MBE Advance Access published online on February 29, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn027
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Research Article |
Long-term Evolutionary Stability of Bacterial Endosymbiosis in Curculionoidea: Additional Evidence of Symbiont Replacement in the Dryophthoridae Family
1 Laboratoire d’Écologie Alpine, CNRS UMR 5553, Université Joseph Fourier, B.P. 53, F-38,041 Grenoble, Cedex 9, France
2 UMR203 Biologie Fonctionnelle Insectes et Interactions, IFR41, INRA, INSA-Lyon, F-69,621 Villeurbanne, France
* Corresponding author: A. HEDDI, Laboratoire de Biologie Fonctionnelle Insectes et Interactions, UMR INRA / INSA de Lyon, Bât. Louis PASTEUR, 20 Avenue Albert EINSTEIN, 69,621 Villeurbanne cedex, France. Tel: 00 334 72 43 88 68, Fax: 00 334 72 43 85 34, E-mail address: Abdelaziz.Heddi{at}insa-lyon.fr
Received for publication May 10, 2007. Revision received July 19, 2007. Revision received October 30, 2007. Revision received January 15, 2008. Accepted for publication January 20, 2008.
Bacterial intracellular symbiosis (endosymbiosis) is well documented in the insect world where it is believed to play a crucial role in adaptation and evolution. However, although Coleopteran insects are of huge ecological and economical interest, endosymbiont molecular analysis is limited to the Dryophthoridae family. Here, we have analyzed the intracellular symbiotic bacteria in two Hylobius species belonging to the Molytinae sub-family (Curculionoidea super-family) that exhibit different features from the Dryophthoridae insects in terms of their ecology and geographical spanning. Fluorescence in situ hybridization (FISH) has shown that both Hylobius species harbor rod-shaped pleiomorphic symbiotic bacteria in the oocyte and in the bacteria-bearing organ (the bacteriome), with a shape and location similar to those of the Dryophthoridae bacteriome. Phylogenetic analysis of the 16S rDNA gene sequences, using the heterogeneous model of DNA evolution, has placed the Hylobius spp. endosymbionts (H-group) at the basal position of the ancestral R-clade of Dryophthoridae endosymbionts named Candidatus Nardonella, but relatively distant from the S-clade of Sitophilus spp. endosymbionts. Endosymbionts from the H-group and the R-clade evolved more quickly compared with free-living enteric bacteria and endosymbionts from the S- and D-clades of Dryophthoridae. They are AT-biased (58.3% A+T) and they exhibit AT-rich insertions at the same position as previously described in the Candidatus Nardonella 16S rDNA sequence. Moreover, the host phylogenetic tree based on the mitochondrial COI gene was shown to be highly congruent with the H-group and the R-clade, the divergence of which was estimated to be around 125 million-years (Myr) ago. These new molecular data show that endosymbiosis is old in Curculionids, going back at least to the common ancestor of Molytinae and Dryophthoridae, and is evolutionary stable, except in two Dryophthoridae clades, providing additional and independent supplementary evidence for endosymbiont replacement in these taxa.
Key Words: Endosymbiosis • evolution • phylogeny • Molytinae • Dryophthoridae • Curculionoidea