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Nematoda: Diplogastridae): Viviparous New Species with Precocious Gonad Development ∗ Matthias HERRMANN 1,Erikj.RAGSDALE 1,Natsumikanzaki 2 and Ralf J

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Nematoda: Diplogastridae): Viviparous New Species with Precocious Gonad Development ∗ Matthias HERRMANN 1,Erikj.RAGSDALE 1,Natsumikanzaki 2 and Ralf J Nematology 15 (2013) 1001-1020 brill.com/nemy Sudhausia aristotokia n. gen., n. sp. and S. crassa n.gen.,n.sp. (Nematoda: Diplogastridae): viviparous new species with precocious gonad development ∗ Matthias HERRMANN 1,ErikJ.RAGSDALE 1,NatsumiKANZAKI 2 and Ralf J. SOMMER 1, 1 Max Planck Institute for Developmental Biology, Department of Evolutionary Biology, Spemannstraße 37, Tübingen, Germany 2 Forest Pathology Laboratory, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan Received: 27 March 2013; revised: 9 May 2013 Accepted for publication: 9 May 2013; available online: 3 July 2013 Summary – Two new species of diplogastrid nematodes, Sudhausia aristotokia n. gen., n. sp. and S. crassa n. gen., n. sp., were isolated from dung beetles (Coleoptera: Scarabaeidae) in Ghana and South Africa, respectively. Sudhausia n. gen. is circumscribed by stomatal morphology, namely the presence of a tube-shaped gymnostom, a pair of conical subventral denticles in the metastegostom, and a disk-like telostegostom bearing minute conical denticles. Other characters distinguishing the new genus are the presence of a bursa in the male and a vulva lined anteriorly and posteriorly by columns of sac-like cells. The two new species, both of which are hermaphroditic, are distinguished from each other by spicule and gubernaculum morphology, male papillae arrangement, bursal shape, vaginal morphology, and phasmid position. A suite of unusual developmental traits that distinguishes Sudhausia n. spp. includes maturation of the gonad and development of juvenile progeny before moulting to adulthood, a two-fold increase in embryo size during development, and constitutive vivipary. A phylogeny inferred from 11 ribosomal protein-coding genes and a fragment of the small subunit rRNA gene show Sudhausia n. gen. to be divergent from other sequenced diplogastrid taxa, including those characterised by a tube-like stoma. The two new species represent useful new reference points for the study of feeding-structure evolution in Diplogastridae. Keywords – androdioecy, description, dung beetles, Ghana, hermaphrodite, molecular, morphology, morphometrics, new genus, new species, Onthophagus, phylogeny, Scarabaeidae, Scarabaeus, South Africa, stoma, taxonomy. The nematode family Diplogastridae Micoletzky, 1922 Given the diversity of feeding structures in diplo- currently includes 31 genera (Sudhaus & Fürst von gastrids (Fürst von Lieven & Sudhaus, 2000; Sudhaus & Lieven, 2003; Kanzaki et al., 2009, 2012a; Mayer et al., Fürst von Lieven, 2003), the isolation of new higher or- 2009; Fürst von Lieven et al., 2011; Susoy & Herrmann, der taxa in the family is particularly valuable for stud- 2012), many of which are associated with insects. Conse- ies of the evolution of form. In addition to the presence quently, intensive sampling of potential insect hosts has of detailed references for diplogastrid stomatal anatomy recently revealed diverse new taxa in the family (Kan- (Baldwin et al., 1997; Bumbarger et al., unpubl.), the es- zaki et al., 2009, 2012a). Scarab beetles (Coleoptera: tablished model system Pristionchus pacificus Sommer, Scarabaeidae) in particular are hosts to many diplogastrid Carta, Kim & Sternberg, 1996 allows genetic and develop- species, especially in Pristionchus Kreis, 1932 (Herrmann mental mechanistic studies of morphology (Bento et al., et al., 2006; Mayer et al., 2007, 2009; Rae et al., 2008; 2010; Sommer & McGaughran, 2013). The potential to Kanzaki et al., 2012a, 2013), but also in Diplogasteroi- extend studies in Pristionchus to other species of diplo- des de Man, 1912, Koerneria Meyl, 1960, Mononchoides gastrids, especially those amenable to laboratory culture, Rahm, 1928, Rhabditidoides Rahm, 1928, and Tylophar- is made more powerful by the discovery of new forms ynx de Man, 1876 (Mayer et al., 2009). to include in a comparative context. Here, we describe a * Corresponding author, e-mail: [email protected] © Koninklijke Brill NV, Leiden, 2013 DOI:10.1163/15685411-00002738 M. Herrmann et al. new genus of Diplogastridae, Sudhausia n. gen., based on SCANNING ELECTRON MICROSCOPY its unique stomatal morphology, sex-specific characters, and a suite of unusual developmental traits. Reflecting the Nematodes were prepared for scanning electron mi- frequent association of diplogastrids with scarab beetles, croscopy (SEM) by fixation in 2.5% glutaraldehyde in both of the new species, S. aristotokia n. gen., n. sp. and M9 buffer and then post-fixed with 1% osmium tetrox- S. crassa n. gen., n. sp., were recorded from dung beetles ide. After several