major hirudinidan lineages and their closest living relatives. Our results suggest that a dramatic reinterpretation of early leech evolution is warranted. We recovered Branchiobdellida as sister to a clade that includes all major lineages of hirudinidans, but found Acanthobdella to be nested within Oceanobdelliformes. These results cast doubt on the utility of Acanthobdella as a "missing link" used to explain the origin of blood-feeding in hirudineans. Further, our results support a deep divergence between predominantly marine and freshwater lineages, while not supporting the reciprocal monophyly of jawed and proboscis-bearing leeches. To sum up, our phylogenomic resolution of early-diverging leeches provides a necessary foundation for illuminating the evolution of host-symbiont associations and key adaptations that have allowed leeches to colonize a wide diversity of habitats worldwide.

Parasite Collections: Overlooked Resources for Integrative Research and Conservation.

Parasite natural history collections form vital scientific infrastructure that play a substantial role in increasing awareness of the importance of parasites to ecosystems, conservation assessments, science, and society. These collections support novel investigations that integrate across taxa, time, and space, and should be cultivated to advance organismal-based science. Promoting and supporting parasite collections will ensure their ongoing stability and accessibility.

Parasite biodiversity faces extinction and redistribution in a changing climate.

Climate change is a well-documented driver of both wildlife extinction and disease emergence, but the negative impacts of climate change on parasite diversity are undocumented. We compiled the most comprehensive spatially explicit data set available for parasites, projected range shifts in a changing climate, and estimated extinction rates for eight major parasite clades. On the basis of 53,133 occurrences capturing the geographic ranges of 457 parasite species, conservative model projections suggest that 5 to 10% of these species are committed to extinction by 2070 from climate-driven habitat loss alone. We find no evidence that parasites with zoonotic potential have a significantly higher potential to gain range in a changing climate, but we do find that ectoparasites (especially ticks) fare disproportionately worse than endoparasites. Accounting for host-driven coextinctions, models predict that up to 30% of parasitic worms are committed to extinction, driven by a combination of direct and indirect pressures. Despite high local extinction rates, parasite richness could still increase by an order of magnitude in some places, because species successfully tracking climate change invade temperate ecosystems and replace native species with unpredictable ecological consequences.

Parasite Microbiome Project: Systematic Investigation of Microbiome Dynamics within and across Parasite-Host Interactions.

Understanding how microbiomes affect host resistance, parasite virulence, and parasite-associated diseases requires a collaborative effort between parasitologists, microbial ecologists, virologists, and immunologists. We hereby propose the Parasite Microbiome Project to bring together researchers with complementary expertise and to study the role of microbes in host-parasite interactions. Data from the Parasite Microbiome Project will help identify the mechanisms driving microbiome variation in parasites and infected hosts and how that variation is associated with the ecology and evolution of parasites and their disease outcomes. This is a call to arms to prevent fragmented research endeavors, encourage best practices in experimental approaches, and allow reliable comparative analyses across model systems. It is also an invitation to foundations and national funding agencies to propel the field of parasitology into the microbiome/metagenomic era.

Parasite vulnerability to climate change: an evidence-based functional trait approach.

Despite the number of virulent pathogens that are projected to benefit from global change and to spread in the next century, we suggest that a combination of coextinction risk and climate sensitivity could make parasites at least as extinction prone as any other trophic group. However, the existing interdisciplinary toolbox for identifying species threatened by climate change is inadequate or inappropriate when considering parasites as conservation targets. A functional trait approach can be used to connect parasites' ecological role to their risk of disappearance, but this is complicated by the taxonomic and functional diversity of many parasite clades. Here, we propose biological traits that may render parasite species particularly vulnerable to extinction (including high host specificity, complex life cycles and narrow climatic tolerance), and identify critical gaps in our knowledge of parasite biology and ecology. By doing so, we provide criteria to identify vulnerable parasite species and triage parasite conservation efforts.

Prevalence, Abundance, and Intensity of Implanted Spermatophores in the Leech Haementeria officinalis (Glossiphoniidae: Hirudinida) from Guanajuato, Mexico.

