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Evolutionary Biology of Parasitic Platyhelminths: the Role of Molecular Phylogenetics D

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Evolutionary Biology of Parasitic Platyhelminths: the Role of Molecular Phylogenetics D Revmew Evolutionary Biology of Parasitic Platyhelminths: The Role of Molecular Phylogenetics D. Blair, A. Campos, M.R Cummings and J.R Laclette As our appreciation of the diversity within the flatworms systematic scheme and names of the major groups has grown, so too has our curiosity about the ways in provided in Ehlers 3,4 (Fig. in Box 1). which these varied creatures are related to one another. In Three rnain questions have emerged from the particular, the parasitic groups (trentatodes, cestodes attd literature. (1) Do the major groups of parasitic flat- monogeneans' have been the focus of enquiry. Llntil worms lie. Trernatoda (including Digenea and recently, morphohk~y, anatomy and lift" histories have pro- Aspidobothrea), Monogenea and Cestoda (including vided the raw data for building hypotheses on ivlationships. Gyrocotylidea, Amphilinidea and Eucestoda)l form a Now, ultrastructural evhtence, and most recently, mol- single clade? The name Neodermata was recent!v ecular &Tta front nucleic acid seqttences, have been brought given to this proposed clade ~. (2) How are these para- to beat" on the topic. Here, David Blair, Andrds Campos, sitic groups related to one another? (3) What are the Michael Cummings attd Juan Pedro Laclette discttss the relationships of the major parasitic groups to other ways in which molecular data, in particular, are helping tts flatworm taxa? recognize the various lineages of flatworms. Do the major parasitic groups form an exclusive The phylum Platyhelnlinthes (flatworms) is a large lineage? (>15000 species) and diverse one, and appears to be Members of the rnain parasitic groups differ con- an early diverging lineage within the Metazoa. Flat- siderablv from one another in structure, habits and worms show great diversity in anatomy, habitat, life life cycles. As a result, several proposals to explain history and size, varying from the 20m long euces- their origins assumed that they did not form a mono- tode Diphylh~bothrium latunt, to species barely visible phyletic group. For example, it has been suggested to the naked eye. They also exhibit considerable gen- that trematodes, monogeneans and cestodes all origi- etic diversity among 18S rRNA gene sequences when nated independently from parasitic rhabdocoelan compared to higher taxa of vertebrates~. The phylum ancestors '',7, or that the monogeneans, from which includes free-living, commensal, mutualist and para- de,~cencled tile cestodes, originated from a free-living sitic species, of which many are significant for medi- rhabdocoelan ancestor and had separate origins from cal and economic reasons. All parasitologists k~ow the trematodes". ot tile threat to human health posed by trematodes Ultrastructural studies were the first to plovide such as alembers of the genus St'hislos(una, or cestodes evidence contrary to such ar~pal~nents. All the major sucla as Echino('(~cc'lts granllloslts. Despite its impor- parasitic groups resemble one another in structural tance, many controversies exist concerning the sys- and dew.,Iopmental aspects of epidermal cilia, sensory tematics of the phylum and, in particular, the origin receptors, flame bulbs and sperm. In addition, in and interrelationships of the major parasitic groups. these taxa the epidermis of tile larva is replaced in tile The evolutionary history of flatworms is still uaclear adul[ by a syncitial 'l~eodernlis'J,~,", a feature that led because of the fragmentary information or, their mor- Ehters~ to propose tile name Neoderrnata for the phology, physiology and lift, cycles, and because group. Studies based on molecular data from the these soft-bodied worms have left few fossil remains. nuclear 18S rRNA gene also strongly support a single A robust phylogeny will also provide insights into origin for these major parasitic groups "-t2. the origins of parasitism in the phylum and the shared evolutionary history of parasitic flatworms Relationships among the main groups of Neodermata and their hostsL Two main clades are recognized within the Neo- In this review, we explore recent findings about dermata oil the basis of ultrastructure and aspects phylogenetic relationships in the flatworms, especially of ontogeny. The Trematoda (Aspidobothrea and Di- the parasitic o~rouF-.