Alexander Gruhl

Myxozoan Evolution, Ecology and Development

This book provides an up-to-date review of the biology of myxozoans, which represent a divergent clade of endoparasitic cnidarians. Myxozoans are of fundamental interest in understanding how early diverging metazoans have adopted parasitic lifestyles, and are also of considerable economic and ecological concern as endoparasites of fish. Synthesizing recent research, the chapters explore issues such as myxozoan origins; evolutionary trends and diversification; development and life cycles; interactions with hosts; immunology; disease ecology; the impacts of climate change on disease; risk assessment; emerging diseases; and disease mitigation. This comprehensive work will appeal to a wide readership, from invertebrate zoologists, evolutionary biologists and developmental biologists to ecologists and parasitologists. It will also be of great practical interest to fisheries and conservation biologists. The identification of key areas for future research will appeal to scientists at all levels

Development and myogenesis of the vermiform Buddenbrockia (Myxozoa) and implications for cnidarian body plan evolution

BackgroundThe enigmatic wormlike parasite Buddenbrockia plumatellae has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of myxozoan evolution and identification of their cnidarian sister group. However, B. plumatellae is less simplified than other myxozoans and therefore is of specific significance for such evolutionary considerations.MethodsWe analyse and describe the development of major body plan features in Buddenbrockia worms using a combination of histology, electron microscopy and confocal microscopy.ResultsEarly developmental stages develop a primary body axis that shows a polarity, which is manifested as a gradient of tissue development, enabling distinction between the two worm tips. This polarity is maintained in adult worms, which, in addition, often develop a pore at the distal tip. The musculature comprises tetraradially arranged longitudinal muscle blocks consisting of independent myocytes embedded in the extracellular matrix between inner and outer epithelial tissue layers. The muscle fibres are obliquely oriented and in fully grown worms consistently form an angle of 12° with respect to the longitudinal axis of the worm in each muscle block and hence confer chirality. Connecting cells form a link between each muscle block and constitute four rows of cells that run in single file along the length of the worm. These connecting cells are remnants of the inner epithelial tissue layer and are anchored to the extracellular matrix. They are likely to have a biomechanical function.ConclusionsThe polarised primary body axis represents an ancient feature present in the last common ancestor of Cnidaria and Bilateria. The tetraradial arrangement of musculature is consistent with a medusozoan affinity for Myxozoa. However, the chiral pattern of muscle fibre orientation is apparently novel within Cnidaria and could thus be a specific adaptation. The presence of independent myocytes instead of Cnidaria-like epitheliomuscular cells can be interpreted as further support for the presence of mesoderm in cnidarians, or it may represent convergent evolution to a bilaterian condition.

Diversification and repeated morphological transitions in endoparasitic cnidarians (Myxozoa: Malacosporea)

Malacosporeans are a poorly known myxozoan clade that uniquely demonstrates a tissue level of organisation. Thus, when exploiting their invertebrate hosts (freshwater bryozoans) they occur as non-motile sacs or vermiform stages capable of active swimming. We combine phylogenetic analyses of SSU and LSU rDNA with morphological observations to substantially enhance understanding of malacosporean diversification. The phylogenetic analyses incorporate the widest taxon sampling and geographic cover to date, reveal four novel malacosporean lineages and several putatively new species, one with a novel morphology of irregular, bulbous sacs and no musculature. This lineage currently forms the earliest branch of malacosporeans. Vermiform stages may have been lost or gained several times within the Malacosporea, even in cases where SSU sequence divergence is very low. Yet, sac and vermiform Buddenbrockia plumatellae appear to be separate species, an inference also supported by their utilisation of different bryozoan hosts. Cryptic speciation is also apparent with two novel, genetically divergent lineages (novel lineage 2 and Buddenbrockia sp. 4) being morphologically indistinguishable from known species. Finally, we provide evidence that fredericellid bryozoans are the main hosts for Tetracapsuloides bryosalmonae and are therefore most relevant for research on the ecology and management of Proliferative Kidney Disease of salmonid fish.

An Introduction to Myxozoan Evolution, Ecology and Development

Cnidarians are familiar invertebrates that are widely recognised as typical representatives of marine and freshwater environments. Yet, until recently, all cnidarians were regarded as free-living animals. It is now clear, however, that a clade of cnidarians diverged in ancient times to become endoparasites that today comprise the Myxozoa—common and occasionally highly problematic parasites of fish known since the 1800s. This chapter introduces our volume that focuses on the evolution, ecology and development of myxozoans in light of their cnidarian origin and comprises the first comprehensive book on the group. In this introductory chapter we briefly describe myxozoan biology and highlight milestones in myxozoan research. We then summarise our contributing chapters that review and synthesise recent research and which collectively provide insights on: myxozoan origins, evolutionary trends and diversification, development and life cycles, interactions with hosts, and disease ecology. Key areas for future research commonly identified in our chapters include: improved knowledge of myxozoan diversity, resolution of life cycles and the implications of environmental change for disease risk. We explore how new technologies (particularly, environmental DNA and-omics approaches) will contribute to understanding these and other issues, such as identifying and linking myxozoan developmental stages with those of free-living cnidarians and identifying virulence factors and other adaptations to parasitism. We conclude that myxozoans now merit broad recognition as a clade exhibiting comparable patterns of species richness and host exploitation to those of macroparasites (cestodes and even trematodes) but which has converged on strategies of microparasites (parasitic protists) for host exploitation.

