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Description of Three Pristionchus Species (Nematoda: Diplogastridae) from Japan That Form a Cryptic Species Complex with the Model Organism P

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Description of Three Pristionchus Species (Nematoda: Diplogastridae) from Japan That Form a Cryptic Species Complex with the Model Organism P Description of Three Pristionchus Species (Nematoda: Diplogastridae) from Japan that Form a Cryptic Species Complex with the Model Organism P. pacificus Author(s): Natsumi Kanzaki, Erik J. Ragsdale, Matthias Herrmann, Werner E. Mayer and Ralf J. Sommer Source: Zoological Science, 29(6):403-417. 2012. Published By: Zoological Society of Japan DOI: http://dx.doi.org/10.2108/zsj.29.403 URL: http://www.bioone.org/doi/full/10.2108/zsj.29.403 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. ZOOLOGICAL SCIENCE 29: 403–417 (2012) ¤ 2012 Zoological Society of Japan Description of Three Pristionchus Species (Nematoda: Diplogastridae) from Japan that Form a Cryptic Species Complex with the Model Organism P. pacificus Natsumi Kanzaki1‡, Erik J. Ragsdale2‡, Matthias Herrmann2‡, Werner E. Mayer2†‡, and Ralf J. Sommer2* 1Forest Pathology Laboratory, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan 2Max Planck Institute for Developmental Biology, Department of Evolutionary Biology, Spemannstraße 37, 72076 Tübingen, Germany Three new species of Pristionchus (P. exspectatus, P. arcanus, and P. japonicus) are described from Japan. They are morphologically similar, with P. e x s p e c t a t u s and P. arcanus being almost indistin- guishable from the model organism P. p a c i f i c u s . Reproductive isolation, namely the inability to pro- duce interfertile F1 hybrids, separates all species pairs in the species complex. Additionally, all three new species are distinguished from P. p a c i f i c u s Sommer, Carta, Kim, and Sternberg, 1996 by having a gonochoristic instead of hermaphroditic mode of reproduction. In addition to its repro- ductive isolation, P. japonicus is distinct from other Pristionchus species by its arrangement of gen- ital papillae. All species in the complex are separated from each other by molecular sequence divergence, as indicated by analysis of 27 nuclear protein-coding genes and unique sequences of the small subunit ribosomal RNA gene. The identification of a species complex that includes P. pacificus is invaluable for studies of population genetics, speciation, and macroevolution, particu- larly the evolution of hermaphroditism in the genus. Key words: hermaphroditism, insects, morphology, phylogeny, reproductive isolation, species concepts, taxonomy et al., 2005; Schlager et al., 2006; Tian et al., 2008), and INTRODUCTION DNA-mediated transformation (Schlager et al., 2009). The The nematode Pristionchus pacificus Sommer et al., isolation of hundreds of worldwide strains of P. pacificus 1996 is a well-established model system for evolutionary (Herrmann et al., 2010) and the support of a robust phylo- developmental biology (Sommer, 2009), drawing strength as genetic infrastructure (Mayer et al., 2007, 2009) now offer a satellite model to that of Caenorhabditis elegans (Maupas, the potential to study the evolution of mechanistic traits 1899) Dougherty, 1953. A suite of analytical tools available within and among species. Invaluable for linking processes for P. pacificus enables comparative, mechanistic studies of of micro- and macroevolution is knowledge of closely related genetics (e.g., Eizinger and Sommer, 1997; Zauner and species, although those close enough to be considered sis- Sommer, 2007; Rudel et al., 2008) and include an extensive ter species to either C. elegans or P. pacificus have been genetic linkage map and physical map (Srinivasan et al., thus far unknown. To address this gap, we report and 2002, 2003), a completely sequenced genome (Dieterich et describe three new species of Pristionchus Kreis, 1932 from al., 2008), forward and reverse genetics capabilities (Zheng Japan that form a species complex with P. pacificus. The genus Pristionchus, of the family Diplogastridae * Corresponding author. Tel. : +49-7071-601441; Micoletzky, 1922, is distributed globally and is particularly Fax : +49-7071-601498; E-mail: [email protected] well known throughout the Holarctic ecozone. Pristionchus † The other authors would like to dedicate this work to Dr. Mayer, species have been often collected from soil and decaying who has passed away since the submission of