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The Evolution of Parasitism in Nematoda

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The Evolution of Parasitism in Nematoda SUPPLEMENT ARTICLE S26 The evolution of parasitism in Nematoda MARK BLAXTER* and GEORGIOS KOUTSOVOULOS Institute of Evolutionary Biology, The University of Edinburgh, Edinburgh EH9 3JT, UK (Received 19 February 2014; revised 16 April 2014; accepted 16 April 2014; first published online 25 June 2014) SUMMARY Nematodes are abundant and diverse, and include many parasitic species. Molecular phylogenetic analyses have shown that parasitism of plants and animals has arisen at least 15 times independently. Extant nematode species also display lifestyles that are proposed to be on the evolutionary trajectory to parasitism. Recent advances have permitted the determination of the genomes and transcriptomes of many nematode species. These new data can be used to further resolve the phylogeny of Nematoda, and identify possible genetic patterns associated with parasitism. Plant-parasitic nematode genomes show evidence of horizontal gene transfer from other members of the rhizosphere, and these genes play important roles in the parasite-host interface. Similar horizontal transfer is not evident in animal parasitic groups. Many nematodes have bacterial symbionts that can be essential for survival. Horizontal transfer from symbionts to the nematode is also common, but its biological importance is unclear. Over 100 nematode species are currently targeted for sequencing, and these data will yield important insights into the biology and evolutionary history of parasitism. It is important that these new technologies are also applied to free-living taxa, so that the pre-parasitic ground state can be inferred, and the novelties associated with parasitism isolated. Key words: Nematoda, nematodes, parasitism, evolution, genome, symbiont, Wolbachia, phylogeny, horizontal gene transfer. THE DIVERSITY OF THE NEMATODA medical and veterinary science. In this paper we discuss the changes in our understanding of the Nematoda is an ancient and biologically diverse diversity and relationships of nematodes, and of the phylum of moulting animals. They range in size biology of their parasitic habits, that have been from 0·2 mm to over 6 m, and can be found in most brought about by study of their genes and, increas- habitats, including within and on host animals and ingly, genomes. plants (Blaxter and Denver, 2012). In many marine Nematoda are part of Ecdysozoa, a superphylum and terrestrial sediments they are the most abundant of animals first defined through analyses of mole- group in terms of individuals (Platonova and Gal’tsova, cular markers (Aguinaldo et al. 1997). Support for 1976), and while only approximately 23000 species Ecdysozoa as distinct from other groupings of proto- have been described (J. Hallan, unpublished; https:// stome taxa is less strong from analyses of morpho- insects.tamu.edu/research/collection/hallan/), the true logical characters (Nielsen, 2001). Ecdysozoan phyla species-level diversity may be 1 million or more are characterized by the presence of a cuticle that is (Lambshead, 1993). Most terrestrial plants and larger periodically moulted during the life cycle, though the animals are associated with at least one species of specifics of the molecular nature of the cuticle and the parasitic nematode, and most of the human popu- orchestration of ecdysis differ between phyla. Other lation experiences nematode parasitism during their shared features adduced as evidence of relatedness lives (with perhaps one quarter to one third of the between these phyla include an absence of cilia in global population infected at any time). Estimates of adults, and in many members the presence of a the number of species of parasitic nematode per host triradiate pharynx. The Ecdysozoa in turn comprises suggest that there may be of the order of 25000 two groups, the Panarthropoda (phyla Tardigrada, nematode parasites just of vertebrates, most of which Onychophora and Arthropoda) and Cycloneuralia remain undescribed (Dobson et al. 2008). Nematodes (Nematoda, Nematomorpha, Priapulida, Kinorhyncha are thus important regulators of plant and animal and Loricifera). Within Cycloneuralia, which may be production. Understanding the evolutionary origins paraphyletic with respect to Panarthropoda, Nematoda of plant and animal parasitism, and the mechanisms are consistently placed as sisters to Nematomorpha in by which parasites locate and invade their hosts, morphological and molecular analyses (Schmidt- avoid host immunity, and acquire nutrition, are Rhaesa, 1997; Dunn et al. 2008). important goals for not only basic, but also for Nematomorpha are a