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Family Tylenchidae (Nematoda): an Overview and Perspectives

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Family Tylenchidae (Nematoda): an Overview and Perspectives Organisms Diversity & Evolution (2019) 19:391–408 https://doi.org/10.1007/s13127-019-00404-4 ORIGINAL ARTICLE Family Tylenchidae (Nematoda): an overview and perspectives Xue Qing1 & Wim Bert1 Received: 7 February 2019 /Accepted: 11 May 2019 /Published online: 29 May 2019 # Gesellschaft für Biologische Systematik 2019 Abstract Nematodes in the Tylenchidae family are one of the most important soil-inhabiting species, yet little is known about this intriguing group. The present review examines newly collected samples of Tylenchidae from worldwide sources as well as slides from museum collections. Together with all available literature, detailed morphology among genera are summarized and com- pared, allowing us to explore the importance of each morphological character in a phylogenetic framework. An updated phylogeny inferred from concatenated 18S and 28S ribosomal RNA dataset is reconstructed; the results suggest that not all didelphic genera may be included in Tylenchidae. In fact, our analyses suggest Tylenchidae should be split into several families, although their phylogeny has not yet fully been resolved. Currently, the Tylenchidae family comprises 44 genera and 412 nominal species; however, diversity estimations for the group ranged from 2000 to 10,000 species, meaning that 75–95% of the species remains undiscovered. This is partially because the biased sampling in agro-ecosystems with most Tylenchidae may present in neglected habitats. Finally, we discussed current difficulties in morphology, taxonomy, and molecular phylogeny research of Tylenchidae and the need for multi-gene phylogeny or phylogenomic approaches to resolve the deep phylogeny in Tylenchidae. Keywords Nematode . Phylogeny . Taxonomy . Tylenchoidea . Tylenchomorpha Introduction their small body size and lack of clearly homologous charac- ters prevent us from deriving a consistent systematic frame- Tylenchidae is one of the most important soil-inhabiting nem- work. As a result, the delimitation of taxa in this group re- atode families (Andrássy 1981), with species diversity often mains poorly documented and highly uncertain (Bongers and contributing up to about 30% of the nematode community in Bongers 1998; Ferris and Bongers 2006; Yeates 2003). any given soil sample (Ferris and Bongers 2006; Yeates and Molecular phylogeny inferred from ribosomal RNA Bird 1994). As early diverging Tylenchomorpha sensu De Ley (rRNA) genes suggests that Tylenchidae is polyphyletic & Blaxter, 2002 (i.e., tylenchids with supposedly ancestral (Bert et al. 2008; Holterman et al. 2006; Subbotin et al. characters), they do not comprise economically important 2006). Although several recent studies have improved our plant-parasites (Bert et al. 2008; Luc et al. 1987; Siddiqi understanding of this family (Atighi et al. 2013; Pereira et al. 2000). Knowledge of their feeding habits remains limited de- 2017; Qing and Bert 2017;Qingetal.2016, 2017; Yaghoubi spite their abundance and high diversity. Yet, this information et al. 2016), they have focused only on specific groups, and is vital for understanding trophic interactions and their role on information on this topic remains largely scattered and disor- soil foodwebs, which is key to assess soil health. Furthermore, ganized. In this study, we examine 43 additional species new- ly collected from worldwide sources, as well as species al- ready archived in museum slides and published studies. The Electronic supplementary material The online version of this article goals of the present study are (a) to give an overview of the (https://doi.org/10.1007/s13127-019-00404-4) contains supplementary material, which is available to authorized users. variation of morphological characters in Tylenchidae, (b) to incorporate all currently available sequences and reconstruct * Xue Qing an updated phylogeny of Tylenchidae, (c) to offer a summary [email protected] of Tylenchidae diversity and ecology, and (d) to outline the problems and obstacles faced in such research and therefore 1 Nematology Research Unit, Department of Biology, Ghent provide suggestions for future studies focused on this nema- University, Ledeganckstraat 35, B-9000 Ghent, Belgium tode group. 