Further species and range extensions of Amazonian bryozoans: chipping away at the iceberg.

A bryozoan survey conducted in the Amazon Basin in the vicinities of Manaus and Santarm during the high water season (May, 2018) revealed four new species described here: Fredericella adrianoi n. sp., Plumatella divae n. sp., Plumatella hartikainenae n. sp., and Plumatella spencerjonesae n. sp. Two of these species were encountered only once, suggesting that other undescribed species are likely to occur in the area. Range extensions were determined for two additional species: Plumatella pirassununga and Timwoodiellina natans. In addition, colonies were collected for the first time for two species previously known only by their statoblasts: Plumatella siolii and Plumatella marcusi. Statoblasts of Tapajosella elongata were encountered near Manaus, but the colonies remained elusive. The discovery of new species collected during two expeditions to the Amazon Basin in different seasons and years suggests that further diversity remains undetected in this and other poorly studied regions of the world. With few exceptions, plumatellid colonies described so far from the Amazon Basin are very similar in appearance, with branches wholly attached to the substratum and body walls that are soft, colorless, and transparent.

Evolutionary Transitions of Parasites between Freshwater and Marine Environments.

Evolutionary transitions of organisms between environments have long fascinated biologists, but attention has been focused almost exclusively on free-living organisms and challenges to achieve such transitions. This bias requires addressing because parasites are a major component of biodiversity. We address this imbalance by focusing on transitions of parasitic animals between marine and freshwater environments. We highlight parasite traits and processes that may influence transition likelihood (e.g., transmission mode, life cycle, host use), and consider mechanisms and directions of transitions. Evidence for transitions in deep time and at present are described, and transitions in our changing world are considered. We propose that environmental transitions may be facilitated for endoparasites because hosts reduce exposure to physiologically challenging environments and argue that adoption of an endoparasitic lifestyle entails an equivalent transitioning process as organisms switch from living in one environment (e.g., freshwater, seawater, or air) to living symbiotically within hosts. Environmental transitions of parasites have repeatedly resulted in novel forms and diversification, contributing to the tree of life. Recognizing the potential processes underlying present-day and future environmental transitions is crucial in view of our changing world and the current biodiversity crisis.

High-throughput sequencing of faeces provides evidence for dispersal of parasites and pathogens by migratory waterbirds.

Examination of faecal material has demonstrated how a broad range of organisms are distributed by bird movements. Such research has largely focused on dispersal of plant seeds by frugivores and of freshwater organisms by waterbirds. However, with few exceptions (e.g. avian influenza, Ebola virus), there is a dearth of evidence for transport of parasites and pathogens. High-throughput sequencing methods now provide a powerful means of addressing this knowledge gap by elucidating faecal contents in unprecedented detail. We collected faeces excreted by a range of migratory waterbirds in south-west Spain and pooled faecal DNA to create libraries reflective of feeding behavior. We created sets of libraries using high-throughput metagenomic and amplicon sequencing. For the latter we employed two sets of primers to broadly target the V4 region of the 18S rRNA gene (one set amplifying the region across all eukaryotes, the other excluding amplification of metazoans). Libraries revealed a wide diversity of eukaryotes, including parasites of the faecal producers themselves, parasites of food items, or those incidentally ingested. We also detected novel microbial eukaryotic taxa and found that parasite assemblage profiles were relatively distinct. Comparing the performance of the methods used supports their joint use for future studies of diversity and abundance. Because viable stages of many parasites are likely to be present in faeces, our results suggest significant levels of bird-mediated dispersal of parasites (both from avian and other hosts). Our methods revealed much hidden biodiversity, and allowed identification of the individuals who produced the faecal samples to species level, facilitating the study of interaction networks.

How to build single-celled cnidarians with worm-like motility: Lessons from Myxozoa.

Metazoans with worm-like morphologies across diverse and disparate groups typically demonstrate motility generated by hydrostatic skeletons involving tissue layers (muscles and epithelia). Here we present representative morphological, behavioural and molecular data for parasitic cnidarians (myxozoans) that demonstrate unprecedented variation in form and function, developing as cellular hydrostats. Motile elongate plasmodia characterise a remarkable radiation of species in the genus Ceratomyxa. The vermiform plasmodia inhabit gall bladders of a range of South American freshwater fish and exhibit undulatory motility reminiscent of nematodes but achieved at the cellular level. Collective insights from ultrastructure, confocal and light microscopy along with videos depicting movements highlight key features that we propose explain the unique motility of the plasmodia. These features include cytoskeletal elements (net forming microfilaments and microtubules), a large internal vacuole, a relatively rigid outer glycocalyx and peripherally arranged mitochondria. These constituents provide collective evidence for repurposing of the cnidarian epitheliomuscular cell to support worm-like motility at the cellular level. The apparent restriction of vermiform ceratomyxids to South American freshwaters suggests an origination via Cretaceous or Miocene marine transgressions and subsequent radiation.

Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa.

Cnidarians are the oldest lineage of venomous animals and use nematocysts to discharge toxins. Whether venom toxins have been recruited to support parasitic lifestyles in the Endocnidozoa (Myxozoa + Polypodium) is, however, unknown. To examine this issue we variously employed transcriptomic, proteomic, associated molecular phylogenies, and localisation studies on representative primitive and derived myxozoans (Malacosporea and Myxosporea, respectively), Polypodium hydriforme, and the free-living staurozoan Calvadosia cruxmelitensis. Our transcriptomics and proteomics analyses provide evidence for expression and translation of venom toxin homologs in myxozoans. Phylogenetic placement of Kunitz type serine protease inhibitors and phospholipase A2 enzymes reveals modification of toxins inherited from ancestral free-living cnidarian toxins, and that venom diversity is reduced in myxozoans concordant with their reduced genome sizes. Various phylogenetic analyses of the Kunitz-type toxin family in Endocnidozoa suggested lineage-specific gene duplications, which offers a possible mechanism for enhancing toxin diversification. Toxin localisation in the malacosporean Buddenbrockia plumatellae substantiates toxin translation and thus illustrates a repurposing of toxin function for endoparasite development and interactions with hosts, rather than for prey capture or defence. Whether myxozoan venom candidates are expressed in transmission stages (e.g. in nematocysts or secretory vesicles) requires further investigation.

Comparative transcriptomics and host-specific parasite gene expression profiles inform on drivers of proliferative kidney disease.

The myxozoan parasite, Tetracapsuloides bryosalmonae has a two-host life cycle alternating between freshwater bryozoans and salmonid fish. Infected fish can develop Proliferative Kidney Disease, characterised by a gross lymphoid-driven kidney pathology in wild and farmed salmonids. To facilitate an in-depth understanding of T. bryosalmonae-host interactions, we have used a two-host parasite transcriptome sequencing approach in generating two parasite transcriptome assemblies; the first derived from parasite spore sacs isolated from infected bryozoans and the second from infected fish kidney tissues. This approach was adopted to minimize host contamination in the absence of a complete T. bryosalmonae genome. Parasite contigs common to both infected hosts (the intersect transcriptome; 7362 contigs) were typically AT-rich (60-75% AT). 5432 contigs within the intersect were annotated. 1930 unannotated contigs encoded for unknown transcripts. We have focused on transcripts encoding proteins involved in; nutrient acquisition, host-parasite interactions, development, cell-to-cell communication and proteins of unknown function, establishing their potential importance in each host by RT-qPCR. Host-specific expression profiles were evident, particularly in transcripts encoding proteases and proteins involved in lipid metabolism, cell adhesion, and development. We confirm for the first time the presence of homeobox proteins and a frizzled homologue in myxozoan parasites. The novel insights into myxozoan biology that this study reveals will help to focus research in developing future disease control strategies.

Broad but restricted detection of malacosporeans in a Neotropical cradle of diversification.

This study undertook the first investigation of malacosporean infections in Neotropical fish. We used polymerase chain reaction detection with a primer set generally targeting known malacosporeans to assay for infection in the kidney of 146 fish in 21 species belonging to 12 families collected from two areas in the Amazon Basin. Infections were found in 13 fish variously belonging to seven species in six families and included the first identification of a malacosporean infection in cartilaginous fish (a freshwater stingray). Based on ssrDNA, all infections represented a single Buddenbrockia species (Buddenbrockia sp. E) that demonstrates an exceptionally broad range of fish species infected, and countered our expectations of high Neotropical malacosporean diversity. Infections were characterized at varying and often high prevalences in fish species but sample sizes were small. Ascertaining whether highly divergent malacosporeans have not been detected by current primers, and more comprehensive sampling may reveal whether malacosporeans are truly as species poor in the Amazon Basin as present data suggest. Our results prompt speculations about evolutionary scenarios including introduction via marine incursions and patterns of host use over time.

PCR-RFLP: a targeted method to reveal host specific malacosporean infection profiles (Cnidaria: Myxozoa: Malacosporea).

