Alison M. Dunn

Widespread vertical transmission and associated host sex ratio distortion within the eukaryotic phylum Microspora

Vertical transmission (VT) and associated manipulation of host reproduction are widely reported among prokaryotic endosymbionts. Here, we present evidence for widespread use of VT and associated sex–ratio distortion in a eukaryotic phylum. The Microspora are an unusual and diverse group of eukaryotic parasites that infect all animal phyla. Following our initial description of a microsporidian that feminizes its crustacean host, we survey the diversity and distribution of VT within the Microspora. We find that vertically transmitted microsporidia are ubiquitous in the amphipod hosts sampled and that they are also diverse, with 11 species of microsporidia detected within 16 host species. We found that infections were more common in females than males, suggesting that host sex–ratio distortion occurs in five out of eight parasite species tested. Phylogenetic reconstruction demonstrates that VT occurs in all major lineages of the phylum Microspora and that sex–ratio distorters are found on multiple branches of the phylogenetic tree. We propose that VT is either an ancestral trait or evolves with peculiar frequency in this phylum. If the association observed here between VT and host sex–ratio distortion holds true across other host taxa, these eukaryotic parasites may join the bacterial endosymbionts in their importance as sex–ratio distorters.

Inherited microorganisms, sex-specific virulence and reproductive parasitism

Parasites show an amazing repertoire of adaptations, highlighted by complex life cycles that allow both survival in the host and transmission among hosts. However, there is one heterogeneous group of microorganisms whose adaptations are perhaps even more surprising: parthenogenesis induction, feminization of genetic males, killing of male hosts and sperm-mediated sterilization of uninfected eggs. The common feature of these microorganisms is their mode of transmission: inheritance from mother to offspring. Here, we present an introduction to hereditary symbiosis, focusing on microsporidia and bacteria that manipulate host reproduction in arthropods (reproductive parasites). We also discuss the implications of one of these microorganisms, Wolbachia, for the control of arthropod pests and vectors and for the therapy of filarial diseases. Finally, we discuss whether some parasites of vertebrates might show sex-specific virulence.

Microsporidian life cycles and diversity: the relationship between virulence and transmission

The microsporidia are obligate intracellular parasites which have diverse life cycles involving both horizontal and vertical transmission and parasitise a wide range of vertebrate and invertebrate hosts. In this paper we consider the life cycles and diversity of the microsporidia. We focus in particular on the relationship between parasite transmission and virulence and its implications for host-parasite coevolution. The use of horizontal and vertical routes of transmission varies between species and there is a strong link between transmission and virulence. Horizontal transmission is characterised by a high parasite burden and associated pathogenicity. In contrast, vertical transmission is characterised by low virulence, which has led to under-reporting of this important transmission route. Vertically transmitted microsporidia may also cause male killing or feminisation of their host, with implications for host population sex ratio and stability. Phylogenetic analysis shows that vertical transmission occurs in diverse branches of the Microspora. We find that there is evidence for vertical transmission in both vertebrate and invertebrate hosts and conclude that it is a common or possibly even ubiquitous transmission route within this phylum.

Parasites and biological invasions.

There is considerable current interest in the role that parasites can play in biological invasions. This review looks at the fate of parasites during a biological invasion and at their impact on native and invasive hosts, and asks whether parasites can mediate invasion success. An introduced species may lose its parasites as a result of the introduction and such release from its natural enemies may be an important factor determining invasion success. In addition, an introduced species may acquire parasites from its new environment or it may introduce novel parasites to hosts in the new range. As a result of local adaptation, parasites tend to have a differential effect on native versus invading hosts. The relative impact on the fitness of natives and invaders can be important for the outcome of an invasion and may, for example, reverse the pattern of competitive dominance seen in uninfected hosts. Parasites may mediate invasion success through their effect on host fitness and thus on host population growth and stability. Furthermore, by modifying host-host interactions (including competition and predation), parasites can be important factors that determine the success of an invasion and its impact on the recipient community.

Diverse effects of parasites in ecosystems: linking interdependent processes

Community ecologists generally recognize the importance of species – such as pollinators – that have clear positive effects within ecosystems. However, parasites – usually regarded in terms of their detrimental effects on the individuals they infect – can also have positive impacts on other species in the community. We now recognize that parasites influence species coexistence and extirpation by altering competition, predation, and herbivory, and that these effects can, in turn, influence ecosystem properties. Parasites and pathogens act as ecosystem engineers, alter energy budgets and nutrient cycling, and influence biodiversity. Equally, because ecosystem properties – such as biodiversity – affect parasite populations, there is the potential for feedback between parasitism and ecosystem states. Using examples from animal and plant systems, we examine this potential bidirectional interdependence and challenge the conventional wisdom that parasites have only negative or inconsequential impacts on ecological communities.

Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach

Invasion ecology urgently requires predictive methodologies that can forecast the ecological impacts of existing, emerging and potential invasive species. We argue that many ecologically damaging invaders are characterised by their more efficient use of resources. Consequently, comparison of the classical ‘functional response’ (relationship between resource use and availability) between invasive and trophically analogous native species may allow prediction of invader ecological impact. We review the utility of species trait comparisons and the history and context of the use of functional responses in invasion ecology, then present our framework for the use of comparative functional responses. We show that functional response analyses, by describing the resource use of species over a range of resource availabilities, avoids many pitfalls of ‘snapshot’ assessments of resource use. Our framework demonstrates how comparisons of invader and native functional responses, within and between Type II and III functional responses, allow testing of the likely population-level outcomes of invasions for affected species. Furthermore, we describe how recent studies support the predictive capacity of this method; for example, the invasive ‘bloody red shrimp’ Hemimysis anomala shows higher Type II functional responses than native mysids and this corroborates, and could have predicted, actual invader impacts in the field. The comparative functional response method can also be used to examine differences in the impact of two or more invaders, two or more populations of the same invader, and the abiotic (e.g. temperature) and biotic (e.g. parasitism) context-dependencies of invader impacts. Our framework may also address the previous lack of rigour in testing major hypotheses in invasion ecology, such as the ‘enemy release’ and ‘biotic resistance’ hypotheses, as our approach explicitly considers demographic consequences for impacted resources, such as native and invasive prey species. We also identify potential challenges in the application of comparative functional responses in invasion ecology. These include incorporation of numerical responses, multiple predator effects and trait-mediated indirect interactions, replacement versus non-replacement study designs and the inclusion of functional responses in risk assessment frameworks. In future, the generation of sufficient case studies for a meta-analysis could test the overall hypothesis that comparative functional responses can indeed predict invasive species impacts.

Transovarial transmission in the microsporidia.

The microsporidia are an ancient and diverse group of protists which have many unusual characteristics. These include prokaryotic-like 70s ribosomes, enclosed nuclear division, a lack of mitochondria and complex life cycles which frequently involve vertical transmission. This use of vertical transmission is unparalleled by other protists and is seen only among bacterial endosymbionts and sex ratio distorters and in host cell organelles. Transovarially transmitted microsporidia can have unusual and profound effects on host population sex ratios. We here consider the mechanisms of transovarial transmission and its implications for parasite evolution. We review parasite/host relationships and the evolution of virulence under transovarial transmission and consider the implications of these parasites for host ecology and evolution.

Microsporidia: diverse, dynamic, and emergent pathogens in aquatic systems

Microsporidia cause important diseases in aquatic organisms. Susceptible hosts span a remarkable taxonomic spectrum, from protists to mammals. Known genera represent a small fraction of extant taxa in global aquatic systems. Transmitting horizontally or vertically, effects range from cryptic to catastrophic; individual level effects being extrapolated to populations and ecosystems. Debate over positioning within the eukaryotes and internal structuring of the phylum has benefited from molecular phylogenetic approaches to taxonomy. Similar tools offer new perspectives on transmission between hosts of differing trophic status and habitats. Accessible models for host-pathogen interaction are emerging from full genome sequencing projects. Hyperparasitism and the close phylogenetic relationship between taxa infecting invertebrates and vertebrates not only underline a ubiquity in aquatic systems but also potential for zoonotic transfer.

Parasite-mediated predation between native and invasive amphipods

Parasites can structure biological communities directly through population regulation and indirectly by processes such as apparent competition. However, the role of parasites in the process of biological invasion is less well understood and mechanisms of parasite mediation of predation among hosts are unclear. Mutual predation between native and invading species is an important factor in determining the outcome of invasions in freshwater amphipod communities. Here, we show that parasites mediate mutual intraguild predation among native and invading species and may thereby facilitate the invasion process. We find that the native amphipod Gammarus duebeni celticus is host to a microsporidian parasite, Pleistophora sp. (new species), with a frequency of infection of 0–90%. However, the parasite does not infect three invading species, G. tigrinus, G. pulex and Crangonyx pseudogracilis. In field and laboratory manipulations, we show that the parasite exhibits cryptic virulence: the parasite does not affect host fitness in single–species populations, but virulence becomes apparent when the native and invading species interact. That is, infection has no direct effect on G. d. celticus survivorship, size or fecundity; however, in mixed–species experiments, parasitized natives show a reduced capacity to prey on the smaller invading species and are more likely to be preyed upon by the largest invading species. Thus, by altering dominance relationships and hierarchies of mutual predation, parasitism strongly influences, and has the potential to change, the outcome of biological invasions.

Predatory Functional Response and Prey Choice Identify Predation Differences between Native/Invasive and Parasitised/Unparasitised Crayfish

Background Invasive predators may change the structure of invaded communities through predation and competition with native species. In Europe, the invasive signal crayfish Pacifastacus leniusculus is excluding the native white clawed crayfish Austropotamobius pallipes. Methodology and Principal Findings This study compared the predatory functional responses and prey choice of native and invasive crayfish and measured impacts of parasitism on the predatory strength of the native species. Invasive crayfish showed a higher (>10%) prey (Gammarus pulex) intake rate than (size matched) natives, reflecting a shorter (16%) prey handling time. The native crayfish also showed greater selection for crustacean prey over molluscs and bloodworm, whereas the invasive species was a more generalist predator. A. pallipes parasitised by the microsporidian parasite Thelohania contejeani showed a 30% reduction in prey intake. We suggest that this results from parasite-induced muscle damage, and this is supported by a reduced (38%) attack rate and increased (30%) prey handling time. Conclusions and Significance Our results indicate that the per capita (i.e., functional response) difference between the species may contribute to success of the invader and extinction of the native species, as well as decreased biodiversity and biomass in invaded rivers. In addition, the reduced predatory strength of parasitized natives may impair their competitive abilities, facilitating exclusion by the invader.