Evolution of parasites in the Anthropocene: new pressures, new adaptive directions.

The Anthropocene is seeing the human footprint rapidly spreading to all of Earth's ecosystems. The fast-changing biotic and abiotic conditions experienced by all organisms are exerting new and strong selective pressures, and there is a growing list of examples of human-induced evolution in response to anthropogenic impacts. No organism is exempt from these novel selective pressures. Here, we synthesise current knowledge on human-induced evolution in eukaryotic parasites of animals, and present a multidisciplinary framework for its study and monitoring. Parasites generally have short generation times and huge fecundity, features that predispose them for rapid evolution. We begin by reviewing evidence that parasites often have substantial standing genetic variation, and examples of their rapid evolution both under conditions of livestock production and in serial passage experiments. We then present a two-step conceptual overview of the causal chain linking anthropogenic impacts to parasite evolution. First, we review the major anthropogenic factors impacting parasites, and identify the selective pressures they exert on parasites through increased mortality of either infective stages or adult parasites, or through changes in host density, quality or immunity. Second, we discuss what new phenotypic traits are likely to be favoured by the new selective pressures resulting from altered parasite mortality or host changes; we focus mostly on parasite virulence and basic life-history traits, as these most directly influence the transmission success of parasites and the pathology they induce. To illustrate the kinds of evolutionary changes in parasites anticipated in the Anthropocene, we present a few scenarios, either already documented or hypothetical but plausible, involving parasite taxa in livestock, aquaculture and natural systems. Finally, we offer several approaches for investigations and real-time monitoring of rapid, human-induced evolution in parasites, ranging from controlled experiments to the use of state-of-the-art genomic tools. The implications of fast-evolving parasites in the Anthropocene for disease emergence and the dynamics of infections in domestic animals and wildlife are concerning. Broader recognition that it is not only the conditions for parasite transmission that are changing, but the parasites themselves, is needed to meet better the challenges ahead.

New insights into avian malaria infections in New Zealand seabirds.

The past few years have been marked by a drastic increase in pathogen spillover events. However, the extent and taxonomic range at which these events take place remain as crucial unanswered questions in many host-pathogen systems. Here, we take advantage of opportunistically sampled bird carcasses from the South Island of New Zealand, with the aim of identifying Plasmodium spp. infections in native and endemic New Zealand seabird species. In total, six samples from five bird species were positive for avian malaria, including four of which were successfully sequenced and identified as Plasmodium matutinum LINN1 lineage. These results provide new Plasmodium infection records in seabirds, including the first documented case in Procellariiformes in New Zealand, highlighting the potential disease risk to these species.

Description and molecular data of a new cestode parasite, Cladotaenia anomala n. sp. (Paruterinidae) from the Australasian harrier (Circus approximans Peale) in New Zealand.

Currently comprising 12 species infecting the gastrointestinal tracts of diurnal raptors (Falconiformes, Accipitriformes), species of Cladotaenia are diagnosed by their branching uterus, testes in two fields reaching the same level anteriorly, and small rostellum armed with taenioid hooks arranged in two rows. In this study we describe a new species of Cladotaenia recovered from a number of Australasian harriers Circus approximans, from the southern half of South Island, New Zealand. The new species is distinguished from other species by its single circle of hooks. It is closest, morphologically, to C. circi, but differs in the shape of the terminal proglottids and the number of uterine branches. Sequences of 28S and cox1 gene are presented. Genetically, Cladotaenia anomala n. sp. is closest to Cladotaenia globifera but differs morphologically in the size of the suckers, testes and eggs. This description constitutes the first record of a Cladotaenia species in New Zealand. We discuss some potential routes this parasite may have taken to arrive in New Zealand.

Gastrointestinal helminths of the Australasian harrier (Circus approximans Peale, 1848) in New Zealand, and description of a new species of nematode, Procyrnea fraseri n. sp. (Habronematidae).

The Australasian harrier Circus approximans, a native of Australia, New Zealand and the South Pacific, is an opportunistic hunter of small prey, although a large part of its diet consists of carrion, mainly from roadkill. Besides a record of a single, unnamed species of capillariid nematode there have been no investigations into the parasites of Australasian harriers in New Zealand. In this study, a helminthological survey of sixty-five deceased harriers from southern New Zealand uncovered a gastrointestinal helminth fauna consisting of six parasite species. Porrocaecum circinum (Nematoda) was previously described only from fragmented females, and a redescription is presented here. Procyrnea fraseri n. sp. (Nematoda) is described, and distinguished from its congeners by its slender body shape and shorter spicules. Strigea falconis (Trematoda) is reported for the first time in New Zealand. Cladotaenia anomalis (Cestoda) and Polymorphus circi (Acanthocephala) were previously described as new species elsewhere. An unnamed species of capillariid appears to be mainly confined to North Island and is rare in South Island. Prevalence and intensity metrics are given, and DNA sequences provided to accompany new re/descriptions. Potential intermediate hosts are discussed, and the origins of the helminths and their potential for pathogenicity are considered.