Malacosporeans are a group of endoparasitic cnidarians (Myxozoa) that use freshwater bryozoans and fish as final and intermediate hosts, respectively. The malacosporean Tetracapsuloides bryosalmonae causes proliferative kidney disease (PKD), an emerging disease in aquaculture and wild fish populations, including threatened salmonids in Europe and the USA. Mixed infections of malacosporeans are often encountered, and a monitoring tool for screening of multiple malacosporean species in either their fish or bryozoan hosts is therefore desirable. We describe an inexpensive method that combines PCR amplification of the partial 18S rRNA gene (~260 bp) and a single-step restriction fragment length polymorphism (RFLP) method for identification of 10 malacosporean lineages and species. We demonstrate and test this methodology on a set of DNA extracted from malacosporeans infecting fish kidney and tissues sampled from bryozoan colonies and compare the results with Sanger sequencing of the same parasite DNA isolates. The PCR-RFLP and Sanger sequencing methods agreed in 100% of cases. The PCR-RFLP method offers a number of opportunities, including screening large panels of host tissue samples to gain insights into infection patterns, characterizing mixed infections, and confirming highly pathogenic T. bryosalmonae infections. The method can also be further refined as new sequence data become available for malacosporeans.

Epidemiology of Polypodium hydriforme in American Paddlefish.

Polypodium hydriforme is a parasitic cnidarian that develops within the eggs of acipenseriform fish in the Old and New Worlds. Currently regarded as monotypic, P. hydriforme has been studied largely in the context of caviar production in Russian sturgeon species. We report the first robust epidemiological study of P. hydriforme in North American acipenseriform fish. We sampled infection prevalences (in 2017 and 2018) and intensities (in 2017) during annual surveys of American Paddlefish, Polyodon spathula, caught during spawning migration in north-eastern Oklahoma. Egg masses were characterized for the presence and intensity of P. hydriforme infection. Prevalences were similar in 2017 and 2018 (49% and 45%, respectively). Generally, a small number of eggs were infected per egg mass, but a few were heavily infected. Longer, heavier and older fish are more likely to be infected and to harbour more severe infections. In addition, infection is linked to decreases in roe fat weight independently of fish length, weight, age or roe weight. Infection thus diminishes Paddlefish energy reserves (roe fat) which could in turn impact host fitness. Our results raise questions about the impacts of infection on caviar production and Paddlefish conservation and suggest insights on infection dynamics and parasite strategies.

To remain or leave: Dispersal variation and its genetic consequences in benthic freshwater invertebrates.

Variation in dispersal capacity may influence population genetic variation and relatedness of freshwater animals thus demonstrating how life-history traits influence patterns and processes that in turn influence biodiversity. The majority of studies have focused on the consequences of dispersal variation in taxa inhabiting riverine systems whose dendritic nature and upstream/downstream gradients facilitate characterizing populations along networks. We undertook extensive, large-scale investigations of the impacts of hydrological connectivity on population genetic variation in two freshwater bryozoan species whose dispersive propagules (statoblasts) are either attached to surfaces (Fredericella sultana) or are released as buoyant stages (Cristatella mucedo) and that live primarily in either lotic (F. sultana) or lentic environments (C. mucedo). Describing population genetic structure in multiple sites characterized by varying degrees of hydrological connectivity within each of three (or four) UK regions enabled us to test the following hypotheses: (1) genetic diversity and gene flow will be more influenced by hydrological connectivity in populations of C. mucedo (because F. sultana dispersal stages are retained); (2) populations of F. sultana will be characterized by greater genetic divergence than those of C. mucedo (reflecting their relative dispersal capacities); and (3) genetic variation will be greatest in F. sultana (reflecting a propensity for genetic divergence as a result of its low dispersal potential). We found that hydrological connectivity enhanced genetic diversity and gene flow among C. mucedo populations but not in F. sultana while higher overall measures of clonal diversity and greater genetic divergence characterized populations of F. sultana. We suggest that genetic divergence over time within F. sultana populations reflects a general constraint of releasing propagules that might eventually be swept to sea when taxa inhabit running waters. In contrast, taxa that primarily inhabit lakes and ponds may colonize across hydrologically connected regions, establishing genetically related populations. Our study contributes more nuanced views about drivers of population genetic structures in passively dispersing freshwater invertebrates as outlined by the Monopolization Hypothesis (Acta Oecologica, 23, 2002, 121) by highlighting how a range of demographic and evolutionary processes reflect life-history attributes of benthic colonial invertebrates (bryozoans) and cyclically parthenogenetic zooplankton. In addition, growing evidence that genetic divergence may commonly characterize populations of diverse groups of riverine taxa suggests that organisms inhabiting lotic systems may be particularly challenged by environmental change. Such change may predispose riverine populations to extinction as a result of genetic divergence combined with limited dispersal and gene flow. OPEN RESEARCH BADGES: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.1tm8705.

