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Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism.

ABSTRACT: BACKGROUND:The nematode Pristionchus pacificus has originally been developed as a satellite organism for comparison to Caenorhabditis elegans. A 10X coverage of the whole genome of P. pacificus is available, making P. pacificus the first non-Caenorhabditis nematode with a fully sequenced genome. The macroevolutionary comparison between P. pacificus and C. elegans has been complemented by microevolutionary studies of closely related strains and species within the genus Pristionchus. In addition, new understanding of the biology of Pristionchus from field studies, demonstrating a close association with various scarab beetles and the Colorado potato beetle, supports consideration of this nematode in studies of ecosystems. In the course of field studies on four continents more than 1,200 isolates were established from 15,000 beetle specimens representing 18 Pristionchus species. Two remarkable features of the Pristionchus-beetle association are the high species specificity of the interaction and the interception of the beetle's sex communication system for host recognition by the nematodes, as suggested by chemotaxis studies. Evolutionary interpretations of differences in developmental, behavioral and ecological patterns require a phylogenetic framework of the genus Pristionchus. RESULTS:Here, we provide a robust phylogeny of all 18 available Pristionchus species based on a set of 27 ribosomal protein genes encompassing a total of 10,971 bp. The phylogenetic tree provides evidence for North American and European clades, which are embedded in a deeper clade that includes Asian species. It also indicates putative invasion events. Of the 18 Pristionchus species, 13 are gonochoristic and five are hermaphroditic. The phylogeny indicates that all hermaphroditic species have arisen independently within the genus Pristionchus. CONCLUSION:Combined ribosomal protein cDNA data can provide the basis for reconstruction of a robust phylogenetic framework for microevolutionary and biogeographic analyses. An additional major implication of our studies is the use of Pristionchus for nematode biodiversity assessments. While some species are represented by more than 100 isolates, others were found less than four times. Such patterns were observed on all continents and in all phylogenetic clades indicating that species asymmetry is a widespread phenomenon, which can now be further investigated by molecular tools.

SUBMITTER: Mayer WE

PROVIDER: S-EPMC1929057 | biostudies-literature | 2007 Jul

REPOSITORIES: biostudies-literature

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Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism.

Mayer Werner E WE Herrmann Matthias M Sommer Ralf J RJ

BMC evolutionary biology 20070702

<h4>Background</h4>The nematode Pristionchus pacificus has originally been developed as a satellite organism for comparison to Caenorhabditis elegans. A 10X coverage of the whole genome of P. pacificus is available, making P. pacificus the first non-Caenorhabditis nematode with a fully sequenced genome. The macroevolutionary comparison between P. pacificus and C. elegans has been complemented by microevolutionary studies of closely related strains and species within the genus Pristionchus. In ad ...[more]

PMID: 17605767

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Project description:The complex orogeny of the Himalaya and the Qinghai-Tibet Plateau (QTP) fosters habitat fragmentation that drives morphological differentiation of mountain plant species. Consequently, determining phylogenetic relationships between plant subgenera using morphological characters is unreliable. Therefore, we used both molecular phylogeny and historical biogeographic analysis to infer the ancestral states of several vegetative and reproductive characters of the montane genus Incarvillea. We determined the taxonomic position of the genus Incarvillea within its family and inferred the biogeographical origin of taxa through Bayesian inference (BI), maximum likelihood (ML) and maximum parsimony (MP) analyses using three molecular data sets (trnL-trnF sequences, nr ITS sequences, and a data set of combined sequences) derived from 81% of the total species of the genus Incarvillea. Within the genus-level phylogenetic framework, we examined the character evolution of 10 key morphological characters, and inferred the ancestral area and biogeographical history of the genus. Our analyses revealed that the genus Incarvillea is monophyletic and originated in Central Asia during mid-Oligocene ca. 29.42 Ma. The earliest diverging lineages were subsequently split into the Western Himalaya and Sino-Himalaya during the early Miocene ca. 21.12 Ma. These lineages resulted in five re-circumscribed subgenera (Amphicome, Olgaea, Niedzwedzkia, Incarvillea, and Pteroscleris). Moreover, character mapping revealed the ancestral character states of the genus Incarvillea (e.g., suffruticose habit, cylindrical capsule shape, subligneous capsule texture, absence of capsule wing, and loculicidal capsule dehiscence) that are retained at the earliest diverging ancestral nodes across the genus. Our phylogenetic tree of the genus Incarvillea differs from previously proposed phylogenies, thereby recommending the placement of the subgenus Niedzwedzkia close to the subgenus Incarvillea and maintaining two main divergent lineages.

Project description:BackgroundThe nematode Pristionchus pacificus has been developed as a satellite organism in evolutionary developmental biology for comparison to Caenorhabditis elegans. Comparative studies have revealed major differences in the regulation of developmental processes between P. pacificus and C. elegans. To place evolutionary developmental biology and the observed developmental differences between species in a comprehensive evolutionary context, such studies have to be complemented with ecological aspects. Knowledge about the ecology of the organism in question might indicate specific environmental conditions that can result in developmental adaptations and could account for species differences in development. To this end, we have started to investigate the ecology of Pristionchus nematodes. In recent field studies in Western Europe we found six Pristionchus species that are closely associated with scarab beetles and the Colorado potato beetle. This Pristionchus-beetle association provides the unique opportunity to combine research in evolutionary developmental biology with ecology. However, it remains unknown how general these findings from Europe are on a global scale.ResultsHere, we describe the Pristionchus species associated with scarab and Colorado potato beetles in the Eastern United States and show striking transatlantic differences and unexpected evolutionary and ecological patterns. Two hundred eighty of 285 (98%) isolates from American scarab beetles belong to five Pristionchus species, all of which are different from the European species. We describe four of them as novel Pristionchus species. The five American Pristionchus species fall into a single phylogenetic clade and have a male-female (gonochoristic) mode of reproduction, whereas the majority of European isolates are hermaphroditic. Crosses between the two most closely related species, P. aerivorus and P. pseudaerivorus n. sp., follow Haldane's rule in that heterogametic F1 males are inviable. We observed P. aerivorus and P. pseudaerivorus n. sp. coexisting on the same scarab beetle and obtained two cases of F1 hybrids from wild beetles. Finally, the Colorado potato beetle is associated with the same nematode, P. uniformis in the United States and Europe. Given the introduction of the Colorado potato beetle to Europe in 1877, our results suggest that P. uniformis was introduced together with its beetle vector.ConclusionTaken together, the Pristionchus-beetle association provides a powerful tool for studying biodiversity, biogeography, speciation and species invasion on a global scale.

Dataset Information

Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism.

Publications

Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism.

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