Phylogenetic position of a whale-fall lancelet (Cephalochordata) inferred from whole mitochondrial genome sequences

Takeshi Kon,Yoshihiro Fujiwara,Teruaki Nishikawa,Yusuke Yamanoue,Masahiro Nohara,Mutsumi Nishida

doi:10.1186/1471-2148-7-127

Abstract

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.

Highlights

The lancelet Asymmetron inferum 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
Features of A. inferum mitogenome The nucleotide sequences from the mitogenomes of the three Asymmetron species have been deposited in DDBJ/ EMBL/GenBank under the accession numbers of AP009352 for A. inferum, AP009353 for Asymmetron sp
The topology of the resulting trees implies that the asymmetrical arrangement of gonads seen paraphyletically in the genus Asymmetron and Epigonichthys can be regarded as a plesiomorphic feature, supporting the hypothesis that the gonadal symmetry in the genus Branchiostoma was derived from the asymmetric Epigonichthys-like ancestor [16]

Summary

Introduction

The 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. It has been believed that the lancelets prefer such aerobic conditions, whereas recently a new lancelet Asymmetron inferum was discovered in an anaerobic and sulfide-rich bottom [7] This species is only distinguishable morphologically from congeners by the number of myomeres [7]. A. inferum is a member of this community [12]

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