this article. We are organic matter (Sudhaus and Fürst von Lieven, 2003), grateful for his contributions to the molecular systematics of although many species are known to be associates of Diplogastridae, which have laid the foundation for comparative insects, especially beetles (Völk, 1950; Fedorko and studies in the Pristionchus system. Stanuszek, 1971; Herrmann et al., 2006a, b, 2007; Kanzaki ‡ Author contributions: NK, EJR, MH, and WEM contributed equally et al., 2011). Directly targeting insects for nematode sam- to this study. NK, EJR: morphological observation and writing of pling has thus led to a boom in the number of Pristionchus manuscript; MH: morphological observation and biological experi- strains recovered (Herrmann et al., 2006a, 2010). Repro- ments; WEM: molecular phylogenetic analysis; RJS: biological ductive biology within Pristionchus is diverse, as hermaph- experiments and writing of manuscript. Supplemental material for this article is available online. roditism has arisen independently at least five times in the doi:10.2108/zsj.29.403 genus (Mayer et al., 2007). Thus with respect to their trac- 404 N. Kanzaki et al. tability in the laboratory, Pristionchus nematodes constitute samples were dehydrated through a graded ethanol series, followed a prime model for the evolution of sex strategies. The dis- by critical point drying from carbon dioxide. Specimens were covery of gonochoristic species close to P. pacificus would mounted on polylysine-coated coverslips, sputter-coated with 20 nm therefore make basic genetics studies in this area feasible. gold/palladium, and then imaged with a Hitachi S-800 field emission Despite increasing research on the biology of Pristionchus scanning electron microscope operating at 20 kV. nematodes, several problems beset taxonomic description Molecular characterization and phylogenetic analysis of the genus. Such problems include insufficient typological To diagnose individual species, we amplified and sequenced characters, intraspecific variation in qualitative and quantita- an 830-bp fragment of the SSU rRNA gene. For phylogenetic anal- tive characters, and many species with unclear descriptions. ysis we employed 27 ribosomal protein genes, which were originally Herrmann et al. (2006b) pointed out these problems and dis- developed as marker loci based on their consistent presence in tinguished several cryptic species from closely related nom- EST libraries of various species (see Mayer et al., 2007). The data- inal species based on molecular sequence divergence and set of ribosomal protein genes comprised a total of 10,971 aligned phylogenetic hypotheses. On this evidence they described coding nucleotides. Genes included in analysis were: rpl-1, rpl-2, four species: P. marianneae Herrmann et al., 2006b, P. rpl-10, rpl-14, rpl-16, rpl-23, rpl-26, rpl-27, rpl-27a, rpl-28, rpl-29, pauli Herrmann et al., 2006b, P. americanus Herrmann et rpl-30, rpl-31, rpl-32, rpl-34, rpl-35, rpl-38, rpl-39, rps-1, rps-8, rps- 14, rps-20, rps-21, rps-24, rps-25, rps-27, and rps-28. Ribosomal al., 2006b and P. pseudaerivorus Herrmann et al., 2006b. protein genes sequenced for P. exspectatus and P. arcanus have Currently, the genus Pristionchus contains 31 recognized been deposited in GenBank under accession numbers JQ399909– species (Sudhaus and Fürst von Lieven, 2003; Herrmann et JQ399956. Ribosomal protein gene sequences for P. japonicus al., 2006b) as well as many undescribed species that have were previously published (Mayer et al., 2007). All information been referred to in recently published works under tentative regarding genes, primers, and PCR conditions is given in Mayer et species codes (Mayer et al., 2007, 2009). In the present study, al. (2007). New sequences generated in the present study are those three new Pristionchus species, including two morphologically for P. exspectatus and P. arcanus, and P. japonicus. All other almost indistinguishable species (= cryptic species), are sequences in analysis were published by Mayer et al. (2007) and described based on their morphology, molecular sequences, thus previously available in the GenBank database. Species selected inferred phylogenetic separation, and biological characters. for analysis include three undescribed species isolated from Japan (Pristionchus sp. 10, Pristionchus sp. 14, and Pristionchus sp. 15) as MATERIALS AND METHODS well as all nominal, morphologically characterized Pristionchus spe- cies with available
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