392 Qing X., Bert W. Materials and methods empirical observations (Qiao et al. 2018;QingandBert2018; Qing et al. 2016, 2017, 2018). Sample collection and morphological analyses The morphological analysis was based on newly generated Results and discussion data and a literature review. A total of 43 species were collect- ed from 11 countries (Supplementary Table S1). Soil samples Brief review of historical and current classification were incubated for 48 h on plastic trays lined with paper towels, and nematodes were subsequently concentrated using The family Tylenchidae was originally proposed by Örley a sieve (25 μm opening). After removing water, nematodes (1880), and it contains tylenchids characterized by conoid- were fixed in formalin (4%, buffered to pH = 7), heated to 60– to filiform-shaped tails, non-overlapping pharynx, and short 80 °C, and consequently transferred to anhydrous glycerin for and delicate stylets. The list of genera for the family, according morphological analyses, following the protocol of Seinhorst to different authors, is summarized in Table 1. The main dis- (1962). Drawings from slides were prepared with a drawing pute regarding Tylenchidae classifications concerns the place- tube mounted on an Olympus BX51 DIC microscope ment of four didelphic genera (Antarctenchus, Atetylenchus, (Olympus Optical, Tokyo, Japan), equipped with a Nikon and Psilenchus) and the taxonomic ranking of subfamilies DS-FI2 camera (Nikon Corporation, Tokyo, Japan) for image Ecphyadophorinae and Tylodorinae sensu Geraert (2008). recording. The three didelphic genera are either considered within Morphological data from the literature were summarized Tylenchidae (Geraert 2008; Geraert and Raski 1987)oras on genus level, and relevant illustrations were edited using separated family Psilenchidae (subfamily Psilenchinae: Adobe Illustrator CS3 and Adobe Photoshop CS6 at the orig- Atetylenchus,andPsilenchus; subfamily Antarctenchine: inal scale. Antarctenchus) (Andrássy 2005; Siddiqi 2000). Ecphyadophorinae consists of nine genera (Chilenchus, Ecphyadophora, Ecphyadophoroidea, Epicharinema, Molecular phylogenetic analyses Lelenchus, Mitranema, Tenunemellus, Tremonema,and Ultratenella)(Geraert2008) or considered to be a separate The sequences used for phylogeny analyses are listed in family with eight genera (similar to that in the previous texts, Supplementary Table S2. Multiple sequence alignments were with the exception of Epicharinema)(Andrássy2005;Siddiqi built using the Q-INS-i algorithm as implemented in MAFFT 2000). Since no conclusive taxonomic assignment is possible v. 7.205 (Katoh and Standley 2013), and the different genes based on current available data, we use the most recent system (i.e., 28S and 18S rRNA) were concatenated using Geneious proposed by Geraert (2008) in this study. The pictorial glos- R6 (Biomatters; http://www.geneious.com). The best-fitting sary of terminology used in this study is given in substitution model GTR + I + G for both rRNAs was estimat- Supplementary Fig. S1. ed using AIC in jModelTest v. 2.1.2 (Darriba et al. 2012). Maximum likelihood (ML) analysis was performed with Morphology and their taxonomic significance 1000 bootstrap (BS) replicates under the GTRCAT model using RAxML 8.1.11 (Stamatakis et al. 2008). Bayesian in- Lip region ference (BI) was carried out with the GTR + I + G model using MrBayes 3.2.3 (Ronquist and Huelsenbeck 2003). Analyses Lip regions are usually round, but laterally elongated (dorso- were run for 5 × 106 generations, and Markov chains were ventrally flattened) in Malenchus, Lelenchus, Ecphyadophoroides, sampled every 100 generations. Burnin was arbitrarily chosen Epicharinema,andTenunemellus. Sensilla consist of six inner to represent 25% of the results. The ML and BI analyses were labial papillae + four outer labial papillae, but the former performed at the CIPRES Science Gateway (Miller et al. are not always visible. Amphidial apertures vary in their 2010). appearance, from pore to long slit. Amphidial foveas are considered taxonomically important at generic level (Qing Estimation of diversity and Bert 2017) and are mostly reduced, but they can be pouch-like in Malenchus, Lelenchus, Ecphyadophoroides, The unknown diversity of the family Tylenchidae was estimated and Tenunemellus. Currently, eight patterns are recog- based on the ratios-between-taxa method following Hawksworth nized, seven from Geraert and Raski (1987) and one (1991). The number of described Tylenchomorpha species was addedbyQingandBert(2018) (see the illustration of approximated based on Andrássy (1992) and Siddiqi (2000). The Fig.1inQingandBert(2018)). Siddiqi (2000)and ratio of Tylenchidae species to obligate plant-parasitic Andrássy (2005) rejected the lip pattern as being impor- Tylenchomorpha species number was estimated based on our tant, as it can vary intraspecifically. This view was also Family Tylenchidae (Nematoda): an overview and perspectives 393 Table 1 Comparison of the taxonomic content of Tylenchidae Authors Maggenti et al. (1987) Siddiqi (2000)Andrássy(2007) Geraert (2008) according to four widely used classifications Genera 33 genera 25 genera 29 genera 42 genera Subfamilies Atylenchinae, Boleodorinae, Boleodorinae, Atylenchinae, Boleodorinae, Duosulciinae, Duosulciinae, Boleodorinae, Tylenchinae, Tanzaniinae, Thadinae, Ecphyadorinae, Ecphyadorinae,
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