Mitochondrial genomes suggest that hexapods and crustaceans are mutually paraphyletic

Abstract

For over a century the relationships between the four major groups of the phylum Arthropoda (Chelicerata, Crustacea, Hexapoda and Myriapoda) have been debated. Recent molecular evidence has confirmed a close relationship between the Crustacea and the Hexapoda, and has included the suggestion of a paraphyletic Hexapoda. To test this hypothesis we have sequenced the complete or near-complete mitochondrial genomes of three crustaceans (Parhyale hawaiensis, Squilla mantis and Triops longicaudatus), two collembolans (Onychiurus orientalis and Podura aquatica) and the insect Thermobia domestica. We observed rearrangement of transfer RNA genes only in O. orientalis, P. aquatica and P. hawaiensis. Of these, only the rearrangement in O. orientalis, an apparent autapomorphy for the collembolan family Onychiuridae, was phylogenetically informative.We aligned the nuclear and amino acid sequences from the mitochondrial protein-encoding genes of these taxa with their homologues from other arthropod taxa for phylogenetic analysis. Our dataset contains many more Crustacea than previous molecular phylogenetic analyses of the arthropods. Neighbourjoining, maximum-likelihood and Bayesian posterior probabilities all suggest that crustaceans and hexapods are mutually paraphyletic. A crustacean clade of Malacostraca and Branchiopoda emerges as sister to the Insecta sensu stricto and the Collembola group with the maxillopod crustaceans. Some, but not all, analyses strongly support this mutual paraphyly but statistical tests do not reject the null hypotheses of a monophyletic Hexapoda or a monophyletic Crustacea. The dual monophyly of the Hexapoda and Crustacea has rarely been questioned in recent years but the idea of both groups' paraphyly dates back to the nineteenth century. We suggest that the mutual paraphyly of both groups should seriously be considered.

The complete mitochondrial genome of the subterranean crustaceanMetacrangonyx longipes(Amphipoda): A unique gene order and extremely short control region

“…Alternatively, one single reversal of the ancestral pancrustacean segment including cob nad6 trnP trnT, followed by a new reversal of the gene nad6 from the -to the + strand, plus three TDRLs could have produced the M. longipes mitogenome gene order. The gene order also differs from the pattern found in the only other amphipod analysed thus far, Parhyale hawaiiensis (Cook et al 2005 and our own data). We have almost completed the sequence for the mitogenome of this species except for a short part of the gene rrnS and the control region [EMBL: FM957525 and FM957526], annotating the genes for trnV, partial rrnS, trnM, trnY, trnC, and locating the gene trnH between nad5 and nad4, which was absent in the previous annotation (Cook et al 2005).…”

“…The gene order also differs from the pattern found in the only other amphipod analysed thus far, Parhyale hawaiiensis (Cook et al 2005 and our own data). We have almost completed the sequence for the mitogenome of this species except for a short part of the gene rrnS and the control region [EMBL: FM957525 and FM957526], annotating the genes for trnV, partial rrnS, trnM, trnY, trnC, and locating the gene trnH between nad5 and nad4, which was absent in the previous annotation (Cook et al 2005). In addition, based on tRNAscan results, we reannotated the tRNA genes trnW and trnG previously annotated as trnC and trnW, respectively (Cook et al 2005; accession number AY639937).…”

“…Argulus americanus C. B. Wilson, 1902 (Branchiura, Maxillopoda) has the highest AT content found so far in any crustacean at 77.80% (Machida et al 2002), while the nearly complete amphipod mitochondrial sequence of Parhyale hawaiiensis reaches 73.66% (Cook et al 2005 and our own data).…”

“…First, phylogenetic analyses of protein-coding genes (PCGs) including the more intensively sampled mitochondrial genomes of Hexapoda suggest a mutual paraphyly of Crustacea and Hexapoda (Carapelli et al 2007;Cook et al 2005). Second, frequent translocation events have apparently changed the mitochondrial gene order in crustaceans compared with the putative ancestral pancrustacean pattern (Kilpert and Podsiadlowski 2006;Yang and Yang 2008).…”

“…Within the malacostracan peracarid order Amphipoda, only a partial mitogenome sequence is currently available in sequence databases: that of Parhyale hawaiiensis (Dana 1853), although it lacks of about 3 Kb including the rrnS gene and parts of rrnL and nad2, and also the control region (Cook et al 2005). In addition, in the peracarid order Isopoda one entire (Ligia oceanica) and two partial mitogenomes (Armadillidium vulgare and Idotea baltica) are known (Kilpert and Podsiadlowski 2006;Podsiadlowski and Bartolomaeus 2006;Marcadé et al 2007).…”