rinses with water, samples were dehy- in Ghana and South Africa, respectively. drated through a graded ethanol series, followed by crit- ical point drying using carbon dioxide. Specimens were mounted on polylysine-coated cover slips, sputter-coated Materials and methods with 20 nm gold/palladium, and then imaged with a Hi- tachi S-800 field emission scanning electron microscope NEMATODE ISOLATION AND CULTIVATION operating at 20 kV. Sudhausia aristotokia n. gen., n. sp. was isolated from MOLECULAR CHARACTERISATION AND PHYLOGENY adult dung beetles as detailed for individual species below. Host beetles were dissected on a 2.0% agar plate, after For species diagnosis and phylogenetic analysis, we which the plate was kept at room temperature for several amplified and sequenced an approximately 500-bp frag- weeks. Nematodes proliferated on bacteria associated ment of the small subunit (SSU) rRNA gene of the two with the host beetle cadavers. Individuals were thereafter new species using the primers SSU18A (5-AAAGATTA transferred to nematode growth medium (NGM) agar AGCCATGCATG-3) and SSU9R (5-AGCTGGAATTA plates seeded with the original microbes from the beetle CCGCGGCTG-3)(Floydet al., 2002). Partial SSU rRNA carcass, and they have been since kept in laboratory sequences of S. aristotokia n. gen., n. sp. and S. crassa n. culture on this medium. gen., n. sp. have been deposited in the GenBank database under accession numbers KC831555 and KC831556, re- MORPHOLOGICAL OBSERVATION AND PREPARATION spectively. Additionally, we amplified and sequenced 11 OF TYPE MATERIAL ribosomal protein-coding genes for the two new species: rpl-2, rpl-6, rpl-9, rpl-10, rpl-14, rpl-23, rpl-35, rps- One- to two-week-old cultures of S. aristotokia n. 7, rps-14, rps-27 and rps-28. All information regarding gen., n. sp. and S. crassa n. gen., n. sp. provided mate- genes, primers and PCR conditions is given in Mayer et rial for morphological observation. Observations by light al. (2009). Except for rps-28, the sequence of which was microscopy (LM) and differential interference contrast less than 200 bp, all ribosomal protein gene sequences for (DIC) microscopy were conducted using live nematodes, S. aristotokia n. gen., n. sp. and S. crassa n. gen., n. sp. which were hand-picked from culture plates. Because of have been deposited in GenBank under accession num- the clarity and integrity of its morphology, live material bers KC831557-KC831566 and KC831567-KC831576, was used for morphometrics. For line drawings, speci- respectively. Phylogenetic analysis included species from mens were mounted into water on slides and then re- all diplogastrid genera for which homologous sequences laxed by applying gentle heat. For morphometrics, spec- have been published (Mayer et al., 2009; Kanzaki et al., imens were mounted on slides with pads of 5% noble 2012a). agar and 0.15% sodium azide and were additionally re- The concatenated dataset of ribosomal protein genes laxed by heat when necessary. To prepare type material, and the partial SSU rRNA gene was aligned using nematodes were isolated from type strain cultures, rinsed MUSCLE (Edgar, 2004), followed by manual alignment in distilled water to remove bacteria, heat-killed at 65°C, in MEGA5.10 (Tamura et al., 2011), which included fixed in TAF to a final concentration of 5% formalin and deletion of ambiguous alignment positions. The final 1.5% triethanolamine, and processed through a glycerin alignment comprised 5963 positions. The alignment was and ethanol series using Seinhorst’s method (see Hooper, partitioned into four subsets: one for the partial SSU 1986). Alternatively, some paratypes were fixed in 5% for- rRNA gene and three according to codon position for malin after heat killing at 65°C. Nomarski micrographs the concatenated set of ribosomal protein genes. Analyses were taken using a Zeiss Axio Imager Z.1 microscope by maximum likelihood (ML) and Bayesian inference, and a Spot RT-SE camera supported by the program Meta- as implemented in RAxML v.7.2.8 (Stamatakis, 2006) Morph v.7.1.3 (Molecular Devices). and MrBayes 3.2 (Ronquist et al., 2012), respectively, 1002 Nematology Sudhausia aristotokia n. gen., n. sp. and S. crassa n. gen., n. sp. were used to infer the phylogeny. Fifty independent runs posterior rim; and ii) a longer posterior region with cu- were performed for the ML analysis, in which trees were ticle refracting to give appearance of a rough texture. inferred under a general time reversible model with a Stegostom comprising: i) a transversely flat rim of cuti- gamma-shaped distribution of rates across sites. Bootstrap cle (pro-/mesostegostom) at anterior margin of muscular support was calculated by 1000 pseudoreplicates on the pharynx; ii) a cylindrical metastegostom bearing a move- most likely tree among all runs. Bayesian analyses were able dorsal tooth, dorsoventrally narrowed for its entire initiated with random starting trees and were
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