Chemical Responses to the Biotic and Abiotic Environment by Early Diverging Metazoans Revealed in the Post-Genomic Age.

For many years methodological constraints limited insights on the molecular biology of non-model organisms. However, the development of various sequencing platforms has led to an explosion of transcriptomic and genomic data on non-model systems. As a consequence the molecular drivers of organismal phenotypes are becoming clearer and the chemicals that animals use to detect and respond to their environments are increasingly being revealed-this latter area inspired our symposium theme. The papers in this volume broadly address this theme by their more specific focus in one of the following general areas: 1) sensory biology and the molecular basis of perception, 2) chemicals deployed to deal with the biotic and abiotic environment, and 3) chemical interactions along the parasite-mutualist continuum. Here we outline and synthesize the content of these papers-an exercise which demonstrates that sophisticated gene repertoires enable early diverging metazoans to encode many of the signaling, sensory, defensive, and offensive capacities typically associated with animals that have complex nervous systems. We then consider opportunities and associated challenges that may delay progress in comparative functional biochemistry, a reinvigorated field that can be expected to rapidly expand with new 'omics data. Future knowledge of chemical adaptations should afford new perspectives on the comparative evolution of chemical mediators.

"Beyond Primary Sequence"-Proteomic Data Reveal Complex Toxins in Cnidarian Venoms.

Venomous animals can deploy toxins for both predation and defense. These dual functions of toxins might be expected to promote the evolution of new venoms and alteration of their composition. Cnidarians are the most ancient venomous animals but our present understanding of their venom diversity is compromised by poor taxon sampling. New proteomic data were therefore generated to characterize toxins in venoms of a staurozoan, a hydrozoan, and an anthozoan. We then used a novel clustering approach to compare venom diversity in cnidarians to other venomous animals. Comparison of the presence or absence of 32 toxin protein families indicated venom composition did not vary widely among the 11 cnidarian species studied. Unsupervised clustering of toxin peptide sequences suggested that toxin composition of cnidarian venoms is just as complex as that in many venomous bilaterians, including marine snakes. The adaptive significance of maintaining a complex and relatively invariant venom remains unclear. Future study of cnidarian venom diversity, venom variation with nematocyst types and in different body regions are required to better understand venom evolution.

Stress-Free Evolution: The Nrf-Coordinated Oxidative Stress Response in Early Diverging Metazoans.

Environmental stress from ultraviolet radiation, elevated temperatures or metal toxicity can lead to reactive oxygen species in cells, leading to oxidative DNA damage, premature aging, neurodegenerative diseases, and cancer. The transcription factor nuclear factor (erythroid-derived 2)-like 2 (Nrf2) activates many cytoprotective proteins within the nucleus to maintain homeostasis during oxidative stress. In vertebrates, Nrf2 levels are regulated by the Kelch-family protein Keap1 (Kelch-like ECH-associated protein 1) in the absence of stress according to a canonical redox control pathway. Little, however, is known about the redox control pathway used in early diverging metazoans. Our study examines the presence of known oxidative stress regulatory elements within non-bilaterian metazoans including free living and parasitic cnidarians, ctenophores, placozoans, and sponges. Cnidarians, with their pivotal position as the sister phylum to bilaterians, play an important role in understanding the evolutionary history of response to oxidative stress. Through comparative genomic and transcriptomic analysis our results show that Nrf homologs evolved early in metazoans, whereas Keap1 appeared later in the last common ancestor of cnidarians and bilaterians. However, key Nrf-Keap1 interacting domains are not conserved within the cnidarian lineage, suggesting this important pathway evolved with the radiation of bilaterians. Several known downstream Nrf targets are present in cnidarians suggesting that cnidarian Nrf plays an important role in oxidative stress response even in the absence of Keap1. Comparative analyses of key oxidative stress sensing and response proteins in early diverging metazoans thus provide important insights into the molecular basis of how these lineages interact with their environment and suggest a shared evolutionary history of regulatory pathways. Exploration of these pathways may prove important for the study of cancer therapeutics and broader research in oxidative stress, senescence, and the functional responses of early diverging metazoans to environmental change.

