Erik J. Ragsdale

A phylogenetic framework for root lesion nematodes of the genus Pratylenchus (Nematoda): Evidence from 18S and D2-D3 expansion segments of 28S ribosomal RNA genes and morphological characters.

The root lesion nematodes of the genus Pratylenchus Filipjev, 1936 are migratory endoparasites of plant roots, considered among the most widespread and important nematode parasites in a variety of crops. We obtained gene sequences from the D2 and D3 expansion segments of 28S rRNA partial and 18S rRNA from 31 populations belonging to 11 valid and two unidentified species of root lesion nematodes and five outgroup taxa. These datasets were analyzed using maximum parsimony and Bayesian inference. The alignments were generated using the secondary structure models for these molecules and analyzed with Bayesian inference under the standard models and the complex model, considering helices under the doublet model and loops and bulges under the general time reversible model. The phylogenetic informativeness of morphological characters is tested by reconstruction of their histories on rRNA based trees using parallel parsimony and Bayesian approaches. Phylogenetic and sequence analyses of the 28S D2-D3 dataset with 145 accessions for 28 species and 18S dataset with 68 accessions for 15 species confirmed among large numbers of geographical diverse isolates that most classical morphospecies are monophyletic. Phylogenetic analyses revealed at least six distinct major clades of examined Pratylenchus species and these clades are generally congruent with those defined by characters derived from lip patterns, numbers of lip annules, and spermatheca shape. Morphological results suggest the need for sophisticated character discovery and analysis for morphology based phylogenetics in nematodes.

A Developmental Switch Coupled to the Evolution of Plasticity Acts through a Sulfatase

Developmental plasticity has been suggested to facilitate phenotypic diversity, but the molecular mechanisms underlying this relationship are little understood. We analyzed a feeding dimorphism in Pristionchus nematodes whereby one of two alternative adult mouth forms is executed after an irreversible developmental decision. By integrating developmental genetics with functional tests in phenotypically divergent populations and species, we identified a regulator of plasticity, eud-1, that acts in a developmental switch. eud-1 mutations eliminate one mouth form, whereas overexpression of eud-1 fixes it. EUD-1 is a sulfatase that acts dosage dependently, is necessary and sufficient to control the sexual dimorphism of feeding forms, and has a conserved function in Pristionchus evolution. It is epistatic to known signaling cascades and results from lineage-specific gene duplications. EUD-1 thus executes a developmental switch for morphological plasticity in the adult stage, showing that regulatory pathways can evolve by terminal addition of new genes.

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

Three new species of Pristionchus (P. exspectatus, P. arcanus, and P. japonicus) are described from Japan. They are morphologically similar, with P. exspectatus and P. arcanus being almost indistinguishable from the model organism P. pacificus. Reproductive isolation, namely the inability to produce interfertile F1 hybrids, separates all species pairs in the species complex. Additionally, all three new species are distinguished from P. pacificus Sommer, Carta, Kim, and Sternberg, 1996 by having a gonochoristic instead of hermaphroditic mode of reproduction. In addition to its reproductive isolation, P. japonicus is distinct from other Pristionchus species by its arrangement of genital 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, particularly the evolution of hermaphroditism in the genus.

Complex Small-Molecule Architectures Regulate Phenotypic Plasticity in a Nematode†

Chemistry the worms way: The nematode Pristionchus pacificus constructs elaborate small molecules from modified building blocks of primary metabolism, including an unusual xylopyranose-based nucleoside (see scheme). These compounds act as signaling molecules to control adult phenotypic plasticity and dauer development and provide examples of modular generation of structural diversity in metazoans.

Rapid diversification associated with a macroevolutionary pulse of developmental plasticity

Developmental plasticity has been proposed to facilitate phenotypic diversification in plants and animals, but the macroevolutionary potential of plastic traits remains to be objectively tested. We studied the evolution of feeding structures in a group of 90 nematodes, including Caenorhabditis elegans, some species of which have evolved a mouthpart polyphenism, moveable teeth, and predatory feeding. Comparative analyses of shape and form, using geometric morphometrics, and of structural complexity revealed a rapid process of diversification associated with developmental plasticity. First, dimorphism was associated with a sharp increase in complexity and elevated evolutionary rates, represented by a radiation of feeding-forms with structural novelties. Second, the subsequent assimilation of a single phenotype coincided with a decrease in mouthpart complexity but an even stronger increase in evolutionary rates. Our results suggest that a macroevolutionary ‘pulse’ of plasticity promotes novelties and, even after the secondary fixation of phenotypes, permits sustained rapid exploration of morphospace. DOI: http://dx.doi.org/10.7554/eLife.05463.001

Feeding plasticity in the nematode Pristionchus pacificus is influenced by sex and social context and is linked to developmental speed.

The increasing evidence for a role of developmental plasticity in evolution offers exciting prospects for testing interactions between ecological and developmental genetic processes. Recent advances with the model organism Pristionchus pacificus have provided inroads to a mechanistic understanding of a developmental plasticity. The developmental plasticity of P. pacificus comprises two discontinuous adult mouth‐forms, a stenostomatous (“narrow mouthed”) and a eurystomatous (“wide mouthed”) form, the latter of which is structurally more complex and associated with predatory feeding. Both forms are consistently present in populations, but fundamental properties guiding fluctuations in their appearance have been poorly understood. Here, we provide a systematic characterization of the mouth plasticity in P. pacificus, quantifying a strong sexual dimorphism and revealing that, in an inbred genetic background, maternal phenotype is linked to that of male offspring. Furthermore, cues from conspecifics influenced the developmental decision in juvenile nematodes. Separating individuals from a population resulted in a lower eurystomatous frequency, which decreased incrementally with earlier isolation. Finally, the time to the reproductively mature stage was, in the presence of an abundant bacterial food supply, less for stenostomatous than for eurystomatous individuals, suggesting the potential for a fitness trade‐off between developmental time and breadth of diet. This study provides a baseline understanding of the mouth dimorphism in P. pacificus as a necessary reference point for comparative analysis.