Description and molecular data for a new acanthocephalan parasite, Polymorphus circi n. sp. (Polymorphidae) from the Australasian harrier (Circus approximans Peale) in New Zealand.

Species of genus Polymorphus Lühe, 1911 (Polymorphidae) are acanthocephalans found in fish-eating birds and waterfowl. Although found in many parts of the world, including Australia, no records exist from New Zealand. Because of the largely aquatic intermediate host, Polymorphus species are rarely found in terrestrial birds of prey. During a study of the helminths of the Australasian harrier Circus approximans Peale specimens of Polymorphus were recovered that were found to be new to science. Polymorphus circi n. sp. is formally described and genetic sequence data presented. Specimens were distinguished from all other species by a combination of characters, including their proboscis hook arrangement (20-22 rows of 11-13 hooks), as well as absence of sexual dimorphism, trunk size, proboscis shape and egg size. These acanthocephalans were found in birds from areas with the potential to support freshwater, brackish or marine amphipods, but as yet the actual intermediate hosts are unknown.

Biases in parasite biodiversity research: why some helminth species attract more research than others.

As the number of known and described parasite species grows every year, one might ask: how much do we actually know about these species beyond the fact they exist? For free-living taxa, research effort is biased toward a small subset of species based on their properties or human-centric factors. Here, using a large data set on over 2500 helminth parasite species described in the past two decades, we test the importance of several predictors on two measures of research effort: the number of times a species description is cited following its publication, and the number of times a species' name is mentioned in the scientific literature. Our analysis highlights some taxonomic biases: for instance, descriptions of acanthocephalans and nematodes tend to receive more citations than those of other helminths, and species of cestodes are less frequently mentioned in the literature than other helminths. We also found that helminths infecting host species of conservation concern receive less research attention, perhaps because of the constraints associated with research on threatened animals, while those infecting host species of human use receive greater research effort. Intriguingly, we found that species originally described by many co-authors subsequently attract more research effort than those described by one or few authors, and that research effort correlates negatively with the human population size of the country where a species was discovered, but not with its economic strength, measured by its gross domestic product. Overall, our findings reveal that we have conducted very little research, or none at all, on the majority of helminth parasite species following their discovery. The biases in study effort we identify have serious implications for future research into parasite biodiversity and conservation.

Physical evidence of direct antagonistic interactions between trematodes in the host gut: the kiss of death?

Although within-host competition among parasites if often assumed to occur based on statistical patterns, actual physical evidence of direct antagonistic interactions between parasites, either intraspecific or interspecific, is very rare. Here, we report such evidence between and within two species of hemiurid trematodes infecting the deep-sea grenadier fish Coryphaenoides subserrulatus. We found pairs of worms attached together, with one worm using its ventral sucker against another worm, and sucking out a large protuberance on the victim. We also found single worms showing clear signs of past attacks. There was no evidence that these interactions were more common at high intensities of infection, where the conditions would be expected to be more conducive to competitive interactions. Our findings provide evidence that trematodes may cause some harm to co-occurring individuals, suggesting a direct form of interference competition among intestinal helminths.

Battle of the sexes: analysis of sex bias in host use and reporting practices in parasitological experiments.

Experimental approaches are among the most powerful tools available to biologists, yet in many disciplines their results have been questioned due to an underrepresentation of female animal subjects. In parasitology, experiments are crucial to understand host-parasite interactions, parasite development, host immune responses, as well as the efficacy of different control methods. However, distinguishing between species-wide and sex-specific effects requires the balanced inclusion of both male and female hosts in experiments and the reporting of results for each sex separately. Here, using data from over 3600 parasitological experiments on helminth-mammal interactions published in the past four decades, we investigate patterns of male versus female subject use and result reporting practices in experimental parasitology. We uncover multiple effects of the parasite taxon used, the type of host used (rats and mice for which subject selection is fully under researcher control versus farm animals), the research subject area and the year of publication, on whether host sex is even specified, whether one or both host sexes have been used (and if only one then which one), and whether the results are presented separately for each host sex. We discuss possible reasons for biases and unjustifiable selection of host subjects, and for poor experimental design and reporting of results. Finally, we make some simple recommendations for increased rigour in experimental design and to reset experimental approaches as a cornerstone of parasitological research.