Fertilization through hypodermic implantation of spermatophores has been recorded in at least 4 groups of leeches: Glossiphoniidae, Piscicolidae, Ozobranchidae, and Erpobdelliformes. In Piscicola respirans (Piscicolidae), vector tissue responsible for sperm transfer from a specialized region of the body to the ovaries has led to the non-random attachment of spermatophores on the body surface of the recipient leech. It has been suggested that in glossiphoniid leeches, spermatophores are implanted in any part of the body surface of the recipient leech without a clear pattern or preference for region. In order to determine if the donor leech implants its spermatophores in a specific area of the conspecific recipient's body, we surveyed 81 specimens of Haementeria officinalis (Clitellata: Glossiphoniidae) from a wild population in Guanajuato, Mexico, and recorded the distribution of the spermatophores over the recipient's body surface. We describe for the first time a spermatophore of H. officinalis using scanning electron and light microscopy. Spermatophores were found attached dorsally between somites XVII and XXI 59.57% of the time, and the rest were found in other parts of the body, including on the ventral surface. The non-specific attachment for spermatophores does not support the presence of specialized tissue responsible for sperm transfer and instead attributes the placement of implantation to mechanical characteristics of the copulation process.

Austrobdella cairae n. sp., an Oioxenous Marine Leech (Clitellata: Piscicolidae) from the Banded Guitarfish, Zapteryx exasperata, in the Northeastern Pacific Ocean.

A new marine leech is herein described from specimens infecting the external surfaces, including the mouth and cloaca, of the banded guitarfish, Zapteryx exasperate, captured in the Gulf of California and eastern Pacific Ocean off the coast of San Diego, California. The leech is assigned to Austrobdella by possessing continuous contractile coelomic channels that lie outside the somatic musculature along the lateral edges of the urosome (marginal lacunae), clitellar gland cells densely packed in the urosome, 5 pairs of testisacs, and 6-annulate mid-body somites. The new leech is distinguished from its 6 congeners on the basis of body size (maximum 10 mm long) and shape (sub-cylindrical trachelosome distinctly demarcated from wider urosome that is ventrally flattened, convex dorsally, and narrowing toward caudal sucker that is narrow, 20-25% of maximum body width), number of eyespots (2 pairs), shape and arrangement of the ovisacs (pyriform and limited to somites XII/XIII), and characteristics of the midgut (1 pair of mycetomes, 6 pairs of simple thin-walled crop ceca, ventral postceca wanting, and 2 pairs of dendritic diverticula emerging from anterior portion of thick-walled intestine). The new species occurs in the northeastern Pacific Ocean on a benthic elasmobranch. Examination of host specificity for each Austrobdella species using the quantitative Index of Phylogenetic Host Specificity revealed that the new species is 1 of 4 oioxenous specialists in the genus, and the remaining 3 congeners are relative generalists herein classified as euryxenous. This is the first time host specificity for members of the Piscicolidae has been quantitatively assessed. The analysis suggests that associations between marine leeches belonging in Austrobdella and their vertebrate hosts are driven by ecological influences rather than host taxonomic placement.

Description of a new leech species of Helobdella (Clitellata: Glossiphoniidae) from Mexico with a review of Mexican congeners and a taxonomic key.

To date, six species of the leech genus Helobdella have been recorded from Mexico: Helobdella atli, Helobdella elongata, Helobdella octatestisaca, Helobdella socimulcensis, Helobdella virginiae and Helobdella temiscoensis n. sp. This new species is characterized by a lanceolate body, the presence of a nuchal scute, uniform brown pigment on both dorsal and ventral surfaces, the absence of papillae, well-separated eyespots, six pairs of testisacs and five pairs of crop caeca, the last of which forms posterior caeca. In addition, we provide new geographic records for Helobdella species from Mexico resulting from our own collections, vouchers deposited at the Colección Nacional de Helmintos from the Instituto de Biología, UNAM, Mexico and vouchers at the Invertebrate Zoology Collection of the Smithsonian's National Museum of Natural History (USNM) Washington D.C., USA. We present a comprehensive review of Mexican Helobdella species, including the new species, with notes on the characteristic morphology and geographic distribution of each species with 91 new records from 20 states. In addition, we provide a taxonomic key for the identification of the Mexican species.

Two new and two redescribed species of Anonchotaenia (Cestoda: Paruterinidae) from South American birds.

