Ascidian mitogenomics: Comparison of evolutionary rates in closely related taxa provides evidence of ongoing speciation events

Francesca Griggio, Ayelet Voskoboynik, Fabio Iannelli, Fabienne Justy, Marie Ka Tilak, Turon Xavier, Graziano Pesole, Emmanuel J P Douzery, Francesco Mastrototaro, Carmela Gissi

Research output: Contribution to journalArticle

Abstract

Ascidians are a fascinating group of filter-feeding marine chordates characterized by rapid evolution of both sequences and structure of their nuclear and mitochondrial genomes. Moreover, they include several model organisms used to investigate complex biological processes in chordates. To study the evolutionary dynamics of ascidians at short phylogenetic distances, we sequenced 13 new mitogenomes and analyzed them, together with 15 other available mitogenomes, using a novel approach involving detailed whole mitogenome comparisons of conspecific and congeneric pairs. The evolutionary rate was quite homogeneous at both intraspecific and congeneric level, and the lowest congeneric rates were found in cryptic (morphologically undistinguishable) and inmorphologically very similar species pairs. Moreover, congeneric nonsynonymous rates (dN) were up to two orders of magnitude higher than in intraspecies pairs. Overall, a clear-cut gap sets apart conspecific from congeneric pairs. These evolutionary peculiarities allowed easily identifying an extraordinary intraspecific variability in the model ascidian Botryllus schlosseri, where most pairs show a dN value between that observed at intraspecies and congeneric level, yet consistently lower than that of the Ciona intestinalis cryptic species pair. These data suggest ongoing speciation events producing genetically distinct B. schlosseri entities. Remarkably, these ongoing speciation events were undetectable by the cox1 barcode fragment, demonstrating that, at low phylogenetic distances, the whole mitogenomehas a higher resolving power than cox1. Our study shows that whole-mito genome comparative analyses, performedon a suitable sample of congeneric and intraspecies pairs, may allow detecting not only cryptic species but also ongoing speciation events.

Original languageEnglish
Pages (from-to)591-605
Number of pages15
JournalGenome Biology and Evolution
Volume6
Issue number3
DOIs
Publication statusPublished - 2014

Keywords

  • Ascidian
  • Evolutionary rate
  • Mitochondrial genome
  • Species identification

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

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    Griggio, F., Voskoboynik, A., Iannelli, F., Justy, F., Tilak, M. K., Xavier, T., Pesole, G., Douzery, E. J. P., Mastrototaro, F., & Gissi, C. (2014). Ascidian mitogenomics: Comparison of evolutionary rates in closely related taxa provides evidence of ongoing speciation events. Genome Biology and Evolution, 6(3), 591-605. https://doi.org/10.1093/gbe/evu041