Cnidarian Origins of the Myxozoa

Now that we have strong evidence for the phylogenetic placement of Myxozoa within the Cnidaria it is of great interest to explore their evolutionary history. In particular, what cnidarian features may have facilitated the transition to an endoparasitic lifestyle and can we identify a potential cnidarian sister group? In this chapter we summarise evidence for characters linking myxozoans to cnidarians and identify cnidarian traits that may have promoted endoparasitism including: their diploblastic condition, their capacity for regeneration, transdifferentiation, and dormancy, the production of novel propagative stages, cell-within-cell development, and asexual reproduction. Equating the basic cnidarian life cycle (benthic polyps and planktonic medusae) with the complex myxozoan life cycle is problematic because of great plasticity in cnidarian development, which can entail the loss of stages and associated transfer of function. The sexual phase of myxozoans involves the production of isogametes but divergent views on their subsequent fusion lead to questions about whether sexual reproduction involves selfing or outcrossing and if it may result in the development of multicellular chimaeras. The apical structures of myxozoan polar capsules closely resemble those of medusozoan but not those of anthozoan nematocysts, thus supporting a medusozoan affinity for Myxozoa.

Ultrastructure of mesoderm formation and development in Membranipora membranacea (Bryozoa: Gymnolaemata)

Mesoderm origin in Bryozoa is largely unknown. In this study, embryonic and early larval stages of Membranipora membranacea, a bryozoan exhibiting a planktotrophic cyphonautes larva, are investigated using mainly ultrastructural techniques. Shortly after the onset of gastrulation, an ectodermal cell, which is situated centrally at the prospective anterior pole of the larva, can be recognized by its constricted apical surface and enlarged basal part. It is also distinct from other ectodermal cells by the composition of its cytoplasm. In later stages, it has left the epidermis, lost its epithelial character, and is situated subepithelially, between the basal sides of the ectodermal and endodermal sheets. A blastocoelic cavity is not present at this stage. This cell divides and gives rise to a group of cells forming a muscular and neuronal strand at the anterior side of the larva. The majority of the larval musculature originates from this ingression. Despite this evidence for an ectodermal origin, additional sources of mesoderm can so far not be excluded. The literature on mesoderm origin in Bryozoa is reviewed and the results are compared to known data from other metazoan taxa.

The central and peripheral nervous system of Cephalodiscus gracilis (Pterobranchia, Deuterostomia)

Nervous systems are important in assessing interphyletic phylogenies because they are conservative and complex. Regarding nervous system evolution within deuterostomes, two contrasting hypotheses are currently discussed. One that argues in favor of a concentrated, structured, central nervous system in the last common ancestor of deuterostomes (LCAD); the other reconstructing a decentralized nerve net as the nervous system of the LCAD. Here, we present a morphological analysis of the nervous system of the pterobranch deuterostome Cephalodiscus gracilis Harmer, 1905 based on transmission electron microscopy, confocal laser scanning microscopy, immunohistochemistry, and computer-assisted 3D reconstructions based on complete serial histological sections. The entire nervous system constitutes a basiepidermal plexus. The prominent dorsal brain at the base of the mesosomal tentacles contains an anterior concentration of serotonergic neurons and a posterior net of neurites. Predominant neurite directions differ between brain regions and synapses are present, indicating that the brain constitutes a centralized portion of the nervous system. Main structures of the peripheral nervous system are the paired branchial nerves, tentacle nerves, and the ventral stalk nerve. Serotonergic neurites are scattered throughout the epidermis and are present as concentrations along the anterior border of the branchial nerves. Serotonergic neurons line each tentacle and project into the brain. We argue that the presence of a centralized brain in C. gracilis supports the hypothesis that a nerve center was present in the LCAD. Moreover, based on positional and structural similarity, we suggest that the branchial nerves in C. gracilis could be homologous to branchial nerves in craniates, a hypothesis that should be further investigated.

Myxozoan Affinities and Route to Endoparasitism

There is now strong evidence that myxozoans have evolved from free-living cnidarians but until recently their higher level relationships have been the subject of considerable controversy. This chapter reviews the morphological and molecular evidence that has contributed to problems in placement and how further collective support has finally resolved their cnidarian affinity. We then consider the inherently difficult but fascinating topic of how myxozoans may have evolved as endoparasitic cnidarians. We first explore how a close association of free-living precursors could have led to the evolution of myxozoans with simple life cycles and the nature of the first myxozoan hosts. We propose that either freshwater bryozoans or fish (or their precursors) were ancestral hosts (in view of the more derived nature of myxozoans that infect annelids and the fact that fish are hosts for most members of all major myxozoan clades) and suggest that the morphological complexity of myxozoans in freshwater bryozoans renders a scenario of fish as first hosts less likely. We then discuss how new hosts may have been adopted subsequently, resulting in the complex life cycles involving invertebrate and vertebrate hosts that now characterise all myxozoans. Cnidarian traits, including life cycle plasticity and a capacity to evolve novel propagative stages, ultimately support many different scenarios regarding the route to endoparasitism.

Myxozoa + Polypodium: A Common Route to Endoparasitism

Recent evidence places the problematic Polypodium, a parasite of fish eggs, firmly as sister taxon to Myxozoa within the Cnidaria. This resolution suggests a single route to endoparasitism in Cnidaria, with larval stages of a common ancestor exploiting fish as first hosts. It also enables new interpretations and insights regarding evolutionary transitions associated with endoparasitism.

Occurrence and Identity of “White Spots” in Phylactolaemata

Localised epidermal gland complexes of unknown function have previously been recognised as “white spots” in Pectinatella magnifica and Lophopodella carteri, but not in other phylactolaemate species. In this study a similar glandular organ is described for Lophopus crystallinus. It is a complex epidermal gland that consists of two types of gland cells, one of which contains light-refracting, possibly lipidic, vesicles. This gland is situated at the anal side of the duplicature, distal to a pore, which most likely resembles the vestibular or statoblast pore. Such a pore had always been postulated, but histological evidence was lacking so far. The most likely functions of the glandular organs could either be connected to statoblast expulsion or to chemical defence.