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PDF Available This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Review Evolutionary Parasitology Evolution of the Apicomplexa: where are we now? David A. Morrison Section for Parasitology, Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, 751 89 Uppsala, Sweden The Apicomplexa is the only large taxonomic group of the Genus Cryptosporidium (http://www.vetsci.usyd. whose members are entirely parasitic and is, therefore, edu. au/staff/JanSlapeta/icrypto/index.htm). presumably of major interest to parasitologists. We might, for example, expect that we know a great deal Why do we need to study Apicomplexan evolution? about the biology of the group by now and that we Probably the two best-known quotations in biology are have a clear phylogenetic framework within which these: ‘On the origin of species by means of natural selec- to organize that knowledge. It might thus come as tion (or the preservation of favoured races in the struggle a surprise to learn that in terms of biodiversity, the for life)’, which is the title of Charles Darwin’s first book [9], Apicomplexa is actually the least-known group of all. and ‘Nothing in biology makes sense except in the light of Furthermore, the taxonomic framework for the Apicom- evolution’, which is the title of a paper by Theodosius plexa is rather tenuous in many respects. This situation Dobzhansky [10]. What these titles have in common is is unlikely to change in the short term. that they express the over-riding importance of evolution- ary thought in modern biology. The Apicomplexa Darwin’s contribution was to recognize that there are The phylum Apicomplexa (sometimes also known as Spor- two distinct types of biological evolution: transformational ozoa) forms a large and diverse group of unicellular protists evolution, in which a single object changes through time, with a wide environmental distribution. They are obligate and variational evolution, in which groups of variable intracellular parasites, the motile invasive stages of which objects change their relative proportions through time. are characterized by the presence of an evolutionarily unique Transformational evolution is common in the physical apical complex (secretory organelles underlying the oral sciences as well as in biology, but variational evolution structure). Many of the species are pathogens of humans has a special place in the biological sciences because iso- and domesticated animals, although all animal species are lated changes in variation will ultimately lead to new believed to play host to at least one Apicomplexan species species. Both types of evolution can best be represented (and probably several). The phylum is now recognized as as a tree-like diagram because this can show the phylesis being closely related to the dinoflagellates and ciliates, form- (changes through time) as relative branch lengths and the ing the taxonomic group known as the Alveolata [1–3]. cladogenesis (speciation) as the relative branching order. The Apicomplexa is traditionally considered to contain All organisms have a phylogenetic (evolutionary) four clearly defined groups [4]: the coccidians, the gregar- history, which can be represented by a phylogenetic tree. ines, the haemosporidians and the piroplasmids. These Charles Darwin drew the first phylogenetic tree in a note- groups are based largely on phenotypic characteristics, book in 1836–1837, and the only illustration in his most such as their associated host and/or vector, and which famous book is a more refined version of that tree, under- particular tissues they inhabit. These groups were origin- lining the importance of such trees in modern biological ally designed to be utilitarian rather than to reflect evol- thinking. It is important that all biologists use and under- utionary history [5,6]; thus, the evolutionary relationships stand phylogenetic trees. Sadly, there is considerable evi- among the four groups and their subsequent taxonomic dence that ‘tree thinking’ (as it is called) is sometimes poor, arrangement are presently unclear. even in biology (Box 1). The current classification of the Apicomplexa is admit- Dobzhansky’s comment might be better stated as: ‘Very tedly a conservative one [7,8] and does not take into little in biology is not made more comprehensible in the account modern molecular data. Even the appropriate light of phylogenetic history’. For this reason, there are pages of the Tree of Life Web Project (http://tolweb.org/ now many biological studies based on phylogenies in all notes/?note_id=4812) have been rather out of date, until sorts of fields, including such diverse subjects as immu- recently. There are very few specialist web resources, nology and epidemiology. In addition, many new areas of notably The Coccidia of the World (http://biology.unm. study that make extensive use of phylogenies, such as edu/biology/coccidia/home.html) and iCRYPTO: Taxonomy evolutionary development (known as evodevo) and evol- utionary ecology, have arisen recently. Elucidating phylo- genies, therefore, is now an important component of nearly Corresponding author: Morrison, D.A. ([email protected]). all of biology. Phylogenies form the framework within 1471-4922/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.pt.2009.05.010 375 Author's personal copy Review Trends in Parasitology Vol.25 No.8 Box 1. Tree thinking There seems to be a great deal of confusion among non-specialists as to how an evolutionary tree should be interpreted. As far as relationships among organisms are concerned, evolutionary trees are intended to replace the traditional Aristotelian ladder (also known as the Great Chain of Being), which arranges organisms in a linear sequence, ending with human beings as the ultimate biological form. Instead, we now use a branching diagram in which humans are merely one twig among many, thus supplanting the traditional anthropocentric viewpoint. Unfortunately, many people seem to be imagining a pine tree, with a single central axis leading to the ‘most derived’ species and many side-branches leading to ‘lesser’ organ- isms, rather than picturing a continuously branching bush-like structure, as originally depicted by Charles Darwin. This leads to several persistent and apparently endemic problems [50,51]. First, an evolutionary tree must have a time direction (from ancestors to descendants), which is provided by the root. Darwin himself came to realize this distinction: in his 1836–1837 notebook, he drew an unrooted tree, which became a rooted tree in his 1859 book. An unrooted tree thus cannot be a picture of evolutionary history, although it can be an important step towards obtaining such a picture. It is, therefore, inappropriate to identify ‘groups’ of species (sometimes called clusters) on an unrooted tree [25,52] because only monophyletic groups (called clades) make any sense in an evolutionary context, these being all of the descendants of a common ancestor. Second, relationships among clades are equal, in the sense that each clade is the sister to some other clade and vice versa. Thus, clades cannot be ‘basal’ or ‘crown’ [53] because each single clade branches from some other single clade, rather than being a side-branch from a main stem. There is no main stem in an evolutionary tree but, instead, there is a series of branches leading to a series of twigs, even if some of the branches have more twigs than others. Furthermore, neither of the sisters in a pair represents the ancestor; instead, they share a common ancestor, which might not look like either of them. Third, characters change through time, so character states can be either ancestral (the original form) or derived (modified in some descendant). However, clades themselves cannot be either ancestral Figure 1. The number of species that are known (i.e. have been described) as a (‘primitive’, ‘lower’) or derived (‘advanced’, ‘higher’) because each percentage of the estimated total number of living species, for most of the major clade will have a combination of ancestral and derived character taxonomic groups. Note that this is a stripe density graph, in which each observation is represented by a horizontal stripe; the size of the stripes is uniform, states. There is no chain leading from ancestral species to derived so the data density is indicated by the apparent clustering of stripes. The eight species. Instead, each species (or group) is the sister to some other groups with <10% coverage are labelled. The data are pooled from Ref. [49] (for species (or group), with which it shares some characters inherited Prokaryota, Plantae and Metazoa) and from Ref. [11] (for all other groups). from their ancestors and from which it differs by some unique characters. Any taxonomic group that is interpreted to be ancestral is paraphyletic (i.e. does not contain all of the descendants from the have no well-known subsets, and so they are the worst- common ancestor) rather than monophyletic and, thus, has no known groups in terms of their biodiversity (Figure 1). The phylogenetic relevance. Apicomplexa is the largest of these groups and, con- sequently, they are the worst-known group, with 6000 which we can best arrange our knowledge of all aspects of named species but perhaps only 0.1% of the total number of the biological sciences.
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