Dataset Information

The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida).

ABSTRACT: BACKGROUND: Mitochondrial genomes form units of genetic information replicating indepentently from nuclear genomes. Sequence data (most often from protein-coding genes) and other features (gene order, RNA secondary structure) of mitochondrial genomes are often used in phylogenetic studies of metazoan animals from population to phylum level. Pycnogonids are primarily marine arthropods, often considered closely related to chelicerates (spiders, scorpions and allies). However, due to their aberrant morphology and to controversial results from molecular studies, their phylogenetic position is still under debate. RESULTS: This is the first report of a complete mitochondrial genome sequence from a sea spider (Nymphon gracile, class Pycnogonida). Gene order derives from that of other arthropods so that presumably 10 single tRNA gene translocations, a translocation of the mitochondrial control region, and one large inversion affecting protein-coding genes must have happened in the lineage leading to Nymphon gracile. Some of the changes in gene order seem not to be common to all pycnogonids, as those were not found in a partial mitochondrial genome of another species, Endeis spinosa. Four transfer RNAs of Nymphon gracile show derivations from the usual cloverleaf secondary structure (truncation or loss of an arm). Initial phylogenetic analyses using mitochondrial protein-coding gene sequences placed Pycnogonida as sister group to Acari. However, this is in contrast to the majority of all other studies using nuclear genes and/or morphology and was not recovered in a second analysis where two long-branching acarid species were omitted. CONCLUSION: Extensive gene rearrangement characterizes the mitochondrial genome of Nymphon gracile. At least some of the events leading to this derived gene order happened after the split of pycnogonid subtaxa. Nucleotide and amino acid frequencies show strong differences between chelicerate taxa, presumably biasing phylogenetic analyses. Thus the affinities between Pycnogonida and Acari (mites and ticks), as found in phylogenetic analyses using mitochondrial genes, may rather be due to long-branch attraction and independently derived nucleotide composition and amino acid frequency, than to a real sister group relationship.

SUBMITTER: Podsiadlowski L

PROVIDER: S-EPMC1636051 | biostudies-literature | 2006

REPOSITORIES: biostudies-literature

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The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida).

Podsiadlowski Lars L Braband Anke A

BMC genomics 20061106

<h4>Background</h4>Mitochondrial genomes form units of genetic information replicating indepentently from nuclear genomes. Sequence data (most often from protein-coding genes) and other features (gene order, RNA secondary structure) of mitochondrial genomes are often used in phylogenetic studies of metazoan animals from population to phylum level. Pycnogonids are primarily marine arthropods, often considered closely related to chelicerates (spiders, scorpions and allies). However, due to their a ...[more]

PMID: 17087824

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Project description:BackgroundThe phylogenetic position of pycnogonids is a long-standing and controversial issue in arthropod phylogeny. This controversy has recently been rekindled by differences in the conclusions based on neuroanatomical data concerning the chelifore and the patterns of Hox expression. The mitochondrial genome of a sea spider, Nymphon gracile (Pycnogonida, Nymphonidae), was recently reported in an attempt to address this issue. However, N. gracile appears to be a long-branch taxon on the phylogenetic tree and exhibits a number of peculiar features, such as 10 tRNA translocations and even an inversion of several protein-coding genes. Sequences of other pycnogonid mitochondrial genomes are needed if the position of pycnogonids is to be elucidated on this basis.ResultsThe complete mitochondrial genome (15,474 bp) of a sea spider (Achelia bituberculata) belonging to the family Ammotheidae, which combines a number of anatomical features considered plesiomorphic with respect to other pycnogonids, was sequenced and characterized. The genome organization shows the features typical of most metazoan animal genomes (37 tightly-packed genes). The overall gene arrangement is completely identical to the arthropod ground pattern, with one exception: the position of the trnQ gene between the rrnS gene and the control region. Maximum likelihood and Bayesian inference trees inferred from the amino acid sequences of mitochondrial protein-coding genes consistently indicate that the pycnogonids (A. bituberculata and N. gracile) may be closely related to the clade of Acari and Araneae.ConclusionThe complete mitochondrial genome sequence of A. bituberculata (Family Ammotheidae) and the previously-reported partial sequence of Endeis spinosa show the gene arrangement patterns typical of arthropods (Limulus-like), but they differ markedly from that of N. gracile. Phylogenetic analyses based on mitochondrial protein-coding genes showed that Pycnogonida may be authentic arachnids (= aquatic arachnids) within Chelicerata sensu lato, as indicated by the name 'sea spider,' and suggest that the Cormogonida theory - that the pycnogonids are a sister group of all other arthropods - should be rejected. However, in view of the relatively weak node confidence, strand-biased nucleotide composition and long-branch attraction artifact, further more intensive studies seem necessary to resolve the exact position of the pycnogonids.

Project description:Background:Sea spiders (Pycnogonida) are an abundant faunal element of the Southern Ocean (SO). Several recent phylogeographical studies focused on the remarkably diverse SO pycnogonid fauna, resulting in the identification of new species in previously ill-defined species complexes, insights into their genetic population substructures, and hypotheses on glacial refugia and recolonization events after the last ice age. However, knowledge on the life history of many SO pycnogonids is fragmentary, and early ontogenetic stages often remain poorly documented. This impedes assessing the impact of different developmental pathways on pycnogonid dispersal and distributions and also hinders pycnogonid-wide comparison of developmental features from a phylogenetic-evolutionary angle. Results:Using scanning electron microscopy (SEM) and fluorescent nuclear staining, we studied embryonic stages and postembryonic instars of three SO representatives of the taxon Pallenopsidae (Pallenopsis villosa, P. hodgsoni, P. vanhoeffeni), the development of which being largely unknown. The eggs are large and yolk-rich, and the hatching stage is an advanced lecithotrophic instar that stays attached to the father for additional molts. The first free-living instar is deduced to possess at least three functional walking leg pairs. Despite gross morphological similarities between the congeners, each instar can be reliably assigned to a species based on body size, shape of ocular tubercle and proboscis, structure of the attachment gland processes, and seta patterns on cheliphore and walking legs. Conclusions:We encourage combination of SEM with fluorescent markers in developmental studies on ethanol-preserved and/or long term-stored pycnogonid material, as this reveals internal differentiation processes in addition to external morphology. Using this approach, we describe the first known cases of pallenopsid development with epimorphic tendencies, which stand in contrast to the small hatching larvae in other Pallenopsidae. Evaluation against current phylogenetic hypotheses indicates multiple gains of epimorphic development within Pycnogonida. Further, we suggest that the type of development may impact pycnogonid distribution ranges, since free-living larvae potentially have a better dispersal capability than lecithotrophic attaching instars. Finally, we discuss the bearing of pycnogonid cheliphore development on the evolution of the raptorial first limb pair in Chelicerata and support a multi-articled adult limb as the plesiomorphic state of the chelicerate crown group, arising ontogenetically via postembryonic segmentation of a three-articled embryonic limb.

Dataset Information

The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida).

Publications

The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida).

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