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Bert Et Al 2008 MPE Tylenchina Phylogeny and Gonoduct Evolution -1.Pdf Molecular Phylogenetics and Evolution 48 (2008) 728–744 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Molecular phylogeny of the Tylenchina and evolution of the female gonoduct (Nematoda: Rhabditida) Wim Bert a,*, Frederik Leliaert b, Andy R. Vierstraete c, Jacques R. Vanfleteren c, Gaetan Borgonie a a Nematology Section, Department of Biology, Ghent University, Ledeganckstraat 35, 9000 Ghent, Belgium b Phycology Research Group and Centre for Molecular Phylogenetics and Evolution, Department of Biology, Ghent University, Krijgslaan 281 S8, 9000 Ghent, Belgium c Research Group Aging Physiology and Molecular Evolution, Department of Biology, Ghent University, Ledeganckstraat 35, 9000 Ghent, Belgium article info abstract Article history: Tylenchina are a morphologically and functionally diverse group of nematode species that range from Received 15 December 2007 free-living bacteriovores, over transitory grazing root-hair feeders to highly specialized plant-parasites Revised 31 March 2008 with complex host associations. We performed phylogenetic analyses of small subunit rDNA sequences Accepted 1 April 2008 from 97 species including an analysis that account for the RNA secondary structure in the models of evo- Available online 14 April 2008 lution. The present study confirms the sister relationship of the bacteriovore Cephalobidae with the pre- dominantly plant-parasitic Tylenchomorpha. All analyses appoint the fungal-feeding Aphelenchidae and Keywords: Aphelenchoididae as being polyphyletic but the morphology based hypothesis of their monophyly could Ancestral state reconstruction not be significantly rejected. Within the Tylenchomorpha, the families that exclusively parasitize higher Bayesian inference Doublet model plants are joined in a single clade. However, only the monophyletic position of the (super)families Hopl- Feeding type olaimidae and Criconematoidea were supported; Anguinidae, Tylenchidae, Belonolaimidae and Pratylen- Gonad chidae appeared to be paraphyletic or polyphyletic. Parsimony and likelihood ancestral state Long branch attraction reconstruction revealed that burrowing endoparasitism and sedentary endoparasitism each evolved, Plant-parasitic nematodes respectively, at least six and at least three times independently, mostly from migratory ectoparasitic Ribosomal DNA ancestors. Only root-knot nematodes have evolved from burrowing endoparasitic nematodes. Traditional Secondary structure model classifications are partially misled by this convergent evolution of feeding type and associated morphol- Tylenchida ogy. Contrastingly, mapping attributes of the gonoduct cellular architecture, including newly obtained data of 18 species belonging to the Aphelenchoidea, Criconematoidea, Anguinidae and Panagrolaimidae, revealed a broad congruence of the gonoduct characters and the molecular phylogenetic hypothesis. Yet, the presence of an offset spermatheca and proliferation of uterus cells has evolved multiple times, the latter associated with derived endoparasitic feeding specialization and resulting reproduction mode. Ancestral state reconstruction further revealed that the gonoduct of the morphologically and ecologically dissimilar tylenchid and cephalobid nematodes evolved from a common ancestor. Ó 2008 Elsevier Inc. All rights reserved. 1. Introduction spread opportunists, but also numerous specialists of sandy soils and extreme temperatures. In desert and mountain soils, Cepha- Nematodes of the suborder Tylenchina sensu De Ley and Blaxter lobomorpha may constitute more than half of the total nematode (2002) include an ecologically and morphologically diverse array of density (De Ley, 1992). Drilonematomorpha are relatively rare species that range from soil dwelling bacteriovores to highly spec- and are mainly parasites of earthworms. The Tylenchomorpha, ialised plant-parasites. De Ley and Blaxter (2002) recognised four the most intensively investigated infraorder within the Tylenchina, infraorders in Tylenchina: Panagrolaimorpha, Cephalobomorpha, comprises the largest and economically most important group of Drilonematomorpha and Tylenchomorpha. Panagrolaimorpha in- plant-parasitic nematodes. They have exploited all plant organs clude insect pathogens (Steinernematidae), amphibian–reptilian including flowers and seeds, but they attack mostly roots. The evo- parasites (Rhabdiasidae), parasites of vertebrates (Strongyloididae) lution of plant-parasitic Tylenchomorpha is of particular interest and highly opportunistic bacteriovores notable to survive in ex- because associations range from transitory grazing by root-hair treme environments, such as vinegar (Panagrolaimidae). Cephalob- feeders to the highly complex host-pathogen interactions of gall- omorpha are bacteriovores, not closely associated with animal inducing nematodes and their hosts. Non-plant-parasitic Tylench- hosts or arthropod vectors, and include some of the most wide- omorpha feed on fungi, algae, lichens, mosses, insects, mites, leeches or frogs (Siddiqi, 2000). However, the evolution of this * Corresponding author. Fax: +32 92645344. diversity of complex feeding traits is not yet fully understood (Sub- E-mail address: [email protected] (W. Bert). botin et al., 2006). 