Invited ReviewThe conceptual basis for a new classification of the coccidia
Introduction
The coccidia are a diverse group of parasitic protozoa. Some species of coccidia are homoxenous and strictly host specific, other species have complex heteroxenous life cycles that involve a broad range of different host species. Since their first description in the 19th century, coccidia have been found in almost every animal examined, including humans. Thus, while the oldest species and genera of coccidia have now been known for more than a century, others have been described and named only recently.
During the 19th and early 20th centuries, classifications of protozoa were based mainly on organelles of locomotion, but with increasing knowledge on their morphology, biology, life cycle, and host specificity, a broad range of phenotypic characters have been used to classify protozoa into different taxonomic groups (reviewed in Cox, 1991). Thus, several schemes for the classification of protozoa, including the coccidia, have been proposed during the second half of the 20th century. The first major reclassification was undertaken by an international ‘Committee on Taxonomy and Taxonomic Problems’ which was set up by the Society of Protozoologists in 1954 and published a revised classification of the phylum Protozoa 10 years later (Honigberg et al., 1964). This classification was based on phenotypic characters of about 48,000 species of protozoa recorded at the time and defined 140 taxa at suprafamilial levels. However, it incorporated only few ultrastructural data, which became available after the advent of electron microscopy in the 1950s and 1960s, and was thus confounded by incomplete knowledge on heteroxenous life cycles such as those of the tissue cyst-forming coccidia that were elucidated only in the 1970s (reviewed in Tenter and Johnson, 1997). Therefore, although the classification by Honigberg et al. (1964) was a major advance over the variety of traditional classification schemes that had been in use until the 1960s, it already appeared to be out of date by the end of the 1970s.
Consequently, in 1980 the ‘Committee on Systematics and Evolution’ of the Society of Protozoologists, again consisting of an international group of experts, published another revised classification of the protozoa that was based on knowledge of more than 65,000 species, of which more than half were extant and about 10,000 were parasitic, and incorporated information gained from ultrastructural data (Levine et al., 1980). This committee classified the Protozoa, then a subkingdom, into seven phyla, gave descriptions for 234 higher taxa down to the level of suborder, and gave examples of representative genera of each. The classification by Levine et al. (1980) was widely adopted by authors of zoological and biological textbooks, and most groups of protozoa defined in it were generally accepted by many protozoologists until the early 1990s. However, a major drawback of this classification was that only few molecular data from protozoa were available when it was produced. Over the past three decades, molecular data have been increasingly used to infer phylogenetic relationships among various protozoa. The results of such molecular phylogenetic studies supported the monophyly of some taxa defined by Levine et al. (1980), but several other taxa described in this classification have been found to be paraphyletic or even polyphyletic. This has led to the recently revised ‘interim’ classifications of unicellular organisms by Cavalier-Smith, 1993, Corliss, 1994. However, these classifications vary greatly from each other. In fact, they probably represent two extremes with respect to the number of taxonomic categories that have been used in modern classifications of protozoa (Fig. 1), and neither has been widely accepted.
Thus, at the beginning of the 21st century, it appears appropriate to undertake another major revision of the classification of protozoa that, for the first time, will be based on both phenotypic and molecular characters. Such a classification should reflect the phylogeny of the taxonomic groups described in it as accurately as possible to ensure its stability for a reasonable number of years, and again should be produced by an international group of experts to encourage wide acceptance. Considering the number of new protozoan species described since 1980, which may now have exceeded well over 100,000, and the large amount of ultrastructural, biochemical, and molecular biological data that have been generated for a broad range of protozoa, such a revision will be an enormous task. A revised classification of the protozoa at higher taxonomic levels is currently being deliberated by another committee of the Society of Protozoologists and is hoped to become available within the next few years.
To contribute to the current efforts of producing a more accurate and stable classification of protozoa, a Controversial Roundtable on ‘New classification of coccidia’ was held during the joint meeting of the 8th International Coccidiosis Conference and the Annual Scientific Meeting of the Australian Society for Parasitology at Palm Cove, Australia, in July 2001. This Roundtable focussed on one group of coccidia, i.e. the eimeriid coccidia which are one of the largest groups of parasitic protozoa and comprise many species of veterinary and medical importance. While changes at higher taxonomic levels usually have no effect on applied areas of parasitology, taxonomic changes at subfamilial levels may change the names of the organisms involved and thus may be less acceptable to a wide community of general parasitologists, practitioners, and clinicians working in applied fields of veterinary and human medicine. However, although stability of nomenclature is greatly desired to aid communication and avoid confusion among protozoologists and non-protozoologists, an accurate classification of unicellular organisms that reflects their natural history also has impact on practical applications such as in the areas of differential diagnosis and drug development. It is also important for the elucidation of unknown life cycles and epidemiological investigations, in particular on emerging diseases. For example, the recognition of the human pathogen Pneumocystis carinii, previously classified with the protozoa, as a fungus increased knowledge and enabled new experiments to improve treatment of pneumocystic pneumonia (Edman et al., 1988).