Tracking life cycles of parasites across a broad taxonomic scale in a marine ecosystem.

Parasitic helminths exhibit remarkable diversity in their life cycles, although few parasite species have their whole life cycles resolved. Owing to the fact that parasite life stages within hosts are often not comparable using morphological data, genetic data provides convincing evidence of transmission pathways between intermediate and definitive hosts. We took this approach to an ecosystem level, genetically matching parasite (acanthocephalan, cestode, nematode and trematode) life stages across a broad taxonomic range of intermediate and definitive hosts (invertebrates, seabirds, elasmobranchs and teleost fish) in Otago's (New Zealand) coastal marine ecosystem. We identified which transmission routes are utilized by the most parasite species and assessed which intermediate hosts are most important in facilitating the transmission of parasites in this ecosystem. Our findings reveal 59 new records of larval parasites infecting their respective intermediate hosts and 289 transmission pathways utilized by 35 helminth species to complete their life cycles. Sprat, triplefin and arrow squid all hosted the highest number of larval parasite species, suggesting they play important roles as intermediate hosts. We then used the new life cycle data to provide a synthetic overview of the life cycles known for various parasite groups in New Zealand. This study highlights how studying parasite life cycles can enhance our understanding of the ecology and evolution of parasites and hosts in natural systems, beyond simply resolving life cycles.

Assigning cause for emerging diseases of aquatic organisms.

Resolving the cause of disease (= aetiology) in aquatic organisms is a challenging but essential goal, heightened by increasing disease prevalence in a changing climate and an interconnected world of anthropogenic pathogen spread. Emerging diseases play important roles in evolutionary ecology, wildlife conservation, the seafood industry, recreation, cultural practices, and human health. As we emerge from a global pandemic of zoonotic origin, we must focus on timely diagnosis to confirm aetiology and enable response to diseases in aquatic ecosystems. Those systems' resilience, and our own sustainable use of seafood, depend on it. Synchronising traditional and recent advances in microbiology that span ecological, veterinary, and medical fields will enable definitive assignment of risk factors and causal agents for better biosecurity management and healthier aquatic ecosystems.

Large-scale genetic investigation of nematode diversity and their phylogenetic patterns in New Zealand's marine animals.

Nematodes constitute one of the most speciose metazoan groups on earth, and a significant proportion of them have parasitic life styles. Zooparasitic nematodes have zoonotic, commercial and ecological significance within natural systems. Due to their generally small size and hidden nature within their hosts, and the fact that species discrimination using traditional morphological characteristics is often challenging, their biodiversity is not well known, especially within marine ecosystems. For instance, the majority of New Zealand's marine animals have never been the subject of nematode studies, and many currently known nematodes in New Zealand await confirmation of their species identity with modern taxonomic techniques. In this study, we present the results of an extensive biodiversity survey and phylogenetic analyses of parasitic nematodes infecting New Zealand's marine animals. We used genetic data to differentiate nematodes to the lowest taxonomic level possible and present phylogenies of the dominant clades to illustrate their genetic diversity in New Zealand. Our findings reveal a high diversity of parasitic nematodes (23 taxa) infecting New Zealand's marine animals (62 of 94 free-living animal species investigated). The novel data collected here provide a solid baseline for future assessments of change in diversity and distribution of parasitic nematodes.

Male-biased selection of holotypes in parasite taxonomy: is it justified?

When a new parasite species is identified, a name-bearing specimen or holotype is designated as its reference standard. For most acanthocephalans and nematodes, the holotype is male, a bias which lacks scientific justification. We propose ways of redressing this imbalance and achieving fuller representation of each species in museum collections.

Decay of parasite community similarity with host phylogenetic and geographic distances among deep-sea fish (grenadiers).

Although parasite community studies are growing in numbers, our understanding of which macro-ecological and evolutionary processes have shaped parasite communities is still based on a narrow range of host­parasite systems. The present study assessed the diversity and endoparasite species composition in New Zealand deep-sea fish (grenadiers, family Macrouridae), and tested the effects of host phylogeny and geography on the structure of endoparasite communities using a distance decay framework. We found that grenadiers from the Chatham Rise harboured a surprisingly high diversity of digeneans, cestodes and nematodes, with different species of grenadiers having different parasite assemblages. Our results demonstrate that community similarity based on the presence/absence of parasites was only affected by the phylogenetic relatedness among grenadier species. In contrast, both phylogenetic distance among grenadiers (measured as the number of base-pair differences of DNA sequences) and geographic distance between sample locations influenced the similarity of parasite communities based on the parasites' prevalence and mean abundance. Our key findings highlight the significant effect of deep-sea host phylogeny in shaping their parasite assemblages, a factor previously neglected in studies of parasite communities in deep-sea systems.

