BackgroundThe lancelet Asymmetron inferum (subphylum Cephalochordata) was recently discovered on the ocean floor off the southwest coast of Japan at a depth of 229 m, in an anaerobic and sulfide-rich environment caused by decomposing bodies of the sperm whale Physeter macrocephalus. This deep sulfide-rich habitat of A. inferum is unique among the lancelets. The distinguishing adaptation of this species to such an extraordinary habitat can be considered in a phylogenetic framework. As the first step of reconstruction of the evolutionary processes in this species, we investigated its phylogenetic position based on 11 whole mitochondrial genome sequences including the newly determined ones of the whale-fall lancelet A. inferum and two coral-reef congeners.ResultsOur phylogenetic analyses showed that extant lancelets are clustered into two major clades, the Asymmetron clade and the Epigonichthys + Branchiostoma clade. A. inferum was in the former and placed in the sister group to A. lucayanum complex. The divergence time between A. inferum and A. lucayanum complex was estimated to be 115 Mya using the penalized likelihood (PL) method or 97 Mya using the nonparametric rate smoothing (NPRS) method (the middle Cretaceous). These are far older than the first appearance of large whales (the middle Eocene, 40 Mya). We also discovered that A. inferum mitogenome (mitochondrial genome) has been subjected to large-scale gene rearrangements, one feature of rearrangements being unique among the lancelets and two features shared with A. lucayanum complex.ConclusionOur study supports the monophyly of genus Asymmetron assumed on the basis of the morphological characters. Furthermore, the features of the A. inferum mitogenome expand our knowledge of variation within cephalochordate mitogenomes, adding a new case of transposition and inversion of the trnQ gene. Our divergence time estimation suggests that A. inferum remained a member of the Mesozoic and the early Cenozoic large vertebrate-fall communities before shifting to become a whale-fall specialist.
Complete mitochondrial (mt) DNA sequences of two lancelets, Epigonichthys maldivensis and E. lucayanus, were compared with those of two Branchiostoma lancelets and several deuterostomes previously surveyed. The mt-gene order of E. lucayanus was quite different from that of E. maldivensis, the latter being identical to the two Branchiostoma species. A remarkable genomic change in E. lucayanus mtDNA was an inversion, indicating the possibility of recombination of the mt-genome. Gene rearrangements, probably attributable to tandem genome duplications and subsequent random deletions, were observed in two parts. Short major unassignable sequences of the examined lancelets were regarded as a part of putative regulative elements, judging from some sequence similarity to the conserved sequence block (CSB) in mammalian mtDNA. The considerable mt-genome reorganization in E. lucayanus seemed to have affected the nucleotide substitution pattern, suggested by base composition analyses. The present analysis also suggested that AGR codons in lancelet mtDNA were likely to correspond to serine residue, rather than glycine. Furthermore, the AGG codon, so far reputed to be unassignable in lancelet mtDNA, was found twice in E. maldivensis, indicating the availability of all four AGN codons in some lancelets. This finding lends support to an alternative hypothesis regarding the evolutionary history of AGR-codon assignment in extant chordates, rather than that previously proposed. A molecular phylogenetic tree of the Epigonichthys and Branchiostoma species based on DNA sequences of the 13 mt-protein genes doubted the monophyly of the former genus, unlike the prevailing classification based on their different gonadal arrangements.
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