~s We emphasize conclusions drawn genea) forms one lineage, and the Cercomeromorphae from DNA sequence data (see Boxes 1,2) and focus on (Monogenea and all groups allied with tile Cestoda) a number of questions that have emerged from the the other. The Cercomeromorphae is characterized by literature. For consistency, we will mostly follow the common possession of a cercornere, ie. a posterior attachment structure bearing hooks that is present at some stage in the life cycle. David Blair is at the Department of Zoology, James Cool< Monophyletic Trematoda. On the basis of morpho- University, Townsville, Queensland 481 I, Australia. Andr6s Campos and Juan Pedro Laclette are at the Department of Immunology, logical and life cycle characteristics2.3,13-% the Aspido- Instib Jto de Investigaciones Blot, ~6dicas, Universidad Nacional bothrea (Fig. la) has been proposed as the sister Aut6noma de M6xico, A.P. 70228, M6xico 04510 D.F., M~xico. group of the digeneans. Molecular studies, using 18S Michael Cummings is at the Department of Botany and Plant rR',JA sequences, have also supported this view 9,u. Sciences, Univel~sityof California, Riverside, CA 92521-0124, USA. However, the possibility that Aspidobothrea is the Tel: +61 77 814322, fax: e61 77 251570, sister group to the remaining Neodermata has not e-mail: [email protected] been ruled out 1LI7. {.)I~ "~ 4758/96/$15.00 Parasitology Today, vol. 12, no. 2, 1996 Reviews Digenea. In the Digenea (Fig. lb), Box 1. Gene Regions Used to Infer Relationships most groupings at low levels There are several different classes of genes that can provide data about phyla- (species, genus) are widely accepted. genetic relationships. Nuclear ribosomal RNA genes, which encode structural Unfortunately, there is still consider- RNA of ribosomes, tend to occur in eukaryotes as a series of tandemly able dispute concerning the higher- repeated units, each contaming three coding regions (5.8S, -150bp; 18S, level (family, order) classification. ~2000bp; 28S, ~4500bp) separated by various spacers. The rate of evolution Information gleaned from morphol- differs both among and within these genes and spacers, providing infor- ogy (including ultrastructure) and mation that is useful at a range of divergence levels. The internal transcribed spacers, located between the 18S and 28S genes and separated by the 5.8S from life cycles has been the main- gene, are the least-conserved regions used m studies, to date, on flatworms. stay of digenean systematics 2. In the Mainly for historical reasons, the gene encoding the 18S subunit (the most view of some workers ~(',~s, the conserved of the ribosomal genes), has been widely used to study relation- amount of homoplasy in the exist- ships of Platyhelminthes (see Fig. b,:iow). A short 5S ribosomal RNA gene ing data sets is such as to render occurs elsewhere in the genome. Studies using this gene for phylogenet~c impossible the accurate reconstruc- inference have been reviewed and dismissed 3". tion of the phylogenetic history of One useful feature of ribosomal repeat uI~its is that they t,~nd to be 'hom- the trematodes. Such clairns l~,ave ogenized' within an individual and among individuals within a species or spurred molecular studies on the population; a process called 'concerted evolution'. As a result, intraspecific variation among ribosomal genes is very low compared to interspecific vari- group: currently, more rnolecular ation. A sequence from one individual should therefore be representative of data are available for Digenea than its species and sample sizes need not be large~.4s. for any other flatworm taxon (see Another source of phylogenetic information is the mitochondrial genome. Fig. in Box 1). This clonally inherited circular molecule usually encodes 37 genes, and is typi- The entire 18S rRNA gene cally less than 20000 bp long in animals 4". Mitochondrial genes often accumu- (1970bp) was evaluated as a source late changes at higher rates than the nuclear genome, and therefore data from of phylogenetic information within this genome are expected to be more useful for relatively recent divergences. the Digenea using sequences from Among the genes encoded by the mitochondrial genome are those for ribo- eight taxa m. Very little phylogenetic somal subunits, which are smaller than their nuclear counterparts and are information was found in the con- derived from the eubacterial ancestor of the mitochondrion. Nuclear protein coding genes have rarely been used in systematic studies served regions of the molecule, of Platyhehninthes (see Fig. belo,v). which make up over half of its length. Most information came from ,e- A the variable domains and especially O4 A A ,e- from the V4 domain 2", which com- o o o o o o o ~:. ¢G prises only about 16% of the mol- ¢5 ¢5 ¢5 e~ 6 6 0 ,- ¢5 o~ 6 d ecule. Data from this region provide N ~N ~ N d d g 6 g c~ ¢5 0; ¢5 c~ c~ (5 c~ d ~d g d o c5 c5 N c5 o c:f c:5 c5 o o ,-- strong support for a number of ei ~ e4 ,-: br familial groupings. For example, lepocreadiids and gyliauchenids are "O closely related to the exclusion of the paramphistomes despite the similar anatomy of the last two"L Although the V4 region is likely to be the target of many future O Z ,~ studies, it (and perhaps the 18S gene as a whole) does not seem to be informative about the earliest di- 1/ vergences among the digeneans. Rhabd0c0ela MonOg ~ neas'° a This is unfortunate because there has been lively debate on this topicN,'. ~. Several families have been proposed as the sister group to f the rest of the digeneans (reviewed I in Ref.
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