Gastrointestinal helminth parasites of the threatened Australasian crested grebe (Podiceps cristatus australis, Gould 1844) in New Zealand, with descriptions of Baruscapillaria kamanae n. sp. (Nematoda: Trichuridae) and Cryptocotyle micromorpha n. sp. (Trematoda: Opisthorchiidae).

The Australasian crested grebe Podiceps cristatus australis, Gould 1844 is restricted to Australia and New Zealand, where it is listed as Threatened and Nationally Vulnerable. For the first time in New Zealand, we report on the parasitic helminths infecting three individuals from Lake Wanaka, Otago, using morphological and molecular tools. Seven helminth species were found in the gastrointestinal tract: 2 nematodes (Contracaecum ovale and Baruscapillaria kamanae n. sp.), 4 trematodes (Australapatemon minor, Cryptocotyle micromorpha n. sp., Tylodelphys darbyi and Neopetasiger neocomensis), and 1 cestode (Confluaria pseudofurcifera). Except for T. darbyi, all are new records for New Zealand. A change of orthography is proposed for Neopetasiger neocomensis and N. pseudoneocomensis. Cryptocotyle micromorpha n. sp. (Opisthorchiidae) is distinguished from similar species by its small size, wholly extracaecal vitellaria and anteriorly looped uterus. Baruscapillaria kamanae n. sp. (Trichuridae) is distinguished from other freshwater species by a combination of vulva and spicule morphology. The helminth parasites found here are mostly the same as those from the grebe in the northern hemisphere, indicating that they have been carried with the host species in its spread to Australasia. However, the parasite fauna may be depauperate due to a diminishing reservoir of intermediate hosts in that geographical migration.

DISTRIBUTION AND DIVERSITY OF DIPLOSTOMIDS IN NEW ZEALAND.

Parasitism is one of the most common consumer strategies and contributes a large portion to biological diversity. Trematodes in the family Diplostomidae are common in freshwater ecosystems worldwide, often residing in the eyes or brain of fish and then infecting fish-eating birds as adults. As a result, some species have broad geographic distributions due to the bird host's motility. In contrast to the cosmopolitan nature of diplostomids, only a single species, Tylodelphys darbyi, has been identified in New Zealand to date, and only from the South Island. Tylodelphys darbyi has a 3-host life cycle consisting of an unidentified snail, a freshwater fish (Gobiomorphus cotidianus), and the Australasian crested grebe (Podiceps cristatus australis). To date, T. darbyi has been found in 2 locations, Lake Hayes, in the eyes of G. cotidianus, and Lake Wanaka, adults recovered from grebes. Considering the near ubiquity of the fish host in New Zealand, it is likely the bird, listed as nationally vulnerable, is the limiting factor in the range of T. darbyi. Up to 10 G. cotidianus were sampled from 10 mountain lakes known to have populations of grebe in the Otago and Canterbury regions of New Zealand's South Island. The eyes of all fish were examined and any metacercariae present were set aside for genetic analysis. In addition to expanding the known range of T. darbyi to at least 4 water bodies across the South Island, 2 new taxa of diplostomid were identified. A lens-infecting metacercariae clustered with Diplostomum spathaceum, while the metacercariae from the humor clustered with Diplostomum baeri.

The people vs science: can passively crowdsourced internet data shed light on host-parasite interactions?

Every internet search query made out of curiosity by anyone who observed something in nature, as well as every photo uploaded to the internet, constitutes a data point of potential use to scientists. Researchers have now begun to exploit the vast online data accumulated through passive crowdsourcing for studies in ecology and epidemiology. Here, we demonstrate the usefulness of iParasitology, i.e. the use of internet data for tests of parasitological hypotheses, using hairworms (phylum Nematomorpha) as examples. These large worms are easily noticeable by people in general, and thus likely to generate interest on the internet. First, we show that internet search queries (collated with Google Trends) and photos uploaded to the internet (specifically, to the iNaturalist platform) point to parts of North America with many sightings of hairworms by the public, but few to no records in the scientific literature. Second, we demonstrate that internet searches predict seasonal peaks in hairworm abundance that accurately match scientific data. Finally, photos uploaded to the internet by non-scientists can provide reliable data on the host taxa that hairworms most frequently parasitize, and also identify hosts that appear to have been neglected by scientific studies. Our findings suggest that for any parasite group likely to be noticeable by non-scientists, information accumulating through internet search activity, photo uploads, social media or any other format available online, represents a valuable source of data that can complement traditional scientific data sources in parasitology.