Morphological examination of novel specimens of paruterinid cestodes from passerine birds from Brazil and Chile and of museum specimens from Paraguay revealed two new species: Anonchotaenia prolixa sp. n. from Elaenia albiceps chilensis Hellmayr from Chile, and Anonchotaenia vaslata sp. n. from Tyrannus melancholicus (Vieillot) (type host) and Myiodynastes maculatus (Statius Muller) from Paraguay. The generic diagnosis of Anonchotaenia Conn, 1900 is amended, prompted by the presence of the armed cirrus and the elongated cirrus sac of A. prolixa. Two species were redescribed: Anonchotaenia brasiliensis Fuhrmann, 1908 from Tachyphonus coronatus (Vieillot) and Thraupis cyanoptera (Vieillot) (new host records) from Brazil, and Thraupis sayaca (Linnaeus) and Volatinia jacarina (Linnaeus) from Paraguay (new host and geographic records); and Anonchotaenia macrocephala Fuhrmann, 1908 from Tachycineta leucorrhoa (Vieillot) (new host record) from Brazil, Tachycineta meyeni (Cabanis) from Chile (new host and geographic record) and Stelgidopteryx ruficollis (Vieillot) from Paraguay (new host and geographic record). Scanning electron microscopy of A. brasiliensis and A. macrocephala revealed less microthrix variation than has been reported for other cyclophyllidean taxa. Sequence data were generated for nuclear ssr- and lsr-DNA and mitochondrial rrnL and cox1 for A. prolixa, A. brasiliensis, and A. macrocephala. Maximum likelihood and Bayesian inference analyses supported each species as distinct, but revealed cryptic diversity among A. brasiliensis specimens from different host families. New host records of A. brasiliensis and A. macrocephala prompted a formal assessment of host specificity. Anonchotaenia prolixa was found to be oioxenous (HS(S) = 0), A. vaslata and A. macrocephala were found to be metastenoxenous (HS(S) = 3.000 and 3.302, respectively), whereas A. brasiliensis was found to be euryxenous (HS(S) = 5.876). Anonchotaenia brasiliensis has been found parasitising several species of different passerine families that participate in mixed-species foraging flocks in the Atlantic Forest. A diversity of species of other families join these flocks and are among the substantial number of South American passerine species yet to be examined for cestodes.

Cucolepis cincta gen.n. et sp.n. (Cestoda: Cyclophyllidea) from the squirrel cuckoo Piaya cayana lesson (Aves: Cuculiformes) from Paraguay.

Cucolepis gen. n. is erected as monotypic for Cucolepis cincta sp. n., a new species of cyclophyllidean cestode of the family Paruterinidae. The new species is described from the squirrel cuckoo, Piaya cayana Lesson (Aves: Cuculiformes), taken from two localities in Paraguay in 1984 and 1985. This new genus is most similar to the genus Triaenorhina Spasskii et Shumilo, 1965 in terms of the hook morphology and large epiphyseal structures extending from both the handle and guard, but differs in several aspects of the strobilar morphology, such as the shape of the cirrus sac, genital atrium, uterus and paruterine organ. The strobilar morphology of the new genus strongly resembles that of the genus Francobona Georgiev et Kornyushin, 1994, especially the shape of the cirrus sac and genital atrium, yet Francobona spp. lack, the developed epiphyseal structures observed in species of Cucolepis and Triaenorhina. Previous records and the nature of parasite-host associations between cuculiform birds and their cestode parasites are discussed.

Bacterial symbiont and salivary peptide evolution in the context of leech phylogeny.

The evolutionary history of leeches is employed as a general framework for understanding more than merely the systematics of this charismatic group of annelid worms, and serves as a basis for understanding blood-feeding related correlates ranging from the specifics of gut-associated bacterial symbionts to salivary anticoagulant peptides. A variety of medicinal leech families were examined for intraluminal crop bacterial symbionts. Species of Aeromonas and Bacteroidetes were characterized with DNA gyrase B and 16S rDNA. Bacteroidetes isolates were found to be much more phylogenetically diverse and suggested stronger evidence of phylogenetic correlation than the gammaproteobacteria. Patterns that look like co-speciation with limited taxon sampling do not in the full context of phylogeny. Bioactive compounds that are expressed as gene products, like those in leech salivary glands, have 'passed the test' of evolutionary selection. We produced and bioinformatically mined salivary gland EST libraries across medicinal leech lineages to experimentally and statistically evaluate whether evolutionary selection on peptides can identify structure-function activities of known therapeutically relevant bioactive compounds like antithrombin, hirudin and antistasin. The combined information content of a well corroborated leech phylogeny and broad taxonomic coverage of expressed proteins leads to a rich understanding of evolution and function in leech history.