Mitochondrial gene order variation in the brachiopod Lingula anatina and its implications for mitochondrial evolution in lophotrochozoans

Abstract

Vertebrate mitochondrial (mt) genomes display highly conserved gene order and relatively low evolutionary rates. However, these features are variable in marine invertebrates. Here we present the mt genome of the lingulid brachiopod, Lingula anatina, from Amami Island, Japan, as part of the nuclear genome project. We obtain ~2000-fold coverage of the 17.9-kb mt genome using Illumina sequencing, and we identify hypervariable regions within the same individual. Transcriptome analyses show that mt transcripts are polycistronic and expressed differentially. Unexpectedly, we find that the mt gene order of Amami Lingula is completely shuffled compared to that of a specimen from Yanagawa, suggesting that there may be cryptic species. Using breakpoint distance analyses with 101 metazoan mt genomes, we show that the evolutionary history of mt gene order among lophotrochozoans is unique. Analyses of non-synonymous substitution rates reveal that mt protein-coding genes of Lingula have experienced rapid evolution comparable to that expected for interspecific comparisons. Whole genome phylogenetic analyses suggest that mt genomes have limited value for inferring the phylogenetic positions of lophotrochozoans because of their high evolutionary rates in brachiopods and bivalves.