Large-scale diversification without genetic isolation in nematode symbionts of figs

A polyphenism discovered to consist of five discrete morphotypes shows that extreme diversification is possible within single species. Diversification is commonly understood to be the divergence of phenotypes accompanying that of lineages. In contrast, alternative phenotypes arising from a single genotype are almost exclusively limited to dimorphism in nature. We report a remarkable case of macroevolutionary-scale diversification without genetic divergence. Upon colonizing the island-like microecosystem of individual figs, symbiotic nematodes of the genus Pristionchus accumulated a polyphenism with up to five discrete adult morphotypes per species. By integrating laboratory and field experiments with extensive genotyping of individuals, including the analysis of 49 genomes from a single species, we show that rapid filling of potential ecological niches is possible without diversifying selection on genotypes. This uncoupling of morphological diversification and speciation in fig-associated nematodes has resulted from a remarkable expansion of discontinuous developmental plasticity.

Adaptive value of a predatory mouth- form in a dimorphic nematode

Polyphenisms can be adaptations to environments that are heterogeneous in space and time, but to persist they require conditional-specific advantages. The nematode Pristionchus pacificus is a facultative predator that displays an evolutionarily conserved polyphenism of its mouthparts. During development, P. pacificus irreversibly executes either a eurystomatous (Eu) or stenostomatous (St) mouth-form, which differ in the shape and number of movable teeth. The Eu form, which has an additional tooth, is more complex than the St form and is thus more highly derived relative to species lacking teeth. Here, we investigate a putative fitness trade-off for the alternative feeding-structures of P. pacificus. We show that the complex Eu form confers a greater ability to kill prey. When adults were provided with a prey diet, Eu nematodes exhibited greater fitness than St nematodes by several measures, including longevity, offspring survival and fecundity when followed by bacterial feeding. However, the two mouth-forms had similar fecundity when fed ad libitum on bacteria, a condition that would confer benefit on the more rapidly developing St form. Thus, the two forms show conditional fitness advantages in different environments. This study provides, to our knowledge, the first functional context for dimorphism in a model for the genetics of plasticity.

Three-Dimensional Reconstruction of the Stomatostylet and Anterior Epidermis in the Nematode Aphelenchus avenae (Nematoda: Aphelenchidae) With Implications for the Evolution of Plant Parasitism

A three‐dimensional model of the stomatostylet and associated structures has been reconstructed from serial thin sections of Aphelenchus avenae, a representative of Tylenchomorpha, a group including most plant parasitic nematodes. The reconstruction is compared with previous work on bacteriovorous cephalobids and rhabditids to better understand the evolution of the stylet and its associated cells. Two arcade syncytia (“guide ring”) line the stylet shaft, supporting the hypothesis that the stylet shaft and cone (into which the shaft extends and which is not lined by syncytia) are homologous with the gymnostom of cephalobids, the sister taxon of tylenchids. Epidermal syncytia, HypA, HypB, HypC, and HypE, line the cephalic framework, vestibule, and vestibule extension, congruent with the hypothesis that these components are homologous with the cephalobid cheilostom. Relative to outgroups, HypC is expanded in A. avenae, enclosing sensilla that fill most of the cephalic framework. The homolog of syncytium HypD in the cephalobid Acrobeles complexus is not observed in A. avenae. Arcade syncytia are reduced compared with those of cephalobids. Stylet protractor muscles in A. avenae are homologous with the most anterior set of radial muscles of cephalobids. Observations to date test and verify our previous hypotheses of homology of the stomatostylet with respect to the stoma of bacteriovorous outgroups. Reconstruction of the stegostom and pharynx will provide further tests of homology and evolution of feeding structure adaptations for plant parasitism. J. Morphol., 2008.

Revised hypotheses for phylogenetic homology of the stomatostylet in tylenchid nematodes

Summary – Molecular phylogenetic systematics suggest that Tylenchida share an immediate ancestor with Cephalobina. This relationship has implications, contradicting classical views, for evolution of the stomatostylet and homology with the cephalobid stoma. Emerging evidence from comparative TEM and 3D modelling is the basis for hypothesising that the tylenchid stylet, specifically the cone and shaft, is homologous with cuticle associated with arcade syncytia of the cephalobid gymnostom; furthermore, the stylet knobs and associated m1 protractors, are prostegostom. The guiding apparatus through which the stylet moves is lined by epidermal syncytia and is homologous with the cephalobid cheilostom. Junctional complexes associated with the epidermal syncytia of the cheilostom and adjacent gymnostom arcade cells occur in both cephalobids and tylenchids, but in the latter the membrane complexes are folded and modified as the guide ring. Testing of the hypothesis requires clearer phylogenetic resolution as well as additional ultrastructural and developmental observations of representatives of tylenchids and outgroups.