The eimeriid coccidia are one of the more controversial groups of protozoa, and their taxonomy and classification have been debated for more than 50 years (reviewed in Cox, 1991, Cox, 1994, Tenter and Johnson, 1997). Therefore, the aim of the Roundtable held at Palm Cove was to initiate discussion on how a new and more comprehensive classification of eimeriid coccidia can be devised. The stimulus came from invited speakers who gave introductions into selected areas relevant to the taxonomy and classification of coccidia. Following these introductions to specific topics, a more general discussion with the audience, which consisted of more than 50 participants with interest in taxonomy, general biology, immunology, or molecular biology of coccidia as well as applied areas of coccidiosis, took place. This publication describes the immediate outcome of the Roundtable and subsequent discussions that continued over the following days of the conference. Individual authors have contributed various sections (taxonomy, Donald W. Duszynski; ultrastructure, Heinz Mehlhorn; molecular characters, John R. Barta; Cryptosporidium, R.C. Andrew Thompson; phenetic/phylogenetic classifications, Ian Beveridge; future steps, David A. Morrison and Patricia A. Conrad) as well as contributions throughout the manuscript. It should be noted that this publication reflects the cooperative efforts of the authors, aided by the opinions of other participants of the Roundtable, and thus does not necessarily represent the views of any one single author. It is not complete and does not cover all aspects relevant to the taxonomy and classification of the coccidia. Rather, it should be taken as a stimulus for further discussion, preferably in conjunction with other conferences of interest to scientists and practitioners working on coccidia and the diseases caused by them.
Section snippets
Traditional classifications of coccidia
The phylum Apicomplexa consists of a diverse group of parasitic protozoa that are characterised by an apical complex consisting of special organelles at the anterior end of their invasive life-cycle stages (Levine, 1970). This apical complex facilitates the entry of the parasites into their host cells (Soldati et al., 2001, Tomley et al., 2001). Except for the, still disputed, addition of the genus Perkinsus to this phylum, the whole group remains essentially identical to the phylum Sporozoa
Defining the terms
Taxonomy is the most basic activity in biology because it involves the discovery, analysis of variation (quantitatively or qualitatively), naming (nomenclature), ordering (classification/systematics), and communication (publication) of the patterns of life-forms. It makes these life-forms (species) historical, temporal, and spatial entities that are the essential elements of biodiversity, i.e. the genealogical packages that store and transmit the information that leads to the interactions
Phenotypic characters used for classifications of eimeriid coccidia
Phenotypic characters traditionally used for the classification of eimeriid coccidia include the morphology of available parasite stages and host specificity (Table 1). One problem with the use of these characters for classification is that in most cases only the oocyst stage and the ‘host’ by which it was shed had been known when a new species was named. Such incomplete species descriptions are confounded by the fact that the ‘host’ described for the new species may not be its true natural
Inference of phylogenetic relationships of eimeriid coccidia based on molecular characters
Molecular characters can expand the range of evolutionarily informative characters that may be used for inferring phylogenetic relationships among different organisms (Sogin and Silberman, 1998). This is especially important for protozoan taxa in the phylum Apicomplexa because of the limited number of phenotypic characters that are suitable for evolutionary studies. Molecular characters can be reasonably assumed to be homologous in an evolutionary sense as well as having sufficient variability
The special case of Cryptosporidium
Recent molecular epidemiological investigations in which Cryptosporidium isolates have been characterised from various host species in different endemic regions support a revision of the species-level taxonomy of Cryptosporidium (Morgan et al., 1999, Thompson et al., 2000, Xiao et al., 2000). Ten species are currently recognised of which the status of four was confirmed within the last few years on the basis of their genetic distinctness. In addition, at least eight genotypes of Cryptosporidium
Transfering from phenetic to phylogenetic classifications
Current controversies in coccidian taxonomy are not unique. Although apparently diverse, they are, arguably, one expression of a phenomenon that is occurring in many branches of parasitology (and other disciplines), in particular in helminthology. If this type of ‘controversy’ is in fact a more general phenomenon, then examination of the broader issues are likely to prove informative. Generalisations are invariably extremely dangerous, but looking back over 30 years, there has been a
How can a new and more comprehensive classification of the eimeriid coccidia be devised?
Widely adopted classifications are neither forced upon scientists as a group nor are they ratified by formal consensus. Such classifications are usually sanctioned because a majority of people who have considered the evidence in their favour have found it convincing. It is therefore the acquisition of convincing evidence that is the key to a stable classification, and if taxonomy is to reflect phylogeny, as is expected in most fields, then it is phylogenetic evidence that is the crucial
Conclusions
Overall, the Controversial Roundtable held at the joint meeting of the 8th International Coccidiosis Conference and the Annual Scientific Meeting of the Australian Society for Parasitology was an important forum for first discussions on how a new and widely accepted classification of the eimeriid coccidia, which takes into consideration both phenotypic and molecular characters, can be devised. The discussions during the Roundtable and thereafter revealed a diversity of concerns regarding the
Acknowledgements
The authors wish to thank the audience of the Controversial Roundtable and other conference participants for stimulating discussion and thoughtful advise, in particular Annette Davidson, David Ferguson, Andrew Hemphill, Michael O'Callaghan, Peter O'Donoghue, Michael Riggs, Jan Slapeta, Rebecca Traub, and Ray Williams.
We also thank Nancy Mugridge for technical assistance and for pre-publication information.
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2021, International Journal for Parasitology: Parasites and WildlifeCitation Excerpt :Derived from the ancient name, “kasumi-no-ura” of Lake Kasumigaura and -ensis (L., belonging to, from) to reflect where the type host was collected. The morphological features of oocysts and sporocysts are of importance as taxonomic keys that influence the description of coccidian species (Tenter et al., 2002; Berto et al., 2014). Here we compares the morphological characteristics of our species alongside the available data of its closest relative, H. lieberkuehni, from P. kl.