fascinating group of obligate * Corresponding author: The Ashworth Laboratories, parasites of terrestrial (Gordioidea) and marine The King’s Buildings, Edinburgh EH9 3JT, UK. (Nectonematoidea) arthropods. These ‘horsehair E-mail: [email protected]. worms’ have a parasitoid life cycle, with the larval Parasitology (2015), 142, S26–S39. © Cambridge University Press 2014. The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution licence http://creativecommons.org/licenses/by/3.0/ doi:10.1017/S0031182014000791 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 24 Sep 2021 at 02:44:31, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182014000791 The evolution of parasitism in Nematoda S27 Ecosystem and Origins of Genomes Genomes Percentage of A Rhabditina Lifecycle strategy Parasitism Published Ongoing named species Rhabditomorpha 1* 1,2* V Bunonematomorpha 7 >30 13 Diplogasteromorpha 2* Brevibuccidae Tylenchina Drilonematomorpha 3 Panagrolaimomorpha 10 4 3 Rhabditida IV Cephalobomorpha 5 >40 17 10, 11, 12 11 Tylenchomorpha 5* 1* 12 Myolaimina Ascaridomorpha Spiruromorpha Spirurina Rhigonematomorpha 6 5 15 26 Oxyuridomorpha 7 4 III Gnathostomatomorpha Dracunculoidea Teratocephalidae 7 Plectida Araeolaimida 0 3 15 5bc 8 Chromadoria Monhysterida Desmodorida Chromadorida Enoplinae (part) Anticomidae Leptosomatidae Anoplostomatidae Oncholaimina Enoplida Oxystominidae Tripyloididae Trefusiida Enoplia Ironina (part) 9 0 1 21 II Alaimina 1 Campydorina Tripylina Tobrilina (part) Prismatolaimoidea Triplonchida Diptherophorina 2 Trichinellida 5 Dorylaimia I Dioctophymatida Mononchida 2 2 7 Mermithida 10 Dorylaimida 3* 19 ~100 terrestrial plant parasite terrestrial/freshwater vertebrate parasite invertebrate parasite freshwater invertebrate association marine microbivore or predator Caenorhabditis briggsae B Caenorhabditis elegans Rhabditomorpha Caenorhabditis angraria Haemonchus contortus V Pristionchus pacificus Diplogasteromorpha Meloidogyne incognita Meloidogyne hapla Bursaphelenchus xylophilus Tylenchomorpha IV Pseudaphelenchus vindai Strongyloides ratti Panagrolaimomorpha Dirofilaria immitis Onchocerca ochengi Litomosoides sigmodontis Loa loa Spiruromorpha Brugia malayi C Wuchereria bancrofti III Ascaris suum Ascaridomorpha Anguillicoloides crassus Dracunculoidea Laxus oneistus Chromadorida Prionchulus punctatus Mononchida Romanomermis culicivorax Mermithida I Trichinella spiralis Trichinellida II Enoplus brevis Enoplinae Milnesium tardigradum Tetranychus urticae Outgroup Drosophila melanogaster 0.1 Bombyx mori species Fig. 1. The phylogenetic structure of the Nematoda and the origins of parasitism (A) A cartoon of the phylogenetic structure of the Nematoda, based on nuclear small subunit ribosomal RNA analyses and interpretation of taxon relationships derived from morphology (De Ley and Blaxter, 2004; Blaxter and Denver, 2012). Taxon systematic Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.58, on 24 Sep 2021 at 02:44:31, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0031182014000791 Mark Blaxter and Georgios Koutsovoulos S28 stages residing within the body cavities of their 2002, 2004). In nSSU analyses the branching order of arthropod hosts, which they kill when they emerge. these three groups is unresolved, though there are The adult sexual stages are free-living in pelagic hints that Enoplia may be the earliest-branching of (Nectonematoidea) or sediment (Gordioidea) habi- the three (van Megen et al. 2009; Blaxter et al. 2014). tats. Infection of the next host is by ingestion of eggs, The inability of nSSU to robustly distinguish the often glued to vegetation eaten by the hosts (Hanelt branching order and thus the root of the phylum is and Janovy, 1999). The generalized life cycle of due to lack of strong signal, exacerbated by the nematomorphs is very similar to that of mermithid phylogenetic distance to the nearest outgroup taxa nematodes, which also have marine and terrestrial (other Ecdysozoa, which likely last shared a common members, and which also infect their hosts as larvae ancestor well before the Cambrian, over 540 My ago). but have free-living adult stages. The placement of It is generally argued that Nematoda has a marine a phylum wherein all members are parasites as sister origin (see Fig. 1A). The Enoplia are largely marine, to all of Nematoda raises the interesting question of and mostly free-living. They are the commonest whether the ancestor to all nematodes was a parasite nematodes in marine sediments, and dominate deep- (with biology similar to nematomorphs or mer- sea ecosystems where they feed on diatoms and mithids), and that the extant free-living groups in marine algae. Members of Enoplia are also found in
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