Diomedenema dinarctos n. sp. (Spiruromorpha: Desmidocercidae), a new species of lung nematode in Fiordland crested penguins (Eudyptes pachyrhynchus; Sphenisciformes), from South Island, New Zealand.

Fiordland crested penguins Eudyptes pachyrhynchus Gray are thick-billed, crested penguins endemic to New Zealand that breed in small colonies in inaccessible places. They are assessed as Vulnerable by the IUCN. This is the first report of helminth parasites from this penguin species. Herein a new species of Diomedenema is described (Spiruromorpha, Desmidocercidae) from the lungs of Fiordland crested penguins. Diomedenema dinarctos n. sp. has only two congeners and is closest morphologically to D. tavaresi. It differs from D. tavaresi in overall larger size, longer buccal cavity and oesophagus, in the distance of the excretory pore and nerve ring from the anterior end, and the ratio of spicule sizes. Eggs are twice the size reported for D. tavaresi. The only other species, D. diomedeae, is far larger in body size, with a shorter buccal cavity and oesophagus and a reduced body length to oesophagus ratio. The position in the body length of the vulva and the spicule ratio also differ strongly. We provide a DNA sequence for the 18S rDNA gene. Species of Diomedenema have been reported as causing death in albatross, so any deceased Fiordland crested penguins should be examined specifically for this worm to enable evaluation of this potentially damaging parasite in the population.

iParasitology: Mining the Internet to Test Parasitological Hypotheses.

Digital data (internet queries, page views, social media posts, images) are accumulating online at increasing rates. Tools for compiling these data and extracting their metadata are now readily available. We highlight the possibilities and limitations of internet data to reveal patterns in host-parasite interactions and encourage parasitologists to embrace iParasitology.

Gastrointestinal helminths of little blue penguins, Eudyptula novaehollandiae (Stephens), from Otago, New Zealand.

Data regarding helminth communities can provide insights into health, feeding interactions, behaviour and evolution of their host organisms. Penguins (Spheniscidae) are important components of marine food webs and tracking their helminth communities can be indicative of ecosystem health. New Zealand is home to 5 of the world's 19 penguin species and little is known about their gastrointestinal helminths. Here, we provide the first study on the gastrointestinal helminths of little blue penguins from south-eastern South Island, New Zealand. The helminth community consisted of two species of tapeworm; Tetrabothrius lutzi and Tetrabothrius sp.; three nematode species, Contracaecum eudyptulae, Capillaria sp. and Stegophorus macronectes; two acanthocephalans, Andracantha sigma and Bolbosoma balaenae; and one trematode, Galactosomum otepotiense. The most prevalent parasites were T. lutzi, A. sigma, and C. eudyptulae. This work includes three new host records and five new geographic records. This is the first report of B. balaenae occurring in a host other than a marine mammal. This study adds to our knowledge about the helminth community of New Zealand little blue penguins, and includes new genetic data on helminth species, providing a baseline against which future studies may be compared.

Morphological and molecular characterisation of a new genus and species of acanthocephalan, Tenuisoma tarapungi n. g., n. sp. (Acanthocephala: Polymorphidae) infecting red-billed gulls in New Zealand, with a key to the genera of the Polymorphidae Meyer, 1931.

Acanthocephalans of the family Polymorphidae Meyer, 1931 are cosmopolitan parasites that infect the intestines of fish-eating birds and mammals. Polymorphid acanthocephalans recovered from the intestines of red-billed gulls (Chroicocephalus scopulinus (Forster)) from the Otago coast, New Zealand, although morphologically similar to the genus Arhythmorhynchus Lühe, 1911 nevertheless have a unique molecular profile showing considerable genetic differentation, and are here diagnosed and described as Tenuisoma tarapungi n. g., n. sp. Characters which distinguish T. tarapungi include a very elongate, cylindrical hindtrunk, swollen anterior trunk with a spinose region, a secondary swelling in males only containing the testes, and hypodermal nuclei distributed throughout the length of the trunk. Molecular data (cox1, 18S, 28S) confirm that the representative of the new genus is closest to, but nonetheless strongly divergent from species of Pseudocorynosoma Aznar, Pérez-Ponce de León & Raga, 2006. Immature specimens are described and illustrated, demonstrating the extreme degree of hindtrunk inversion occurring in immature individuals of this species. We provide a key to the genera of the family Polymorphidae.