Malacosporean myxozoans exploit a diversity of fish hosts.

Myxozoans are widespread and common endoparasites of fish with complex life cycles, infecting vertebrate and invertebrate hosts. There are two classes: Myxosporea and Malacosporea. To date about 2500 myxosporean species have been described. By comparison, there are only five described malacosporean species. Malacosporean development in the invertebrate hosts (freshwater bryozoans) has been relatively well studied but is poorly known in fish hosts. Our aim was to investigate the presence and development of malacosporeans infecting a diversity of fish from Brazil, Europe and the USA. We examined kidney from 256 fish belonging variously to the Salmonidae, Cyprinidae, Nemacheilidae, Esocidae, Percidae, Polyodontidae, Serrasalmidae, Cichlidae and Pimelodidae. Malacosporean infections were detected and identified by polymerase chain reaction and small subunit ribosomal DNA sequencing, and the presence of sporogonic stages was evaluated by ultrastructural examination. We found five malacosporean infections in populations of seven European fish species (brown trout, rainbow trout, white fish, dace, roach, gudgeon and stone loach). Ultrastructural analyses revealed sporogonic stages in kidney tubules of three fish species (brown trout, roach and stone loach), providing evidence that fish belonging to at least three families are true hosts. These results expand the range of fish hosts exploited by malacosporeans to complete their life cycle.

Measuring Biodiversity and Extinction-Present and Past.

How biodiversity is changing in our time represents a major concern for all organismal biologists. Anthropogenic changes to our planet are decreasing species diversity through the negative effects of pollution, habitat destruction, direct extirpation of species, and climate change. But major biotic changes-including those that have both increased and decreased species diversity-have happened before in Earth's history. Biodiversity dynamics in past eras provide important context to understand ecological responses to current environmental change. The work of assessing biodiversity is woven into ecology, environmental science, conservation, paleontology, phylogenetics, evolutionary and developmental biology, and many other disciplines; yet, the absolute foundation of how we measure species diversity depends on taxonomy and systematics. The aspiration of this symposium, and complementary contributed talks, was to promote better understanding of our common goals and encourage future interdisciplinary discussion of biodiversity dynamics. The contributions in this collection of papers bring together a diverse group of speakers to confront several important themes. How can biologists best respond to the urgent need to identify and conserve diversity? How can we better communicate the nature of species across scientific disciplines? Where are the major gaps in knowledge about the diversity of living animal and plant groups, and what are the implications for understanding potential diversity loss? How can we effectively use the fossil record of past diversity and extinction to understand current biodiversity loss?

Extensive Uncharted Biodiversity: The Parasite Dimension.

Parasites are often hidden in their hosts and exhibit patchy spatial distributions. This makes them relatively difficult to detect and sample. Consequently we have poor knowledge of parasite diversities, distributions, and extinction. We evaluate our general understanding of parasite diversity and highlight the enormous bias in research on parasites such as helminths and arthropods that infect vertebrate hosts. We then focus on Myxozoa as an exemplary case for demonstrating uncharted parasite diversity. Myxozoans are a poorly recognized but speciose clade of endoparasitic cnidarians with complex life cycles that have radiated to exploit freshwater, marine, and terrestrial hosts by adopting strategies convergent to those of parasitic protists. Myxozoans are estimated to represent some 20% of described cnidarian species-greatly outnumbering the combined species richness of scyphozoans, cubozoans, and staurozoans. We summarize limited understanding of myxozoan diversification and geographical distributions, and highlight gaps in knowledge and approaches for measuring myxozoan diversity. We close by reviewing methods and problems in estimating parasite extinction and concerns about extinction risks in view of the fundamental roles parasites play in ecosystem dynamics and in driving host evolutionary trajectories.

Persistence, impacts and environmental drivers of covert infections in invertebrate hosts.

