Resolving phylogenetic relationships within the order Enoplida (Phylum Nematoda)

Abstract

The Order Enoplida (Phylum Nematoda) has been proposed as a divergent
nematode lineage—Enoplid nematodes are thought to exhibit morphological and
developmental characteristics present in the ‘ancestral nematode’. However, previous molecular phylogenies have failed to unequivocally confirm the position of this group. The Enoplida is primarily comprised of free-living marine species; if these taxa represent close relatives of the nematode ancestor, this relationship would presumably imply a marine origin for the phylum. Prior to this investigation, few publically available gene sequences existed for Enoplid nematodes, and published sequences represented only shallow water fauna from Northwest Europe. This study has aimed to improve resolution at the base of the nematode tree, using drastically increased taxon-sampling within the previously neglected Enoplid clade. Morphological identifications, nuclear gene sequences (18S and 28S rRNA), and mitochondrial gene sequences (Cox1) were obtained from marine specimens representing a variety of deep-sea and intertidal habitats. Molecular data were used to assess the phylogenetic placement of the Enoplid clade, resolve internal taxonomic relationships within this group, and investigate relationships between shallow water and deep-sea fauna.
Despite rigorous empirical testing and comprehensive taxon sampling, large-scale phylogenetic analyses based on 18S rRNA sequences (using both Maximum Likelihood and Bayesian Inference methods) failed to provide added resolution at the base of the nematode tree. Molecular data from the 18S rRNA gene was unable to confirm the placement of Enoplida as a divergent lineage representing the sister taxon to all other nematodes. These findings highlight the limitations of the 18S gene for resolving the deepest evolutionary splits amongst nematode clades. Analysis of internal relationships reveals that the Enoplida is split into two main clades, with groups consisting of terrestrial and primarily marine fauna, respectively. For marine taxa, deep-sea and shallow-water specimens from the same genus consistently appear as sister taxa. Deep-sea nematode species may have arisen via several evolutionary routes; some deep-sea clades appear to represent recently derived forms, while other groups seem to have radiated much earlier. Nematodes from deep-sea sites exhibit no obvious clustering according to depth or geographic location, and specimens represent a wide taxonomic range within the Enoplida. In addition, there seems to be some molecular evidence for purportedly cosmopolitan nematode species; identical gene sequences were recorded between distant shallow water locations, as well as between deep-sea and shallow water habitats. Data from Enoplid nematodes suggests an intriguing pattern for nematode species distributions—validating these preliminary insights will require a large amount of molecular data from many additional geographic locations. Future studies will also need to incorporate data from additional genetic loci (or use phylogenomic methods) in order to build robust deep phylogenies.

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