1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.04.011 W. Bert et al. / Molecular Phylogenetics and Evolution 48 (2008) 728–744 729 Despite their remarkably diverse ecological traits, Tylenchina ex- tides (e.g. Savill et al., 2001; Murray et al., 2005; Telford et al., hibit relatively simple morphologies and superficial similarities may 2005), although other studies have only shown minor effects of dif- be the result of convergent evolution. Hence, the limited number of ferent evolutionary models in phylogenetic reconstruction (Russo characters and especially the lack of objective criteria for assessing et al., 1996; Leliaert et al., 2007). homology of these characters has hampered the reconstruction of Nematodes are very attractive in evolutionary biology given the their phylogeny. Furthermore, the ontogeny of nematodes is poorly species richness of the phylum and the easiness with which several understood and there is a lack of an informative fossil record (e.g. of these species can be cultured under laboratory conditions (Som- Poinar, 2003). Such difficulties have led to the erection of multiple, mer, 2005). The reproductive system is herein of crucial impor- at least partially conflicting classifications. Traditional long-stand- tance for the study of fundamental problems in cell biology and ing classifications have unified (e.g. Andrássy, 1976) the parasitic developmental biology (Hubbard and Greenstein, 2000). Hence, strongyloids and steinernematids together with the bacteriovore the somatic gonad or gonoduct is intensively studied in the model cephalobs and panagrolaims within the predominantly bacteriovor- organism Caenorhabditis elegans (Kimble and Hirsh, 1979; Hubbard ous order Rhabditida, while the mainly plant-parasitic aphelenchs and Greenstein, 2000) and the satellite model organism Pristion- and tylenchs were considered as a separate order Tylenchida. How- chus pacificus (Rudel et al., 2005). However, multiple species com- ever, major parasitic groups were downgraded by De Ley and Blaxter parisons of detailed gonoduct characteristics are limited to vulval (2002) in their hierarchical position to a level which conforms better development analysis (e.g. Felix et al., 2000). Thus, data on the to their phylogenetic history than to their previously anthropocen- reproductive structure that cover an adequate part of the Tylenchi- trically determined position. In this new classification the morpho- na are largely limited to fragmentised light-microscopic data. The logically dissimilar panagrolaims, steinernematids, strongyloids, reproductive system is a complex organ composed of both somatic tylenchs and cephalobs were included in a single suborder Tylenchi- and germ line tissues and exhibits a variation in form (Chitwood na because of moderate support of their common origin in small sub- and Chitwood, 1950), and its cellular architecture appears to be unit (SSU) rDNA inferred phylogenies. This support is affirmed in stable for a certain species (Geraert, 1983). Whereas in rhabditid recent phylogenetic analyses (Holterman et al., 2006; Meldal et al., nematodes the gonoduct structure varies significantly across gen- 2007), although, a phylogeny based on large subunit (LSU) rDNA era (Geraert et al., 1980), the oviduct and uterus structure in analysis rejects inclusion of Steinernema in Tylenchina (Nadler Tylenchomorpha is more conserved. The number and spatial et al., 2006a). arrangement of spermatheca cells have been regarded as valuable Holterman et al. (2006), Meldal et al. (2007) produced phylum- characters to differentiate genera or species in the latter group wide SSU rDNA phylogenies and their identification of the major (Geraert, 1983; Bert et al., 2002, 2003, 2006). Typically the mainly clades is based on a wider sampling compared to the first molecu- plant-parasitic Tylenchomorpha have a mono- or didelphic repro- lar phylogenetic framework of the phylum Nematoda (Blaxter ductive system with an oviduct comprising two rows of four cells, et al., 1998). Within Tylenchina, LSU rDNA sequences have been a distinct spermatheca comprising 10–20 cells, and a uterus com- used to infer relationships among Cephalobomorpha and Panagro- posed of mostly regular rows
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