BACKGROUND: Persistent covert infections of the myxozoan, Tetracapsuloides bryosalmonae, in primary invertebrate hosts (the freshwater bryozoan, Fredericella sultana) have been proposed to represent a reservoir for proliferative kidney disease in secondary fish hosts. However, we have limited understanding of how covert infections persist and vary in bryozoan populations over time and space and how they may impact these populations. In addition, previous studies have likely underestimated covert infection prevalence. To improve our understanding of the dynamics, impacts and implications of covert infections we employed a highly sensitive polymerase chain reaction (PCR) assay and undertook the first investigation of covert infections in the field over an annual period by sampling bryozoans every 45 days from three populations within each of three rivers. RESULTS: Covert infections persisted throughout the year and prevalence varied within and between rivers, but were often > 50%. Variation in temperature and water chemistry were linked with changes in prevalence in a manner consistent with the maintenance of covert infections during periods of low productivity and thus poor growth conditions for both bryozoans and T. bryosalmonae. The presence and increased severity of covert infections reduced host growth but only when bryozoans were also investing in the production of overwintering propagules (statoblasts). However, because statoblast production is transitory, this effect is unlikely to greatly impact the capacity of bryozoan populations to act as persistent sources of infections and hence potential disease outbreaks in farmed and wild fish populations. CONCLUSIONS: We demonstrate that covert infections are widespread and persist over space and time in bryozoan populations. To our knowledge, this is the first long-term study of covert infections in a field setting. Review of the results of this and previous studies enables us to identify key questions related to the ecology and evolution of covert infection strategies and associated host-parasite interactions.

Tetracapsuloides bryosalmonae abundance in river water.

Tetracapsuloides bryosalmonae is a myxozoan parasite of freshwater bryozoans and salmonids, causing proliferative kidney disease in the latter. To date, detection of the parasite has required collection of hosts and subsequent molecular or histological examination. The release of infectious spores from both hosts offers an opportunity to detect the parasite in water samples. We developed a novel SYBR® Green quantitative real-time PCR (qPCR) assay for T. bryosalmonae in water samples which provides an estimation of bryozoan malacospore numbers and tested the assay in 3 rivers in southern England (UK) over a period of 5 wk. The assay proved to be both highly sensitive and specific to the parasite, detecting low levels of spores throughout the study period. Larger-volume samples afforded greater detection likelihood, but did not increase the number of spores detected, possibly as a result of low and patchy spore distributions and lack of within-site replication of large-volume samples. Based on point-measurements, temperature was positively associated with the likelihood of detecting spores, possibly reflecting the temperature dependence of spore shedding from bryozoan hosts. The presence of T. bryosalmonae in water samples was predominantly influenced by spatial (sites within rivers, amongst rivers) and temporal (sampling dates) factors, while the latter also influenced quantification cycle (Cq) values and spore abundance. Environmental monitoring for infectious stages can complement traditional methods, providing faster and easier detection and avoiding potentially prolonged searching, collecting and destructive sampling of invertebrate and vertebrate hosts.

The evolution of transmission mode.

This article reviews research on the evolutionary mechanisms leading to different transmission modes. Such modes are often under genetic control of the host or the pathogen, and often in conflict with each other via trade-offs. Transmission modes may vary among pathogen strains and among host populations. Evolutionary changes in transmission mode have been inferred through experimental and phylogenetic studies, including changes in transmission associated with host shifts and with evolution of the unusually complex life cycles of many parasites. Understanding the forces that determine the evolution of particular transmission modes presents a fascinating medley of problems for which there is a lack of good data and often a lack of conceptual understanding or appropriate methodologies. Our best information comes from studies that have been focused on the vertical versus horizontal transmission dichotomy. With other kinds of transitions, theoretical approaches combining epidemiology and population genetics are providing guidelines for determining when and how rapidly new transmission modes may evolve, but these are still in need of empirical investigation and application to particular cases. Obtaining such knowledge is a matter of urgency in relation to extant disease threats.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.

Conditional persistence and tolerance characterize endoparasite-colonial host interactions.

Colonial hosts offer unique opportunities for exploitation by endoparasites resulting from extensive clonal propagation, but these interactions are poorly understood. The freshwater bryozoan, Fredericella sultana, and the myxozoan, Tetracapsuloides bryosalmonae, present an appropriate model system for examining such interactions. F. sultana propagates mainly asexually, through colony fragmentation and dormant propagules (statoblasts). Our study examines how T. bryosalmonae exploits the multiple transmission routes offered by the propagation of F. sultana, evaluates the effects of such transmission on its bryozoan host, and tests the hypothesis that poor host condition provokes T. bryosalmonae to bail out of a resource that may soon be unsustainable, demonstrating terminal investment. We show that infections are present in substantial proportions of colony fragments and statoblasts over space and time and that moderate infection levels promote statoblast hatching and hence effective fecundity. We also found evidence for terminal investment, with host starvation inducing the development of transmission stages. Our results contribute to a growing picture that interactions of T. bryosalmonae and F. sultana are generally characterized by parasite persistence, facilitated by multiple transmission pathways and host condition-dependent developmental cycling, and host tolerance, promoted by effective fecundity effects and an inherent capacity for renewed growth and clonal replication.